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Article Contents

1 introduction, 2 research framework and data preparation, 3 knowledge-mapping model, 4 conclusions, conflicts of interest.

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The impact of agricultural chemical inputs on environment: global evidence from informetrics analysis and visualization

Lu Zhang and Chengxi Yan contribute equally to this work.

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Lu Zhang, Chengxi Yan, Qing Guo, Junbiao Zhang, Jorge Ruiz-Menjivar, The impact of agricultural chemical inputs on environment: global evidence from informetrics analysis and visualization, International Journal of Low-Carbon Technologies , Volume 13, Issue 4, December 2018, Pages 338–352, https://doi.org/10.1093/ijlct/cty039

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This paper identifies and analyzes salient research frontiers, research hotspots and high-frequency terms using aggregated and multiple-source literature records related to the topic of ‘effects of agricultural chemical inputs on the environment.’ We employ a set of Informetrics Theory methods (i.e. document co-citation analysis, document clustering and co-words analysis via co-occurrence network of subject terms) for our analysis. Our findings suggest that in the past 30 years, research about this topic can be divided into three stages, namely the early stage (1990–99), the middle stage (2000–07) and the late stage (2008–16). Research directions for the three identified stages deal primarily with (a) the effects of pesticides and veterinary drugs on the environment, (b) the influence of fertilizer application on the environment and food safety and (c) the technologies and strategies to monitor and control the impact of agricultural chemical inputs on the environment. Particularly, we find that research in the topic of interest primarily focusses on agricultural scenarios of food crop production and fish farming. In terms of agricultural chemical inputs, major attention is given to pesticides and fertilizers. With respect to the impact of agricultural inputs, pollutant formation and transferring process, nitrogen and phosphorous cycles, impact assessment indicators, as well as pollution prevention and reduction strategies are the most researched areas, and soil and water constitute the main researched environmental media. Finally, institutions and organization based in North America, East Asia and Europe are main research contributors on this topic.

Agricultural inputs broadly refer to the materials used or added in the process of agricultural production and include biological inputs, chemical inputs, and agricultural facilities and equipment. In particular, agricultural chemical inputs denote the different types of chemical applications in agricultural production, such as pesticides (including natural and biological pesticides), chemical fertilizers, veterinary drugs and feed additives, among others.

Agricultural management practices—for example, an increased use of agricultural chemicals or fertilizers—are often evaluated based on their benefits for economic efficiencies in production (e.g. reduction in total production costs and increased production yield) while less attention is generally given to their potential environmental effects [ 1 ]. For example, pesticide and fertilizer application plays a vital role in increasing agricultural production and ensuring the supply of agricultural products. Pesticide spraying can significantly reduce or offset the economic costs from plant diseases, insect pests, and weeds on agricultural production and fertilizer application can provide a variety of nutrients required for the growth of crops and for an increased yield in production. However, many countries have reported alarming residues of agricultural chemicals in soil, water, air, agricultural products, and even in human blood and adipose tissue [ 2 , 3 ].

Research suggests that the massive use of inorganic fertilizers world-wide is associated with the accumulation of contaminants, e.g. arsenic (As), cadmium (Cd), fluorine (F), lead (Pb) and mercury (Hg) in agricultural soils [ 1 ]. In the USA, according to a survey of 51 major river basins and aquifer systems by the US Geological Survey, pesticides were detected 97% of the time in samples from stream water in agricultural areas [ 4 ]. In Japan, pesticides were frequently detected in the air of residential environments and childcare facilities following the application of pesticides—this is consistent with the findings that outside pesticide applications are major contributors to indoor air pollution in agricultural communities [ 5 ].

In most developing countries, the pollution caused by agricultural chemicals is even more serious [ 6 , 7 ]. The usage volume of fertilizers and pesticides in China has been the recorded as the highest in the world. Specifically, its chemical fertilizer usage volume has reached more than 59 million tons and pesticide more than 1.8 million tons [ 8 ]. Alarmingly, the total utilization rate of fertilizers and pesticides is only ~35% [ 9 ], and thus, any fertilizer and pesticide losses are likely to contaminate soil, surface water and groundwater. In China, estimates indicate that contaminated arable land area is ~150 million acres, accounting for 8.3% of the total arable land in the nation [ 10 ]. In addition, nearly half of the groundwater resources have been inordinately polluted by agricultural chemicals, which seriously threaten the safety of drinking water in China, especially in rural areas. [ 11 ] reports that consequences of an increased use of agricultural chemicals transcend the environment. Farmers in developing countries are experiencing, either short-term or long-term, health effects from exposures to agricultural chemicals, including severe symptoms (e.g. headaches, skin rashes, eye irritations) and some chronic effects (e.g. cancer, endocrine disruption, birth defects).

Policy makers recognize that the excessive and unsystematic application of agrichemical inputs, pesticides and fertilizers in particular, is an obstacle to the development of sustainable agriculture, and poses a threat to the environment and humans alike. Several countries have enacted policies to regulate the usage volume and types of agricultural chemicals [ 12 , 13 ]. For instance, in the USA, the 1972 Federal Environmental Pesticide Control Act (FEPCA) and subsequent amendments acknowledge the negative effects of pesticide applications on both the environment and human health, regulate the use of pesticides and enforce compliance against banned pesticide products. The 2003, European Union Regulation EC No. 2003/2003 establishes that electrical conductivity fertilizers should meet a specific criteria in terms of nutrient content, safety and absence of adverse effects to the environment [ 14 ]. In 2015, the Chinese Ministry of Agriculture introduced the ‘Action to Achieve Zero Growth in the Application of fertilizer’ and ‘Action Plan for Zero Growth in the Application of Pesticide’, which both set specific goals, strategies, plans and relevant safeguard measures for controlling the usage of agricultural chemicals by year 2020 [ 15 ].

Scholars in the fields of agriculture, chemistry, environmental science, ecology, medicine and economics have also been highly concerned about the threat of excessively using agricultural chemicals to the environment and human health. In the last two decades, researchers have mainly focused on the following four areas regarding the increased use of agrichemicals and their impact. First, prior literature has explored the pollution derived from using pesticides and chemical fertilizers for the natural environment (i.e. soil microbial community response, agricultural water pollution, agricultural greenhouse gas emissions, agricultural fertilizer loss) [ 16 – 18 ]. Secondly, researchers have investigated the effects of using pesticides and fertilizers on agricultural production (i.e. soil fertility, farmland diseases, farmland weeds and farmland pests) [ 16 , 18 , 19 ]. Thirdly, other research has focused on the impact of using pesticides and fertilizers for society (i.e. social economy, food security and human health) [ 20 – 22 ]. Finally, extant literature has explored the interactions among chemical inputs, crop yield and the ecological environment [ 23 , 24 ].

Previous literature review studies documenting the impact of agricultural chemicals on the environment have normally employed qualitative methods (e.g. manual investigation and literature classification) rather than quantitative methods (e.g. Informetrics analysis and visualization), and have used limited sources of data (e.g. key documents and reports) to perform the reviews. In addition, the research scale for most review studies has been narrow, focusing on a specific type of agricultural chemical input (e.g. pesticides or fertilizers) and analyzing its impact on a single environmental element (e.g. soil, water or air). To our knowledge, only a few scholars have reviewed the impact of agricultural chemicals on water, soil and human health conjunctively [ 1 , 25 , 26 ].

The present study addresses these limitations and utilizes a robust quantitative approach (i.e. information metrology) to exploit the data richness from aggregated and multiple-source records to perform the review. We aim to systematically and objectively present the research evolution of the literature conducted on the macro-environmental effects induced by excessive use chemical inputs (i.e. fertilizers and pesticides) in agriculture (i.e. fertilizers and pesticides) and to provide further insight into future research directions or intersections that may of interest for researchers and policy makers.

2.1 Research framework

The field of Informetrics deals with the quantitative analysis of information, aiming to reveal patterns and associations of information objects, their production, structure and dissemination [ 27 ]. Citation analysis is a core method in Informetrics. With feature statistics, citation analysis can effectively find common domains of knowledge for analyzed records. Based on citation analysis, generalized Informetrics—a combination of statistical description, mathematical model and machine learning—has become a cross-discipline approach for scientific knowledge evaluation, and includes popular methods, such as ‘co-word network,’ ‘clustering Analysis’ and ‘mapping knowledge domain.’

Co-word network is a relational network based on the co-occurrence of keywords or subject terms in the literature; this method belongs to the catalog of ‘Content Analysis Method’. Cluster analysis comes from the notion of automatic categorization for similar abstract objects based on the theory of machine learning, and aims to cluster analogous members and divide unrelated objects. Mapping knowledge domain enables to reveal relevant research frontiers and frameworks, and intuitively demonstrates the development process of a discipline or knowledge using graphical representations and tools.

2.2 Data retrieval and preprocessing

First, we ascertain scientific subject terms through the platform ‘LCSH’ (Library of Congress Subject Headings) from which candidate words are examined using query entries via the function ‘LC Linked Data Service’. Second, we conduct the preprocessing stage (i.e. data cleaning, knowledge representation, formation of co-word matrix) using 16 459 articles retrieved from the core data set of web of science (WOS). The result of the latter phase is the development and creation of a knowledge-mapping model with focus on the main theme of ‘agricultural chemical inputs and environmental impact.’

Query reformulation is a critical phase of searching and collecting target articles [ 28 ]. In this paper, the preliminary query formulation is formed according to the integration of candidate words, including ‘agricultural chemicals’, ‘farm chemicals’, ‘pesticides’, ‘fertilizers’, ‘fertilizers’, ‘manures’ and ‘environment’. Through associated retrieval by the ‘LC Linked Data Service’ tool, ‘agricultural chemicals’, ‘pesticides’, ‘fertilizers’ and ‘manures’ are identified as conception topics. ‘Agricultural chemicals’ is the extension of the concept terms ‘pesticides’ and ‘fertilizers’ (i.e. broader term relationship). ‘Manures’, by contrast, is a narrower term for ‘pesticides’ (i.e. narrower term relationship). ‘Fertilizers’ and ‘farm chemicals’ should not be taken as independent subject terms as they are lexical variants of ‘fertilizers’ and ‘agricultural chemicals.’ Therefore, for this study the independent subject terms are as follows: ‘agricultural chemicals’, ‘pesticides’, ‘fertilizers’ and ‘environment’.

After identifying the subject terms, we scanned selected databases (i.e. SCI-E, SSCI, A&HCI, CPCI-S and CPCI-SSH) in WOS. Specifically, the query reformulation of term collocation is ‘(TOPIC: (agricultural chemical) AND TOPIC: (environment)) OR (TOPIC: (pesticides) AND TOPIC: (environment)) OR (TOPIC: (fertilizers) AND TOPIC: (environment))’. The time span used for this query is from 1990 to 2016 (last updated on 21 October 2016).

The data preprocessing phase aims to unify inconsistent formats and units of data from different systems or platforms [ 29 ]. This paper adopts three methods (i.e. data cleaning, knowledge representation and automation formation of co-word matrix) to conduct the data preprocessing. For data cleaning and in anticipation that WOS records may be subject to noise or missing data, we conduct an artificial exclusion and consistency check by removing unrecognizable keywords with high frequency, such as ‘u 238’ or ‘34’. Then, for knowledge representation, we use citation network analysis via CitesSpace and formed 6 079 nodes and 5 217 edges. Finally, based on the revised pagerank index, we employ the Gelphi platform to form a co-work matrix, which is an efficient method for analyzing and exploring potential rules and interplay amid various literature records.

Constructing a knowledge-mapping model for the topic ‘the impact of agricultural chemicals on environment’ can provide further guidance on the research directions, hot topics and research frontiers, as well as on the distributions and discipline evolution. Figure 1 shows the knowledge-mapping model established in this paper. The part A of Figure 1 shows a green highlighted area in the middle of the network called ‘giant component’ and represents the tightest and most stable part of the overall knowledge network about ‘the impact of agricultural chemicals on environment’. This paper analyzes different aspects of the ‘giant component’ network. Special attention is paid to mining and interpreting the distinctive nodes in order to further understand the knowledge baseline and research frontiers for the topic of interest. Using clustering and visualization analysis with the construction of a co-word matrix, this study offers a summary of the main and timely areas of interest or concern, as well as major objects and research methods used in the research of this topic. The following section provides the results for a set of Informetrics Theory-based analyses: document co-citation analysis, document citation-clustering and co-words analysis via co-occurrence network of subject terms.

Global and macro-scope view based on citation analysis.

3.1 Co-citation analysis

Citation analysis explores the citation relationship and co-occurrence patterns of original papers and their references. It aims to reveal the knowledge connection, knowledge structure and knowledge rules of the target scientific area. A time-dimensional visualized intellectual landscape is constructed and provided in Part B of Figure 1 . In the past 30 years, researches on the environmental impacts from agricultural chemical inputs could be divided into three stages, namely early stage from 1990 to1999 (B1), middle stage from 2000 to 2007 (B2) and late stage from 2008 to 2016 (B3). Using the results from citation analysis, we identify two proliferous authors, Yi-fan Li and Dana W. Kolpin, for the research topic of interest (i.e. the impact of agricultural chemical inputs on the environment). These two authors were selected based on the number of authored and published journal articles and their consistent contribution to the aforementioned research topic in the last three decades. For illustration purposes, we use their research to exemplify the evolution of the lines of inquiry and investigation in the discipline over the three identified stages.

As shown, in the early stage, researches mainly focused on the application of agricultural chemicals, pollutants emissions and the degree of concentration in the environment. The measurement of pollution in the environment is the salient line of inquiry in this early stage. For example, a distinguished scholar in research related to the topic of interest is Yi-Fan Li, a scientist in the Atmospheric Quality Institute, Dalian Maritime University and Harbin Institute of Technology in Canada. For decades, he has dedicated his career to study the effects of persistent organic pollutants (POPs) on the ecological environment. In the first stage, articles authored or co-authored by Li focus on the pollution degree of POPs, the usage rate of hexachlorocyclohexane and their impact on the environment [ 30 – 32 ]. Another salient author in the early stage in Dana W. Kolpin, head of the US Geological Survey’s Emerging Contaminants Project, who has dedicated decades to the investigation of how pharmaceuticals and other contaminants move through the environment. In the first stage, his researches mainly focused on assessing the levels of selected pesticides and their metabolites in groundwater or streams in the USA [ 33 – 38 ].

Articles published within the period of the middle stage focused on to the analysis of influence mechanisms, including pollutant generation mechanism, source analysis, transmission channel and source sink relationship. During this stage, Li and colleagues studied the gridded emission inventories of hexachlorocyclohexane and the aspects that stimulate the transport of hexachlorocyclohexane. His research concentrated in exploring the sources and transport mechanism of POPs in the environment [ 39 – 42 ]. Similarly, Kolpin, in the second stage, mainly focused on the environmental occurrence, transport and the ultimate fate of many synthetic organic chemicals after their intended use. He paid special attention to the organic wastewater contaminants in the groundwater and streams in the USA. Specifically, he monitored the concentrations, analyzed the source and transport paths, mined the impact on the environment and put forward relevant control strategies [ 43 – 47 ].

In the late stage, researchers mainly studied the specific types of pollutants (e.g. pharmaceuticals, polycyclic aromatic hydrocarbons (PAHs)), discussed their impacts on the environmental media (e.g. air, soil or water), as well as compared changes under different conditions (e.g. spatial and temporal variations, varying types of crops and agricultural inputs). Publications during this stage normally focused on a specific geographical area (e.g. Dalian in China or Iowa in the USA), or an agricultural production environment (e.g. basins containing livestock farming operations or a high corn and soybean producing region). Articles by Li, in the third stage, mainly researched sources and distributions of Dechlorane plus or PAHs in specific parts of China and their implications for human exposure. His studies further explored the sources, characteristics and potential human health risks of POPs in water, soil and the atmosphere within a certain geographical area [ 48 – 53 ]. Kolpin, in the late stage, primarily investigated the occurrence of chemical contaminants in water plants (e.g. sewage treatment plants) or bodies of water (e.g. wastewater-impacted streams, agricultural basins). In his recent studies, he analyzed the chemicals contaminants’ spatial and temporal variations and exposures to fish (e.g. smallmouth bass), livestock and human health [ 54 – 64 ].

Our findings suggest that the three stages identified (i.e. B1, B2 and B3) for the topic of interest reflect the evolution and sequential advancement of knowledge in the field. The B1 stage mirrors the foundational knowledge research conducted about the presence of pollutants in the environmental media. As observed, the B1 stage informs the B2 phase by providing scientific data and evidence about agricultural chemical inputs and chemical contaminants in the environment. The B3 stage is the current research frontier, which explores the occurrence and potential risks of chemical pollutants in specific contexts. For instance, in the latter stage, publications mainly revolve around the response mechanisms of environmental systems to chemical pollutants and on the potential risk for human health and ecological health induced by chemical pollutants. The transition from the initial stage (B1) to the current research frontier (B3) reflect the gradual progression in research for this topic: assessment of the situation, evaluation of overall impact, and analysis of transdisciplinary and context-specific impact.

3.2 Citation-clustering analysis

Top five highest-frequency articles in the first two clusters and top dive pivot nodes in Cluster A3.

To assess the research focus of environmental impacts induced by agricultural chemical inputs, this paper conducts cluster optimization with the relevant literature review. The results show that researches about this topic primarily consists of three clusters, namely A1 (the upper part in Figure 2 ), A2 (the middle part in Figure 2 ) and A3 (the lower part in Figure 2 ).

Network of high-cited frequency clusters.

Research studies within the A1 cluster largely focus on the effects of pesticides and veterinary drugs on the environment. The A1 cluster can be further divided in two Subclusters A1_1 and A1_2 where the former concentrates in the study of chemical residues in various environmental media after their application and their impact on human health in countries or regions [ 42 , 65 – 67 ], while the latter deals with research on veterinary drug residues in various environmental media as well as the pollutants monitoring techniques and methods (i.e. passive sampling techniques) are studied [ 44 , 70 , 71 , 84 , 85 ]. Particularly, the distinctive light green region on the left side of A1 represents key research on the impact of pesticide exposure on wildlife and human conducted at end of 1990s [ 72 , 73 , 86 ]. It is worth noting that articles in cluster A1 have been frequently cited since year 2000, and may be conceived as the initial stage of research on agricultural chemicals and their impact on the environmental.

Furthermore, the A2 cluster contains publications with emphasis on the effects of chemical fertilizer applications for the environment, especially on farmland. Specifically, the research in the A2 cluster addresses the topic of soil problems due to the improper application of chemical fertilizer. For example, articles within this cluster study the loss of soil elements due to the non-proportional application of chemical fertilizer and soil acidification due to the excessive use of chemical fertilizers [ 52 , 74 , 76 , 77 ]. This cluster also embodies investigations on ways to promote sustainable management practices for cultivated land without compromising the global food demands and security [ 75 , 87 , 88 ].

Finally, the A3 cluster distinctively connects A1–A2, serving as an ‘information bridge’. Research within cluster A3, represented nodes situated in the middle of the network, includes novel methods and technologies for monitoring and controlling the environmental impact of agricultural chemicals inputs [ 79 , 80 , 89 , 90 ]. Specifically, these methods include techniques to determine pollutant sources (e.g. stable isotope analysis), to measure the toxicity of pollutants, and to evaluate the negative effects of pesticides on environment, as well as methods to control the spread of pollutants and to reduce the negative effects of agricultural chemicals [ 79 , 83 ]. As shown in Figure 3 , three areas are circled out in A3, which represent five significant records. For instance, studies within Cluster A3 explore specific techniques to monitor chemical pollutants in the environment and lays the foundation for pollutant measurement, sources and characteristic analysis and environmental impact assessment. Interestingly, research stem from this line of inquiry connects previous research on pesticide contamination and monitoring captured by Clusters A1 and A2 [ 85 , 89 , 91 – 97 ]. Finally, A3 cluster research dealing with techniques to control chemical pollutants in the environment connects previous research on the environmental impact of the application of chemical fertilizer (Cluster A1) and studies on strategic practices for reducing environmental impact of fertilizer pollutants while ensuring food security and promoting the sustainable development of agricultural industry (Cluster A2) [ 87 , 98 – 100 ].

pivot nodes in the knowledge area ‘A3’.

3.3 Co-occurrence network of subject terms analysis

Top five subject terms in seven categories.

The carrier category in Table 2 represents the carrier of chemical pollutants, namely the subject that exerts influence on the environment. The most frequent terms in this category are pesticide and fertilizer. Other high-frequency terms include organochlorine pesticides and nitrogen fertilizer. Our findings reveal that based on the evaluated records, pesticide and fertilizer in agricultural chemicals are the main source of pollutants research in the literature.

The category of environmental object represents objects affected by agricultural chemical inputs. In the context of our study, the most frequent terms (objects) are soil, water and air. Other high-frequency words include groundwater, wastewater, surface water and sewage sludge. Our results indicate that water, soil and air are the most researched environmental media when it comes to pollution derived from pesticides and fertilizers. Specifically, our findings suggest that researchers have focused on monitoring the concentration and diffusion of agricultural chemicals in soil, water and atmosphere. In addition, climate change is a frequent term in this category, with emphasis on the impact mechanism of agricultural chemicals on the atmospheric environment.

The process category include research dealing with the process of agricultural chemicals exerting impacts on the environment. The most frequency terms include pollute, leach, irrigation, runoff and eutrophication. It indicates that studies about the phenomenon of water eutrophication caused by the loss of nitrogen and phosphorus in the process of rainfall or irrigation has been of great concern and merited the attention of researchers.

The cycle category represents the biogeochemical cycle, that is, the transfer process of the chemical elements needed by a living organism between the organism and the environment. Nitrogen and phosphorus have the highest frequency among chemical elements, and it indicates that studies mainly focus on effects of excessively using agricultural chemicals on the process of nitrogen and phosphorus cycles. Meanwhile, the degradation of nitrogen, phosphorus and other chemical pollutants in the environment, especially biodegrade, appear to be another salient topic.

The method category represents research methods and management strategies, including research methods for exploring the environmental impact of agricultural chemical inputs, as well as management strategies for reducing the environmental hazards induced by agricultural chemicals. Model and risk assessment are the top two frequency terms. Other high-frequency terms include bioremediation, integrated pest management, monitor and passive sample. This indicates that assessing the environmental risk and controlling the usage of agricultural chemicals based on various models have deemed relevant and timely issues in the literature. For example, researchers have collected samples based on various means (such as passive air samplers) and used various risk indicators to assess the environmental impact of agricultural chemicals. In addition, studies have extensively explored measures and strategies (e.g. bioremediation and integrated pest management) to reduce and mitigate environmental hazards caused by agricultural chemical inputs.

The agricultural object category includes the high-frequency words, such as wheat, fish, maize, rice, plant and crop. Overall, this category reflects the major research emphasis on the crops and fisheries. Interestingly, the word ‘China’ is also the key word in this category, indicating that with high consumption and low efficiency of agricultural chemicals inputs, China has become one of the main researched geographical region in terms of environmental problems.

Indicator category includes the different factors used when assessing the environmental impact induced by agricultural chemicals. The most frequent terms include heavy metal, nitrate, POP, organophosphate, pesticide residue and endocrine disruptor. Our results indicate that chemical pollutants including metal nitrate, pesticide and residue heavy have been widely investigated as major determinants of pollution. Importantly, we find that the extant literature has predominantly examined the effect and risk of pollutants for bodies of water, soil organism, air, fishes, bees and human health.

Finally, to better understand the key nodes and their relationships among the categories, we conduct a visualized analysis in the Gephi platform based on the co-occurrence relationship, PageRank value and the seven identified categories (see Figure 4 ). Based on the PageRank value, we identified the top three categories. ‘Carrier’, ‘agricultural object’ and ‘indicator’ are the top three categories, which indicate that scholars have largely paid attention to analyze the transport process of chemical pollutants and assessing their impact on the environment, especially under agricultural production scenarios. The difference in thickness for the graphed lines denote the strength of links or connections. As shown in Figure 4 , agriculture and environment, pollute and environment, pesticide and environment, and nitrate and leach have a strong semantic relation.

Co-occurrence network of filtered subject terms.

3.4 Academic cooperation and knowledge sharing among countries and institutions

The mutually beneficial cooperation among different research institutes and countries plays a key role in promoting the development of science and technology. Citation number analysis and co-authorship analysis are important methods for evaluating the cooperation and research level of different institutes and countries. In the present paper, we first summarize the global development trends based on citation statistics of different countries. Then, we employ co-authorship metrics to analyze the scientific knowledge communication and organization distribution in the collaboration network. Ultimately, we present an overall knowledge-sharing network among different countries and institutions.

From a time sequence perspective, the relevant and selected 16 459 articles on ‘the environmental impact of agricultural chemical inputs’ demonstrate an exponential growth (see Figure 5 ). This indicates that based on direction, the current research is in the middle and preliminary stage of a rapid forecasted development, and the volume of scientific knowledge is expected to grow dramatically with optimistic future predictions. Our findings suggest that prior to 2006, Asian and South American countries, such as China, India and Brazil, lagged far behind in terms of technological advancement when compared to developed countries such as the USA, Canada, Australia and some European countries (e.g. UK, France, Germany and Holland), the same trend is observed for the number of publication amounts generated and growth rates. In recent years, the gap has narrowed down significantly, which can be attributed to the strengthening and investment in science and technology (especially the advancement of environmental science and ecological science) in Asian and South American countries. It is noticeable that, in China, the number of articles grew significantly from 54 to 267 during 2006–15 period. Then in 2015, the number of publications (267 articles) produced by China surpassed the number of publications generated in USA (239 articles). Interestingly, the citation growth rate has gradually decreased in developed countries, such as the UK and Holland, but has steadily increased in developing countries, such as India and Brazil. This result reveal the cooperation among countries in the newly advanced economic development (i.e. Brazil, Russia, India, China and South Africa) in order to advance and promote the technology and innovation in the agricultural sector.

Rapid increase of scientific papers on the world-wide scale.

Moreover, results from co-authorship network analysis suggest that institutions and organizations based in North America, East Asia and Europe are the major research contributors; this trend is visualized via Google Earth View (see part A of Figure 6 ). Each area has established close cooperation relations. Leading countries, such as the USA and Canada in North America, and France and Germany in Europe have dominating effects upon scientific development and collaboration. Data statistics and visualization can help to discover rules and distributions of academic collaborations within this topic. As shown in part B of Figure 6 , the co-author communities are identified in the large linked network. Greater density indexes are marked by deeper colors in the thermodynamic diagram. Some hubs are most prominent, such as the Chinese Academy of Sciences ‘Chinese AcadSci,’ the Public Scientific and Technical Research Establishment in France ‘CNRS,’ the United States Department of Agriculture—Agricultural Research Service ‘USDA ARS,’ the Canadian Natural Resources ‘Nat Resource Canada,’ and the University of Paris Diderot, Paris 7 ‘University Paris 07.’ Darker color vertices have relatively higher diameter and can be observed as a side-by side comparison demonstrated in above four-part visualized images. As seen, CNRS ranks first with 17 units and is followed by Chinese Academy of Sciences with 15 units.

Visualization of Academic collaboration network.

Detailed information of scientific research organizations-based co-authorship weights.

Using informetrics theory-based methods (i.e. document co-citation analysis, document clustering and co-words analysis via co-occurrence network of subject terms), this study distinguishes and further explores research frontiers, research hotspots and high-frequency terms using aggregated and multiple-source literature records related to the topic of ‘effects of agricultural chemical inputs on the environment.’

From a macro-level view, citation network analysis shows that the impact of agricultural chemicals on the environment can be divided into three periods. In the early stage (1990–99), studies mainly focus on the application of agricultural chemicals, pollutant emissions and their concentration in various environmental media. During the middle stage (2000–07), studies mainly focus on the production mechanism, source apportionment, transmission channel and source/sink relationship of pollutants. In the late stage (2008–16), studies mainly focus on discussing the influence of specific pollutants on various environmental medias and comparing the changes under different conditions.

Citation-clustering analysis, a meso-level method, shows that the main research directions include the effects of pesticides and veterinary drugs on the environment (A1), the influence of fertilizer application on environmental and food safety (A2), and the technologies and strategies for monitoring and controlling the impact of agricultural chemicals on environment (A3). The A3 cluster contains special pivot nodes in the knowledge network, connecting A1 and A2, providing research in A1 and A2 with technical supports for revealing the impacts.

From a micro-level perspective, results from co-occurrence network of subject terms analysis, show that pesticides and chemical fertilizer are the main types of agricultural chemicals. As for pollutant types, POPs, heavy metals, nitrates and pesticide residue in environmental media appear to be of major interest and concern. Moreover, agricultural chemical inputs and their environmental impact derived from the production of wheat, maize and rice seem to be main focal point. For environmental objects impacted by agricultural chemicals, particular attention in the literature has been paid to soil, air and water, studying the potential risks of environmental pollution to fishes, bees and human health. Major concern is given to the process of environmental pollution caused by agricultural chemicals. For example, the impact process of excessively using agricultural chemicals on nitrogen and phosphorus cycles, as well as water eutrophication and other problems caused by this process, has raised widespread concern. Close attention has been paid to methods to control these negative effects. For example, these is research about methods to biodegrade nitrogen, phosphorus and other chemical pollutants in environmental media, to achieve the sustainable development of agriculture.

Citation analysis suggests that the volume of scientific knowledge and contributions, as measured by number of publications related to the topic, has grown dramatically with an optimistic future forecast. The gap of publication numbers between developing and developed countries is gradually narrowing down. The co-authorship analysis shows that authors based in North America (USA and Canada), East Asian (China, South Korea and Japan) and Europe (France and Germany) are the major research contributors for the topic of interest. National academic research organizations (e.g. Chinese Academy of Sciences), equipped with comprehensive and interdisciplinary expertise and social influence, have adopted leading research roles as compared to universities and other educational research institutes. In particular, the Chinese Academy of Sciences (China), National Institute of Agricultural Research (France), French National Center for Scientific Research (France), US Department of Agri/culture (the USA) and Cornell University (the USA) constitute the main hubs for research concerning the impact of agricultural chemicals on the environmental media.

Though the results of this study provide a useful summary of last three decades of research conducted in the topic of the effects of agricultural inputs on the environment, this research is not exempt from limitations. For example, the salient agricultural inputs used for the analysis (i.e. pesticides and fertilizers) have distinctive uses in agricultural activities and their effects on the environment may greatly vary by input. In addition, pesticides can further be divided based on their function (e.g. fumigants, insecticides, biopesticides, herbicides, etc.) and the impact of these on the environment may differ. The same is true for agricultural fertilizers which are often classified based on their efficiency, origin and phase. Finally, future literature review research may benefit from a narrower focus for targeting records that concern a single environmental media.

This work was supported by the Natural Sciences Foundation of China (41501213 and 71333006); the Fundamental Research Funds for Central Universities (2662017PY045); the Key Project for Studies of Philosophy and Social Sciences by Ministry of Education (15JZD014); the Major Program of National Social Science Foundation of China (15ZDC038); the project of philosophy and social sciences of Guangdong Province (GDXK201721); the project of Guangdong Institute for International Strategies (17ZDA19) and the University of Florida International Center’s Global Fellowship Award.

The authors declare no conflict of interest.

Udeigwe TK , Teboh JM , Eze PN , et al.  . Implications of leading crop production practices on environmental quality and human health . J Environ Manage 2015 ; 151 : 267 – 79 .

Google Scholar

Alvarez A , Saez JM , Costa JSD , et al.  . Actinobacteria: current research and perspectives for bioremediation of pesticides and heavy metals . Chemosphere 2017 ; 166 : 41 – 62 .

Ridolfi AS , Alvarez GB , Rodríguez Giraul ME . Organochlorinated contaminants in general population of Argentina and other Latin American Countries. In Alvarez A , Polti M (eds) . Bioremediation in Latin America. Current Research and Perspectives . Springer , 2014 : 17 – 40 .

Google Preview

Gilliom RJ . Pesticides in U.S. streams and groundwater . Environ Sci Technol 2007 ; 41 : 3408 – 14 .

Kawahara J , Horikoshi R , Yamaguchi T , et al.  . Air pollution and young children’s inhalation exposure to organophosphorus pesticide in an agricultural community in Japan . Environ Int 2005 ; 31 : 1123 – 32 .

Tunstall-Pedoe H , Woodward M , Tavendale R , et al.  . Pesticide pollution remains severe after cleanup of a stockpile of obsolete pesticides at Vikuge, Tanzania . Ambio A J Hum Environ 2004 ; 33 : 503 – 8 .

Tirado R , Englande AJ , Promakasikorn L , et al.  . Use of agrochemicals in Thailand and its consequences for the environment. Green Piece Research Laboratories Technical Note . 2008 http://www.greenpeace.to/publications/GPSEA_agrochemical-use-in-thailand.pdf .

National Bureau of Statistics of P. R. China . China statistical yearbook 2013 . China Statistics Press , 2014 .

Ministry of Agriculture of P. R. China . Trends of Agricultural Science and Education: Key Period Report about Controlling Agricultural Non - point Source Pollution . Ministry of Agriculture of P. R. China , 2016 . http://www.moa.gov.cn/ztzl/mywrfz/jbxx/201604/t20160419_5098842.htm .

He CC . Food security-Century Challenge and Response . Social Science Academic Press , 2013 .

Rother HA . South African farm workers’ interpretation of risk assessment data expressed as pictograms on pesticide labels . Environ Res 2008 ; 108 : 419 – 27 .

Carey AE , Kutz FW . Trends in ambient concentrations of agrochemicals in humans and the environment of the United States . Environ Monit Assess 1985 ; 5 : 155 – 63 .

Gong P , Liang L , Zhang Q . China must reduce fertilizer use too . Nature 2011 ; 473 : 284 – 5 .

Ciavatta C , Manoli C , Cavani L , et al.  . Chromium-containing organic fertilizers from tanned hides and skins: a review on chemical, environmental, agronomical and legislative aspects . J Environ Prot 2012 ; 03 : 1532 – 41 .

Ministry of Agriculture of P. R. China . Notice of the Ministry of Agriculture on Printing and Distributing the Action Plan for Zero-growth of Chemical Fertilizer Use to 2020 and the Action Plan for Zero-growth of Pesticide Use to 2020 . Ministry of Agriculture , 2015 . http://www.moa.gov.cn/zwllm/tzgg/tz/201503/t20150318_4444765.htm .

Carpenter SR , Caraco NF , Correll DL , et al.  . Nonpoint pollution of surface waters with phosphorus and nitrogen . Ecol Appl 1998 ; 8 : 559 – 68 .

Rivera XCS , Bacenetti J , Fusi A , et al.  . The influence of fertiliser and pesticide emissions model on life cycle assessment of agricultural products: the case of Danish and Italian barley . Sci Total Environ 2017 ; 592 : 745 – 57 .

Relyea RA . The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities . Ecol Appl 2005 ; 15 : 618 – 27 .

Ikoyi I , Fowler A , Schmalenberger A . One-time phosphate fertilizer application to grassland columns modifies the soil microbiota and limits its role in ecosystem services . Sci Total Environ 2018 ; 630 : 849 – 58 .

Pimentel D , Acquay H , Biltonen M , et al.  . Environmental and economic costs of pesticide use . Bioscience 1992 ; 42 : 750 – 60 .

van der Werf HMG . Assessing the impact of pesticides on the environment . Agric Ecosyst Environ 1997 ; 60 : 81 – 96 .

Machado CS , Fregonesi BM , Alves RI , et al.  . Health risks of environmental exposure to metals and herbicides in the Pardo River, Brazil . Environ Sci Pollut Res 2017 ; 24 : 20160 – 72 .

Zhu ZL , Chen DL . Nitrogen fertilizer use in China—contributions to food production, impacts on the environment and best management strategies . Nutr Cycling Agroecosystems 2002 ; 63 : 117 – 27 .

Tscharntke T , Clough Y , Wanger TC , et al.  . Global food security, biodiversity conservation and the future of agricultural intensification . Biol Conserv 2012 ; 151 : 53 – 9 .

Wauchope RD . The pesticide content of surface water draining from agricultural fields—a review . J Environ Qual 1978 ; 7 : 459 – 72 .

Coulter BS , Murphy WE , Culleton N , et al.  . A survey of fertilizer use in 2000 for grassland and arable crops . Soc Sci Electron Publishing 2005 ; 35 : 135 – 6 .

Marcia JB , Mary NM . Encyclopedia of Library and Information Sciences, Third Edition (Print Version) . CRC Press , 2009 : 2570 – 85 .

Huang Y , Schuehle J , Porter AL , et al.  . A systematic method to create search strategies for emerging technologies based on the web of science: illustrated for ‘big data’ . Scientometrics 2015 ; 105 : 2005 – 22 .

Famili A , Shen WM , Weber R , et al.  . Data preprocessing and intelligent data analysis . Intell Data Anal 1997 ; 1 : 3 – 23 .

Li YF , McMillan A , Scholtz MT . Global HCH usage with 1×1 longitude/latitude resolution . Environ Sci Technol 1996 ; 30 : 3525 – 33 .

Li YF , Cai DJ , Singh A . Technical hexachlorocyclohexane use trends in China and their impact on the environment . Arch Environ Contam Toxicol 1998 ; 35 : 688 – 97 .

Li YF . Global technical hexachlorocyclohexane usage and its contamination consequences in the environment: from 1948 to 1997 . Sci Total Environ 1999 ; 232 : 121 – 58 .

Kolpin DW , Kalkhoff SJ . Atrazine degradation in a small stream in Iowa . Environ Sci Technol 1993 ; 27 : 134 – 9 .

Kolpin DW , Thurman EM , Goolsby DA . Occurrence of selected pesticides and their metabolites in near-surface aquifers of the Midwestern United States . Environ Sci Technol 1995 ; 30 : 335 – 40 .

Kolpin DW , Goolsby DA , Thurman EM . Pesticides in near-surface aquifers: an assessment using highly sensitive analytical methods and tritium . J Environ Qual 1995 ; 24 : 1125 – 32 .

Kolpin DW , Sneck-Fahrer D , Hallberg GR , et al.  . Temporal trends of selected agricultural chemicals in lowa’s groundwater, 1982–1995: are things getting better? J Environ Qual 1997 ; 26 : 1007 – 17 .

Kolpin DW . Agricultural chemicals in groundwater of the midwestern United States: relations to land use . J Environ Qual 1997 ; 26 : 1025 – 37 .

Kolpin DW , Barbash JE , Gilliom RJ . Occurrence of pesticides in shallow groundwater of the United States: initial results from the National Water-Quality Assessment Program . Environ Sci Technol 1998 ; 32 : 558 – 66 .

Li YF , Scholtz MT , Heyst BV . Global gridded emission inventories of beta-hexachlorocyclohexane . J Geophys Res Atmos 2000 ; 105 : 6621 – 32 .

Li YF , Cai DJ , Shan ZJ , et al.  . Gridded usage inventories of technical hexachlorocyclohexane and lindane for China with 1/6 latitude by 1/4 longitude resolution . Arch Environ Contam Toxicol 2001 ; 41 : 261 – 6 .

Li YF , Macdonald RW , Jantunen LMM , et al.  . The transport of β-hexachlorocyclohexane to the western Arctic Ocean: a contrast to α-HCH . Sci Total Environ 2002 ; 291 : 229 – 46 .

Li YF , Macdonald RW . Sources and pathways of selected organochlorine pesticides to the Arctic and the effect of pathway divergence on HCH trends in biota: a review . Sci Total Environ 2005 ; 342 : 87 – 106 .

Kolpin DW , Thurman EM , Linhart SM . Occurrence of cyanazine compounds in groundwater: degradates more prevalent than the parent compound . Environ Sci Technol 2001 ; 35 : 1217 – 22 .

Kolpin DW , Furlong ET , Meyer MT , et al.  . Pharmaceuticals, hormones, and other organic wastewater contaminants in US streams, 1999–2000: a national reconnaissance . Environ Sci Technol 2002 ; 36 : 1202 – 11 .

Kolpin DW , Skopec M , Meyer MT , et al.  . Urban contribution of pharmaceuticals and other organic wastewater contaminants to streams during differing flow conditions . Scie Total Environ 2004 ; 328 : 119 – 30 .

Glassmeyer ST , Furlong ET , Kolpin DW , et al.  . Transport of chemical and microbial compounds from known wastewater discharges: potential for use as indicators of human fecal contamination . Environ Sci Technol 2005 ; 39 : 5157 – 69 .

Kolpin DW , Thurman EM , Lee EA , et al.  . Urban contributions of glyphosate and its degradate AMPA to streams in the United States . Sci Total Environ 2006 ; 354 : 191 – 7 .

Li YF , Harner T , Liu L , et al.  . Polychlorinated biphenyls in global air and surface soil: distributions, air−soil exchange, and fractionation effect . Environ Sci Technol 2009 ; 44 : 2784 – 90 .

Wang DG , Yang M , Qi H , et al.  . An Asia-specific source of dechlorane plus: concentration, isomer profiles, and other related compounds . Environ Sci Technol 2010 ; 44 : 6608 – 13 .

Ma WL , Li YF , Qi H , et al.  . Seasonal variations of sources of polycyclic aromatic hydrocarbons (PAHs) to a northeastern urban city, China . Chemosphere 2010 ; 79 : 441 – 7 .

Sverko E , Tomy GT , Reiner EJ , et al.  . Dechlorane plus and related compounds in the environment: a review . Environ Sci Technol 2011 ; 45 : 5088 – 98 .

Guo JH , Liu XJ , Zhang Y , et al.  . Significant acidification in major Chinese croplands . Science 2010 ; 327 : 1008 – 10 .

Qi H , Li WL , Zhu NZ , et al.  . Concentrations and sources of polycyclic aromatic hydrocarbons in indoor dust in China . Sci Total Environ 2014 ; 491 : 100 – 7 .

Kinney CA , Furlong ET , Kolpin DW , et al.  . Bioaccumulation of pharmaceuticals and other anthropogenic waste indicators in earthworms from agricultural soil amended with biosolid or swine manure . Environ Sci Technol 2008 ; 42 : 1863 – 70 .

Barnes KK , Kolpin DW , Furlong ET , et al.  . National reconnaissance of pharmaceuticals and other organic wastewater contaminants in the United States—(I) Groundwater . Sci Total Environ 2008 ; 402 : 192 – 200 .

Focazio MJ , Kolpin DW , Barnes KK , et al.  . A national reconnaissance for pharmaceuticals and other organic wastewater contaminants in the United States—(II) untreated drinking water sources . Sci Total Environ 2008 ; 402 : 201 – 16 .

Watkinson AJ , Murby EJ , Kolpin DW , et al.  . The occurrence of antibiotics in an urban watershed: from wastewater to drinking water . Sci Total Environ 2009 ; 407 : 2711 – 23 .

Schultz MM , Furlong ET , Kolpin DW , et al.  . Antidepressant pharmaceuticals in two US effluent-impacted streams: occurrence and fate in water and sediment, and selective uptake in fish neural tissue . Environ Sci Technol 2010 ; 44 : 1918 – 25 .

Phillips PJ , Smith SG , Kolpin DW , et al.  . Pharmaceutical formulation facilities as sources of opioids and other pharmaceuticals to wastewater treatment plant effluents . Environ Sci Technol 2010 ; 44 : 4910 – 6 .

Kolpin DW , Blazer VS , Gray JL , et al.  . Chemical contaminants in water and sediment near fish nesting sites in the Potomac River basin: determining potential exposures to smallmouth bass ( Micropterus dolomieu ) . Sci Total Environ 2013 ; 443 : 700 – 16 .

Barber LB , Keefe SH , Brown GK , et al.  . Persistence and potential effects of complex organic contaminant mixtures in wastewater-impacted streams . Environ Sci Technol 2013 ; 47 : 2177 – 88 .

Hladik ML , Kolpin DW , Kuivila KM . Widespread occurrence of neonicotinoid insecticides in streams in a high corn and soybean producing region, USA . Environ Pollut 2014 ; 193 : 189 – 96 .

King DN , Donohue MJ , Vesper SJ , et al.  . Microbial pathogens in source and treated waters from drinking water treatment plants in the United States and implications for human health . Sci Total Environ 2016 ; 562 : 987 – 95 .

Givens CE , Kolpin DW , Borchardt MA , et al.  . Detection of hepatitis E virus and other livestock-related pathogens in Iowa streams . Sci Total Environ 2016 ; 566 : 1042 – 51 .

Weber J , Halsall CJ , Muir D , et al.  . Endosulfan, a global pesticide: a review of its fate in the environment and occurrence in the Arctic . Sci Total Environ 2010 ; 408 : 2966 – 84 .

Qiu X , Zhu T , Yao B , et al.  . Contribution of dicofol to the current DDT pollution in China . Environ Sci Technol 2005 ; 39 : 4385 – 90 .

Jaward FM , Farrar NJ , Harner T , et al.  . Passive air sampling of PCBs, PBDEs, and organochlorine pesticides across Europe . Environ Sci Technol 2004 ; 38 : 34 – 41 .

Hites RA . Polybrominated diphenyl ethers in the environment and in people: a meta-analysis of concentrations . Environ Sci Technol 2004 ; 38 : 945 – 56 .

Qiu X , Zhu T , Li J , et al.  . Organochlorine pesticides in the air around the Taihu Lake, China . Environ Sci Technol 2004 ; 38 : 1368 – 74 .

Daughton CG , Ternes TA . Pharmaceuticals and personal care products in the environment: agents of subtle change? Environ Health Perspect 1999 ; 107 : 907 .

Mazzella N , Dubernet JF , Delmas F . Determination of kinetic and equilibrium regimes in the operation of polar organic chemical integrative samplers: application to the passive sampling of the polar herbicides in aquatic environments . J Chromatogr A 2007 ; 1154 : 42 – 51 .

Colborn T , vomSaal FS , Soto AM . Developmental effects of endocrine-disrupting chemicals in wildlife and humans . Environ Health Perspect 1993 ; 101 : 378 .

Halling-Sørensen B , Nielsen SN , Lanzky PF , et al.  . Occurrence, fate and effects of pharmaceutical substances in the environment—a review . Chemosphere 1998 ; 36 : 357 – 93 .

Ju XT , Xing GX , Chen XP , et al.  . Reducing environmental risk by improving N management in intensive Chinese agricultural systems . Proc Natl Acad Sci 2009 ; 106 : 3041 – 6 .

Cordell D , Drangert JO , White S . The story of phosphorus: global food security and food for thought . Glob Environ Change 2009 ; 19 : 292 – 305 .

Galloway JN , Townsend AR , Erisman JW , et al.  . Transformation of the nitrogen cycle: recent trends, questions, and potential solutions . Science 2008 ; 320 : 889 – 92 .

Vitousek PM , Naylor R , Crews T , et al.  . Nutrient imbalances in agricultural development . Science 2009 ; 324 : 1519 – 20 .

Godfray HCJ , Beddington JR , Crute IR , et al.  . Food security: the challenge of feeding 9 billion people . Science 2010 ; 327 : 812 – 8 .

Damalas CA , Eleftherohorinos IG . Pesticide exposure, safety issues, and risk assessment indicators . Int J Environ Res Public Health 2011 ; 8 : 1402 – 19 .

Henry M , Beguin M , Requier F , et al.  . A common pesticide decreases foraging success and survival in honey bees . Science 2012 ; 336 : 348 – 50 .

Desneux N , Decourtye A , Delpuech JM . The sublethal effects of pesticides on beneficial arthropods . Annu Rev Entomol 2007 ; 52 : 81 – 106 .

Mullin CA , Frazier M , Frazier JL , et al.  . High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health . PLoS One 2010 ; 5 : e9754 .

R Development Core Team . R: A language and environment for statistical computing . R Foundation for Statistical Computing , 2011 . http://www.r-project.org .

Heberer T . Occurrence, fate, and removal of pharmaceutical residues in the aquatic environment: a review of recent research data . Toxicol Lett 2002 ; 131 : 5 – 17 .

Alvarez DA , Petty JD , Huckins JN , et al.  . Development of a passive, in situ , integrative sampler for hydrophilic organic contaminants in aquatic environments . Environ Toxicol Chem 2004 ; 23 : 1640 – 8 .

Kelce WR , Stone CR , Laws SC , et al.  . Persistent DDT metabolite p,p′-DDE is a potent androgen receptor antagonist . Nature 1995 ; 375 : 581 – 5 .

Tilman D , Balzer C , Hill J , et al.  . Global food demand and the sustainable intensification of agriculture . Proc Natl Acad Sci USA 2011 ; 108 : 20260 – 64 .

Foley JA , Ramankutty N , Brauman KA , et al.  . Solutions for a cultivated planet . Nature 2011 ; 478 : 337 – 42 .

Schwarzenbach RP , Escher BI , Fenner K , et al.  . The challenge of micropollutants in aquatic systems . Science 2006 ; 313 : 1072 – 7 .

Parnell AC , Inger R , Bearhop S , et al.  . Source partitioning using stable isotopes: coping with too much variation . PLoS One 2010 ; 5 : e9672 .

Stuer-Lauridsen F . Review of passive accumulation devices for monitoring organic micropollutants in the aquatic environment . Environ Pollut 2005 ; 136 : 503 – 24 .

MacLeod SL , McClure EL , Wong CS . Laboratory calibration and field deployment of the polar organic chemical integrative sampler for pharmaceuticals and personal care products in wastewater and surface water . Environ Toxicol Chem 2007 ; 26 : 2517 – 29 .

Alvarez DA , Huckins JN , Petty JD , et al.  . Chapter 8 tool for monitoring hydrophilic contaminants in water: polar organic chemical integrative sampler (POCIS) ☆ . Compr Anal Chem 2007 ; 48 : 171 – 97 .

Loos R , Gawlik BM , Locoro G , et al.  . EU-wide survey of polar organic persistent pollutants in European river waters . Environ Pollut 2009 ; 157 : 561 – 8 .

Loos R , Locoro G , Comero S , et al.  . Pan-European survey on the occurrence of selected polar organic persistent pollutants in ground water . Water Res 2010 ; 44 : 4115 – 26 .

Mazzella N , Lissalde S , Moreira S , et al.  . Evaluation of the use of performance reference compounds in an Oasis-HLB adsorbent based passive sampler for improving water concentration estimates of polar herbicides in freshwater . Environ Sci Technol 2010 ; 44 : 1713 – 9 .

Lissalde S , Mazzella N , Fauvelle V , et al.  . Liquid chromatography coupled with tandem mass spectrometry method for thirty-three pesticides in natural water and comparison of performance between classical solid phase extraction and passive sampling approaches . J Chromatogr A 2011 ; 1218 : 1492 – 1502 .

Tilman D , Cassman KG , Matson PA , et al.  . Agricultural sustainability and intensive production practices . Nature 2002 ; 418 : 671 – 7 .

Erisman JW , Sutton MA , Galloway J , et al.  . How a century of ammonia synthesis changed the world . Nat Geosci 2008 ; 1 : 636 – 9 .

Robertson GP , Vitousek PM . Nitrogen in agriculture: balancing the cost of an essential resource . Annu Rev Environ Resour 2009 ; 34 : 97 – 125 .

Luo W , Lu Y , Giesy JP , et al.  . Effects of land use on concentrations of metals in surface soils and ecological risk around Guanting Reservoir, China . Environ Geochem Health 2007 ; 29 : 459 – 71 .

Yu HY , Zhang BZ , Giesy JP , et al.  . Persistent halogenated compounds in aquaculture environments of South China: implications for global consumers’ health risk via fish consumption . Environ Int 2011 ; 37 : 1190 – 5 .

Wang T , Khim JS , Chen C , et al.  . Perfluorinated compounds in surface waters from Northern China: comparison to level of industrialization . Environ Int 2012 ; 42 : 37 – 46 .

Liu Q , Guo Y , Giesy JP . Spatio-temporal effects of fertilization in Anhui province, China . Environ Dev Sustainabil 2015 ; 17 : 1197 – 1207 .

Jin X , Liu F , Wang Y , et al.  . Probabilistic ecological risk assessment of copper in Chinese offshore marine environments from 2005 to 2012 . Mar Pollut Bull 2015 ; 94 : 96 – 102 .

Swaney DP , Hong B , Ti C , et al.  . Net anthropogenic nitrogen inputs to watersheds and riverine N export to coastal waters: a brief overview . Curr Opin Environ Sustainabil 2012 ; 4 : 203 – 11 .

Fleming M , Tai Y , Zhuang P , et al.  . Extractability and bioavailability of Pb and As in historically contaminated orchard soil: effects of compost amendments . Environ Pollut 2013 ; 177 : 90 – 7 .

Dietrich KN , Eskenazi B , Schantz S , et al.  . Principles and practices of neurodevelopmental assessment in children: lessons learned from the centers for children’s environmental health and disease prevention research . Environ Health Perspect 2005 ; 113 : 1437 – 46 .

Stevem R , Peterm G , Jenniferc J , et al.  . Accumulation of carbon and nitrogen in residential soils with different land-use histories . Ecosystems 2011 ; 14 : 287 – 97 .

Ma L , Ma WQ , Velthof GL , et al.  . Modeling nutrient flows in the food chain of China . J Environ Qual 2010 ; 39 : 1279 – 89 .

Gao B , Ju X , Su F , et al.  . Nitrous oxide and methane emissions from optimized and alternative cereal cropping systems on the North china plain: a two-year field study . Sci Total Environ 2014 ; 472 : 112 – 24 .

Li G , Ittersum MKV , Leffelaar PA , et al.  . A multi-level analysis of China’s phosphorus flows to identify options for improved management in agriculture . Agric Syst 2016 ; 144 : 87 – 100 .

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Fertilizer use, soil health and agricultural sustainability.

Conflicts of Interest

• Amanullah, A.; Iqbal, A.; Ali, S.; Fahad, S.; Parmar, B. Nitrogen source and rate management improve maize productivity of smallholders under semiarid climates. Front. Plant Sci. 2016 , 7 , 1773. [ Google Scholar ] [ CrossRef ] [ PubMed ] [ Green Version ]
• Wang, Z.; Hassan, M.U.; Nadeem, F.; Wu, L.; Zhang, F.; Li, X. Magnesium Fertilization Improves Crop Yield in Most Production Systems: A Meta-Analysis. Front. Plant Sci. 2020 , 10 , 1727. [ Google Scholar ] [ CrossRef ] [ PubMed ] [ Green Version ]
• Liu, Q.; Xu, H.; Yi, H. Impact of Fertilizer on Crop Yield and C:N:P Stoichiometry in Arid and Semi-Arid Soil. Int. J. Environ. Res. Public Health 2021 , 18 , 4341. [ Google Scholar ] [ CrossRef ] [ PubMed ]
• Stewart, R.E. Fertilizer. Encyclopedia Britannica. Available online: https://www.britannica.com/topic/fertilizer (accessed on 18 March 2022).
• Understanding Fertilizer and Its Essential Role in High Yielding Crops. Available online: https://www.cropnutrition.com/resource-library/understanding-fertilizer-and-its-essential-role-in-high-yielding-crops (accessed on 18 March 2022).
• Yousaf, M.; Li, J.; Lu, J.; Ren, T.; Cong, R.; Fahad, S.; Li, X. Effects of fertilization on crop production and nutrient-supplying capacity under rice-oilseed rape rotation system. Sci. Rep. 2017 , 7 , 1270. [ Google Scholar ] [ CrossRef ] [ PubMed ]
• Pahalvi, H.N.; Rafiya, L.; Rashid, S.; Nisar, B.; Kamili, A.N. Chemical Fertilizers and Their Impact on Soil Health. In Microbiota and Biofertilizers ; Dar, G.H., Bhat, R.A., Mehmood, M.A., Hakeem, K.R., Eds.; Springer: Cham, Switzerland, 2021; Volume 2, pp. 1–20. [ Google Scholar ] [ CrossRef ]
• Ozlu, E.; Kumar, S. Response of Soil Organic Carbon, pH, Electrical Conductivity, and Water Stable Aggregates to Long-Term Annual Manure and Inorganic Fertilizer. Soil Sci. Soc. Am. J. 2018 , 82 , 1243. [ Google Scholar ] [ CrossRef ]
• Ning, J.; Arai, Y.; Shen, J.; Wang, R.; Ai, S. Effects of Phosphorus on Nitrification Process in a Fertile Soil Amended with Urea. Agriculture 2021 , 11 , 523. [ Google Scholar ] [ CrossRef ]
• Pan, X.; Lv, J.; Dyck, M.; He, H. Bibliometric Analysis of Soil Nutrient Research between 1992 and 2020. Agriculture 2021 , 11 , 223. [ Google Scholar ] [ CrossRef ]
• Skorupka, M.; Nosalewicz, A. Ammonia Volatilization from Fertilizer Urea—A New Challenge for Agriculture and Industry in View of Growing Global Demand for Food and Energy Crops. Agriculture 2021 , 11 , 822. [ Google Scholar ] [ CrossRef ]
• Wan, L.-J.; Tian, Y.; He, M.; Zheng, Y.-Q.; Lyu, Q.; Xie, R.-J.; Ma, Y.-Y.; Deng, L.; Yi, S.-L. Effects of Chemical Fertilizer Combined with Organic Fertilizer Application on Soil Properties, Citrus Growth Physiology, and Yield. Agriculture 2021 , 11 , 1207. [ Google Scholar ] [ CrossRef ]
• Feder, F. Effects of Fertilisation Using Organic Waste Products with Mineral Complementation on Sugarcane Yields and Soil Properties in a 4 Year Field Experiment. Agriculture 2021 , 11 , 985. [ Google Scholar ] [ CrossRef ]
• Gao, Y.-H.; Lu, X.-H.; Guo, R.-J.; Hao, J.-J.; Miao, Z.-Q.; Yang, L.; Li, S.-D. Responses of Soil Abiotic Properties and Microbial Community Structure to 25-Year Cucumber Monoculture in Commercial Greenhouses. Agriculture 2021 , 11 , 341. [ Google Scholar ] [ CrossRef ]
• Li, X.; Su, Y.; Ahmed, T.; Ren, H.; Javed, M.R.; Yao, Y.; An, Q.; Yan, J.; Li, B. Effects of Different Organic Fertilizers on Improving Soil from Newly Reclaimed Land to Crop Soil. Agriculture 2021 , 11 , 560. [ Google Scholar ] [ CrossRef ]
• Luo, H.; Robles-Aguilar, A.A.; Sigurnjak, I.; Michels, E.; Meers, E. Assessing Nitrogen Availability in Biobased Fertilizers: Effect of Vegetation on Mineralization Patterns. Agriculture 2021 , 11 , 870. [ Google Scholar ] [ CrossRef ]
• Orden, L.; Ferreiro, N.; Satti, P.; Navas-Gracia, L.M.; Chico-Santamarta, L.; Rodríguez, R.A. Effects of Onion Residue, Bovine Manure Compost and Compost Tea on Soils and on the Agroecological Production of Onions. Agriculture 2021 , 11 , 962. [ Google Scholar ] [ CrossRef ]
• Oueriemmi, H.; Kidd, P.S.; Trasar-Cepeda, C.; Rodríguez-Garrido, B.; Zoghlami, R.I.; Ardhaoui, K.; Prieto-Fernández, Á.; Moussa, M. Evaluation of Composted Organic Wastes and Farmyard Manure for Improving Fertility of Poor Sandy Soils in Arid Regions. Agriculture 2021 , 11 , 415. [ Google Scholar ] [ CrossRef ]
• Zenda, T.; Liu, S.; Dong, A.; Duan, H. Revisiting Sulphur—The Once Neglected Nutrient: It’s Roles in Plant Growth, Metabolism, Stress Tolerance and Crop Production. Agriculture 2021 , 11 , 626. [ Google Scholar ] [ CrossRef ]
• Ivanova, A.; Denisova, E.; Musinguzi, P.; Opolot, E.; Tumuhairwe, J.B.; Pozdnyakov, L.; Manucharova, N.; Ilichev, I.; Stepanov, A.; Krasilnikov, P. Biological Indicators of Soil Condition on the Kabanyolo Experimental Field, Uganda. Agriculture 2021 , 11 , 1228. [ Google Scholar ] [ CrossRef ]
• Wang, R.; Zou, R.; Liu, J.; Liu, L.; Hu, Y. Spatial Distribution of Soil Nutrients in Farmland in a Hilly Region of the Pearl River Delta in China Based on Geostatistics and the Inverse Distance Weighting Method. Agriculture 2021 , 11 , 50. [ Google Scholar ] [ CrossRef ]
• Amanullah; Fahad, S. Integrated Nutrient Management in Corn Production: Symbiosis for Food Security and Grower’s Income in Arid and Semiarid Climates. In Corn—Production and Human Health in Changing Climate ; Amanullah, Fahad, S., Eds.; IntechOpen: London, UK, 2018; pp. 3–12. [ Google Scholar ]
• Bhardwaj, D.; Ansari, M.W.; Sahoo, R.K.; Tuteja, N. Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb. Cell Fact. 2014 , 13 , 66. [ Google Scholar ] [ CrossRef ] [ PubMed ] [ Green Version ]
• Wang, X.; Yan, J.; Zhang, X.; Zhang, S.; Chen, Y. Organic manure input improves soil water and nutrients use for sustainable maize ( Zea mays L.) productivity on the Loess Plateau. PLoS ONE 2020 , 15 , e0238042. [ Google Scholar ] [ CrossRef ] [ PubMed ]

Share and Cite

Krasilnikov, P.; Taboada, M.A.; Amanullah. Fertilizer Use, Soil Health and Agricultural Sustainability. Agriculture 2022 , 12 , 462. https://doi.org/10.3390/agriculture12040462

Krasilnikov P, Taboada MA, Amanullah. Fertilizer Use, Soil Health and Agricultural Sustainability. Agriculture . 2022; 12(4):462. https://doi.org/10.3390/agriculture12040462

Krasilnikov, Pavel, Miguel Angel Taboada, and Amanullah. 2022. "Fertilizer Use, Soil Health and Agricultural Sustainability" Agriculture 12, no. 4: 462. https://doi.org/10.3390/agriculture12040462

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• Published: 28 April 2017

Effects of fertilization on crop production and nutrient-supplying capacity under rice-oilseed rape rotation system

• Muhammad Yousaf 1 ,
• Jifu Li 1 ,
• Jianwei Lu 1 ,
• Tao Ren 1 ,
• Rihuan Cong 1 ,
• Shah Fahad 2 &
• Xiaokun Li 1  

Scientific Reports volume  7 , Article number:  1270 ( 2017 ) Cite this article

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• Environmental sciences
• Fertilization

Incredible accomplishments have been achieved in agricultural production in China, but many demanding challenges for ensuring food security and environmental sustainability remain. Field experiments were conducted from 2011–2013 at three different sites, including Honghu, Shayang, and Jingzhou in China, to determine the effects of fertilization on enhancing crop productivity and indigenous nutrient-supplying capacity (INuS) in a rice ( Oryza sativa L.)-rapeseed ( Brassica napus L.) rotation. Four mineral fertilizer treatments (NPK, NP, NK and PK) were applied in a randomized complete block design with three replicates. Crop yields were increased by 19–41% (rice) and 61–76% (rapeseed) during the two years of rice-rapeseed rotation under NPK fertilization compared to PK fertilization across the study sites. Yield responses to fertilization were ranked NPK > NP > NK > PK, illustrating that N deficiency was the most limiting condition in a rice-rapeseed rotation, followed by P and K deficiencies. The highest and lowest N, P and K accumulations were observed under NPK and PK fertilization, respectively. The INuS of the soil decreased to a significant extent and affected rice-rapeseed rotation productivity at each site under NP, NK, and PK fertilization when compared to NPK. Based on the study results, a balanced nutrient application using NPK fertilization is a key management strategy for enhancing rice-rapeseed productivity and environmental safety.

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Introduction.

Agriculture farming, previously dominated by production, currently has diverse objectives. The study of the environmental impacts of crops, the reduced costs of production and the balanced use of fertilization are among the main objectives of modern agriculture 1 . Rice-upland rotations are important agricultural production systems in South Asian countries 1 , covering an estimated 26.7 million hectares 2 . The rice in rotation is followed by next crop called upland crop. This type of rotation has many different sequences, where numerous grain and industrial crops could be rotated with paddy rice. E.g. rice-rapeseed, rice-wheat, rice-potato, rice-Chinese milk vetch etc. In China and other Asian countries, continuous rice planting has had a negative impact on soil properties, such as reduced soil nitrogen supply and organic carbon content 3 . Paddy-rice-upland crop rotations have been recommended and used to improve soil quality and reduce input 3 . In China, these rice-based rotations contribute to 72% of the total cereal production and cover an area of approximately 13 million hectares. Rice ( Oryza sativa L.) is an important global food crop that ensures food security for many countries. In China, rice is one of the most vital staple food crops, accounting for ~28% of the total grain-sown area and 43% of total grain production 4 . With a constantly growing population, Asian irrigated rice production must increase by 43% over the next 30 years 1 . However, further expansion of the rice planted area is a challenge because a majority of the arable land is already utilized for rice production or has been converted into urban infrastructure 5 . Food security advances must be achieved by constantly improving grain yield per unit area 6 . Oilseed rape ( Brassica napus L.) is the second most significant source of edible oil globally, with a high nutritional value and a favorable composition of fatty acids for both food and feed 7 . Consequently, its demand is increasing considerably all over the world 8 . China is the leading producer of oilseed rape, containing 23.3% of the cultivated area and contributing 22.2% of global oilseed rape production 1 . Therefore, rice-oilseed rape rotation is of great significance to the economy and food security of China.

The Yangtze River basin in China is a major planting area for the rice-oilseed rape rotation system, contributing 70% of the total rice 9 and 91% of the total oilseed rape production 10 . Oilseed rape in this area is usually cultivated under the single rice-oilseed rape system or the double rice-oilseed rape system, which limits the crop duration and the soil nutrient supply accessible for increasing yield 11 . Conversely, the yields of rice-upland rotations faced significant decline or yield stagnation with deterioration in soil fertility 12 . Concerns are also increasing about the loss of soil organic matter and the reduced nutrient-supplying capacity of soils under rice-upland rotations, which may be due to the increasing cropping intensity 13 . Farmers have resorted to the use of imbalanced fertilization (i.e., one fertilizer application; for example, in north-central China and the middle and lower reaches of the Yangtze River, only N fertilizer but no P and K fertilizers were applied by farmers, while in northeast China, N and P were applied but not K) or excessive fertilization to maintain yield levels 14 , 15 , 16 . This over-fertilization by farmers, driven by the desire for higher yields, does not always contribute to high yield but it has recently become a common practice for farmers in China nonetheless 15 . Unfortunately, over-fertilization decreases the efficiency of nutrient use 6 and causes a series of economic and environmental problems 17 . However, balanced mineral fertilizer inputs have played an important role in increasing the rice and oilseed rape yields 18 .

Managing agricultural nutrients to provide a safe food supply and secure the environment remains one of the immense challenges of the 21 st century 19 . Crop nutrient uptake and crop yields are the principal factors that determine optimal fertilization practices 20 . Therefore, it is very important to apply fertilizers in an efficient way to minimize loss and to improve the nutrient use efficiency 21 . To the best of our knowledge, previous studies on fertilization responses were rarely conducted on rice and oilseed rape crops individually, and no one has reported fertilization responses in the rice-oilseed rape rotation, particularly in China. In this study, on-farm experiments were conducted at three sites across the Hubei province in central China from May 2011 to May 2013 to study the influence of different mineral fertilizer applications on rice and oilseed rape yield and on the nutrient-supplying capacity of soil during a rice-oilseed rape rotation. These estimates will be helpful for improving fertilizer recommendations and for achieving sustainable production in rice-oilseed rape rotations in central China.

Yield of rice and oilseed rape in response to fertilization

The effect of the different fertilization treatments on rice and oilseed rape yield was significant at each study site (Table  1 ). In 2011–2012 (year one), the rice and oilseed rape yields varied from 5302 to 9048 kg ha −1 and 233 to 1687 kg ha −1 , respectively, while in 2012–2013 (year two), the yields ranged from 4781 to 10746 kg ha −1 and 639 to 2600 kg ha −1 for rice and oilseed rape, respectively. Depending on the fertilization treatment, overall, the total yield during 2011–2013 (total rotation) varied from 10083 to 19635 kg ha −1 and 827 to 4287 kg ha −1 for rice and oilseed rape, respectively. Among the sites, the highest rice and oilseed rape yield was observed at the JZ site followed by SY and HH. Compared to PK fertilization, NPK, NK and NP fertilizations significantly increased the rice and oilseed rape yield at each site. At all three sites, the highest rice and oilseed rape yield was observed under NPK application followed by NP and NK, while the lowest yield was observed under PK fertilization. Compared to NPK fertilization, the highest yield reduction was observed under PK followed by NK and NP, at all three sites. These results indicated that fertilization under NPK for rice and oilseed rape was statistically better than the other fertilizer treatments.

Nitrogen, phosphorus and potassium uptake in rice and oilseed rape

Total N, P and K uptake in aboveground plant parts of rice and oilseed rape under different fertilization treatments at each study site are shown in Table  2 . Total N uptake was enhanced under NPK fertilization compared with PK treatment. In 2011–2012 (year one), the total N uptake by rice and oilseed rape varied from 82 to 200 kg ha −1 (highest uptake at SY site) and 9 to 91 kg ha −1 (highest uptake at JZ site), respectively. In 2012–2013 (year two), the total N uptake by aboveground plant parts decreased for rice (72 to 169 kg ha −1 ) and increased for oilseed rape (23 to 108 kg ha −1 ), with the highest N uptake for both recorded at the JZ site. Across the sites, the total N uptake during 2011–2013 (total rotation) was higher for the NPK treatment than for the PK treatment, with the highest uptake at the JZ site for both rice and oilseed rape, followed by the SY and HH sites for rice and the HH and SY sites for oilseed rape.

Phosphorus uptake in both rice and oilseed rape was greater at all study sites under NPK fertilization compared with NK treatment. Across all sites, P uptake in the total rotation (2011–2013) varied from 75 to 88 kg ha −1 and 12 to 34 kg ha −1 for rice and oilseed rape, respectively, under NPK fertilization. Compared with NP treatment, potassium uptake in both rice and oilseed rape was enhanced under NPK fertilization in 2011–2012 (year one) and 2012–2013 (year two) at each study site.

Finally, the total K uptake of two consecutive annual rice-oilseed rape rotations (2011–2013) ranged from 344 to 428 kg ha −1 for rice and 131 to 249 kg ha −1 for oilseed rape under NPK fertilization. Furthermore, the highest N, P and K uptake was observed at the JZ site followed by SY and HH. This illustrated that NPK fertilization treatment was better than the other treatments for improving the N, P and K accumulation of a rice-oilseed rape rotation (Table  3 ).

Indigenous nutrient supply for nitrogen, phosphorus and potassium in rice and oilseed rape

In this study, we chose the N, P and K uptake by rice and oilseed rape under no-N, P and K treatment to represent the INS, IPS, and IKS of the soil, respectively. In the first rotation (2011–2012) of rice-oilseed rape across all study sites, INS ranged from 103 to 157 kg N ha −1 (Fig.  1 ), IPS ranged from 45 to 48 kg P ha −1 (Fig.  2 ), and IKS ranged from 257 to 298 kg K ha −1 (Fig.  3 ). In the second rotation (2012–2013), the ranges were 105 to 120 kg N ha −1 , 43 to 53 kg P ha −1 , and 206 to 264 kg K ha −1 for INS, IPS and IKS, respectively. Compared to NPK fertilization, INS decreased significantly across all sites, by 39–56% in 2011–2012 and 56–57% in 2012–2013 (Fig.  1 ). IPS decreased by 14–19% and 11–35% in 2011–2012 and 2012–2013, respectively (Fig.  2 ), while IKS decreased by 7–13% in 2011–2012 and 12–28% in 2012–2013 (Fig.  3 ), although there were no consistently significant differences between IPS and IKS across all sites. INS and IKS were highest at JZ and lowest at the HH site while IPS was highest at SY and lowest at the HH site.

Nitrogen supplying capacity (kg ha −1 ) in 1 st (2011–2012) and 2 nd (2012–2013) rotation. HH, SY and JZ represent Honghu, Shayang and Jingzhou respectively. Each value represent the standard error ( n  = 3). Within a season, bars with different letters are significantly different at P  < 0.05 according to LSD.

Phosphorus supplying capacity (kg ha −1 ) in 1 st (2011–2012) and 2 nd (2012–2013) rotation. HH, SY and JZ represent Honghu, Shayang and Jingzhou respectively. Each value represent the standard error ( n  = 3). Within a season, bars with different letters are significantly different at P  < 0.05 according to LSD.

Potassium supplying capacity (kg ha −1 ) in 1 st (2011–2012) and 2 nd (2012–2013) rotation. HH, SY and JZ represent Honghu, Shayang and Jingzhou respectively. Each value represent the standard error ( n  = 3). Within a season, bars with different letters are significantly different at P  < 0.05 according to LSD.

Sustained crop productivity relies on constant renewal when the supply of nutrients becomes a constraint to plant growth and development. Application of chemical fertilizers is necessary for enhancing crop yields and sustaining soil fertility 12 . However, inappropriate or excessive fertilizer application does not guarantee constantly increasing yields, might result in low nutrient use efficiency, and can cause environmental problems in agro-ecosystems 22 , 23 . Compared with PK fertilization, grain and seed yields of both rice and oilseed rape were significantly increased at each site by NPK, NP and NK, which indicates the importance of N for improving crop productivity (Table  1 ). Among all treatments, NPK fertilization produced the highest yield of both rice-oilseed rape rotations. This high yield was due to the balanced supply of all important nutrients to the plants. Other treatments, such as NP, NK and PK, were lacking at least one major nutrient, i.e., either N, P or K, and thus may induce a specific nutrient deficiency stress and retard overall growth of rice and oilseed rape with a concomitant reduction in yield. Nevertheless, the contributions of chemical fertilizers were diverse. Rice and oilseed rape yields of the 0-N fertilization were significantly lower than those of the 0-P and 0-K fertilizations, showing that N deficiency was the most limiting condition for crop yields 14 , 24 , followed by P and K deficiencies. The variations in the yields of rice and oilseed rape at different sites in different years were mainly the consequence of different fertilization treatments associated with soil fertility and the N, P and K uptake ratio by aboveground parts of rice and oilseed rape (Table  2 ). Furthermore, this discrepancy could also be partly explained by differences in weather conditions and soil physical-chemical properties at different experimental sites (Fig.  4 and Table  4 ). These results were in agreement with previous studies 25 , 26 that reported that yield components were affected by the fertilizations, and consequently, crop yields were usually greater depending on the soil fertility 27 . A close positive correlation between nutrient uptake and crop yield has also been reported previously 13 , 28 . The highest rice and oilseed rape yields were observed at the JZ site, followed by SY and HH, due to their correspondingly higher N, P and K uptakes. In addition to the nutrient uptakes, consideration was also given to their interactions. Many researchers have observed the complicated interactions among N, P and K in crop productivity 29 , 30 . In our study, P and K uptake was higher when applied with N, as evidenced by greater P and K accumulation in NPK than in PK treated sites, which clearly indicates the synergistic effect of N on P and K uptake (Table  3 ). Significantly higher N, P and K uptake was observed under NPK treatment, and the lowest uptake was observed under PK treatment. The remarkable synergistic consequences of N on P 31 and K 30 uptake were reported previously. Our results revealed that a balanced NPK treatment was best at improving the yield and nutrient accumulations for rice-oilseed rape rotation. Similar results were documented in a previous study that reported a linear increase in grain yield if nutrients were taken up in balanced amounts, until the yield reached approximately 60 to 70% of the yield potential 32 .

Monthly total rainfall and monthly mean temperature during the crops growth season at the experimental sites in Hubei province of China. HH, SY and JZ represent Honghu, Shayang and Jingzhou respectively.

The indigenous nutrient supply of soil can be assessed utilizing different strategies and indicators, including soil properties such as the soil organic C, total N, Olsen-P, NH 4 OA C -K, and plant markers such as crop yields and nutrient uptake under a specific nutrient omission treatment 14 , 24 , 33 . We selected the nutrient uptake by rice and oilseed rape under a specific nutrient omission treatment to represent the INS, IPS and IKS instead of performing a soil test. Many attempts have been made by researchers to predict INuS with a soil test 34 , 35 , but soil chemical analysis is not a reliable tool for quantifying nutrient-supplying capacity 36 . The yield decreased significantly when INS decreased (Table  1 and Fig.  1 ) for rice and oilseed rape at each site during both rotations (2011–2013), indicating that the yield response to N fertilizer is closely associated with INS. A significant correlation was observed between the crop yield and N uptake under no-N treatment for both oilseed rape 14 and rice 24 . Conversely, the crop yield also decreased by decreasing IPS (Fig.  2 ) and IKS (Fig.  3 ), but with an inconsistent significant response, and this reduction was not minimal when compared with yield loss under decreasing INS. However, the IPS and IKS decreased gradually in the second rotation (2012–2013) compared to the first rotation (2011–2012), indicating that P and K fertilizer were still essential for achieving high crop productivity. The variation in INS, IPS and IKS was due to differences in soil chemical properties at the different experimental sites (Table  4 ). Nutrient dynamics in soil were studied 37 at different sites, and it was observed that the nutrient fixation, uptake and availability were associated with the content of organic carbon and humic substances in soils. The other components, such as crop, accessibility of other nutrients, nutrient leaching and weather, may also be responsible for the differences in indigenous nutrient supplies. These results demonstrated the impact of INS, IPS and IKS on crop yields, and should therefore be considered during N, P and K fertilization, even though these parameters are frequently ignored 38 . The results reveal that the indigenous nutrient supply of soils is not sufficient to support the intensive cropping system of rice-oilseed rape rotations in central China.

In summary, balanced fertilizer application is not only essential for producing top quality crops in high yields but also for environmental sustainability. Plots that were treated with the combined NPK application had significantly higher rice and oilseed rape yields than plots with no NPK treatment at each experimental site. The lowest yields were observed in the no-N plots (PK), which indicated that N deficiency was the most limiting condition for rice and oilseed rape production. The results revealed that the addition of P and K fertilizer had a considerably positive effect on crop productivity when they were balanced with N. A similar trend was observed for P and K accumulation by aboveground parts of rice and oilseed rape, indicating that it is possible to enhance P and K accumulation when they are applied in combination with N fertilizer. Central China’s agriculture is exhaustive and high yielding and based on multiple cropping systems. The nutrient-supplying capacity of study soils has a significant influence on crop yield and nutrient accumulation. Hence, balanced fertilization of these soils is requisite for avoiding further deterioration of soil fertility and for increasing the productivity of rice-oilseed rape rotations. This fertilization not only improves the yields of the first crop in the rotation but also gives a significant residual advantage to subsequent crops. Agricultural profitability and improved nutrient use efficiency can be achieved through better plant nutrient management, which includes optimum fertilizer applications. Further studies are required on N, P and K fertilizer distribution for rice-oilseed rape rotations to address the variability of economic income and the risk of environmental pollution.

Description of study sites

The two-year field experiment was conducted from 2011 to 2013 on the rice and winter oilseed rape rotation at three different sites in the Hubei province of China: Honghu (HH), Shayang (SY) and Jingzhou (JZ). The previous land uses of these sites were also rice-rapeseed rotations planted by famers. The water requirement for rice was irrigation, while oilseed rape depended on rainfall. The climate of the study regions is a subtropical type, with a mean temperature ranging from 22.3 to 29.4 °C for the two growing seasons of rice and 3.8 to 23.0 °C during the two growing seasons of oilseed rape. Monthly rainfall varied from 10.8 to 475.3 mm in 2011, 7.4 to 213.8 mm in 2012 and 8.7 to 244.6 mm in 2013. During the over-winter oilseed rape cropping season period from January to February, the temperature was usually low (4 °C or lower) with little precipitation (<120 mm) (Fig.  4 ). The locations of the experimental sites and the soil properties of the plow layers (0–20 cm) at these sites before the commencement of the on-farm experiments are given in Table  4 .

Experimental design and operation

The experiment was conducted in a randomized complete block design in three replicates with four treatments: chemical N, P and K fertilization (NPK); chemical P and K fertilization (PK) with no N; chemical N and K fertilization (NK) with no P; chemical N and P fertilization (NP) with no K. All fertilization treatments in rice and oilseed rape received N as urea at 180 kg ha −1 (N 46.4%). The N was applied in three splits with 50% as a base fertilizer, 25% at the tillering stage and 25% at the panicle initiation stage for the rice seasons 24 . The N supplies for the oilseed rape seasons were applied with 60% just before seeding, 20% in the over-wintering stage, and 20% at the initiation of stem elongation 39 . The P fertilizers were applied entirely as a base application at 60 kg ha −1 as calcium superphosphate (P 5.2%) 40 for both the rice and oilseed rape seasons. In the K-fertilized plots, 90 kg ha −1 was applied as potassium chloride (K 52.3%) 40 with applications of 70% before sowing of rice and oilseed rape and 30% either at the panicle initiation stage for rice seasons or at the initiation of stem elongation for oilseed rape seasons. Boron fertilizer (15 kg ha −1 ) was added as a base application in the form of borax (B 12%) for each treatment of the oilseed rape season (but not for rice) to meet its nutritional requirements for normal growth 41 . The plot size for each treatment was 20 m 2 (3 m × 6.7 m) for both rice and oilseed rape 1 .

The experimental fields at each site were thrice plowed and leveled to an approximately 20-cm depth with a rotary tiller in a dry condition, and the base fertilizers were incorporated during the final plowing. Straw residues were removed before the construction of the experimental plots and the sowing of each crop. Local varieties, Y-liangyou no. 1 and Hua-youza no. 9, widely cultivated in the experimental region with high yields and extensive adaptability, were used for rice and oilseed rape, respectively. The nurseries were raised near the experimental sites on the seed bed with high fertility soils 42 and were transplanted to the field after 30 days. All other field operations, such as planting density, irrigation, herbicide application and disease and pest control were performed uniformly by methods described previously 42 . No major incidence of weeds, disease, pest or weather was recorded during the growing seasons of the nursery and fields. Planting densities were uniformly set at 200,000 ha −1 and 112,500 ha −1 for both growing seasons of rice and oilseed rape, respectively. The seeding, transplanting and harvesting times of rice and oilseed rape at each site are shown in Table  5 .

Sampling and measurement

Sampling and measurements of the soil and plants were conducted using the same protocols across all study sites. Soil samples were collected at a depth of 0–20 cm at 20 random points when each experimental site was established. A sub-sample of fresh soil was used for the measurement of inorganic N 43 . The remaining soil was air-dried and ground to pass through a 2-mm sieve for the measurements of pH (1:2.5 soil/water ratio), organic C (dichromate oxidation method), total N (Kjeldahl acid-digestion method), Olsen-P values (using a spectrophotometer), NH 4 OA C -K values (using a flame photometer), and soil type (the hydrometer method).

To investigate the overall effects of the fertilizer applications, plants were sampled at maturity for both crops to determine plant dry matter (kg ha −1 ) and nutrient uptake (kg ha −1 ) 42 . The plant samples were washed with deionized water and divided into seeds, stems, and pod walls for oilseed rape and grains or straw for rice 1 . Each aboveground fraction was separately chopped and dried to a constant weight at 65 °C, and then the entirely dried and milled plant samples were digested with H 2 SO 4 –H 2 O 2 44 . Total plant N and P concentrations were determined using an automated continuous flow analyzer (AA3, Bran and Luebbe, Norderstedt, Germany). Total plant K concentrations were determined using a flame photometer (FP640). Nutrient uptake was calculated by multiplying the crop dry matter with the nutrient concentrations in the aboveground parts of rice and oilseed rape 40 . At maturity, rice and oilseed rape were harvested manually from each plot, and yields were adjusted to a moisture content of 14% and 8–12%, respectively.

Data analysis and calculations

Analysis of variance (ANOVA) was conducted on data separated by year. The data were statistically analyzed using the SPSS 17.0 (IBM) software program. The differences between the treatments were calculated using the least significance difference test (LSD) at a 0.05 probability level. Figures were prepared using Origin 8.0 (Origin Lab) software.

Indigenous nitrogen supply (INS) was measured as total plant N accumulation at maturity in 0-N plots, indigenous phosphorus supply (IPS) was measured as total plant P accumulation at maturity in 0-P plots, and indigenous potassium supply (IKS) was measured as total plant K accumulation at maturity in 0-K plots 45 .

Yousaf, M. et al . Nitrogen fertilizer management for enhancing crop productivity and nitrogen use efficiency in a rice-oilseed rape rotation system in China. Front Plant Sci 7 , doi: 10.3389/fpls.2016.01496 (2016).

Timsina, J. & Connor, D. Productivity and management of rice–wheat cropping systems: issues and challenges. Field Crops Res 69 , 93–132, doi: 10.1016/S0378-4290(00)00143-X (2001).

Article   Google Scholar  

Chen, S. et al . Effect of long-term paddy-upland yearly rotations on rice (Oryza sativa) yield, soil properties, and bacteria community diversity. The Scientific World Journal 279641–279641 (2012).

Huang, J., Rozelle, S., Hu, R. & Li, N. China’s rice economy and policy: Supply, demand, and trade in the 21st century. Developments in the Asian rice economy 3–5 (2002).

Horie, T. et al . Can yields of lowland rice resume the increases that they showed in the 1980s? Plant Prod Sci 8 , 259–274, doi: 10.1626/pps.8.259 (2005).

Peng, S. et al . Strategies for overcoming low agronomic nitrogen use efficiency in irrigated rice systems in China. Field Crops Res 96 , 37–47, doi: 10.1016/j.fcr.2005.05.004 (2006).

Article   ADS   Google Scholar  

Foley, J. A. et al . Solutions for a cultivated planet. Nature 478 , 337–342, doi: 10.1038/nature10452 (2011).

Article   ADS   CAS   PubMed   Google Scholar  

Kim, I. S., Binfield, J., Patton, M., Zhang, L. & Moss, J. Impact of increasing liquid biofuel usage on EU and UK agriculture. Food Policy 38 , 59–69, doi: 10.1016/j.foodpol.2012.10.006 (2013).

Tian, X., Luo, H., Zhou, H. & Wu, C. Research on heat stress of rice in China: progress and prospect. Chin Agric Sci Bull 25 , 166–168 (2009).

Google Scholar  

van Egmond, K., Bresser, T. & Bouwman, L. The European nitrogen case. AMBIO: A Journal of the Human Environment 31 , 72–78, doi: 10.1579/0044-7447-31.2.72 (2002).

Zhang, Q.-C., Guang-Huo, W. & Weng-Xia, X. Soil organic N forms and N supply as affected by fertilization under intensive rice cropping system. Pedosphere 16 , 345–353, doi: 10.1016/S1002-0160(06)60062-3 (2006).

Article   CAS   Google Scholar  

Yadav, R. et al . Yield trends, and changes in soil organic-C and available NPK in a long-term rice–wheat system under integrated use of manures and fertilisers. Field Crops Res 68 , 219–246, doi: 10.1016/S0378-4290(00)00126-X (2000).

Timsina, J. et al . Nutrient uptake and apparent balances for rice-wheat sequences. I. Nitrogen. J Plant Nutr 29 , 137–155, doi: 10.1080/01904160500416539 (2006).

Li, H. et al . Yield response to N fertilizer and optimum N rate of winter oilseed rape under different soil indigenous N supplies. Field Crops Res 181 , 52–59, doi: 10.1016/j.fcr.2015.06.012 (2015).

Xu, X. et al . Yield gap, indigenous nutrient supply and nutrient use efficiency for maize in China. PLoS One 10 , e0140767, doi: 10.1371/journal.pone.0140767 (2015).

Article   PubMed   PubMed Central   Google Scholar  

Ata-Ul-Karim, S. T. et al . In-season estimation of rice grain yield using critical nitrogen dilution curve. Field Crops Res 195 , 1–8, doi: 10.1016/j.fcr.2016.04.027 (2016).

Ju, X., Kou, C., Zhang, F. & Christie, P. Nitrogen balance and groundwater nitrate contamination: Comparison among three intensive cropping systems on the North China Plain. Environ Pollut 143 , 117–125, doi: 10.1016/j.envpol.2005.11.005 (2006).

Article   CAS   PubMed   Google Scholar  

WeiNi, W. et al . Study on fertilization effect and fertilizer contribution rate of different crops at present production conditions. Sci Agric Sin 43 , 3997–4007 (2010).

ADS   Google Scholar  

Zhang, F. et al . 1 integrated nutrient management for food security and environmental quality in China. Adv agron 116 , 1–40, doi: 10.1016/B978-0-12-394277-7.00001-4 (2012).

Ju, X. & Christie, P. Calculation of theoretical nitrogen rate for simple nitrogen recommendations in intensive cropping systems: A case study on the North China Plain. Field Crops Res 124 , 450–458, doi: 10.1016/j.fcr.2011.08.002 (2011).

Li, X., Lu, J., Wu, L. & Chen, F. The difference of potassium dynamics between yellowish red soil and yellow cinnamon soil under rapeseed ( Brassica napus L.)–rice ( Oryza sativa L.) rotation. Plant Soil 320 , 141–151, doi: 10.1007/s11104-008-9879-7 (2009).

Guo, J. et al . Significant acidification in major Chinese croplands. Science 327 , 1008–1010, doi: 10.1126/science.1182570 (2010).

Tilman, D., Balzer, C., Hill, J. & Befort, B. L. Global food demand and the sustainable intensification of agriculture. Proc Natl Acad Sci 108 , 20260–20264, doi: 10.1073/pnas.1116437108 (2011).

Article   ADS   CAS   PubMed   PubMed Central   Google Scholar  

Wang, W. et al . Evaluating regional mean optimal nitrogen rates in combination with indigenous nitrogen supply for rice production. Field Crops Res 137 , 37–48, doi: 10.1016/j.fcr.2012.08.010 (2012).

Article   ADS   CAS   Google Scholar  

Zhang, H.-c., Wang, X.-q., Dai, Q.-g., Huo, Z.-y. & Xu, K. Effects of N-application rate on yield, quality and characters of nitrogen uptake of hybrid Rice Variety Liangyoupeijiu [J]. Sci Agric Sin 7 , 011 (2003).

Pan, S.-g. et al . Effects of N management on yield and N uptake of rice in central China. J Integr Agric 11 , 1993–2000, doi: 10.1016/S2095-3119(12)60456-0 (2012).

Hossain, M. et al . The efficiency of nitrogen fertiliser for rice in Bangladeshi farmers’ fields. Field Crops Res 93 , 94–107, doi: 10.1016/j.fcr.2004.09.017 (2005).

Witt, C. et al . Crop rotation and residue management effects on carbon sequestration, nitrogen cycling and productivity of irrigated rice systems. Plant Soil 225 , 263–278, doi: 10.1023/A:1026594118145 (2000).

Yang, L. et al . Seasonal changes in the effects of free-air CO 2 enrichment (FACE) on phosphorus uptake and utilization of rice at three levels of nitrogen fertilization. Field Crops Res 102 , 141–150, doi: 10.1016/j.fcr.2007.03.004 (2007).

QiangSheng, W. et al . Effect of potassium application rates on nitrogen absorption and utilization of different types of rice. Acta Agronomica Sinica 35 , 704–710, doi: 10.3724/SP.J.1006.2009.00704 (2009).

Yang, X. et al . Characteristics and correlation analysis of N and P uptake and utilization of early maturing late Japonica under different N fertilizer levels. Act Agron Sin 38 , 174–180, doi: 10.3724/SP.J.1006.2012.00174 (2012).

Xu, X. et al . Estimating nutrient uptake requirements for rice in China. Field Crops Res 180 , 37–45, doi: 10.1016/j.fcr.2015.05.008 (2015).

Li, J. et al . Soil testing and formula fertilization index for early rice in Fujian province. Plant Nutrition and Fertilizer Science 4 , 025 (2010).

CAS   Google Scholar  

Roberts, T., Ross, W., Norman, R., Slaton, N. & Wilson, C. Predicting nitrogen fertilizer needs for rice in Arkansas using alkaline hydrolyzable-nitrogen. Soil Sci Soc Am J 75 , 1161–1171, doi: 10.2136/sssaj2010.0145 (2011).

Spargo, J. T., Alley, M. M., Thomason, W. E. & Nagle, S. M. Illinois soil nitrogen test for prediction of fertilizer nitrogen needs of corn in Virginia. Soil Sci Soc Am J 73 , 434–442, doi: 10.2136/sssaj2007.0437 (2009).

Cassman, K. et al . Soil organic matter and the indigenous nitrogen supply of intensive irrigated rice systems in the tropics. Plant Soil 182 , 267–278, doi: 10.1007/BF00029058 (1996).

Blake, L. et al . Potassium content in soil, uptake in plants and the potassium balance in three European long-term field experiments. Plant Soil 216 , 1–14, doi: 10.1023/A:1004730023746 (1999).

Peng, S. et al . Improving nitrogen fertilization in rice by site-specific N management. A review. Agron Sustain Dev 30 , 649–656, doi: 10.1051/agro/2010002 (2010).

Lu, Z. et al . Differences on photosynthetic limitations between leaf margins and leaf centers under potassium deficiency for Brassica napus L. Sci Rep 6 (2016).

Su, W. et al . Influence of rice straw mulching on seed yield and nitrogen use efficiency of winter oilseed rape ( Brassica napus L.) in intensive rice-oilseed rape cropping system. Field Crops Res 159 , 53–61, doi: 10.1016/j.fcr.2014.01.007 (2014).

Wang, Y. et al . Winter oilseed rape productivity and nutritional quality responses to Zinc fertilization. Agron J 106 , 1349–1357, doi: 10.2134/agronj14.0029 (2014).

Wang, Y. et al . Establishment method affects oilseed rape yield and the response to nitrogen fertilizer. Agron J 106 , 131–142, doi: 10.2134/agronj2013.0374 (2014).

Rowell, D. Soil science: Methods and applications. Department of soil science, University of Reading (Prentice-Hall, Englewood Cliffs, ISBN 0-582-08784-8, 1994).

Bao, S. D. Soil and agricultural chemistry analysis. Agriculture Publication, Beijing 355–356 (2000).

Wang, G., Dobermann, A., Witt, C., Sun, Q. & Fu, R. Performance of site-specific nutrient management for irrigated rice in southeast China. Agron J 93 , 869–878, doi: 10.2134/agronj2001.934869x (2001).

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Acknowledgements

We thank S.T. Ata-Ul-Karim for his assistance in revision of this article. We acknowledge funding by National Natural Science Foundation of China (41401324), Special Fund for Agro-scientific Research in the Public Interest (201303103), and the Fundamental Research Funds for the Central Universities (2662015PY135).

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Muhammad Yousaf, Jifu Li, Jianwei Lu, Tao Ren, Rihuan Cong & Xiaokun Li

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T.R., R.C. and X.L. initiated and designed the research, M.Y. and J.F.L. performed the experiments and collected the data, M.Y., J.L. and X.L. analyzed the data and wrote the manuscript. J.L., S.F. and X.L. edited the manuscript and provided guidance during experimentation.

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Yousaf, M., Li, J., Lu, J. et al. Effects of fertilization on crop production and nutrient-supplying capacity under rice-oilseed rape rotation system. Sci Rep 7 , 1270 (2017). https://doi.org/10.1038/s41598-017-01412-0

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• Microorganisms

Biofertilizer: The Future of Food Security and Food Safety

Augustine innalegwu daniel.

1 Plant Omics Laboratory, Department of Biotechnology, University of the Western Cape, Robert Sobukwe Road, Bellville 7530, South Africa; az.ca.cwuym@7317714 (O.A.); az.ca.cwuym@4136623 (S.F.)

2 Department of Biochemistry, Federal University of Technology, P.M.B 65, Minna 920101, Niger State, Nigeria

Adewale Oluwaseun Fadaka

3 Department of Science and Innovation/Mintek Nanotechnology Innovation Centre, Biolabels Node, Department of Biotechnology, University of the Western Cape, Robert Sobukwe Road, Bellville 7530, South Africa; az.ca.cwu@akadafa (A.O.F.); az.ca.nus@moyuv (V.M.)

4 Department of Plant Sciences, Qwaqwa Campus, University of the Free State, Phuthadithjaba 9866, South Africa; az.ca.sfu@alukog

Olalekan Olanrewaju Bakare

5 Environmental Biotechnology Laboratory, Department of Biotechnology, University of the Western Cape, Robert Sobukwe Road, Bellville 7530, South Africa; az.ca.cwuym@0799773 (O.O.B.); az.ca.cwuym@4688323 (A.F.B.); az.ca.cwu@retsyekm (M.K.)

Omolola Aina

Stacey fisher, adam frank burt, vuyo mavumengwana.

6 Division of Molecular Biology and Human Genetics, Faculty of Medicine and Health Sciences, DST-NRF Centre of Excellence for Biomedical Tuberculosis Research, South African Medical Research Council Centre for Tuberculosis Research, Stellenbosch University, Cape Town 7505, South Africa

Marshall Keyster

Ashwil klein, associated data.

Not applicable.

There is a direct correlation between population growth and food demand. As the global population continues to rise, there is a need to scale up food production to meet the food demand of the population. In addition, the arable land over time has lost its naturally endowed nutrients. Hence, alternative measures such as fertilizers, pesticides, and herbicides are used to fortify the soil and scale up the production rate. As efforts are being made to meet this food demand and ensure food security, it is equally important to ensure food safety for consumption. Food safety measures need to be put in place throughout the food production chain lines. One of the fundamental measures is the use of biofertilizers or plant growth promoters instead of chemical or synthesized fertilizers, pesticides, and herbicides that poise several dangers to human and animal health. Biofertilizers competitively colonize plant root systems, which, in turn, enhance nutrient uptake, increase productivity and crop yield, improve plants’ tolerance to stress and their resistance to pathogens, and improve plant growth through mechanisms such as the mobilization of essential elements, nutrients, and plant growth hormones. Biofertilizers are cost-effective and ecofriendly in nature, and their continuous usage enhances soil fertility. They also increase crop yield by up to about 10–40% by increasing protein contents, essential amino acids, and vitamins, and by nitrogen fixation. This review therefore highlighted different types of biofertilizers and the mechanisms by which they elicit their function to enhance crop yield to meet food demand. In addition, the review also addressed the role of microorganisms in promoting plant growth and the various organisms that are beneficial for enhancing plant growth.

1. Introduction

Global demand for agricultural products is increasing due to the increasing human population [ 1 ]. There are already about 7.9 billion people on the planet, and this number is expected to rise, with a projected growth of almost 10 billion in the next 50 years [ 2 , 3 , 4 ]. As the world’s population continues to increase, so does the demand for food; hence, feeding the current vast population, which will certainly grow with time, is a significant task [ 5 ]. To meet the challenges of food scarcity caused by the rise in population, various agricultural alternatives such as the use of chemical or synthetic fertilizers, pesticides, and insecticides have been used to produce crops with high yield within the shortest time possible and to protect them from insects and pest attack during and after harvest [ 6 ]. However, the use of these fertilizers and insecticides has raised much public concern about the sustainability, safety, and security of the food supply [ 7 , 8 ]. Studies have shown that there is a significant amount of pesticide residue present in foodstuffs long after they are taken away from farms for human consumption [ 9 ]; hence, the need for alternatives such as biofertilizer in ensuring food safety and security [ 6 ]. Moreover, synthetic fertilizers that consist of various nutrients such as nitrogen (N 2 ), phosphorus (P), potassium (K), and sulfur may become harmful if used beyond the required amount [ 2 ]. The harmful effects of these fertilizers include the weakening of plant roots, the high rate of disease incidence, soil acidification [ 10 ], and eutrophication of ground water and other water bodies [ 11 ]. Nutrients such as nitrates leach to groundwater and cause “blue baby syndrome”, also called “acquired methemoglobinemia” [ 2 ]. The impact of these chemicals will not only affect the present but also future generations. Therefore, there is need to search for eco-friendly approaches such as biofertilizers, which play a major role in sustainable agriculture [ 2 ].

Biofertilizers are microorganisms that support the growth of plants by enhancing the nutrient supply to the host plant when given to seeds, plants, or the soil [ 2 , 12 , 13 ]. They colonize the rhizosphere or the inside of the plants. This entails the use of plant growth-promoting microorganisms that participate in a variety of biotic activities in the soil ecosystem in order to make it dynamic and sustainable for crop development. Biofertilizers are widely used to accelerate microbial activities that increase the availability of nutrients that plants can easily absorb. They increase soil fertility by fixing atmospheric N 2 and solubilizing insoluble phosphates in the soil, resulting in plant growth-promoting chemicals [ 14 ]. These biofertilizers make use of the naturally available biological system of nutrient mobilization, which greatly enhances soil fertility and, as a result, crop productivity. [ 14 ]. It has been reported that the biofertilizer market is estimated to grow at a compound annual growth rate (CAGR) of 14.0% from 2015 to 2020 and is expected to reach USD 1.88 billion by 2025 [ 15 ]. Because of strict regulations on the use of chemical fertilizers, biofertilizers are the most widely used in Europe and Latin America [ 15 ].

The words “food security” and “food insecurity” are commonly used in discussions of global conditions and prospects. Food security is defined as the availability and accessibility of safe and nutritious food that fits the dietary requirements of a healthy and active lifestyle. Food insecurity occurs when people do not have enough access to safe and nutritious food, and thus do not consume enough to live an active and healthy life. This could be due to a lack of food, a lack of purchasing power, or inefficient use of resources at the household level [ 16 ]. Another factor that may be responsible for food insecurity may be the depletion of soil nutrients resulting from continuous tillage and the use of chemical or synthetic fertilizers for continuous agricultural production. This have made the soil lose its fertility, and most of the agricultural produce consumed is not safe because of the chemical residues that are left in them. This review highlights the role of biofertilizers in crop improvement and the production of safe and secure food, the mechanisms of microorganisms in enhancing plant growth, and the various types of organisms used as plant growth-promoting microorganisms.

2. Biofertilizers

Microbial inoculants, also known as biofertilizers, are organic products that contain specific microorganisms obtained from plant roots and root zones. They have been found to boost plants’ growth and yield by 10–40% [ 16 ]. These bioinoculants colonize the environment when applied to the rhizosphere and the interior of the plant to promote plant growth [ 17 ]. They not only add nutrients to the soil to improve soil fertility and crop yield, but they also protect the plant against pests and diseases. They have been shown to enhance seedling survival, extend the root system’s life, eliminate harmful chemicals, and shorten flowering time [ 11 ]. Another advantage is that biofertilizers are no longer necessary after 3–4 years of continuous use, since the parental inocula are sufficient for growth and multiplication [ 18 ]. Plants require 17 essential elements for effective growth and development. N 2 , P, and K are all required in significant amounts [ 18 ]. Several microorganisms, including nitrogen-fixing soil bacteria and cyanobacteria, phosphate-solubilizing bacteria, molds, and mushrooms, are routinely utilized as biofertilizers [ 19 ]. Similarly, microorganisms that produce phytohormones are used in the production of biofertilizers. They feed the plant with growth-promoting compounds such as indole acetic acid (IAA), amino acids, and vitamins, as well as improving the soil’s productivity and fertility while conserving crop yield [ 20 ].

2.1. Types of Biofertilizers

Biofertilizers are divided into groups based on their functions and mechanisms of action. The most commonly used biofertilizers are nitrogen-fixers (N-fixers), potassium solubilizers (K solubilizers), phosphorus solubilizers (P solubilizer), and plant growth-promoting rhizobacteria (PGPR) [ 17 ]. One gram of rich soil can contain up to 10 10 cfu bacteria, with a live weight of 2000 kg/ha [ 21 ]. Cocci (spheres with a diameter of 0.5 m), bacilli (rods with a diameter of 0.5–0.3 m), and spirals with a diameter of 1–100 m are all types of soil bacteria. The frequency of bacteria in the soil is influenced by the physical and chemical properties of the soil, organic matter, and phosphorus concentration, as well as cultural activities. Nutrient fixation and improvements in plant growth by bacteria, on the other hand, are critical components for accomplishing future sustainable agricultural goals. Microbes also help the ecosystem’s numerous nutrient cycles. Table 1 summarizes the classification of biofertilizers based on the type of microbe utilized and the mechanism of action, as well as appropriate examples.

Classification of biofertilizers and their mechanism of action.

2.2. The Role of Plant Growth-Promoting Microorganisms in Crop Production

Plants are exposed to diverse microorganisms in their natural habitat, including bacteria, fungi, algae, and protozoa. The majority of these microorganisms occur in the soil’s rhizosphere in various types of association, some as free-living organisms, while others associate with plant roots or even live within root or shoot tissues as endophytes [ 26 , 27 ]. In the instance of a symbiotic relationship with nitrogen-fixing bacteria in the root nodules of leguminous plants, these connections may be advantageous to the plant, while others may be parasitic, pathogenic, or have no known effect on plant growth or development [ 27 ]. Microorganisms that promote plant growth are involved in a variety of biotic activities in the soil ecosystem to keep it dynamic and sustainable for crop production [ 28 ]. They colonize plant roots competitively and improve plant growth through a variety of mechanisms, including phosphate solubilization [ 29 ]; nitrogen fixation [ 30 ]; production of indole-3-acetic acid (IAA), siderophores [ 31 ], 1-amino-cyclopropane-1-carboxylate (ACC) deaminase, and hydrogen cyanate [ 32 ]; degradation of environmental pollutants; and the production of hormones, antibiotics, and lytic enzymes [ 33 ]. Furthermore, some plant growth-promoting rhizobacteria may be able to stimulate additional particular plant growth-promoting properties, such as heavy metal detoxification, salinity tolerance, and biological control of phytopathogens and insects [ 34 ].

Desulfovibrio , Rhodospirillum , and Rhodopseudomonas are examples of beneficial microbes that create symbiotic partnerships with plants, exchanging carbon-based photo-assimilates for minerals ingested by the microbe. Plant and soil biologists have paid extensive attention to beneficial symbiotic microorganisms in recent years, with major goals being the identification and adoption of new, environmentally beneficial lines of plant growth-promoting (PGP) microorganisms. Plant growth stimulators have also been found in other biostimulators, such as those found in seaweed extracts or decomposed vegetation [ 26 ].

3. Mechanisms of Action of Plant Growth-Promoting Rhizobia

There are different mechanisms by which plant growth-promoting rhizobacteria stimulate the growth of plants. They are widely classified as direct or indirect mechanisms [ 35 ]. Moreover, depending on their association with the plants, plant growth-promoting rhizobacteria are grouped as both symbiotic bacteria and free-living rhizobacteria [ 35 ]. Examples of plant growth-promoting bacteria include the free-living bacteria which form distinct symbiotic relationships with plants, endophytic bacteria which colonize some portions of plant tissue, and cyanobacteria [ 35 ]. Despite the differences that exist among the bacteria, they all show a similar type of mechanism while promoting bacterial growth [ 35 ]. The bacteria may use one of two methods to promote plant growth by (i) directly by improving resource acquisition or changing the plant’s hormone levels, or (ii) indirectly by lowering the inhibitory effects of various pathogenic agents on plant growth and development ( Figure 1 ).

Mechanisms of plant growth-promoting rhizobia.

3.1. Direct Mechanisms

3.1.1. facilitating resource acquisition.

Biofertilizer aids in nitrogen fixation, iron sequestration, and phosphate solubilization, allowing plants to use these complex organic molecules.

3.1.2. Nitrogen Fixation

One of the most important nutrients for plant growth is nitrogen. Although our atmosphere contains around 80% gaseous nitrogen, green plants are unable to utilize it directly [ 36 ]. Biological nitrogen fixation is the conversion of atmospheric nitrogen to ammonia by soil-borne microbes. About 175 × 10 6 tons of nitrogen are fixed globally each year by nitrogen-fixing bacteria [ 37 ]. Biological nitrogen fixation is a critical component of microbial activities. Only prokaryotes, which can be symbiotic or free-living in nature, are able to produce the nitrogenase enzyme to fix nitrogen biologically. The enzyme nitrogenase catalyzes biological nitrogen fixation. Some soil bacteria and blue-green algae can convert nitrogen from the air into ammonia in their cells. Diazotrophy, or nitrogen fixation, is the process of nitrogen reduction [ 29 , 37 , 38 , 39 , 40 ]. N-fixers, also known as diazotrophs, are microbes that reduce atmospheric nitrogen. Plants can directly utilize the ammonia produced during nitrogen fixation.

3.1.3. Rhizobacteria

The Rhizobiaceae (α-proteobacteria) are a family of symbiotic N 2 -fixing rhizobacteria that live in a symbiotic association with leguminous plant roots. This relationship necessitates a complicated interaction between the host and the symbiont, which leads to the creation of nodules that house the rhizobia as an intracellular symbiont [ 41 ]. The rhizobia include Rhizobium , Bradyrhizobium , Sinorhizobium , Azorhizobium , and Mesorhizobium as a group. Rhizobacteria that fix nitrogen in non-leguminous plants are known as non-symbiotic rhizobacteria. They are also known as diazotrophs, and they can create a non-obligate relationship with their hosts [ 42 ]. The nitrogen fixation process is carried out by nitrogenase, a complex enzyme structure that includes dinitrogenase reductase, which has iron (Fe) as a cofactor, and dinitrogenase, which has iron (Fe) and molybdenum (Mo) as cofactors [ 39 ]. In Figure 2 , dinitrogenase reductase produces electrons and uses them to decrease N 2 to NH 3 [ 43 ]. Mo-nitrogenase, V-nitrogenase, and Fe-nitrogenase are three different nitrogenase complexes based on changes in the cofactor of dinitrogenase [ 40 , 44 , 45 ]. N 2 fixation genes, also known as Nif genes, are found in both symbiotic and free-living nitrogen-fixing microorganisms [ 44 ]. Nif genes are structural genes involved in Fe–protein activation, Fe–Mo cofactor biosynthesis, electron donation, and serve as regulatory genes required for enzymatic synthesis and activity [ 45 ]. Despite being a negative regulator of Nif gene expression, oxygen is required for Rhizobium sp. bacteroid respiration [ 46 ]. Because bacterial leghemoglobin has a high affinity for oxygen, it can keep the enzyme active even in the absence of oxygen ( Figure 2 ). To efficiently pursue the nitrogen fixation process, sufficient O 2 supply to the bacteroid for respiration must occur concurrently with prevention of the O 2 supply to the nitrogenase enzyme complex. The simplest way to accomplish this objective is to use genetic engineering to introduce bacterial hemoglobin (Hb) that binds O 2 to the rhizobacteria [ 47 ]. Following this strategy, it was discovered that after transforming Rhizobium etli with the Hb gene of Vitreoscilla sp. (a Gram-negative bacterium), the rhizobial cells had a two- to threefold faster respiration rate than non-transformed rhizobial cells [ 30 ]. Because Vitreoscilla sp. has Hb-producing genes, inserting this gene into rhizobial cells resulted in Hb production in the transformed cells. Despite the low availability of O 2 , the Hb generated in this way could bind to it with a high affinity. When the altered Rhizobium was inoculated to bean plants, the plants had 68% greater nitrogenase activity than plants inoculated with wild-type R. etli . The resulting seeds had a 25–30% increase in leaf content and a 16% rise in nitrogen content as a result of this change [ 48 ].

Plant growth-promoting rhizobacteria’s molecular N 2 fixing mechanism. The nitrogen fixation process is carried out by the nitrogenase enzyme complex, which comprises dinitrogenase reductase and dinitrogenase. Dinitrogenase reductase produces electrons, which dinitrogenase uses to convert N 2 to NH 3 . Because the enzyme complex can attach to O 2 and become inactive, oxygen is a powerful inhibitor. Bacterial leghemoglobin, on the other hand, has a higher affinity for oxygen and hence binds to free oxygen more effectively. As a result, the presence of leghemoglobin protects the nitrogenase enzyme complex from oxygen, keeping it active [ 16 ].

Nodule development is another key component of Rhizobium . To accommodate the symbiotic bacteria Rhizobium , most bean plants generate root lateral organs de novo, known as “root nodules”. Symbiotic bacterial infection of the legume plant stimulates the creation of new organs, such as nodules, by altering the fate of differentiated cortical cells [ 49 ]. To establish optimal nodule development, two regulatory events, bacterial infection and nodule organogenesis, must be coordinated in the epidermis and cortical cells, respectively, during this process [ 50 ]. The symbiotic reactions between the host legume plants and Rhizobium are sustained by nodulation factors (Nod factors), which are lipochitin oligosaccharides released by rhizobia [ 51 ]. Plant ethylene levels were found to be higher after Rhizobium sp. infection of legumes, and this higher ethylene concentration inhibited further rhizobial infection and nodule development [ 16 ]. By producing a small compound molecule called “rhizobitoxine”, some rhizobial strains can enhance the number of nodules formed on the host bean plant’s roots by restricting the rise in ethylene production [ 52 ].

Rhizobitoxine is a phytotoxin that inhibits ethylene biosynthesis by chemically inhibiting the enzyme 1-aminocyclopropane-1-carboxylate (ACC) synthase [ 53 ]. ACC deaminase is an enzyme produced by some rhizobial strains that eliminates some of the ACC (the immediate precursor to ethylene in plants) before it is converted to ethylene. The plant’s nodule production and biomass increase by 25–40% as a result of this reduction [ 54 ]. Because around 1–10% of rhizobial strains in the field naturally contain ACC deaminase, it is possible to improve the nodulation effectiveness of rhizobia strains without ACC deaminase by genetically engineering them with rhizobia ACC deaminase genes [ 3 ]. The introduction of an ACC deaminase gene from Rhizobium leguminosarum bv. viciae into the chromosomal DNA of a Sinorhizobium meliloti strain that lacked this enzyme enhanced nodule numbers by 35% and host alfalfa plant biomass by 40% compared with the wild-type control strain [ 30 , 48 ]. Azorhizobium is a stem nodule-forming symbiotic bacterium that forms stem nodules and fixes N 2 , among other Rhizobium strains [ 55 ]. They also make a large amount of indole acetic acid (IAA), which helps plants thrive. Bradyrhizobium is a good nitrogen fixer, and when it was inoculated into Mucuna seeds, it boosted total organic carbon, N 2 , P, and K levels in the soil. As a result, it boosted plant growth, soil microbial population, and plant biomass and lowered the weed population [ 11 ].

3.1.4. Azospirillum

Azospirillum is a Gram-negative, aerobic nitrogen-fixing bacteria that do not form nodules and belong to the Spirilaceae family [ 56 ]. Although there are several species in this genus, such as Azospirillum amazonense , Azospirillum halopraeferens , and Azospirillum brasilense , Azospirillum lipoferum and A. brasilense are the most beneficial [ 57 ]. Because they develop and fix nitrogen on the organic salts of malic and aspartic acid, Azospirillum forms associative symbiosis with many plants, notably those with the C 4 dicarboxylic pathway (Hatch–Slack pathway) of photosynthesis [ 58 ]. As a result, it is mostly suggested for maize, sugarcane, sorghum, pearl millet, and other crops. They make growth stimulants (IAA, gibberellins, and cytokinin) that help in root development and nutrient uptake (N, P, and K). Inoculation with Azospirillum has a significant impact on root development and exudation [ 59 ]. When A. brasilense sp. 245 was inoculated to maize, the production of various phytohormones increased noticeably, resulting in a significant increase in maize growth [ 16 ]. The root physiology and architecture of maize were altered as a result of the increased synthesis of several phytohormones, resulting in an increase in mineral intake by the plant [ 16 ]. Inoculation with Azospirillum and Pseudomonas altered the cultivable bacterial community in the wheat rhizosphere, according to Naiman et al. [ 60 ]. They also found that inoculating the soil microflora with Azospirillum and Pseudomonas altered the profiles of carbon source use during the tillering and grain filling stages [ 60 ]. Inoculation with two A. brasilense strains (40 and 42 M) isolated from maize roots was also found to affect the community-level physiological profiles of the cultivable microbial communities associated with rice [ 59 ].

3.1.5. Azotobacter

Azotobacter is a genus of non-symbiotic, free-living, aerobic, photoautotrophic bacteria belonging to the Azotobacteriaceae family. Azotobacter chroococcum is the most frequent species in arable soils [ 61 ]. They are usually found in neutral and alkaline soils. Azotobacter vinelandii , Azotobacter beijerinckii , Azotobacter insignis , and Azotobacter macrocytogenes are among the other species identified [ 57 ]. They produce the Vitamin B complex and various phytohormones such as gibberellins, naphthalene acetic acid (NAA), and other compounds that prevent root infections while promoting root growth and mineral uptake [ 62 ]. Azotobacter has been found to release chemicals that limit the growth of certain root infections while also improving root growth and nutrient uptake [ 16 ]. Azotobacter has also been found to add 15–93 kg N/ha to Paspalum notatum roots [ 11 ]. Another strain, Azotobacter indicum , can produce a variety of antifungal antibiotics that are utilized to reduce seedling mortality by inhibiting the growth of many harmful fungi in the root region [ 63 ]. Azotobacter populations are often low in the rhizosphere of crop plants and in uncultivated soils, according to research. This organism has been found in the rhizosphere of a variety of crops, including rice, maize, sugarcane, bajra, vegetables, and plantation crops [ 64 ].

3.1.6. Blue-Green Algae (Cyanobacteria)

The blue-green algae are photosynthetic organisms that belongs to eight different families. They promote plant growth by generating auxin, indole acetic acid, and gibberllic acid, as well as fixing roughly 20–30 kg N/ha in submerged rice fields [ 57 ]. For lowland rice production, nitrogen is one of the main nutrients required in high quantities. Soil nitrogen and biological nitrogen fixation (BNF) by related microorganisms are the two main sources of nitrogen [ 43 , 65 ]. Fungi, liverworts, ferns, and flowering plants create symbiotic relationships with blue-green algae [ 45 ]. Anabena oryzae , Nostoc calcicola , and Spirulina sp. are three blue-green algae that have been shown to reduce the quantity of galls and egg masses induced by the root-knot nematode Meloidogyne incognita infecting cowpea, and to improve plant growth [ 16 ].

3.1.7. Azolla

Azolla has a 4–5% nitrogen content on a dry basis and 0.2–0.4% on a wet basis. In rice production, it can be a valuable source of organic manure and nitrogen [ 57 ]. The important aspect of using Azolla as a biofertilizer is that it decomposes quickly in the soil and provides nitrogen to rice plants efficiently. In addition, it adds to the provision of phosphorus, potassium, zinc, iron, molybdenum, and other micronutrients [ 66 ]. Prior to rice cultivation, Azolla can be utilized as a green biofertilizer in the fields. Azolla pinnata is the most commonly used species in India, and it may be produced commercially through vegetative techniques [ 14 ]. Azolla caroliniana , Azolla microphylla , Azolla filiculoides , and Azolla mexicana are some of the other Azolla species that have been introduced to India for their huge biomass output [ 57 ].

3.1.8. Phosphate Solubilization

Despite the fact that phosphorus is abundant in the soil, the majority of it is insoluble and hence is inaccessible to support plant growth, since plants only absorb it in two soluble forms: monobasic and dibasic. Inorganic phosphorus, such as apatite, or organic phosphorus, such as inositol phosphate (soil phytate), phosphomonoesters, and phosphotriesters, may be present [ 67 ]. Furthermore, much of the soluble inorganic phosphorus used in chemical fertilizers is quickly immobilized after being applied to the field. As a result, it is unavailable to plants and hence is wasted [ 67 ]. This has prompted researchers to look for environmentally benign and cost-effective ways to boost crop output in low-phosphorus soils. Microbes that can solubilize inorganic phosphorus play a critical role in these settings as a potential option for providing phosphorus to the plants. As a result, they are regarded as a promising biofertilizer, since they may provide the necessary phosphorus to plants, even from low-quality sources [ 14 ].

Organic acids with a low molecular weight such as gluconic and citric acids, which are generated by several soil microorganisms, are responsible for inorganic phosphorus solubilization [ 30 ]. Figure 3 depicts a schematic diagram of phosphate solubilization by microorganisms. The hydroxyl and carboxyl groups in these low-molecular-weight organic acids can chelate the cations attached to phosphate, resulting in the conversion of insoluble phosphorous to its soluble form. The mineralization of organic phosphorus, on the other hand, is accomplished by the production of several phosphatases that catalyze the hydrolysis of phosphoric esters [ 68 ]. Above all, phosphate solubilization and mineralization can occur in the same bacterial strain [ 69 ]. Pseudomonas , Bacillus , Rhizobium , Burkholderia , Achromobacter , Agrobacterium , Micrococcus , Acetobacter , Flavobacterium , and Erwinia are among the bacteria that have the ability to solubilize insoluble inorganic phosphorus [ 11 ]. Phosphate-solubilizing bacteria are commonly found in large numbers in soils and plant rhizospheres. These comprise aerobic and anaerobic strains, with aerobic strains being more common in submerged soils [ 69 ]. However, it has been discovered that the rhizosphere has a larger concentration of phosphate-solubilizing bacteria (PSB) than non-rhizosphere soil [ 11 ]. PSB stimulate the efficacy of biological nitrogen fixation (BNF) by nitrogen-fixing bacteria, in addition to delivering phosphorus in soluble form to plants [ 70 ].

Phosphate-solubilizing rhizobacteria solubilize inorganic phosphorus. Inorganic phosphorus is solubilized by bacteria using organic acids with a low molecular weight such as gluconic and citric acids. These acids’ hydroxyl (OH) and carboxyl (COOH) groups chelate the phosphate-bound cations, converting insoluble phosphorus into a soluble organic form. Mineralization of soluble phosphorus is accomplished through the production of several phosphatases, which catalyze the hydrolysis process. When plants absorb these solubilized and mineralized phosphorus molecules, their overall growth and crop output improve dramatically [ 11 ].

3.1.9. Sequestering Iron

Iron is an essential ingredient for practically all living things. Iron is required by all plants, animals, and microbes [ 16 ]. Iron exists as Fe 3+ in an aerobic environment and is prone to generating insoluble hydroxides and oxyhydroxides. As a result, the majority of iron is unavailable for absorption by bacteria and plants [ 16 ]. In general, bacteria obtain iron via secreting siderophores, which are low-molecular-weight iron chelators with a high affinity for complex iron ( Figure 4 ). The majority of siderophores are water-soluble, and they are classified as extracellular or intracellular siderophores [ 16 ]. Rhizobacteria differ in their ability to use siderophore cross-linking. Some Rhizobacteria use homologous siderophores proficiently, while others use heterologous siderophores [ 45 , 71 ]. Iron is reduced from Fe 3+ to Fe 2+ in the bacterial membrane in both Gram-positive and Gram-negative bacteria, and then released into the cell through siderophores via a gating mechanism that connects the inner and outside membranes ( Figure 4 ). Under iron-limiting conditions, siderophores operate as solubilizing agents for iron from minerals or organic molecules [ 72 ]. Similar to iron, siderophores create stable complexes with other heavy metals, as well as radioactive particles such as uranium and neptunium [ 73 ]. The concentration of soluble metal increases when the siderophores bind to a heavy metal. As a result, bacterial siderophores assist the host plant to reduce the stress caused by elevated heavy metal levels in the soil [ 30 ]. Plants absorb iron from bacterial siderophores using a variety of processes, including chelation and release, direct uptake of siderophore–Fe complexes, and ligand exchange reactions [ 74 ]. According to Thomine and Lanquar [ 74 ], siderophores facilitated iron transfer in oat plants and elevated plant growth. Rhizophore-produced siderophores delivered iron to the oat plant, which possesses a mechanism for utilizing Fe siderophores when iron is scarce [ 74 ]. Pseudomonas fluorescens C 7 generated the Fe–pyoverdine complex, which was taken up by Arabidopsis thaliana plants, resulting in a rise in iron levels in plant tissues and improved plant growth [ 71 ]. When plants are exposed to stress situations such as heavy metal pollution, the availability of iron to plants by soil bacteria becomes extremely important. In this case, siderophores can also assist plants to cope with the stress caused by high amounts of heavy metals [ 73 ].

Plant growth-promoting rhizobacteria produce siderophores, which are used to sequester iron. Bacteria release low-molecular-weight iron chelators known as “siderophores,” which have high affinity for Fe 3+ , bind firmly to it, and are taken up by bacteria. Fe 3+ is converted to Fe 2+ inside the bacterial membrane, and Fe 2+ is discharged into the cell via a gated channel that connects the bacteria’s inner and outer membranes. The total plant growth improves significantly when the host plant integrates these soluble Fe 2+ molecules produced by the bacteria.

3.1.10. Modulation of Phytohormone Levels

Plant hormones, also known as phytohormones, play a crucial role in plant growth and development [ 16 ]. When plants are exposed to growth-limiting environmental conditions, evidence suggests that they modify their endogenous phytohormone levels to reduce the detrimental impacts of environmental stress [ 16 ]. Microorganisms in the rhizosphere have been found to produce or modify phytohormone levels in the host plants. As a result, by modifying the level of endogenous phytohormones in the host plants, they can considerably influence the hormonal balance and stress response of the host plant [ 30 ]. For a long period, scientists have known that bacteria produce the phytohormone auxin (indole-3-acetic acid/indole acetic acid/IAA). According to one study, 80% of microorganisms isolated from the rhizosphere of diverse crops are capable of generating and releasing auxins as secondary metabolites [ 72 ].

Indole-3-acetic acid (IAA) is involved in many aspects of plant growth and development, as well as defense responses. The exceptional complexity of IAA biosynthesis, its transport mechanisms, and the different signaling pathways involved in IAA synthesis and transport reflects this diversity of roles [ 75 ]. In general, IAA stimulates seed and tuber germination; increases the rate of xylem and root development; controls vegetative growth processes; initiates lateral and adventitious root formation; mediates responses to light, gravity, and fluorescence; and affects photosynthesis and pigment formation, the biosynthesis of various metabolites, and stress resistance [ 28 ]. Because IAA is involved in various cell division and vascular bundle creation processes, it appears that a higher level of IAA in the host legume plants is required for nodule development [ 29 ]. Furthermore, bacterial IAA increases the root surface area and root length, allowing the plant to acquire soil nutrients more easily [ 29 ].

Furthermore, rhizobacterial IAA loosens plant cell walls, allowing for greater root exudation, which offers additional nutrients to sustain bacterial development [ 29 ]. As a result, rhizobacterial IAA has been identified as a crucial effector molecule in both disease and phytostimulation in plant–microbe interactions [ 29 ]. The amino acid tryptophan is an important component that influences IAA production levels. Tryptophan has been identified as the principal precursor of IAA and has been shown to have an important role in altering IAA biosynthesis levels [ 16 ]. Starting with tryptophan, at least five distinct processes for the synthesis of IAA have been reported, most of which are comparable with the mechanisms discovered in plants, but a few intermediates differ in each case [ 76 ]. The production of IAA via indole-3-pyruvic acid and indole-3-acetic aldehyde is the first pathway. The majority of bacteria, including Rhizobium , Azospirillum , Erwinia herbicola , Klebsiella , and others, use this pathway. The conversion of tryptophan to indole-3-acetic aldehyde is the second process, which may include an alternate pathway by which tryptamine is generated. Pseudomonas and Azospirilla use this route. The biosynthesis of IAA occurs via indole-3-acetamide in the third route. Agrobacterium tumefaciens , Pseudomonas syringae , and other phytopathogenic bacteria use this pathway. The conversion of tryptophan into indole-3-acetonitrile is the fourth step for IAA biosynthesis. Cyanobacteria have this mechanism. The last mechanism, which is more widespread in plants, Cyanobacteria, and Azospirilla , is the production of IAA via a tryptophan-independent pathway. Although bacterial IAA has been implicated in almost every aspect of plant growth and development, the acquisition of bacterial IAA may modify the endogenous pool of plant IAA. The degree of endogenous IAA in plants is critical in determining whether bacterial IAA stimulates or hinders plant growth in this respect. Endogenous IAA has been determined to be either ideal or sub-optimal for plant root development [ 30 ].

3.2. Indirect Mechanisms

Synthesizing multiple types of antibiotics is the most common way for plant growth-promoting bacteria (PGPB) to limit plant pathogen proliferation [ 77 , 78 ]. Many of the compounds have been thoroughly researched and some have even been marketed. The majority of commercialized rhizobacterial products function as bio-inoculants to combat plant diseases rather than to improve plant nutrition or reduce abiotic stressors [ 77 ]. Plant illnesses caused by pathogens such as Fusarium spp., Pythium spp., Rhizoctonia spp., and Sclerotium spp. have been reported to be treated by using biofertilizers such as Trichoderma harzianum , P. fluoresecens , and Bacillus subtilis , which boost plant growth and overall output. Hydrogen cyanide (HCN), phenazines, pyrrolnitrin, 2,4-diacetylphloroglucinol, pyoluteorin, viscosinamide, and tensin are among the antifungal metabolites produced by various Rhizobacteria [ 38 ]. It has also been observed that the contact between some Rhizobacteria and plant roots can protect the host plant from pathogenic fungi, bacteria, and viruses. Induced systemic resistance (ISR) is the term for this phenomenon [ 79 ]. Furthermore, ISR does not necessitate any direct interaction between the pathogens and the resistance-inducing PGPB [ 30 ].

Induced systemic resistance (ISR) is caused by jasmonate and ethylene signaling in the host plant, which acts as a defense mechanism against a range of plant pathogens [ 30 ]. Many individual bacterial components, such as lipopolysaccharides (LPS), flagella, siderophores, cyclic lipopeptides, 2,4-diacetylphloroglucinol, and homoserine lactones, as well as volatile compounds such as 2,3 butanediol and acetonin, have been reported to cause ISR in the host plant, allowing the host plant to combat a variety of plant pathogens [ 79 ]. Some biocontrol bacteria generate enzymes such as chitinases, cellulases, 1,3-gluconases, proteases, and lipases that can lyse a section of the cell wall of many pathogenic fungi such as Botrytis cinerea , Sclerotium rolfsii , Fusarium oxysporum , Phytophthora spp., Rhizoctonia solani , and Pythium ultimum [ 80 , 81 ]. Some PGPB strains produce siderophores, which operate as a biocontrol agent. In this approach, PGPB’s siderophores prevent pathogens from acquiring adequate iron, limiting their growth and proliferation [ 80 ]. Because the siderophores produced by PGPB have a higher affinity for iron than the pathogens, this technique is effective. As a result, the infections’ ability to utilize iron is diminished and they are unable to multiply in the rhizosphere [ 30 ]. Plants have been reported to synthesize ethylene in response to a range of stressors, including fungal phytopathogenic infections [ 82 ]. When plant cells become infected, ethylene causes a stress/senescence response in the plant, which results in the death of cells that are either infected or present near the fungal infection site [ 82 ]. As a result, increasing levels of ethylene build up, as well as the infection caused by plant pathogens, causing a large amount of the harm to the plant. Exogenous ethylene has also been shown to exacerbate the severity of fungal infections. As a result, lowering the ethylene response is one strategy to reduce the harm produced by phytopathogen infections of the host plants [ 3 ]. Ethylene inhibitors have been found to not only reduce the ethylene response level but also to diminish the severity of fungal infections. When the host plant is affected by pathogens, the enzyme ACC deaminase found in PGPB can adjust the ethylene level [ 16 ]. As a result, the most straightforward strategy to reduce ethylene levels is to apply PGPB harboring the ACC deaminase gene to the plants (usually the roots or seeds).

4. Benefits of Biofertilizers in Food Production

To meet the increased need for food, continuous and indiscriminate usage of synthetic or chemical fertilizers has unquestionably resulted in contamination and ecosystem modification [ 16 ]. Even so, the long-term impacts of using synthetic or chemical fertilizers lower soil fertility and have resulted in the production of disease-prone crops [ 83 , 84 ]. The amount of food produced today compared with the amount required to feed everyone in 2050 is drastically lower. By 2050, the world’s population will have swelled to about 10 billion people, with roughly 4.5 billion more mouths to feed than in 2022. People will consume more resource-intensive, animal-based diets as their wages rise. To feed the growing population with a deficit amount of available nutrients, the world certainly needs to encourage agricultural productivity in a sustainable and ecofriendly way. Hence, it is necessary to re-evaluate many of the existing agricultural approaches, which include the use of chemical fertilizers, pesticides, herbicides, fungicides, and insecticides [ 85 ]. In light of the harmful effects of chemical or synthetic fertilizers, biofertilizers are supposed may be a safe alternative to chemical inputs and minimize alteration of the ecosystem to a great extent. Biofertilizers are cost-effective and ecofriendly in nature, and their prolonged use enhances soil fertility substantially [ 16 ]. It has been found that using biofertilizers increases crop yield by 10–40% by increasing protein, vital amino acids, and vitamins, and nitrogen fixation [ 86 ]. Biofertilizers provide a number of advantages, including being a low-cost source of nutrients, excellent suppliers of micro-compounds and micronutrients, organic matter suppliers, growth hormone producers, and a means of counteracting the negative effects of chemical fertilizers [ 87 ]. Different microorganisms are important components of soil, and they play a key role in a variety of biotic activities in the soil ecosystem that keep the soil active for nutrient mobilization and long-term crop development [ 45 ].

5. Conclusions and Future Perspectives

The continuous rise in the global population has translated to a direct increase in the demand for food production. The use of these biofertilizers has been reported to boost the food production rate, and they are a safer farm product for consumers; hence, biofertilizers remains a better alternative for producing safer crops and enhancing global food security. In recent years, the plant nutrient gap between removal and supply through chemical fertilizer was over 10 million tons. Over-dependence on chemical fertilizers, in terms of both cost and environmental impact, is not a viable strategy in the long run due to the costs involved in setting up fertilizer plants and maintaining production, both in terms of domestic resources and foreign exchange. Biofertilizers are products that, once adequate information is available to producers and farmers, are likely to be commercially promising in the long run. The use of biofertilizers in the world will not only have an impact on the economic development of sustainable agriculture, but it will also contribute to a sustainable ecosystem and the overall wellbeing of humans.

Funding Statement

This research received no external funding. The APC was funded by the Department of Science and Innovation and the Technology Innovation Agency distributed by GrainSA (Grant numbers: GB0200065 and GB0200066). The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

Author Contributions

Conceptualization, A.I.D. and A.K.; methodology, A.I.D., A.O.F., A.G., O.O.B., O.A., S.F. and A.F.B.; software, A.I.D. and A.O.F.; validation, A.I.D. and A.O.F.; formal analysis, A.I.D. and A.O.F.; resources, A.K., A.I.D., A.O.F. and M.K.; writing—original draft preparation, A.I.D. and A.O.F.; writing—review and editing, A.I.D., A.O.F., O.O.B., A.G., V.M., M.K. and A.K.; supervision, M.K. and A.K.; project administration, A.K. and M.K.; funding acquisition, A.K. and M.K. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Informed consent statement, data availability statement, conflicts of interest.

The authors declare no conflict of interest.

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Something’s Poisoning America’s Land. Farmers Fear ‘Forever’ Chemicals.

Fertilizer made from city sewage has been spread on millions of acres of farmland for decades. Scientists say it can contain high levels of the toxic substance.

Jordan Vonderhaar for The New York Times

Hiroko Tabuchi traveled to Texas and Michigan and interviewed ranchers, scientists, investigators and wastewater-treatment experts for this article.

Aug. 31, 2024

Supported by

For decades, farmers across America have been encouraged by the federal government to spread municipal sewage on millions of acres of farmland as fertilizer. It was rich in nutrients, and it helped keep the sludge out of landfills.

But a growing body of research shows that this black sludge, made from the sewage that flows from homes and factories, can contain heavy concentrations of chemicals thought to increase the risk of certain types of cancer and to cause birth defects and developmental delays in children.

Known as “forever chemicals” because of their longevity, these toxic contaminants are now being detected, sometimes at high levels, on farmland across the country , including in Texas, Maine, Michigan, New York and Tennessee. In some cases the chemicals are suspected of sickening or killing livestock and are turning up in produce. Farmers are beginning to fear for their own health.

The national scale of farmland contamination by these chemicals — which are used in everything from microwave popcorn bags and firefighting gear to nonstick pans and stain-resistant carpets — is only now starting to become apparent. There are now lawsuits against providers of the fertilizer, as well as against the Environmental Protection Agency, alleging that the agency failed to regulate the chemicals, known as PFAS.

In Michigan, among the first states to investigate the chemicals in sludge fertilizer, officials shut down one farm where tests found particularly high concentrations in the soil and in cattle that grazed on the land. This year, the state prohibited the property from ever again being used for agriculture. Michigan hasn’t conducted widespread testing at other farms, partly out of concern for the economic effects on its agriculture industry.

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Open Access

Peer-reviewed

Research Article

The effects of chemical and organic fertilizer usage on rhizosphere soil in tea orchards

Roles Data curation, Formal analysis, Investigation, Writing – original draft

Affiliations Fujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, China, Key Laboratory of Crop Ecology and Molecular Physiology, Fujian Agriculture and Forestry University, Fuzhou, China

Roles Data curation

Affiliations Key Laboratory of Crop Ecology and Molecular Physiology, Fujian Agriculture and Forestry University, Fuzhou, China, Key Laboratory for Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education / College of Crop Science, Fujian Agriculture and Forestry University, Fuzhou, China

Roles Formal analysis

Affiliation Fujian Vocational College of Agriculture, Fuzhou, China

Roles Writing – original draft

Roles Formal analysis, Project administration

* E-mail: [email protected] (WL); [email protected] (ZL)

Roles Project administration, Supervision, Writing – review & editing

Affiliations Fujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, China, Key Laboratory of Crop Ecology and Molecular Physiology, Fujian Agriculture and Forestry University, Fuzhou, China, Key Laboratory for Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education / College of Crop Science, Fujian Agriculture and Forestry University, Fuzhou, China

• Weiwei Lin, 
• Manhong Lin, 
• Hongyan Zhou, 
• Hongmiao Wu, 
• Zhaowei Li, 
• Wenxiong Lin

• Published: May 28, 2019
• https://doi.org/10.1371/journal.pone.0217018
• Reader Comments

Sustainable agriculture is an important global issue. The use of organic fertilizers can enhance crop yield and soil properties while restraining pests and diseases. The objective of this study was to assess the effects of long-term use of chemical and organic fertilizers on tea and rhizosphere soil properties in tea orchards. Inductively coupled plasma mass spectrometry (ICP-MS) and high-throughput sequencing technology analyses were used to investigate heavy metals content and bacterial composition in rhizosphere soils. Our results indicated that organic fertilizer treatment significantly decreased Cu, Pb and Cd contents in rhizosphere soil sample. The results also showed that treatment with organic fertilizer significantly decreased the contents of Cd, Pb and As in tea leaves. Furthermore, organic fertilizer significantly increased the amino acids content of tea and the pH of the soil. The use of organic fertilizer significantly increased in the relative abundance of Burkholderiales , Myxococcales , Streptomycetales , Nitrospirales , Ktedonobacterales , Acidobacteriales , Gemmatimonadales , and Solibacterales , and decreased the abundance of Pseudonocardiales , Frankiales , Rhizobiales , and Xanthomonadales . In conclusion, organic fertilizer can help to shape the microbial composition and recruit beneficial bacteria into the rhizosphere of tea, leading to improved tea quality and reduced heavy metals content in rhizosphere soil and tea leaves.

Citation: Lin W, Lin M, Zhou H, Wu H, Li Z, Lin W (2019) The effects of chemical and organic fertilizer usage on rhizosphere soil in tea orchards. PLoS ONE 14(5): e0217018. https://doi.org/10.1371/journal.pone.0217018

Editor: Fuzhong Wu, Sichuan Agricultural University, CHINA

Received: December 13, 2018; Accepted: May 2, 2019; Published: May 28, 2019

Copyright: © 2019 Lin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: This work was supported by: National Natural Science Foundation of China (No. 31701329, 81573530); Fujian-Taiwan Joint Innovative Center for Germplasm Resources and Cultivation of Crop (Fujian 2011 Program, No.2015-75, China); the Natural Science Foundation of Fujian Province (No. 2016J01100); and the Project Funded by China Postdoral Science Foundation (No. 2015M580560).

Competing interests: The authors have declared that no competing interests exist.

Introduction

Camellia sinensis, commonly known as tea plant, is a mountainous crop and an important agricultural product for many farmers in China. Due to its richness in beneficial antioxidants, vitamins, and amino acids, the popularity of tea has been steadily growing. And the amino acids, tea polyphenols, and caffeine are key elements in determining both taste and quality of tea. In 2016, China produced 2.41 million tons of tea with a monetary value of 170.2 billion yuan. However, soil degradation and substantial quality and yield decrease have been observed in the long-term monoculture of tea bushes, and have become key problems in the sustainable development of tea orchards [ 1 ]. With growing demand and limited land availability, farmers have been increasingly using nitrogen fertilizers in order to increase crop yield. However, nitrogen fertilizers can have undesirable effects, including a decline in tea quality, soil acidification, heavy metals pollution, soil compaction, and changes in soil microbiome [ 2 – 3 ]. We have previously shown that long-term tea cultivation with nitrogen fertilizers altered the bacterial composition of soil and significantly decreased soil pH and microbial metabolic activity, resulting in a reduction of beneficial bacteria [ 1 , 4 – 5 ]. Therefore, it is essential to understand the impact of nitrogen fertilizers beyond their effects on crop yield in order to achieve a balance between benefits and harms in modern agricultural practices.

The sustainability of agricultural systems is an important global issue. This has resulted in the potential benefits of organic fertilizers application have being highlighted. Organic fertilizers are derived from natural sources (e.g., livestock and poultry excreta, plant residues, biogas residue, and agricultural by-products), and their usage can have a positive impact on pollution. The potential benefits of organic fertilizers have been documented in a number of studies in which investigators observed a raise in soil microbial activities, which in turn improved crop growth and restrained pests and diseases [ 6 – 7 ]. Soil contains a large number of microbial species as well as other organisms that together form a highly complex ecosystem. Microorganisms are essential for nutrient recycling, healthy plant development, and decomposition of organic matter [ 8 ]. However, environmental conditions and cultivation practices are likely to influence the microbiome, resulting in alterations in soil characteristics or ecosystem [ 9 ]. Researchers have found that tea cultivated with bio-organic fertilizers has superior color and taste compared to tea treated with chemical fertilizers [ 10 – 11 ]. Studies have also suggested that the use of organic fertilizers resulted in higher seedling biomass and significantly improved the soil fungal to bacterial ratio as well as soil enzyme activity [ 12 – 13 ]. In addition, while long-term application of chemical fertilizers could lead to serious soil acidification, nutritional imbalance, and deterioration of the rhizosphere micro-ecological environment, further increased the activity of heavy metal ions in soil. The use of organic fertilizer could alleviate soil acidification, resulting in increased plant yields [ 14 ]. However, little information is available concerning the contents changes of microbial community and heavy metal ions using long-term chemical fertilizers and organic fertilizer.

Recent studies have raised concerns regarding the long-term effects of fertilization practices on biological properties of soils, but most studies focused mainly on tea plant yield and changes in soil nutrients [ 15 – 17 ]. Moreover, the effects of long-term use of organic fertilizer on rhizosphere bacterial composition and heavy metals in tea gardens have not been carefully investigated. In this study, we have used ICP-MS and high-throughput sequencing technology to determine the effects of organic and chemical fertilizers on bacterial taxa and heavy metals content in the rhizosphere of tea orchards. Herein we evaluated potential mechanisms of organic fertilizers application as a means to improve the quality of tea. These results could provide practical guidance to the design of sustainable tea garden ecology.

Materials and methods

Field experiment and soil sampling.

The experimental station is located in the Zudun township of Nanping in the Fujian Province of China (27°24ʹN, 118°33ʹE). This is one of the main tea producing region in Fujian and is under sub-tropical monsoon climate with an average annual temperature of 18.1°C and an average annual rainfall of 1557–1743 mm. Zudun township of Fujian Province is the most important producing area of white tea in China. The two different planting and management patterns were the long-term organic fertilizer (mainly contain rape cake and sheep dung) ecological tea garden and the conventional nitrogen fertilizer management tea garden. These tea orchards had similar environmental characteristics such as altitute, slope position and slope aspect, and similar agronomic management. The tea orchards were typical red acidity soils in southern China. These experimental fields were established in 1990 and have since been used for tea planting. The tea orchards have cultivated the Fuding white tea and the tea stand ages were more than 30 years old, were selected in this study, and each had three landscape-level replications. The organic tea orchards have been certified under the US National Organic program 7 CFR Part 205 by the certification of environmental standards Gmbh (CERES) in 2015.

Soil samples were collected from the rhizosphere of fields treated with organic fertilizer (OrgS) or chemical fertilizer (NorS) fon June 4, 2018. At the same time, non-rhizosphere soils were also collected from the organic (CKOrgS) and chemical (CKNorS) fertilizer treated tea orchards. The rhizosphere and non-rhizosphere soils of tea trees were taken from each experimental plot by a 5-point sampling method. For each sample, three replicates were performed. Tea leaves from the OrgS and NorS treatment groups were sampled in the fields. After sieving (2 mm mesh) to remove stones and plant residues, soil samples were stored at −80°C.

Analysis of tea biochemical properties

Tea leaves were roasted, dried and ground into a fine powder testing. The amino acid content was measured using the ninhydrin colorimetric methods. Tea polyphenols and caffeine contents were determined using a Waters HPLC system (C18 column: Inertsil ODS-SP, 4.6 × 250 mm, 5 μm). The chromatographic conditions were as follows for tea polyphenols: mobile phase A: mixture solution (water: acetic acid: acetonitrile = 90:0.1:10, v/v/v); mobile phase B: acetonitrile; elution gradient: mobile phase B 0% (0 min)→0% (10 min)→10% (20 min)→0% (25 min)→0% (30 min); oven temperature: 40°C; detection wavelength: 280 nm; velocity: 1 mL/min. For caffeine: mobile phase A: water; mobile phase B: methanol; elution gradient: mobile phase B 65% (0 min)→65% (35 min); detection wavelength: 275 nm; velocity: 1 mL/min.

Analysis of soil chemical properties

Soil chemical properties analysis included pH, total nitrogen (TN), total phosphorus (TP), total potassium (TK), available nitrogen (AN), available phosphorus (AP), and available potassium (AK). Soil pH was determined using a glass electrode pH meter (1:2.5 soil to water suspensions). TN, TP, and TK were determined using Kjeldahl digestion, sodium carbonate fusion, and NaOH melts flamer methods, respectively [ 18 ]. AN was determined using the alkaline hydrolyzable method. AP was extracted with hydrochloric acid and ammonium fluoride, and contents were measured using the molybdenum blue method. AK was extracted with ammonium acetate, and measured by flame photometry [ 19 ].

Analysis of heavy soil metal

The microwave digestion system (Milestone ETHOS UP, Italy) was used to extract cuprum (Cu), plumbum (Pb), cadmium (Cd) and arsenic (As) from soil samples. The contents of these metals were determined by Inductively coupled plasma mass spectrometry (ICP-MS, PerkinElmer NexION 300X, U.S.A), using parameters listed in Table 1 .

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https://doi.org/10.1371/journal.pone.0217018.t001

Genomic DNA purification and PCR amplification

Total soil DNA was extracted using the BioFast soil Genomic DNA Extraction kit (BioFlux, Hangzhou, China), following the manufacturer’s instructions. For each soil sample, three independent DNA extractions were performed. DNA was diluted to a concentration of 1 ng/μL in sterile water. The variable regions 3 to 4 (V3–V4) were amplified with the specific primers 338F/806R (338F, 5’-ACTCCTACGGGAGGCAGCA-3’ ; 806R, 5’-GGACTACHVGGGTWTCTA AT-3’ ). The PCR reactions were conducted in a 50 μL mixture system, using TransStart Fastpfu DNA Polymerase (TransGen Biotechnology, Beijing, U.S.A). The PCR condition was initiated denaturation with 5 min at 95°C, followed by 35 cycles of 40 s at 95°C, 40 s at 58°C, 60 s at 72°C and final elongation with 5 min at 72°C. PCR products were purified using the Qiagen Gel Extraction Kit (Qiagen, Germany), and subjected to sequencing on the Illumina HiSeq 2500 platform (Allwegene Technologies Co., Ltd., Beijing, China).

Statistical analysis

The FLASH method [ 20 ] was used to merge paired-end reads. Following quality filtering and chimera removal [ 21 ], the effective tags were used to perform OTU clustering and species annotation. Species annotation was performed using the Silva database ( http://www.arb-silva.de ) [ 22 ]. For each remaining sequences, the RDP classifier (Version 2.2) algorithm [ 23 ] was used to annotate taxonomic information via the GreenGen database [ 24 ]. Mothur version 1.31.2 [ 25 ] was used to analyze the alpha diversities. Beta diversities were then calculated to analyze the complexity of species diversity. The Statistical Package for the GraphPad Prism version 5.1 and the Data Processing System (DPS) version 7.05 were used for statistical analysis. Differences among the treatments were calculated and statistically analyzed using the analysis of variance (ANOVA) and the LSD multiple range tests (p < 0.05).

Tea and soil chemical characteristics

In this study, we found that the use of organic fertilizer significantly increased the amino acids content of tea ( Fig 1 ). The contents of polyphenol did not reach statistical significance in tea samples from fields treated with organic fertilizer compared to those treated with chemical fertilizer. In contrast, tea under long-term treatment with chemical fertilizer showed significantly higher contents of caffeine compared to tea with organic fertilizer.

Columns with different letters are statistically different (LSD test, P < 0.05).

https://doi.org/10.1371/journal.pone.0217018.g001

Table 2 summarized the chemical properties of soil from tea orchards treated with either organic or chemical fertilizers. Contents of total nitrogen, total potassium, available nitrogen, available phosphorus, and available potassium were similar between the two treatment groups (P > 0.05). However, soil pH level was significantly higher in the organic fertilizer treatment group compared to the chemical fertilizer treatment group ( Table 2 ).

https://doi.org/10.1371/journal.pone.0217018.t002

Tea orchards with long-term organic or chemical fertilizer treatment showed significant differences in soil chemical properties ( Fig 2 ). Treatment with organic fertilizer resulted in significantly lower contents (P < 0.05) of cuprum (Cu), plumbum (Pb) and cadmium (Cd) in rhizosphere soils compared to the chemical fertilizer treatment group. A small decrease in arsenic (As) level was also detected in the organic fertilizer treatment group, but the difference was not statistically significant. Similar trends were observed in non-rhizosphere soil samples. Our results also showed that treatment with organic fertilizer significantly decreased contents of Cd, Pb and As in tea leaves ( Fig 3 ).

https://doi.org/10.1371/journal.pone.0217018.g002

https://doi.org/10.1371/journal.pone.0217018.g003

Alpha diversity indices of microbial community

A total of 544,096 effective clean tags with bacterial species annotation were obtained from 12 soil samples. Alpha diversity was calculated to determine the complexity of species diversity. We observed a significantly higher bacterial composition and Chao1 indices with samples from the organic fertilizer treatment group compared to samples from the chemical fertilizer treatment group. Long-term organic fertilizer treatment also had a positive effect on non-rhizosphere soil. Our results showed that chemical fertilizer significantly increased Shannon’s diversity indices in rhizosphere soil in comparison to all treatments ( Fig 4 ).

https://doi.org/10.1371/journal.pone.0217018.g004

Beta diversity indices of microbial composition

We used weighted unifrac heatmap, hierarchical clustering, and principal component analysis to identify differences in bacterial composition structure between the treatment groups ( Fig 5 ). In comparison to CKNorS, higher distances were observed among the OrgS, CKOrgS, and NorS samples. The PC1 and PC2 components of PCoA accounted for 45.93% and 26.65% of the total bacterial composition variations, respectively. We found that the bacterial composition of OrgS and CKOrgS soil samples belonged to the same group based on the principal component analysis. In contrast, the bacterial composition of NorS and CKNorS samples fell into two separate groups that were distinct from OrgS and CKOrgS samples.

(A) Weighted unifrac heatmap; (B) Hierarchical clustering analysis; (C) Principal Component Analysis.

https://doi.org/10.1371/journal.pone.0217018.g005

Shifts in soil bacterial composition structure

In this study, the classified sequences were affiliated with 24 bacterial phyla among the treatment groups. The majority of the phyla were assigned to Actinobacteria , Chloroflexi , Proteobacteria , Acidobacteria , Gemmatimonadetes , and Cyanobacteria ( S1 Fig ). Meanwhile, clear trends in variation at the phylum level were observed between the organic fertilizer and chemical fertilizer treatment groups. The number of OTUs exclusively found in OrgS and NorS samples were 78 (4.59%) and 88 (5.18%), respectively. The shared number of exclusive OTUs between OrgS and NorS were 1022 (60.19%). The shared number between OrgS and CKOrgS were 1109 (65.31%), and they dropped to 696 (41.10%) between NorS and CKNorS ( Fig 6 ).

https://doi.org/10.1371/journal.pone.0217018.g006

The relative abundance of these bacterial orders varied among the different soil samples. A comparison between OrgS and NorS showed that organic fertilizer treatment resulted in a significant increase in the relative abundance of Burkholderiales , Myxococcales , Streptomycetales , Nitrospirales , Ktedonobacterales , Acidobacteriales , Gemmatimonadales , and Solibacterales , and a decrease in Pseudonocardiales , Frankiales , Rhizobiales , and Xanthomonadales ( S1 Table and Fig 7 ). Heat map analysis of the top 20 most abundant genera within the hierarchical cluster showed clear variations in bacterial composition structure across the four groups of soil samples, and these differences were statistically significant. Treatment with chemical fertilizer resulted in increased abundance of Acidothermus , Acidicaldus , and Acidobacterium , and decreased abundance of the potentially beneficial Nitrospira and Burkholderia in comparison with the organic fertilizer treatment group. No significant differences were detected in comparisons between OrgS and CKOrgS groups, as well as between NorS and CKNorS groups ( Fig 8 ).

https://doi.org/10.1371/journal.pone.0217018.g007

https://doi.org/10.1371/journal.pone.0217018.g008

Effects of soil chemical properties on dominant genera

Redundancy analysis (RDA) was performed to study the relationship between soil chemical properties and abundance of dominant genera. The first two RDA components (RDA1 and RDA2) separated the organic fertilizer treated soils from the chemical fertilizer treated soils ( Fig 9 ). The chemical fertilizer treated samples (NorS) were positively related to the cadmium (Cd), Cuprum (Cu) and plumbum (Pb).

TP: total phosphorus, TN: total nitrogen, TK: total potassium, AN: available nitrogen, AK: available potassium, AP: available phosphorus.

https://doi.org/10.1371/journal.pone.0217018.g009

The organic fertilizer treated samples (OrgS and CKOrgS) were positively related to a higher relative abundance of Catenulispora , Candidatus_Solibacter , Burkholderia-Paraburkholderia , Gemmatirosa , Nitrospira , Rhizomicrobium and negatively related to Acidobacterium , Acidothermus and Acidicaldus . Strong associations were found among total nitrogen (TN), total phosphorus (TP), available phosphorus (AP), available nitrogen (AN), cadmium (Cd), Cuprum (Cu) and plumbum (Pb) with the abundance of Acidothermus , Acidobacterium and Acidicaldus . The abundance of Acidibacter , Catenulispora , Burkholderia-Paraburkholderia , Gemmatirosa , Nitrospira , Candidatus _ Solibacter , Rhizomicrobium and Sorangium were found to be highly associated with soil pH.

For centuries, the use of organic fertilizer is a common practice to maintain soil fertility and crop yield in China [ 26 – 27 ]. With increased availability of chemical fertilizers since the late 1970s and rise of labor costs since the 1980s, the utilization of organic fertilizer has dramatically declined [ 26 , 28 ]. In order to prevent food shortage worldwide and maximize crop yield, large amounts of chemical fertilizers have been applied to arable fields over the past few decades [ 29 – 30 ]. However, excessive use of chemical fertilizers has led to several issues such as serious soil degradation, nitrogen leaching, soil compaction, reduction in soil organic matter, and loss of soil carbon. In addition, the efficacy of chemical fertilizers on crop yield has been decreasing over time [ 29 , 31 – 32 ]. Because of these concerns, there is a growing demand for development of organic agriculture. In this study, we found that N, P and K contents were not significantly different between organic and chemical fertilizer treatments. These results indicated that organic fertilizers provide similar nutrient elements as chemical fertilizer. In recent years, soil acidification has become a serious problem for modern agriculture in China [ 33 ]. The major cause of rising soil acidity is increased use of acidifying nitrogen fertilizers or incomplete cycling of nitrogen species in the soil [ 33 – 34 ]. Our previous studies have found tea orchards soil pH, tea amino acids, and phenolic compounds significantly decreased with increasing years of monoculturing [ 1 , 5 ]. Furthermore, our data showed that organic fertilizer treatment improved soil pH, and increased the contents of tea polyphenols and amino acids. It is well known that acidification can increase the mobility of heavy metals into the soil where they could be taken up by plants [ 35 – 36 ]. The RDA analysis showed the some acidic microbes were highly associated with heavy metals. Previous studies have verified the heavy metal polluted soil would affect the microbial community structure, microbial biomass and microbial residues [ 37 – 39 ]. Some specific microorganism have the ability to adsorb heavy metal [ 40 – 41 ]. We found that the contents of heavy metals (Cu, Pb, Cd, As) were lower in soil and plant samples under organic fertilizer treatment compared to those treated with chemical fertilizer. The future research should focus the potential mechanism of intrinsic linkages between microbial community and heavy metal under the organic fertilizer treatments.

Healthy and asymptomatic plants in nature are colonized by a rich diversity of microbes, with the complex plant-associated microbial community referred to as a second genome of the plant because of its effect on plant growth and productivity [ 42 – 43 ]. In this study, we found that the long-term use of organic fertilizer significantly increased the bacterial diversity in terms of species richness. Our data are in agreement with the findings of Sun et al. [ 29 ], who reported that the NPK chemical fertilizers caused a significant decrease in bacterial diversity. Significant differences in soil bacterial composition were also observed in tea orchards under long-term treatment with chemical or organic fertilizers. The most abundantly identified bacteria phyla were assigned to the Actinobacteria , Chloroflexi , Proteobacteria , and Acidobacteria phyla. Similar results were observed with long-term continuous cropping tea orchard systems [ 5 , 44 ]. Further analysis showed that Acidothermus , Acidobacterium and Acidicaldus , increased significantly in soil samples treated with chemical fertilizer, which are acidophilic and capable of proliferating in an acidic environment. In our RDA analysis, Acidibacter were found to be highly associated with soil pH. It has been well documented that soil pH has a marked influence on the composition of the microbial community [ 45 ]. Our previous study have shown the plant–microbe interactions contribute to the increased acidity and create a new environment to mediate changes in the microbial community structure in the R . pseudostellariae rhizosphere under continuous monoculture regimes [ 46 ]. We speculate that long-term application of chemical fertilizers decreased soil pH, promoted the proliferation of some specific microbes and activated the heavy metal ions in soil, further deteriorated the physicochemical properties and quality of tea. However, the long-term application of organic fertilizer was able to alleviate some of this negative effect.

Positive plant-soil feedback depends on beneficial interactions between plant roots and microorganisms for growth promotion, nutrient acquisition and disease suppression [ 4 ]. Previous studies reported that increasing years of consecutive monoculturing resulted in a significant increase in abundance of pathogens and a decrease in beneficial microorganisms in the rhizosphere of plants [ 47 – 48 ]. The significant decrease in beneficial plant bacteria was also observed in the rhizosphere soil of continuously monocultured tea [ 5 ]. In this study, the relative abundance of Burkholderia , Nitrospira , and Streptomycetales was significantly higher with organic fertilizer treatment. Previous studies have found that Burkholderia was able to inhibit the growth of pathogens and in effect acted as a Bio-organic fertilizer to improve plant growth [ 49 – 50 ]. Nitrospira is a ubiquitous bacterium that has a role in the nitrogen cycle by performing nitrite oxidation in the second step of nitrification [ 51 – 52 ]. Furthermore, Streptomycetales can act as PGPR (rhizosphere growth-promoting bacteria) to reduce plant disease and are associated with plant disease suppression in many soils [ 53 – 54 ]. These results suggested that organic fertilizer could improve the soil environment to create a new condition for the growth of potentially beneficial microbes.

In conclusion, long-term application of organic fertilizer treatment will improve the rhizosphere environment in tea orchards. And the organic fertilizer improved tea quality and decreased the level of heavy metals in rhizosphere soil. Furthermore, soil pH and shift in microbiomes were related to fertilizers treatments. Our findings suggest that organic fertilizer can shape microbial composition and recruit beneficial bacteria into the rhizosphere of tea. These results provide a promising strategy to tea orchards by treatment with organic fertilizers.

Supporting information

S1 table. relative abundance of the bacterial order among the different samples..

https://doi.org/10.1371/journal.pone.0217018.s001

S1 Fig. The relative abundance of the bacterial phylum in the four different soil samples.

https://doi.org/10.1371/journal.pone.0217018.s002

Acknowledgments

This work was supported by by the National Natural Science Foundation of China (No. 31701329, 81573530), Fujian-Taiwan Joint Innovative Center for Germplasm Resources and Cultivation of Crop (Fujian 2011 Program, No.2015-75, China), the Natural Science Foundation of Fujian Province (No. 2016J01100), and the Project Funded by China Postdoral Science Foundation (No. 2015M580560).

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• 18. Bao SD. Soil and Agricultural Chemistry Analysis, second ed. Beijing: China Agriculture Press. 2000; 263–270.
• 19. Pansu M, Gautheyrou J. Handbook of Soil Analysis: Mineralogical, Organic and Inorganic Methods. Berlin: Springer. 2006; 3–13

Phosphate solubilization potential of PSB: an advance approach to enhance phosphorous availability for phytostimulation

• Research Article
• Published: 11 September 2024

Cite this article

• Aqsa Tariq 1 &
• Ambreen Ahmed 1  

Rhizosphere engineering approach is considered a quantum leap in plant sciences. The current study focused on investigating rhizobacterial efficiency to mobilize bioavailable phosphate from insoluble-phosphate source. Four efficient phosphate-solubilizing bacterial isolates, i.e., Pseudomonas songnenensis (GR3), Stutzerimonas stutzeri (HH2), Bacillus bingmayongensis (KH3), and Achromobacter aegrifaciens (MH1) were selected for the current study. Interactions between various physiological parameters and phosphate solubilization efficiency of isolates revealed that glucose significantly facilitated phosphorus solubilization at 37 ℃, with media having pH 7 and 0.5% phosphorous. Additionally, positive correlation among P-solubilization potential, acids produced, and pH was observed. Plant microbe-interaction analysis was performed to evaluate the efficiency of these bacterial isolates on various morpho-physiological responses of Zea mays L. For this purpose, various concentrations of tricalcium phosphate (TCP) (0, 10, 20, 30, 40, and 50 mM) were applied to plants in the presence and absence of bacterial isolates. The results showed that lower phosphate levels (10 and 20 mM) trigger shoot development and improve plant weight and leaf formation whereas higher phosphate concentrations (30 mM and above) stimulated the development of longer root system. The bacterial isolates, KH3 and HH2, were observed as efficient phosphate-solubilizing bacteria (PSB) that positively stimulated various plant growth and biochemical attributes over untreated plants. At lower phosphate levels, substantial increase of 92, 65, and 200% in shoot length, fresh weight, and number of leaves was recorded with bacterial isolate HH2, whereas, at 30 mM TCP, increase of 165% was observed in root length of plants treated with bacterial isolate KH3 compared to control. Similarly, at lower phosphate levels, increment of 57.3, 76.7, and 217% in phosphate, protein, and auxin content was recorded in plants treated with bacterial isolate HH2, and increase of 188.8% in total soluble carbohydrates was observed in plants treated with bacterial isolate KH3 as compared to control. Contrarily, increment in total chlorophyll content was most substantial (207%) by the bacterial isolate KH3 when provided with 30 mM TCP. Hence, the current study reviled that the use of these phosphates (KH3 and HH2)-solubilizing PGPR, as an efficient phytostimulator used for crop production in the replacement of chemical fertilizers, is carcinogenic and deteriorating our eco-system.

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Adebayo AA, Faleye TOC, Adeosun OM, Alhaji IA, Egbe NE (2023) Plant growth promoting potentials of novel phosphate-solubilizing bacteria isolated from rumen content of White Fulani cattle, indigenous to Nigeria. Biol Plant 78(6):201–215. https://doi.org/10.1007/s11756-022-01227-z

Article   CAS   Google Scholar  

Adnan M, Zahir S, Fahad S, Arif M, Mukhtar A, Imtiaz AK, Ishaq AM, Abdul B, Hidayat U, Muhammad A, Inayat-Ur R, Saud S, Muhammad ZI, Yousaf J, Amanullah HMH, Wajid N (2018) Phosphate-solubilizing bacteria nullify the antagonistic effect of soil calcification on bioavailability of phosphorus in alkaline soils. Sci Rep 8:4339. https://doi.org/10.1038/s41598-018-22653-7

Adnan M, Fahad S, Khan IA, Saeed M, Ihsan MZ, Saud S, Riaz M, Wang D, Wu C (2019) Integration of poultry manure and phosphate solubilizing bacteria improved availability of Ca bound P in calcareous soils. 3 Biotech 9(10):368. https://doi.org/10.1007/s13205-019-1894-2

Article   Google Scholar  

Adnan M, Fahad S, Muhammad Z, Shahen S, Ishaq AM, Subhan D, Zafar-ul-Hye M, Martin LB, Raja MMN, Beena S, Saud S, Imran A, Zhen Y, Martin B, Jiri H, Rahul D (2020) Coupling phosphate-solubilizing bacteria with phosphorus supplements improve maize phosphorus acquisition and growth under lime induced salinity stress. Plants 9(7):900. https://doi.org/10.3390/plants9070900

Adnan M, Fahad S, Saleem MH, Ali B, Mussart M, Ullah R, Marc RA (2022) Comparative efficacy of phosphorous supplements with phosphate solubilizing bacteria for optimizing wheat yield in calcareous soils. Sci Rep 12(1):11997. https://doi.org/10.1038/s41598-022-16035-3

Ahmed A, Hasnain S (2020) Extraction and evaluation of indole acetic acid from indigenous auxin-producing rhizosphere bacteria. JAPS: J Anim Plant Sci 30(4):1024–1036. https://doi.org/10.36899/JAPS.2020.4.0117

Ait-Ouakrim EH, Chakhchar A, El Modafar C, Douira A, Amir S, Bnsouda-Koraichi S, Filali-Maltouf A (2023) Valorization of Moroccan phosphate sludge through isolation and characterization of phosphate solubilizing bacteria and assessment of their growth promotion effect on Phaseolus vulgaris. Waste Weight Valor 14(8):2673–2690. https://doi.org/10.1007/s12649-023-02054-2

Bargaz A, Elhaissoufi W, Khourchi S, Benmrid B, Borden KA, Rchiad Z (2021) Benefits of phosphate solubilizing bacteria on belowground crop performance for improved crop acquisition of phosphorus. Microbiol Res 252:126842. https://doi.org/10.1016/j.micres.2021.126842

Blanco-Vargas A, Rodríguez-Gacha LM, Sánchez-Castro N, Garzón-Jaramillo R, Pedroza-Camacho LD, Poutou-Piñales RA, Pedroza-Rodríguez AM (2020) Phosphate-solubilizing Pseudomonas sp., and Serratia sp., co-culture for Allium cepa L. growth promotion. Heliyon 6(10):e05218. https://doi.org/10.1016/j.heliyon.2020.e05218

Borden KA, Mafa-Attoye TG, Dunfield KE, Thevathasan NV, Gordon AM, Isaac ME (2021) Root functional trait and soil microbial coordination: implications for soil respiration in Riparian agroecosystems. Front Plant Sci 12:1–12. https://doi.org/10.3389/FPLS.2021.681113

Bradstreet RB (1954) Kjeldahl method for organic nitrogen. Anal Chem 26(1):185–187. https://doi.org/10.1021/ac60085a028

DuBois M, Gilles K, Hamilton J, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356. https://doi.org/10.1021/ac60111a017

Etesami H (2020) Enhanced phosphorus fertilizer use efficiency with microorganisms. In: Meena R (ed) Nutrient dynamics for sustainable crop production. Springer, Singapore, pp 215–245. https://doi.org/10.1007/978-981-13-8660-2_8

Chapter   Google Scholar  

Flatian AN, Anas I, Sutandi A (2021) The ability of some microbes to solubilize the hardly soluble phosphorous and potassium from various sources in vitro. In : IOP Conference Series: Earth Environ Sci IOP Publishing 648(1):012143. https://doi.org/10.1088/1755-1315/648/1/012143

Habib S, Ahmed A (2022) Expression profiling of stress protectants in Zea mays L. plants treated with Bacillus pumilus : surfactant-producing bioeffector. Int J Environ Sci Technol 20:4435–4446. https://doi.org/10.1007/s13762-022-04089-9

Hii YS, San CY, Lau SW, Danquah MK (2020) Isolation and characterisation of phosphate solubilizing microorganisms from peat. Biocatal Agric Biotechnol 26:101643. https://doi.org/10.1016/j.bcab.2020.101643

Iqbal M, Naveed M, Sanaullah M, Brtnicky M, Hussain MI, Kucerik J, Holatko J, Mustafa A (2023) Plant microbe mediated enhancement in growth and yield of canola ( Brassica napus L.) plant through auxin production and increased nutrient acquisition. J Soils Sediments 23(3):1233–1249. https://doi.org/10.1007/s11368-022-03386-7

Jain R, Bhardwaj P, Guleria S, Pandey A, Kumar S (2023) Polyamine metabolizing rhizobacteria Pseudomonas sp. GBPI_506 modulates hormone signaling to enhance lateral roots and nicotine biosynthesis in Nicotiana benthamiana . Plant Physiol Biochem 195:193–205. https://doi.org/10.1016/j.plaphy.2023.01.010

Kaur C, Selvakumar G, Upreti KK (2021) Organic acid profiles of phosphate solubilizing bacterial isolates in the presence of different insoluble phosphatic sources under. J Pure Appl Microbiol 15(2):1006–1016. https://doi.org/10.22207/JPAM.15.2.59

Khan H, Akbar WA, Shah Z, Rahim HU, Taj A, Alatalo JM (2022) Coupling phosphate-solubilizing bacteria (PSB) with inorganic phosphorus fertilizer improves mungbean ( Vigna radiata ) phosphorus acquisition, nitrogen fixation, and yield in alkaline-calcareous soil. Heliyon 8(3):e09081. https://doi.org/10.1016/j.heliyon.2022.e09081

Kirui CK, Njeru EM, Runo S (2022) Diversity and phosphate solubilization efficiency of phosphate solubilizing bacteria isolated from semi-arid agroecosystems of Eastern Kenya. Microbiol Insights 15:11786361221088992. https://doi.org/10.1177/11786361221088991

Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in diferent solvents. Biochem Soc Trans 11(5):591–592. https://doi.org/10.1042/bst0110591

Liu D (2021) Root developmental responses to phosphorus nutrition. J Integr Plant Biol 63(6):1065–1090. https://doi.org/10.1111/jipb.13090

Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275. https://doi.org/10.1016/S0021-9258(19)52451-6

Lu J, Liu S, Chen W, Meng J (2023) Study on the mechanism of biochar affecting the effectiveness of phosphate solubilizing bacteria. World J Microbiol Biotechnol 39(3):87. https://doi.org/10.1007/s11274-023-03533-3

Mahadevan A (1984) AGRIS. In: Growth regulators, microorganisms and diseased plants, vol 31. Oxford and IBH Publishing Company, India, pp 363–460

Mohamadpoor M, Amini J, Ashengroph M, Azizi A (2022) Evaluation of biocontrol potential of Achromobacter xylosoxidans isolate CTA8689 against common bean root rot. Physiol Mol Plant Pathol 117:101769. https://doi.org/10.1016/j.pmpp.2021.101769

Moradali MF, Rehm BHA (2020) Bacterial biopolymers: from pathogenesis to advanced materials. Nat Rev Microbiol 18:195–210. https://doi.org/10.1038/s41579-019-0313-3

Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36. https://doi.org/10.1016/S0003-2670(00)88444-5

Nacoon S, Seemakram W, Ekprasert J, Jogloy S, Kuyper TW, Mongkolthanaruk W, Riddech N, Somdee T, Boonlue S (2022) Promoting growth and production of sunchoke (Helianthus tuberosus) by co-inoculation with phosphate solubilizing bacteria and arbuscular mycorrhizal fungi under drought. Front Plant Sci 13:1022319. https://doi.org/10.3389/fpls.2022.1022319

Naureen Z, Sham A, Al Ashram H, Gilani SA, Al Gheilani S, Mabood F, AbuQamar SF (2018) Effect of phosphate nutrition on growth, physiology and phosphate transporter expression of cucumber seedlings. Plant Physiol Biochem 127:211–222. https://doi.org/10.1016/j.plaphy.2018.03.028

Pantoja-Guerra M, Valero-Valero N, Ramírez CA (2023) Total auxin level in the soil–plant system as a modulating factor for the effectiveness of PGPR inocula: a review. Chem Biol Technol Agric 10(1):6. https://doi.org/10.1186/s40538-022-00370-8

Pathania P, Rajta A, Singh PC, Bhatia R (2020) Role of plant growth-promoting bacteria in sustainable agriculture. Biocatal Agric Biotech 30:101842. https://doi.org/10.1016/j.bcab.2020.101842

Pohan SD, Silaban LM, Amrizal A, Puspitasari WD, Masni E (2019) The induction of root nodule and increasing of nitrogen content of common bean ( Phaseolus vulgaris L.) by using Rhizobium plus fertilizer. In Proceedings SATREPS Conference 1 2(1):129–136

Romero-Perdomo F, Beltrán I, Mendoza-Labrador J, Estrada-Bonilla G, Bonilla R (2021) Phosphorus nutrition and growth of cotton plants inoculated with growth-promoting bacteria under low phosphate availability. Front Sustain Food Syst 4:618425. https://doi.org/10.3389/fsufs.2020.618425

Samal DK, Sukla LB (2022) Isolation and characterization of phosphate-solubilizing bacteria from rice field of Odisha and their growth promoting effect on agricultural-sectors. Geomicrobiol J 40(2):152–160. https://doi.org/10.1080/01490451.2022.2129882

Sanchez-Gonzalez ME, Mora-Herrera ME, Wong-Villarreal A, De La Portilla-López N, Sanchez-Paz L, Lugo J, Yañez-Ocampo G (2022) Effect of pH and carbon source on phosphate solubilization by bacterial isolates in Pikovskaya medium. Microorganisms 11(1):49. https://doi.org/10.3390/microorganisms11010049

Santana MM, Rosa AP, Zamarreño AM, García-Mina JM, Rai A, Cruz C (2022) Achromobacter xylosoxidans and Enteromorpha intestinalis extract improve tomato growth under salt stress. Agronomy 12(4):934. https://doi.org/10.3390/agronomy12040934

Shirmohammadi E, Alikhani HA, Pourbabaei AA, Etesami H (2020) Improved phosphorus (P) uptake and yield of wheat fed with P fertilizer by drought tolerant phosphate–solubilizing fluorescent pseudomonads isolates: a field study in drylands. Soil Sci Plant Nutr 20:2195–2211. https://doi.org/10.1007/s42729-020-00287-x

Suleman M, Yasmin S, Rasul M, Yahya M, Atta BM, Mirza MS (2018) Phosphate solubilizing bacteria with glucose dehydrogenase gene for phosphorus uptake and beneficial effects on wheat. PLoS One 13(9):e0204408. https://doi.org/10.1371/journal.pone.0204408

Sun N, Huang L, Zhao H, Zhang N, Lin X, Sun C (2022) Beneficial bacterium Azospirillum brasilense induces morphological, physiological and molecular adaptation to phosphorus deficiency in Arabidopsis . PCP 63(9):1273–1284. https://doi.org/10.1093/pcp/pcac101

Tan Z, Yang X, Gao J, Li Y, Gong B (2022) The mechanism of phosphate solubilizing of Pseudomonas sp. TC952 and its solubilizing process on TC removal. Environ Sci Pollut Res 30(10):26234–26243. https://doi.org/10.1007/s11356-022-23847-3

Tariq A, Ahmed A (2022b) Auxins interkingdom signaling molecules. In: Hano C (ed) Plant hormones: recent advances, new perspectives and applications. IntechOpen, London

Google Scholar  

Tariq A, Ahmed A (2022a) Phosphate solubilizing Rhizobacteria as sustainable management strategy in agrobiology. In: Suratman MN, Azlin E Ariff RE (eds), Sustainable management of natural resources. IntechOpen. https://doi.org/10.5772/intechopen.108657

Wagi S, Ahmed A (2019) Bacillus spp.: potent microfactories of bacterial IAA. PeerJ 7:e7258. https://doi.org/10.7717/peerj.7258

Wang Y, Wang S, Yan X, Gao S, Man T, Yang Z, Wang P (2022) Preparation of liquid bacteria fertilizer with phosphate-solubilizing bacteria cultured by food wastewater and the promotion on the soil fertility and plants weight. J Clean Prod 370:133328. https://doi.org/10.1016/j.jclepro.2022.133328

Wu F, Li J, Chen Y, Zhang L, Zhang Y, Wang S, Liang J (2019) Effects of phosphate solubilizing bacteria on the growth, photosynthesis, and nutrient uptake of Camellia oleifera Abel. Forests 10(4):348. https://doi.org/10.3390/f10040348

Wu Y, Lu Q, Gong Y, Zhang Y, Xu Y, Cai M, Zhang Q (2023) Optimizing nitrogen, phosphorus, and potassium fertilization levels for container plants of Lagerstroemia Indica ‘Whit III’based on the comprehensive quality evaluation. HortScience 58(2):222–230. https://doi.org/10.21273/HORTSCI16980-22

Wu Q, Wan W (2023) Insight into application of phosphate-solubilizing bacteria promoting phosphorus availability during chicken manure composting. Bioresour Technol 128707. https://doi.org/10.1016/j.biortech.2023.128707

Yadava P, Dayaman V, Agarwal A, Kumar K, Singh I, Verma R, Kaul T (2022) Fine-tuning the transcriptional regulatory model of adaptation response to phosphate stress in maize ( Zea mays L.). Physiol Mol Biol Plants 28(4):885–898. https://doi.org/10.1007/s12298-022-01155-x

Zeng Q, Wu X, Wang J, Ding X (2017) Phosphate solubilization and gene expression of phosphate-solubilizing bacterium Burkholderia multivorans WS-FJ9 under different levels of soluble phosphate. J Microbiol Biotechnol 27(4):844–855. https://doi.org/10.4014/jmb.1611.11057

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Acknowledgements

University of the Punjab, Quaid-e-Azam Campus, Lahore, Pakistan, is gratefully acknowledged for the accomplishment of the current research study.

The present study was funded by University of the Punjab, Quaid-e-Azam Campus, Lahore 54590, Pakistan.

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AA and AT contributed to conceptualization of study; AA contributed to the formal analysis, investigation, funding acquisition, resources, and supervision. AT provided methodology and performed writing—original draft preparation, and writing—review and editing.

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Tariq, A., Ahmed, A. Phosphate solubilization potential of PSB: an advance approach to enhance phosphorous availability for phytostimulation. Environ Sci Pollut Res (2024). https://doi.org/10.1007/s11356-024-34934-y

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Received : 06 November 2023

Accepted : 04 September 2024

Published : 11 September 2024

DOI : https://doi.org/10.1007/s11356-024-34934-y

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