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Review

A Bibliometric Review of Plant Growth-Promoting Rhizobacteria in Salt-Affected Soils

by
Xixi Ma
1,2,3,
Jing Pan
1,3,
Xian Xue
1,3,*,
Jun Zhang
4 and
Qi Guo
4
1
Key Laboratory of Desert and Desertification, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou 730000, China
2
College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100049, China
3
Drylands Salinization Research Station, Key Laboratory of Desert and Desertification, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou 730000, China
4
Institute of Biology, Gansu Academy of Sciences, Lanzhou 730000, China
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(10), 2304; https://doi.org/10.3390/agronomy12102304
Submission received: 31 August 2022 / Revised: 17 September 2022 / Accepted: 22 September 2022 / Published: 26 September 2022
(This article belongs to the Topic Plant Responses and Tolerance to Salinity Stress)
Browse Figures
Versions Notes

Abstract

:
As a primary form of land degradation in arid and semi-arid areas, soil salinity can adversely affect plant nutrient balance, photosynthesis, protein synthesis, energy metabolism, and other functions. Plant growth-promoting rhizobacteria (PGPR) inoculation of plants is an environmentally friendly strategy to alleviate salt stress and improve salt tolerance. Based on the Web of Science Core Collection (WoSCC) database, in terms of the number of publications and citations, collaboration networks, and keywords, this bibliometric analysis employed VOSviewer 1.6.17 and HistCite Pro 2.1 software to map the scientific knowledge of related research, comprehensively review knowledge structure and provide an outlook on future research topics. The results showed that publications and citations increased exponentially between 1978 and 2021. Regarding knowledge structure, Asian nations conducted research in a more concentrated manner, developed close collaborative relationships, and produced rich research results. Halotolerant PGPR, sustainable agriculture, microbial community, soil salinization, microbiome, oxidative stress, and biofertilizer, are currently hot topics. This bibliometric study will provide a meaningful reference for investigating the field’s evolution and pinpointing the research frontiers.

1. Introduction

Plants growing in natural environments are often prevented from expressing their full genetic potential for reproduction and are considered “stressed” [1]. Salinity is one of the significant abiotic stresses limiting plant growth and crop yield in arid and semi-arid regions [1,2]. Secondary salinization of soils is becoming more and more prominent due to human activities such as global population growth, excessive agricultural fertilization, and improper irrigation practices. According to data from the Food and Agriculture Organization of the United Nations (FAO) on 21 October 2021, saline soils cover more than 833 million hectares worldwide (8.7% of the earth’s surface area), most of which are located in arid or semi-arid zones in Africa, Asia, and Latin America. It was estimated that around 20 to 50 percent of irrigated lands worldwide are salt-affected [3]. The area of salt-affected soils continues to increase at a rate of 10% per year [4]. Excessive soluble salts in soils disrupt plant growth and have already reduced yields of major cereal crops by 70% [5], posing a threat to global food security. As highlighted in the 2018 Global Agricultural Productivity (GAP) Index, the current growth rate of agricultural output is not enough to meet the projected food demand of 10 billion people in 2050 [6].
Part of the salinized land has been utilized through appropriate soil amelioration treatments, such as engineering, physical, chemical, and plant treatments [7]. However, there are lots of limitations. For example, engineering treatments require favorable irrigation and drainage conditions, physical measures such as salt flushing are difficult in areas with low precipitation, and adding chemical amendments is very costly and only a short-term solution to overcome salinization [2,8,9]. Improving the salt tolerance of plants is also one of the strategies for utilizing saline lands. The use of transgenic technology to enhance salt tolerance in plants has been carried out worldwide. Still, some controversy exists. Whether salinity activates specialized genes involved in salt stress remains uncertain [2,10,11]. Manchanda and Garg concluded that salt tolerance does not appear to be conferred by unique genes [12]. Therefore, the application of transgenic technology in mitigating salt stress in plants has had limited success. One of the most promising methods is employing plant growth-promoting microorganisms to promote stress tolerance and growth [13,14,15]. Among plant growth-promoting microorganisms, plant growth-promoting rhizobacteria (PGPR) are of great importance because of their direct association with plant roots. The definition of PGPR was introduced in 1978 [16]. Before the 1980s, several compounds secreted by PGPR, such as iron-chelating siderophores, antibiotics, and hydrogen cyanide, had been identified to compete for energy-yielding nutrients, induce plant resistance and mineralize soil nutrients, thus inhibiting soilborne plant pathogens and promoting plant growth [17,18,19]. Since the 1990s, research on the role of PGPR in mitigating salt stress and promoting plant growth has been widely conducted [20,21]. It has been demonstrated that PGPR can alter various biochemical processes in host plants through various pathways such as the production of 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase, phytohormones, and antibiotics, as well as nitrogen fixation and phosphorus solubilization, thus enhancing salt tolerance of plants [22,23,24].
PGPR’s potential for agricultural applications has been partially proven. Nevertheless, the rapidly increasing number of publications makes it more and more difficult for researchers to keep up with the latest findings. Although several reviews and meta-analyses surrounding this topic could offer researchers basic information and innovative guidance, a systematic analysis of this literature has been lacking so far. The measurement system of bibliometrics provides various qualitative and quantitative indicators of scientific and technological achievements [25,26,27]. These indicators, such as the number of publications, the collaboration network, and the prediction of future research hotspots, are essential for sorting out the development of the field and grasping the future research direction. This bibliometric analysis, employing VOSviewer 1.6.17 (Eck and Waltman, Centre for Science and Technology Studies, Leiden University, the Netherlands), and HistCite Pro 2.1 (Qing Wang, University of Science and Technology of China), in terms of the number of publications, country, and author collaboration networks, and keyword co-occurrences, examines global research trends and provides a preliminary discussion of research limitations and future research hotspots. This study aims to establish an essential reference and perspective for using PGPR to alleviate plant salt stress, enhance plant salt tolerance, and effectively exploit salt-affected soils.

2. Materials and Methods

2.1. Data Source and Search Strategy

To complete data retrieval, we searched the Web of Science Core Collection: Science Citation Index Expanded (WoSCC: SCI-EXPANDED). The search strategy was: “TS = (PGPR OR Plant Growth-Promoting Rhizobacteri* OR PGPB OR plant growth-promoting bacteri* OR rhizosphere bacteri* OR rhizobacteri*) AND TS = (salt stress OR salinity stress)”. After selecting published journal articles, excluding irrelevant literature, and removing duplicates, 875 valid documents were obtained as the final dataset and exported as “full record and cited references” for further analysis. (Figure 1).

2.2. Data Extraction

By using the “analyze search results” and “create citation report” functions in WoS, we obtained the number of publications (NP), number of citations (NC), h–index, and average citations per item (ACI). The growth rate of publications over time was calculated with the following formula [28]:
(NPlast year/NPfirst year)1/(last year − first year) − 1) × 100
Local citation score (LCS) and local cited references (LCR) were proposed and designed as the fundamental bibliometric indicators [29,30]. The LCS of a publication is the number of times it is cited in the local database (the selected database of bibliometric analysis), and the higher the LCS of a publication implies its greater importance and higher recognition by peers. The LCR of a publication refers to the number of references in the local database, and the higher the LCR of an article, the more likely it is to be a review article.

2.3. Data Analysis and Knowledge Mapping

This study used Origin2021a (OriginLab Corporation, Northampton, MA, USA), SPSSAU 22.0 (QingSi Technology Ltd, Beijing, China), and ArcGIS 10.2 (Environmental Systems Research Institute, Inc., Redlands, CA, USA) for data analysis and graphing. Bibliometric and visualization analyses were conducted by two bibliometric tools, VOSviewer 1.6.17 and HistCite Pro 2.1. The VOSviewer 1.6.17 was used to identify co-authors’ countries, author co-citations, and keyword co-occurrence. Mapping of country and author collaboration can provide information on the geographical distribution (macro-scale) and significant academic forces (micro-scale) of relevant research, guiding in finding disciplinary leaders, knowledge borrowing, and teamwork. Keyword co-occurrence mapping allows quick capture of hot and foreword topics in the field [28,31,32]. HistCite Pro 2.1 was used to map the literature citation network. A literature citation network can quickly pinpoint critical literature from different periods, which is conducive to a preliminary understanding of the field’s evolution [30].

3. Results

3.1. Number of Publications and Citations

After the literature screening mentioned above, 875 publications, including 832 original articles and 43 reviews, were included in the final analysis. Annual publications and citations are shown in Figure 2. The earliest year of publication is 1995. Despite decreasing at some years, NP and NC increase significantly in an exponential form with R2 of 0.9757 and 0.9914, respectively. Two critical points are in 2003 and 2013. From 1995 to 2003, the first stage, the field developed more slowly, and the average annual NP was less than 3; the TNC was 176, and the average annual NC was about 19.56. From 2004 to 2013, in the second phase, NP and NC increased steadily, with an average annual NP of about 14.7 and a growth rate of 16.10%; TNC was 2103, and the average annual NC was about 210.30. The third phase of the field evolution after 2014. During this period, NP and NC increased dramatically, with an average annual NP of almost 88.625, a growth rate of 25.51%, a TNC of 20,055, and an average annual NC of about 2506.88.

3.2. Knowledge Structures

3.2.1. Most Productive Regions/Countries

A world map depicting the contribution of each country is shown in Figure 3A. Although we collected only 875 publications, the number of relevant study participants counted was 1316 because of the inter-regional/inter-country collaboration. Most of the research on PGPR to increase salt tolerance in plants has been widely conducted in Asia, Europe, and North America, which account for 88.30% of NP worldwide. Asian countries, participating in 770 studies, accounting for 58.51% of the global NP, are the regions where research is concentrated and active. Europe, North America, and Africa account for 20.13%, 9.65%, and 6.07% of the global NP, respectively. Australian and South American states contribute no more than 6% of the global NP. Analysis of the countries involved in the publication of the literature reveals that the top three countries, in terms of NP, are India (NP = 181, 20.69%), China (NP = 160, 17.60%), and Pakistan (NP = 131, 14.97%), accounting for 53.26% of the total NP. In contrast, the remaining countries have NP of less than 100 (Figure 3A).
Among the top 20 countries, NP is a significantly positive correlation with their corresponding h–index (r = 0.920, p < 0.05), but not with ACI (r = 0.056, p = 0.816) (Figure 3B). The ACI of India, China, and Pakistan are 32.82, 21.55, and 31.51, respectively, which are far lower than some European and American countries such as Canada (89.03), Germany (52.37), and the UK (58.8). Therefore, Asian countries should emphasize the overall quality of publications.

3.2.2. Most Influential Researchers

There are over 3000 researchers involved in this field of study. Among them, Z.A. Zahir from the University of Agriculture Faisalabad in Pakistan is the most productive contributor, participating in and publishing 25 significant publications from 1995 to 2021. A. Bano from Integral University in India, and B.R. Glick from the University of Waterloo in Canada contributed 22 publications. I.J. Lee from Kyungpook National University in South Korea ranks third with 17 publications. Z.A. Zahir (18) has the highest h–index, followed by B.R. Glick (15), I.J. Lee (13), and D. Egamberdieva (13). Nevertheless, considering the ACI, B.R. Glick (91.23) is the highest, followed by D. Egamberdieva, with an ACI of 71.56; Z.A. Zahir ranks third with an ACI of 55.48 (Figure 4). The weights of NP, h–index and ACI were calculated utilizing AHP hierarchical analysis [33] and were 24.39%, 16.64%, and 58.97%, respectively. Hence, we obtained a comprehensive score from scientists. The result showed that B.R. Glick scores 61.66 and ranks first, followed by D. Egamberdieva (48.27), Z.A. Zahir (41.81), and I.J. Lee (25.11).

3.2.3. Network of Collaboration

Although China and Saudi Arabia initiated their research relatively late, China exhibited the strongest total link strength, followed by Pakistan, Saudi Arabia, the United States, and India, in that order. The strongest collaborative relationships were between China and Pakistan, India and Korea, and Saudi Arabia, indicating extensive cooperation among Asian countries in this field in the past five years (Figure 5A). Collaborative mapping of the authors shows two larger research groups and two smaller ones (Figure 5B), with fewer associations between the distinct groups. Each research group is centered on several authors. For example, the largest group consisted of 11 contributors. In this group, I.J. Lee, M.A. Khan, S.M. Kang, and S. Asaf had a total link strength of more than 50 and were also the top four contributors. M.A. Khan and Khan, S.M. both belong to the workgroup of Prof. I.J. Lee of Kyungpook National University (Republic of Korea). In this dataset, M.A. Khan has the highest total link strength of 62. However, this group is a late entry into the field, with the earliest entry being the group of Prof. Z.A. Zahir from the University of Agriculture Faisalabad (Pakistan) (Figure 5B). Z.A. Zahir is the core author in the second primary cluster with a total link strength of 46, and his team members S.M. Nadeem, M. Naveed, and M. Arshad have a total link strength of 24, 24, and 23, respectively.

3.3. Review and Hot Topics

3.3.1. Highly-Cited Publications

Based on the LCS, the 875 literature records were ordered, and then the top 30 records were picked to map the citation network. Each box represents a publication. The number in the box is the ordinal number of the publication in the current database, and the size of the box is proportional to the LCS of the corresponding publication. The arrows between boxes show the citation connections between publications, and the arrows point to the cited literature. The number of node linkages is 98, and the LCS is between 29 and 174. Thirty papers published between 1997 and 2018 represent the principal evolution in the PGPR-mediated salinity tolerance in plants.
Before 2003, there were fewer relevant literature reports, which was in line with the slowly initiated phase delineated in the previous section. Since 2004, there has been an increasing interest in the relevant literature. Prominent literature chains 10-43-46-67-107, 27-46-67-107, and 28-49-67-98 occurred between 2004 and 2013, which correspond to the steady exploration phase delineated in the previous section (Figure 6). These publications were mostly concerned with the identification and biochemical analysis of salt-tolerant strains, specific functional PGPRs such as ACC deaminase-producing, extracellular polysaccharides, and other PGPR inoculations for the alleviation of salt stress for vegetable crops and food crops, laying a solid background for a more profound mechanistic exploration and therefore, a higher LCS. Document no. 200 had a high LCR of 30 and was a review article [34]. It was published in 2014, coinciding with the year of the onset of the third phase, the booming phase, delineated in the previous section. In this article, D. Paul and H. Lade provided a systematic discussion regarding the roles of PGPR in hormone synthesis, ACC catabolism, maintenance of ionic homeostasis, cellular osmolyte accumulation, antioxidant enzyme synthesis, and disease defense. However, the defensive mechanisms involved in the interaction of the above PGPR-regulated processes with plants were poorly explored. Document no. 391, also a review by M. Numan et al., suggested that salinity tolerance, such as osmolyte synthesis and activation of antioxidant enzyme activity, was the ability of the plant itself to develop under saline conditions and the presence of PGPR played a role in compensating for the salinity tolerance of the plant [35]. M. Numan et al., also proposed that microorganisms produce volatile organic compounds (VOCs) and N-acyl-L-homoserine lactones (AHLs) that alter gene expression in shoots and roots, thereby controlling cell growth and defense responses. In addition, some critical insights, including the expression of hormone-specific genes ion transporter protein genes, and systemic resistance genes, illustrated specific pathways of microbial-mediated salinity tolerance in plants, which, together with the systematic elaboration of nutrient assimilation processes such as iron-producing carriers, nitrogen fixation, and phosphate solubilization by strains, were essential for a profound understanding of the mechanisms and the rationalization of the utilization of specific functional strains. In general, these two reviews by D. Paul and H. Lade, and M. Numan are bridging contributions to the evolution of the interlinked field.

3.3.2. Keyword Co-Occurrence

Keywords represent the main topics and core content of a specific subject. Keyword co-occurrence is a prevalent way to identify hot research topics [28,31,36]. Figure 7 shows the keyword co-occurrence mapping using VOSviewer. The earlier keywords are shown in purple, while the more recent ones are in yellow. Earlier keywords include strains (Pseudomonas, Rhizobium, Azospirillum, Bacillus, etc.), strain characteristics (ACC deaminase, nitrogen fixation, phosphate solubilization, etc.), crops (soybean, cotton, sunflower, wheat, maize, rice, soybean, tomato), indicating that the research of different PGPR in improving salt tolerance in crops has been abundantly fruitful, both in terms of mechanism elucidation and agricultural applications. Relatively, the latest keywords are “halotolerant PGPR”, “sustainable agriculture”, “microbial community”, “soil salinization”, “microbiome”, “oxidative stress”, and “biofertilizer”, indicating that these topics are receiving increasing attention and are becoming research hotspots in the immediate future.

4. Discussion

4.1. The Effectiveness of Employing PGPR to Enhance Salt Tolerance in Plants Is Attracting Attention

Global arable land is limited, and saline soils are an essential backup resource. PGPR inoculation provides a feasible approach to cope with salt stress. The mutual collaboration between microorganisms and plants facilitates water uptake and nutrient acquisition by the roots and plays a part role in microbial activity, population diversity, and the formation of soil aggregates. Research results are published in papers, patents, reports, etc. Valuable research leads the way, gains attention and recognition, and thus stimulates more profound scientific questions. Therefore, the number of publications and citations in each period can directly reflect the trend of the discipline in a particular field [28]. NP and NC increased significantly in an exponential manner year by year. Based on the number of publications and citations, we roughly divided it into three phases (Figure 2), namely the slowly starting phase (1995~2006), the stably exploring phase (2007~2013), and the flourishing phase (2014~2021), with the years 2006 and 2013 as segmentation points. Currently, it is in a booming stage of development, with rapid growth in the number of publications and citations. The topic of PGPR inoculum to enhance salt tolerance in plants is gaining attention, and more resources (funding, scholars) are being put towards it.

4.2. Intensive Research Has Had Weak Academic Influence among Asian Countries

Most publications regarding PGPR to increase plant salt tolerance came from regions such as Asia, Europe, and North America (Figure 3A). Asia was the most active and concentrated region for conducting related research. The top five countries in terms of the number of publications were all in Asia, namely India, China, Pakistan, Korea, and Iran (Figure 3B). In our increasingly interdependent and globalized world, cross-country and inter-organizational collaboration are important ways to improve research quality and productivity [28]. For our study, the countries with the most active international cooperation were Pakistan, China, Saudi Arabia, and India, which the following facts can explain. The net changes in soil salinity/sodicity and the total area of salt-affected soils had been geographically highly variable. Nevertheless, the continents with the highest salt-affected locations were Asia (particularly China, Kazakhstan, and Iran) [37]. In the background of global warming, the intensification of persistent soil salinization was expected to threaten food production on 40% of agricultural land [24]. Scientific solutions for managing saline land productivity were urgently needed.
To avoid the bias caused by a single evaluation indicator, AHP hierarchical analysis was used to assign weights to the three indicators of NP, h–index, and ACI, respectively. Hence, we obtained a total score for each scientist’s contribution. B.R. Glick (the University of Waterloo in Canada) was in the top position, followed by D. Egamberdieva (National University of Uzbekistan). And Z.A. Zahir (the University of Agriculture Faisalabad in Pakistan) and I.J. Lee (Kyungpook National University in the Republic of Korea) ranked third and fourth, respectively. A. Bano from India was ranked 7th in terms of the total score, although it was ranked second in NP. Therefore, Asian countries must strengthen their international academic influence.

4.3. Rich Research Themes and Outstanding Research Results

By sorting out the academic connections among researchers, it can be found that several influential academics had groups with which they were closely connected, and there were also some connections among the groups which formed the principal research force in the field, such as Prof. I.J. Lee of Kyungpook National University (Republic of Korea) and Prof. Z.A. Zahir of University of Agriculture Faisalabad (Pakistan) (Figure 5B). The research subjects of Prof. I.J. Lee and Prof. Z.A. Zahir were concerned with the isolation of PGPRs (intracellular and extracellular), screening of superior biocontrol strains, and bioassay evaluation. The screening of superior biocontrol strains was based on their ability to secrete indole-3-acetic acid (IAA), dissolve phosphorus, fix nitrogen, and produce iron carriers. The bioassay assessment was that the PGPR was applied to plants affected by salt stress, thus evaluating the strain’s growth-promoting ability by measuring plant phenotype, biomass, nutrient uptake, endogenous hormone levels, osmolytes, antioxidant enzymatic and non-enzymatic substance activity, and gene expression [13,38,39,40]. Prof. I.J. Lee’s team isolated and screened a variety of PGPRs from coastal halophytes such as Arthrobacter, Microbacterium, Bacillus, and Pseudomonas to alleviate salt stress in major cash crops such as soybean and rice. The potential of PGPR as a commercial biofertilizer has been confirmed in the aspects of nutrient utilization, hormone production, antioxidant enzyme activity, and salt tolerance gene expression [40,41,42]. In response to the problem of irrational fertilizer application, M.A. Khan et al. also emphasized that combined application of inorganic fertilizers and PGPR can minimize inorganic fertilizer inputs and enhance plant resistance to biotic and abiotic stresses, and thus reduce environmental pollution [40]. In recent years, the research subjects of Prof. I.J. Lee’s research groups also covered the defense effects of plant endophytic fungi in abiotic stresses and growth-promoting characteristics of heat-tolerant bacteria inside the root system of halophytes, which made substantial contributions to the application of biological methods to increase plant stress tolerance [43,44].
Prof. Z.A. Zahir is the second largest group of central authors. Earlier, Prof. Z.A. Zahir focused on the effects of PGPR containing ACC deaminase, synergistic effects of rhizobia and PGPR on biomass and nutrient uptake of wheat, maize, and mung bean crops in salt-affected soils [45,46,47,48,49,50], providing a far-reaching guideline for the development of biofertilizers and the utilization of saline soils. Considering the lack of good quality irrigation water in arid and semi-arid areas, Prof. Z.A. Zahir investigated the response to PGPR inoculation of maize under brackish irrigation conditions and suggested that PGPR inoculation can effectively reduce the adverse effects. In addition, crops were far more salt tolerant in the late reproductive stage than in the seedling stage, thus allowing the use of higher quality water in the nutritional stage and the application of brackish water in the reproductive stage, which could result in less crop yield loss [51]. This research provided an excellent guide to sustainable crop production in areas with water scarcity and deteriorating water resources. Liquid bacterial inoculum applied to the soil under natural conditions may fail due to various environmental constraints. Prof. Z.A. Zahir was also involved in studying the differential response of PGPR solid bacterial fertilizers prepared with different properties of carrier materials to alleviate plant salt stress, suggesting that compost and digestate seem to best enhance the efficacy of PGPR in promoting plant growth under salt stress, possibly because these carrier materials provided the optimal microenvironment for PGPR to survive and maintain physiological activity [52]. It further contributed novel approaches to enhancing the quality and yield of crops. Prof. Z.A. Zahir also directed several field experiments to test the growth-promoting ability of specific strains under natural soil and climate conditions [53,54,55]. Meanwhile, to reduce the cost of fertilizer, they conducted a study on the effects of the combined application of organic fertilizers, chemical fertilizers, and PGPR on crops [54], which was a practical guide for sustainable agriculture.

4.4. Future Research Hotspots

Halotolerant PGPR, sustainable agriculture, microbial community, soil salinization, microbiome, oxidative stress, and biofertilizer, are the hot topics of research in the next period. PGPR, as biofertilizers to help mitigate abiotic stresses and improve yields in plants, is a more cost-effective and environmentally friendly alternative that could be accomplished in a relatively short period [56,57,58,59]. The strengthening of soil salinity has put more demanding requirements on the development of more effective biofertilizers using high-quality and resistant strains. Therefore, soil salinization, halotolerant PGPR, and oxidative stress continue to be hot topics of research in the future.
Inoculation methods and inoculum types affected the inoculation efficiency. Liquid inoculants were the preferred material, and seeds were the most common inoculum treatment [60]. Alternative methods of inoculation have been proposed, including in-furrow at sowing, soil surface spray, and leaf spray [61,62]. Meta-analysis results showed that leaf spray inoculation was comparable to seed treatment [63]. However, there is still little research on inoculation methods, and additional comparative experiments are needed to conclude, especially for leaf spray and in-furrow inoculation. Application of liquid inoculum to the inter-root zone could fail to promote crop growth due to various environmental constraints, such as inadvertent treatment resulting in the spread of cells into the atmosphere or groundwater and failure of liquid inoculum due to its short shelf life. Therefore, there is a need to select carriers or materials with a long shelf life and support microbial growth and delivery to the inter-root [64]. Several studies have shown the higher inoculation efficiency of solid inoculum compared to liquid inoculants, but the studies are still insufficient [52]. Identification of effective “biofertilizers” continues to be a hot research topic.
The environment can also affect the efficiency of microbial fertilizers. In arid areas, the rhizosphere of halophytes cultivates unique microbial communities, which are an effective source of biological inoculants [5,65]. In the foreseeable future, attention should also be paid to the microbiome and microbial community, which are crucial for elucidating the ecological linkages in salt-affected soil agriculture [5]. Previous studies concerning PGPR–plant interrelationships have been confined to some controlled experimental settings, such as hydroponics and potting trials, and fewer and less focused on assessing the potential of salt-tolerant microorganisms as biofertilizers in the field [66]. The challenge remains to employ PGPR more effectively in crop production. This will require further understanding of microbial and soil environment response mechanisms and plant feedback mechanisms to rhizospheric microorganisms to adopt rational approaches to conserve and maintain land, water, plant, and animal genetic resources and achieve production patterns for sustainable agriculture. Hence, sustainable agriculture is the core research outlet.

5. Conclusions

The first bibliometric analysis of studies related to PGPR to enhance plant salt tolerance from 1995 to 2021 found that microbial measures to alleviate salinity stress and improve performance for plants inhabiting salt-affected soils have gradually attracted the attention of scholars. Asian national institutions conducted more intensive research, formed specialized groups, and developed closer collaborations. National and international researchers obtained outstanding results in isolation, molecular identification, salt tolerance testing, and salt tolerance mechanisms of PGPR (intracellular and extracellular) under laboratory and field conditions. Eventually, well-performing PGPR has been screened for biological control agents. Future research will focus on the following topics: halotolerant PGPR, sustainable agriculture, microbial communities, soil salinization, microbiome, oxidative stress, and biofertilizer. In response to environmental pollution and low quality and yield of crops, it is an emerging trend to explore and enhance the functions of microorganisms, promoting the conservation and sustainable use of marginal land resources by enhancing soil quality and plant health.

Author Contributions

Conceptualization, X.M., J.P. and X.X.; methodology, X.M. and J.P.; software, X.M.; formal analysis, X.M. and J.P.; writing—original draft preparation, X.M. and J.P.; writing—review and editing, J.P. and X.X.; visualization, X.M.; supervision, J.P., X.X., J.Z. and Q.G.; project administration, J.P. and X.X.; funding acquisition, J.P. and X.X. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Key Research and Development Program of Gansu (no. 21YF5FA151), and the National Natural Science Foundation of China (no. 42107513).

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Flowchart of document retrieval. “*” is a wildcard and indicates any groups of characters, including blank characters.
Figure 1. Flowchart of document retrieval. “*” is a wildcard and indicates any groups of characters, including blank characters.
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Figure 2. The trend of the number of publications (NP) and citations (NC) regarding PGPR enhancing salt tolerance in plants from 1995 to 2021.
Figure 2. The trend of the number of publications (NP) and citations (NC) regarding PGPR enhancing salt tolerance in plants from 1995 to 2021.
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Figure 3. (A): a world map depicting the contribution of each country based on publication counts; (B): NP of the top 20 most productive lands and their corresponding h–index, ACI.
Figure 3. (A): a world map depicting the contribution of each country based on publication counts; (B): NP of the top 20 most productive lands and their corresponding h–index, ACI.
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Figure 4. The number of publications (NP) of the top 10 most productive authors and their corresponding h–index, ACI.
Figure 4. The number of publications (NP) of the top 10 most productive authors and their corresponding h–index, ACI.
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Figure 5. (A): intensity of cooperation among countries was generated by VOSviewer software; (B): a collaboration network of authors was generated by VOSviewer software. Take total link strength as the weight. The larger the total link strength, the larger the volume of the node. Lines between countries/authors indicate that they collaborated with the same researchers. The node’s color corresponds to the year when the country/author conducts more active research.
Figure 5. (A): intensity of cooperation among countries was generated by VOSviewer software; (B): a collaboration network of authors was generated by VOSviewer software. Take total link strength as the weight. The larger the total link strength, the larger the volume of the node. Lines between countries/authors indicate that they collaborated with the same researchers. The node’s color corresponds to the year when the country/author conducts more active research.
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Figure 6. The top 30 publications highly cited by peers in the final database by HistCite Pro. “# ”indicates serial number.
Figure 6. The top 30 publications highly cited by peers in the final database by HistCite Pro. “# ”indicates serial number.
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Figure 7. Overlay visualization map of keyword co-occurrence analysis generated by VOSviewer software.
Figure 7. Overlay visualization map of keyword co-occurrence analysis generated by VOSviewer software.
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Ma, X.; Pan, J.; Xue, X.; Zhang, J.; Guo, Q. A Bibliometric Review of Plant Growth-Promoting Rhizobacteria in Salt-Affected Soils. Agronomy 2022, 12, 2304. https://doi.org/10.3390/agronomy12102304

AMA Style

Ma X, Pan J, Xue X, Zhang J, Guo Q. A Bibliometric Review of Plant Growth-Promoting Rhizobacteria in Salt-Affected Soils. Agronomy. 2022; 12(10):2304. https://doi.org/10.3390/agronomy12102304

Chicago/Turabian Style

Ma, Xixi, Jing Pan, Xian Xue, Jun Zhang, and Qi Guo. 2022. "A Bibliometric Review of Plant Growth-Promoting Rhizobacteria in Salt-Affected Soils" Agronomy 12, no. 10: 2304. https://doi.org/10.3390/agronomy12102304

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