Next Article in Journal
Ambidextrous Marketing Capabilities, Exploratory and Exploitative Market-Based Innovation, and Innovation Performance: An Empirical Study on China’s Manufacturing Sector
Next Article in Special Issue
Bacterial Plant Biostimulants: A Sustainable Way towards Improving Growth, Productivity, and Health of Crops
Previous Article in Journal
Irrigation, Technical Efficiency, and Farm Size: The Case of Brazil
Previous Article in Special Issue
Exopolysaccharides Producing Bacteria for the Amelioration of Drought Stress in Wheat
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Sustainability
Volume 13
Issue 3
10.3390/su13031140
sustainability-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Plant Growth Promoting Rhizobacteria (PGPR) as Green Bioinoculants: Recent Developments, Constraints, and Prospects

by
Anirban Basu
1,
Priyanka Prasad
2,
Subha Narayan Das
2,
Sadaf Kalam
3,*,
R. Z. Sayyed
4,*,
M. S. Reddy
5 and
Hesham El Enshasy
6,7
1
Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Telangana 500046, India
2
Department of Botany, Indira Gandhi National Tribal University, Amarkantak 484887, India
3
Department of Biochemistry, St. Ann’s College for Women, Hyderabad 500028, India
4
Department of Microbiology, PSGVP Mandal’s Arts, Science and Commerce College, Shahada 425409, India
5
Asian PGPR Society for Sustainable Agriculture & Auburn Ventures, Department of Plant Pathology and Entomology, Auburn University, Auburn, AL 36849, USA
6
Institute of Bioproduct Development (IBD), Universiti Teknologi Malaysia (UTM), Skudai, Johor Bahru 81310, Malaysia
7
City of Scientific Research and Technology Applications, Alexandria 21934, Egypt
*
Authors to whom correspondence should be addressed.
Sustainability 2021, 13(3), 1140; https://doi.org/10.3390/su13031140
Submission received: 24 December 2020 / Revised: 12 January 2021 / Accepted: 18 January 2021 / Published: 22 January 2021
(This article belongs to the Special Issue Recent Trends in Plant-Growth-Promoting Rhizobacteria Research for 21st-Century Sustainable Agriculture)
Browse Figures
Versions Notes

Abstract

:
The quest for enhancing agricultural yields due to increased pressure on food production has inevitably led to the indiscriminate use of chemical fertilizers and other agrochemicals. Biofertilizers are emerging as a suitable alternative to counteract the adverse environmental impacts exerted by synthetic agrochemicals. Biofertilizers facilitate the overall growth and yield of crops in an eco-friendly manner. They contain living or dormant microbes, which are applied to the soil or used for treating crop seeds. One of the foremost candidates in this respect is rhizobacteria. Plant growth promoting rhizobacteria (PGPR) are an important cluster of beneficial, root-colonizing bacteria thriving in the plant rhizosphere and bulk soil. They exhibit synergistic and antagonistic interactions with the soil microbiota and engage in an array of activities of ecological significance. They promote plant growth by facilitating biotic and abiotic stress tolerance and support the nutrition of host plants. Due to their active growth endorsing activities, PGPRs are considered an eco-friendly alternative to hazardous chemical fertilizers. The use of PGPRs as biofertilizers is a biological approach toward the sustainable intensification of agriculture. However, their application for increasing agricultural yields has several pros and cons. Application of potential biofertilizers that perform well in the laboratory and greenhouse conditions often fails to deliver the expected effects on plant development in field settings. Here we review the different types of PGPR-based biofertilizers, discuss the challenges faced in the widespread adoption of biofertilizers, and deliberate the prospects of using biofertilizers to promote sustainable agriculture.

1. Introduction

The advent of the Green Revolution in the latter part of the twentieth century triggered a worldwide boom in the agriculture sector. By introducing new high-yielding seed varieties and increasing the use of synthetic fertilizers, pesticides, and other agrochemicals, the Green Revolution contributed significantly to enhanced plant productivity and crop yields [1]. The global agricultural landscape has drastically changed since then. Rampant overuse of synthetic agrochemicals for enhancing crop productivity has deteriorated the biological and physicochemical health of the arable soil, leading to a declining trend in agricultural productivity across the globe over the past few decades [2,3,4]. In the present scenario, there is a shrinkage of land resources and the depletion of biological wealth. In order to fulfill the escalating demand for sustainable agriculture, the yield and productivity of agricultural crops need to be concurrently increased with the production of agriculture-related commodities. There is no single or straightforward solution to the above-mentioned intricate, ecological, socio-economic, and technical glitches existing in promoting sustainable agriculture [1].
Promoting sustainable agriculture with a gradual decrease in the use of synthetic agrochemicals and more prominent utilization of the biowaste-derived substances [5,6] as well as the biological and genetic potential of crop plants and microorganisms is an effective strategy to combat the rapid environmental deterioration while ensuring high agricultural productivity and better soil health [7]. In addition to the genetic manipulation of the crop physiology and metabolism for yield enhancement, certain members of the soil microbial community, particularly those residing in the plant rhizosphere, might assist plants in preventing or partially overcoming the environmental stresses [8,9]. Search for eco-friendly alternatives to mitigate the harmful effects of toxic agrochemicals led to the discovery and subsequent use of biofertilizers and other microbial-based products, including organic extracts and vermicompost teas [10,11,12]. These microbial products are non-toxic, environment-friendly, and act as potential tools for plant growth promotion and disease control. Thus, the biological potential and fertility of soil could be increased, whereas the hazardous effects of agrochemicals could be decreased by employing microbial formulations to fertilize agricultural crops [13,14,15]. The use of efficient plant growth promoting rhizobacteria (PGPR) as biofertilizers and biological control agents is deliberated as a suitable substitute for minimizing the use of synthetic agrochemicals in crop production [16,17,18,19]. This review concisely and holistically provides deeper insights into the various aspects of PGPR-based biofertilizers, their prospects and constraints, and finally the roadmap to their commercialization.

2. Biofertilizers

During the past two decades, the term biofertilizer or bioinoculant has been derived in various ways due to the commendable progress achieved in the studies of the association between microorganisms and plants. A biofertilizer is most commonly defined as “a substance which contains living microorganisms which, when applied to seed, plant surfaces, or soil, colonizes the rhizosphere or the interior of the plant and promotes growth by increasing the supply or availability of primary nutrients to the host plant” [16]. Dineshkumar et al. [20] later proposed a modified definition of biofertilizers as “products (carrier or liquid based) containing living or dormant microbes (bacteria, actinomycetes, fungi, algae) alone or in combination, which help in fixing atmospheric nitrogen or solubilizers soil nutrients in addition to the secretion of growth promoting substances for enhancing crop growth and yield”.
The microorganisms present in the biofertilizers employ several mechanisms to provide benefits to the crop plants. They can either be efficient in nitrogen fixation, phosphate solubilization, and plant growth promotion or can possess a combination of all such traits [21,22,23,24]. Biofertilizers can fix atmospheric N2 through the biological nitrogen fixation (BNF) process, solubilize nutrients required by the plants, such as phosphate, zinc, and potassium, and also secrete plant growth promoting substances, including various hormones [25,26]. Further, when applied as seed or soil inoculants, biofertilizers can multiply, participate in nutrient cycling, and help in crop production for sustainable farming [27,28,29].
The microbial inoculants possess several advantages over their chemical counterparts [30,31,32]. They are eco-friendly, sound sources of renewable nutrients required for maintaining soil health and biology [13,23,29]. Furthermore, they exhibit antagonistic activity against several agricultural pathogens and combat abiotic stresses [8,33,34,35,36]. Various microbial taxa have been commercially used as efficient biofertilizers, based on their ability to obtain nutrients from the soil, fix atmospheric N2, stimulate the solubilization of nutrients, and act as biocontrol agents [37].

3. Plant Growth Promoting Rhizobacteria (PGPR)—The Phyto-Friendly Soil Microbes

Plant rhizosphere, the narrow zone of soil surrounding the root system of growing plants, represents a hotspot for microbial activity in the soil [38]. The rhizosphere is colonized by a wide range of microbial taxa, including both prokaryotes (archaea, bacteria, and viruses) and eukaryotes (fungi, oomycetes, nematodes, protozoa, algae, and arthropods), out of which bacteria and fungi comprise the most abundant groups [39,40] exhibiting fundamental ecological functions. Free-living soil bacteria that thrive in the rhizosphere, aggressively colonize plant roots, and facilitate plant growth are designated as plant growth promoting rhizobacteria (PGPR), a term introduced by Kloepper and Schroth in 1978 [41].
This heterogeneous group of bacteria, representing a vital component of the soil microbiome, is known to produce and secrete various regulatory chemicals in the plant roots’ vicinity that aid in plant growth promotion [42,43]. PGPRs influence plants’ overall health by contributing to enhanced nutrient acquisition by host plants, protecting against phytopathogenic microbes, and promoting resistance to various abiotic stresses [30,44]. Different PGPR strains are capable of increasing crop yields, exhibit biocontrol, enhance resistance to foliar pathogens, promote nodulation in legumes, and enhance the emergence of seedlings [45,46,47,48,49,50]. Reported PGPRs include members of the genera Acinetobacter, Aeromonas, Agrobacterium, Allorhizobium, Arthrobacter, Azoarcus, Azorhizobium, Azospirillum, Azotobacter, Bacillus, Bradyrhizobium, Burkholderia, Caulobacter, Chromobacterium, Delftia, Enterobacter, Flavobacterium, Frankia, Gluconacetobacter, Klebsiella, Mesorhizobium, Micrococcus, Paenibacillus, Pantoea, Pseudomonas, Rhizobium, Serratia, Streptomyces, Thiobacillus, and others [16,43,44,46,51,52,53]. An overview of the diverse phytobeneficial effects of PGPRs is represented in Table 1.

3.1. Characteristics of an Ideal PGPR

A rhizobacterial strain is considered to be a putative PGPR if it possesses specific plant growth promoting traits and can enhance plant growth upon inoculation. An ideal PGPR strain should fulfill the following criteria [45]:
(1)
It should be highly rhizosphere-competent and eco-friendly.
(2)
It should colonize the plant roots in significant numbers upon inoculation.
(3)
It should be able to promote plant growth.
(4)
It should exhibit a broad spectrum of action.
(5)
It should be compatible with other bacteria in the rhizosphere.
(6)
It should be tolerant of physicochemical factors like heat, desiccation, radiations, and oxidants.
(7)
It should demonstrate better competitive skills over the existing rhizobacterial communities.

3.2. Mechanisms of PGPR Action

Being the dominant rhizosphere microbial community, PGPRs are actively or passively involved in plant growth promotion. They can act as biofertilizers that promote plants’ growth and development by facilitating biotic and abiotic stress tolerance and supporting host plants’ nutrition [64,86,91,92]. These beneficial groups of bacteria, through their multifaceted modes of action, including root colonization, positive effects on plant physiology and growth, biofertilization, induced systemic resistance, biocontrol of phytopathogens, etc., offer protection to plants and facilitate plant growth promotion. The detailed mechanisms of PGPR action and their specific contribution to plant growth promotion have been reviewed comprehensively [30,41,42,43,44,47,48,49,51,52,93,94,95,96,97,98,99,100,101,102]. The modes of action by which PGPRs promote plant growth have been traditionally classified into direct and indirect mechanisms occurring inside and outside the plant, respectively [51,99] (Figure 1).
Direct modes of PGPR action include improving plant nutrition by providing phytonutrients like fixed nitrogen or solubilized minerals from the soil (like P, K, Zn, Fe, and other essential mineral nutrients) and/or stimulating plant growth and development by regulating phytohormone levels (like auxins, cytokinins, gibberellins, abscisic acid, and ethylene) [44,46,95]. The indirect effects of PGPRs include influencing the plant health by suppressing phytopathogens and other deleterious microorganisms through parasitism, competing for nutrients and niche within the rhizosphere, producing antagonistic substances (like hydrogen cyanide, siderophores, antibiotics, and antimicrobial metabolites) and lytic enzymes (like chitinases, glucanases, and proteases), and inducing systemic resistance in plants against a broad spectrum of root and foliar pathogens [32,81,103,104]. Due to these direct and indirect effects elicited by PGPRs on host plants, they prove to be ideal candidates to be formulated and commercialized as bioinoculants and phytoprotective microbial products. However, the mode and mechanism of PGPR action vary with the host plant type [105]. In addition to this, certain other factors also influence PGPR action, viz. biotic factors like plant genotype, developmental stages, plant defense mechanisms, and presence of other members of the microbial community and abiotic factors like soil type, composition, soil management history, and prevalent environmental conditions [95,106].

4. Global Biofertilizer Market

During the past few decades, the biofertilizer market has seen a global boom in its production and utilization. Due to the unavailability of cultivable land and to cater to the need of the exploding population for agricultural products, the global biofertilizers market has gathered enough momentum. The global biofertilizer market represents a tiny fraction of the synthetic agrochemicals market [107]. The nitrogen-fixing biofertilizers dominate the market with the lion’s share of about 80%, followed by the phosphate-solubilizing biofertilizers with a meager 14% share (Figure 2) [107,108]. Rhizobium spp., Azotobacter spp., and Azospirillum spp. are the major nitrogen-fixing biofertilizers available in the market. Although these nitrogen-fixing biofertilizers are primarily used for growing pulses and other leguminous crops, they are also applied to grow selected cereals and cash crops as well [107,109].
Geographically, the global biofertilizer market canopies several regions of the world, such as North America, Europe, Asia-Pacific, Latin America, Middle East, and Africa (Figure 3). In terms of revenues generated from biofertilizer production, North America (USA, Canada, and Mexico) dominates the global biofertilizer market, followed by Europe (Germany, UK, Spain, Italy, Hungary, and France) and the Asia-Pacific region (China, Japan, India, Australia, New Zealand, and the rest of Asia). As of 2017, the biofertilizer markets were valued at USD 495 million in North America, USD 450 million in Europe, USD 284 million in Asia-Pacific, USD 240 million in South America, and USD 44 million in Africa [108]. It is estimated that the global biofertilizer market would reach USD 3.5 billion by 2025. Some of the commonly used PGPR-based biofertilizer products commercially available across the globe are represented in Table 2.

5. Challenges and Constraints with PGPR-Based Biofertilizers

Presently, there is an escalating interest in the use of microbial-based products as bioinoculants. Still, their use is associated with several challenges moving from the lab to the field. The preliminary use of these bioinoculants has been made on crop plants such as legumes and cereals [119]. For developing a new PGPR strain as an effective bioinoculant, an initial laboratory screening is required, which depends on specific direct and indirect mechanisms of plant growth promotion by PGPRs. Mere primary screening of axenic culture isolates for PGPR traits does not guarantee efficacious plant growth promotion under field conditions. Parallelly, those pure culture isolates that exhibit less in vitro growth promoting activities might possess different plant growth promotion strategies. Because these mechanisms are not fully understood, such isolates exhibit difficulty in screening under standard conditions. Henceforth, sometimes such useful strains exhibiting these mechanisms get discarded due to their poor in vitro performance [120]. The large-scale utilization and application of PGPRs necessitate addressing several important issues and overcoming quite a few challenges and constraints (Figure 4).

5.1. Biological Constraints

Selection of specific PGPR strain(s) for biofertilizer development is a challenge in itself. The strain(s) should not be selective or highly targeted (to specific crops) in nature, and it should exhibit a broad host range. One of the main limiting issues is their selectivity. Conventional agrochemicals tend to impact the entire resident microbiota, whereas PGPRs remain highly targeted and specific. Nevertheless, the quality and efficacy of these PGPRs under field conditions invariably changes due to the presence of several other microorganisms. Potential isolates should be selected based on their performance under field conditions with a wide range of crops across diverse soil types and environmental conditions [32]. The strains must be effective in replacing the native inefficient strains and should not antagonize with other beneficial microbes in the rhizosphere [31].
As biofertilizers, PGPRs should be able to sufficiently colonize host plant roots, create a proper rhizosphere for plant growth, and increase the bioavailability of N, P, K, and antagonistic properties [16,45]. PGPRs should possess specific characteristics for their utilization as an efficient and successful bioinoculant. It should be able to survive in soil, compatible with the crop on which it is inoculated, and interact with indigenous microflora in soil and abiotic factors. Necessary measures should be taken to avoid any non-target effect of the bioinoculant and stabilize them in soil systems. These measures will guarantee the durability of the plant growth effect and the good performance of introduced PGPRs as bioinoculants.
An important factor in PGPR colonization is PGPR dynamics, which mainly changes with the host crop, the midterm and long-term effects, the crop-rotation impact, and site variation. Another challenge using PGPRs is their diverse mode of action, as all the rhizobacteria do not possess the same mechanisms of action for plant growth promotion [121]. Several Gram-negative rhizobacteria are known to exhibit biocontrol potential. The constraint arises in their formulation, as they are difficult to formulate because of their inability to produce spores. In addition to this, their formulations lack a longer shelf life, and the bacteria are prone to get killed upon desiccation [51,122,123].

5.2. Technical Constraints

One of the significant challenges encountered during the development of a biofertilizer and the commercialization of an effective PGPR strain is its shelf life [22,124]. Biofertilizers with a short shelf life carry the risk of recycling if they are not used or sold before expiry resulting in a net monetary loss to the marketing agency. Since biofertilizers contain live microbial cells, their storage and transportation require extra care and precaution. The technical constraints involve the risk of deterioration of the product due to shorter shelf life or spontaneous mutations arising during fermentation or storage [31]. The mutations result in a net reduction in bioinoculant effectiveness and lead to a severe problem that raises the cost of production and quality of the bioinoculant. Inadequate availability of soil-specific strains region-wise considerably limits the widespread use of bioinoculants.

5.3. Regulatory Constraints

Regulatory constraints include the challenges in product registration and patent filing. The rules often vary between different regions and nations and are not consistent. In addition, the regulatory processes are quite complex, and the fees, though variable, are mostly on the higher side [32,107]. The documentation procedures for product registration are equally extensive and complicated. The absence of a standardized legal and regulatory definition for “plant biostimulants” is the primary reason behind the lack of a globally coordinated uniform regulatory policy [30,125].
The process of registering the biocontrol agent within a country is normally in two phases and is quite lengthy and complicated [32,107]. Generally, in any country, the active ingredient present within a biofertilizer must get an authorization certificate from the Directorate-General for Health and Consumer Affairs, and after that, the formulated product has to be nationally approved. The Food Safety Authority and the National Commission of any country will critically analyze and give relevant comments followed by several rounds of review by experts, sometimes taking an additional two to three years. Thus, the entire process starting from registration to commercializing a potential biofertilizer is lengthy and might stretch to several years. The countries have their own guidelines and norms to respond in their specific language, and the registering agency can also require even additional data.

5.4. Infrastructural Constraints

Manufacturing and quality control of biofertilizers involve sophisticated technology and qualified and trained human resources. Lack of sophisticated technology, necessary technical support and proper equipment, trained workforce, and skilled technical personnel are the major infrastructural constraints [31].

5.5. Financial Constraints

Lack of sufficient financial resources in the large-scale production of biofertilizers is a significant drawback [124]. Once the biofertilizer is manufactured, small producers do not have enough funds to distribute on their own. Because of this delay in distribution, lowering of the quality of the product occurs, deteriorating its biocontrol potential [31].

5.6. Marketing Constraints

One of the major limitations for developing the product in the market is the unavailability of proper transportation services along with storage facilities. Farmers possess little or inadequate knowledge regarding the advantages of biofertilizers over hazardous agrochemicals for sustainable agriculture. Thus, the demand for such eco-friendly products is reduced. The establishment of extension centers does not help in creating awareness among farmers due to the lack of well-qualified technical staff [31].
The biofertilizer developers face a significant problem because the agricultural crops are grown under various physicochemical and environmental conditions, including diverse ranges of temperature, rainfall, soil type, and crop variety. These conditions tend to change from farm to farm or even within a single field. Therefore, such variations cause a discrepancy in the efficacy of PGPR-based biofertilizers [122,126].
There is a general strategy followed in any state within a country before any microbial products attain the stage of commercialization. The ministry/department of agriculture gives a green signal for placing orders mostly from their own production units. From here, biofertilizer packets are transported to several districts. A chain of extension workers gets involved in the next step before these packets reach the field. During this course, the microorganisms present as bioinoculants get exposed to high temperatures (above 40 °C), which might lead to either their inactivation or death, thus rendering them low- or poor-quality biofertilizers. Henceforth, these low-quality packets will be disadvantageous for the farmers, as well as for the entire crop yield.

5.7. Field-Level Constraints

The response of crops toward the applied biofertilizers is very slow and sometimes futile since the inoculum will take time to build its concentration and root colonization. This results in a low level of acceptance of biofertilizers by the farmers. The purity of inoculants, along with inoculation techniques, play a vital role in field application. The effectiveness of biofertilizers gets reduced because of the harmful residual effects of synthetic chemicals and existing unfavorable abiotic conditions [31,127]. Environmental stresses such as salt and drought in certain areas play another important role in reducing biological activity. The inoculants are under biotic and abiotic stresses [124]. In addition to these factors, several other factors that holistically result in poor performance of the bioinoculants include acidity and alkalinity of the soil and application of pesticides and high concentrations of nitrate in the soil, limiting the N-fixing ability of the bioinoculants. Many soils possess toxic concentrations of heavy metals like Cd, Hg, Cr, etc., and a deficiency of other important nutrients like P, Cu, Mo, and Co that reduce the biological potential of the PGPR-based fertilizers [23,128].
PGPRs function through a series of mechanisms. The foremost step in plant growth promotion is the colonization of plant roots by the microbe, which is an intricate process requiring the ability of bacteria to compete in the rhizosphere soil for a suitable niche to bring about a positive plant-microbe interaction [129]. In addition to this, the abiotic factors, viz. soil type, temperature, pH, radiation, oxygen concentration, nutrient availability, and the degree of interaction with the native soil microbiota, too drastically affect the plant-microbe interaction, affecting their existence and survivability within the host plant. Thus, the success of the field application of PGPRs depends upon the climatic factors required for a particular variety of cultivated crops [21]. Identification of region-specific microbial strains is highly recommended to exhibit maximum effectiveness by the employed PGPR strain. Quite often, PGPRs are directly used as an inoculum for host plants without mixing them with an appropriate carrier. In addition to this, their quantities are insufficient to allow efficient rhizosphere colonization existing in a field because of the competition with the already existing soil micro- and macro-biota [130].
Broad-spectrum biocidal fumigants are generally used to fumigate soils associated with high-value crops. These fumigants result in altering the microbial community of such soils. As a consequence of long-term fumigation, soil microbial community, and their beneficial interactions that help host plants obtain nutrients and mobilization, get largely affected [131]. This leads to decreased rhizosphere colonization by the PGPR inoculant.

5.8. Quality Control Constraints

The most important parameter which the farmers look for in any biofertilizer is quality control. Being natural products, living microorganisms possess a very short shelf life [32]. The failure of any microbial-based product in fields can be due to the supply of low- or spurious-quality products. Presently, there is the unavailability of any quality check for biofertilizers. Henceforth, in order to prove the plant growth promoting efficacy in the fields, setting up quality control standards for biofertilizers is quite essential [31].

5.9. Biofertilizer Carrier

A suitable carrier is required for field application of biofertilizer because of the short shelf life of the bioinoculant agent. Thus, the unavailability of an appropriate carrier proves to be one of the major constraints for its large-scale use in fields. Ideal carriers used in biofertilizer production are peat, charcoal, lignite, etc. These carriers again pose technical constraints because most of them are unavailable in developing countries like India. There is a lack of sufficient quantities and a desirable quality of these carriers. Only charcoal is readily available in the Indian market, and therefore it can be used as a formulating agent [31]. Peat is recognized as the most suitable carrier among the available carriers, but the challenge is its shorter shelf life, which is less than six months. Due to its ability to improve soil and plant health, biochar can be used as a suitable carrier for biofertilizers [14,30]. In order to prove itself as an efficient and potential carrier, the bioinoculant should possess several other characteristics. It should be of low cost, the organic matter content and water-holding capacity should be high, and the organism-retention capacity should be longer. It should be nearly sterile, with zero moisture content, and it should be non-polluting, non-toxic, and with nearly neutral pH so that the biofertilizer is of good quality [132].

5.10. Biosafety of PGPRs

PGPRs are considered to be practical candidates for sustainable agriculture. An essential characteristic of PGPRs and other biofertilizer agents is that these microbes should not elicit any harmful effects on the environment or humans. According to the guidelines on biosafety in microbiological and biomedical laboratories, published by the U.S. Department of Health and Human Services in 1999 and World Health Organization guidelines on the usage of microorganisms, biosafety levels (BSLs) were made to categorize the usable microorganisms in a range of biosafety classes, based on the different categories of risk posed by them [32]. The communicable agents were classified into four risk groups (BSL-1–4) based on their pathogenicity to human health, mode of transmission, and available treatments. These levels have to be strictly followed in handling these microorganisms. The microbial strains selected for biofertilizer development should preferably belong to the low-risk group of non-pathogenic BSL-1 microorganisms.

6. Guidelines and Precautions for Using PGPRs as Biofertilizers

The major safety measures and guidelines [31] essential for using PGPRs as biofertilizers are:
(1)
It is essential that the supplied biofertilizer to be used in fields is of good quality, contains 107 viable cells per gram as an inoculum, and is purchased from a reputed manufacturer only.
(2)
Since the biofertilizer exhibits specificity, it should only be used for the crop(s) specified on the commercially available product packet.
(3)
The culture bag should have a tag of the name of the crop for which it has to be used.
(4)
While inoculating, excess culture should be inoculated, or any remnants/residual culture should be immediately put in grooves of the field so that inoculum microorganisms start interacting with other microbiota in the rhizosphere and begin colonizing the rhizosphere.
(5)
Since the biofertilizers are microbial products, for achieving better shelf life, before their application in fields, they should be stored in cool and shady places, preferably at room temperature (25–28 °C).
(6)
During storage or application, direct contact of the biofertilizers with agrochemicals (herbicides/weedicides/pesticides) should be strictly avoided.
(7)
Generally speaking, 200g biofertilizer can be effectively used to treat 10 kg of seeds.
(8)
In the case of unfavorable soil conditions, especially where the soil is strongly acidic, soil amendments such as lime or rock phosphate, are usually preferred.

7. Roadmap to the Commercialization of PGPR-Based Biofertilizers

Using PGPRs as biofertilizers for promoting plant growth and crop yield, improving soil fertility, and biocontrol of phytopathogens promotes sustainable agriculture by offering eco-friendly alternatives to synthetic agrochemicals like chemical fertilizers and pesticides. The development and commercialization of PGPR-based biofertilizers generally follow the following roadmap (Figure 5) [30,108].

8. Conclusions and Future Perspectives

Among various industries present within a nation, the agriculture industry not only plays a pivotal role in survival but also facilitates meeting the demands of the growing population and economic exports. Post Green Revolution, the agroindustry has witnessed several scientific advances that resulted in better crop productivity but with environmental complications. Chemical fertilizers prove detrimental to soil and environmental health, while biofertilizers are natural products and do not pose threats to the ecosystem. Thus, to manage long-term soil fertility and sustain crop productivity, natural-products-based fertilizers prove to be an integral and vital component of sustainable agriculture. The last decade has inevitably seen a revolution because of the increased use of biological inoculants instead of agrochemicals for sustainable agriculture globally. The triad of interactions existing between the bioinoculant microorganism(s), resident soil microbiota, and host plant(s) is vital not only for the overall growth and higher productivity of the crop plants but also for maintaining the integrity of our planet’s health and proper biogeochemical cycling.
A growing apprehension concerning food safety and the rising need for controlling food production quality to cater to the changing consumer demand is expected to shift farmers’ attention toward organic farming and adopt sustainable agricultural practices. Thus, while seeking eco-friendly alternatives to toxic chemicals, there is a need to consider the three crucial “Ps”, which include the people, prosperity, and the planet. Before its complete implementation, however, this microbial product-based technology needs to be researched profoundly and improved to elicit desired results and gain the trust of the farmers, the real stakeholders of agriculture. The thrust areas that need to be further focused on for research include quantifying commercial production, strain improvement, and authentication. Governments and federal agencies should promote the use of biofertilizers as eco-friendly alternatives for crop improvement. Entrepreneurs should invest more in the biofertilizer industry and provide financial assistance for start-ups. In addition to this, mass public awareness is required to educate the farmers and consumers alike on the advantages of using microbe-based biofertilizers for ensuring a greener tomorrow.

Author Contributions

Conceptualization, A.B. and S.K.; writing—original draft preparation, A.B., P.P., S.N.D., and S.K.; writing—review and editing, S.K., R.Z.S., M.S.R., and H.E.E. All authors have read and agreed to the published version of the manuscript.

Funding

H.E.E. would like to thank Universiti Teknologi Malaysia (UTM) for financial support through project No. QJ130000.3609.02M43 and All Cosmos Industries Sdn. Bhd. for financial support with project No. R.J130000.7344.4B200.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

A.B. and P.P. acknowledge University Grants Commission (UGC), New Delhi, India, for research fellowships. A.B. acknowledges his mentor, Prof. Appa Rao Podile, Vice-Chancellor, University of Hyderabad, for his constant support and encouragement. S.N.D. acknowledges the UGC start-up research grant for financial support. S.K. acknowledges Principal Sister Amrutha, St. Ann’s College for Women, Hyderabad, Telangana, India, for her incessant support and Department of Biotechnology (DBT), New Delhi, India, for infrastructural support to the department under the DBT-STAR College Scheme.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Kesavan, P.C.; Swaminathan, M.S. Modern technologies for sustainable food and nutrition security. Curr. Sci. 2018, 115, 1876–1883. [Google Scholar] [CrossRef]
  2. Pingali, P.L. Green revolution: Impacts, limits, and the path ahead. Proc. Natl. Acad. Sci. USA 2012, 109, 12302–12308. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Yang, X.; Fang, S. Practices, perceptions, and implications of fertilizer use in East-Central China. Ambio 2015, 44, 647–652. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Bishnoi, U. Agriculture and the dark side of chemical fertilizers. Environ. Anal. Ecol. Stud. 2018, 3, EAES.000552.2018. [Google Scholar] [CrossRef]
  5. Fascella, G.; Montoneri, E.; Ginepro, M.; Francavilla, M. Effect of urban biowaste derived soluble substances on growth, photosynthesis and ornamental value of Euphorbia × lomi. Sci. Hortic. 2015, 197, 90–98. [Google Scholar] [CrossRef]
  6. Fascella, G.; Montoneri, E.; Francavilla, M. Biowaste versus fossil sourced auxiliaries for plant cultivation: The Lantana case study. J. Clean. Prod. 2018, 185, 322–330. [Google Scholar] [CrossRef]
  7. Liu, J.; Ma, K.; Ciais, P.; Polasky, S. Reducing human nitrogen use for food production. Sci. Rep. 2016, 6, 30104. [Google Scholar] [CrossRef] [Green Version]
  8. Ilangumaran, G.; Smith, D.L. Plant growth promoting rhizobacteria in amelioration of salinity stress: A systems biology perspective. Front. Plant Sci. 2017, 8, 1768. [Google Scholar] [CrossRef]
  9. De Souza, R.; Ambrosini, A.; Passaglia, L.M.P. Plant growth-promoting bacteria as inoculants in agricultural soils. Genet. Mol. Biol. 2015, 38, 401–419. [Google Scholar] [CrossRef]
  10. Mishra, S.; Wang, K.-H.; Sipes, B.S.; Tian, M. Suppression of root-knot nematode by vermicompost tea prepared from different curing ages of vermicompost. Plant Dis. 2017, 101, 734–737. [Google Scholar] [CrossRef] [Green Version]
  11. Arancon, N.Q.; Owens, J.D.; Converse, C. The effects of vermicompost tea on the growth and yield of lettuce and tomato in a non-circulating hydroponics system. J. Plant Nutr. 2019, 42, 2447–2458. [Google Scholar] [CrossRef]
  12. Akinnuoye-Adelabu, D.B.; Steenhuisen, S.; Bredenhand, E. Improving pea quality with vermicompost tea and aqueous biochar: Prospects for sustainable farming in Southern Africa. S. Afr. J. Bot. 2019, 123, 278–285. [Google Scholar] [CrossRef]
  13. Raklami, A.; Bechtaoui, N.; Tahiri, A.; Anli, M.; Meddich, A.; Oufdou, K. Use of rhizobacteria and mycorrhizae consortium in the open field as a strategy for improving crop nutrition, productivity and soil fertility. Front. Microbiol. 2019, 10, 1106. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Jabborova, D.; Wirth, S.; Kannepalli, A.; Narimanov, A.; Desouky, S.; Davranov, K.; Sayyed, R.Z.; El Enshasy, H.; Malek, R.A.; Syed, A.; et al. Co-Inoculation of rhizobacteria and biochar application improves growth and nutrients in soybean and enriches soil nutrients and enzymes. Agronomy 2020, 10, 1142. [Google Scholar] [CrossRef]
  15. Sharma, S.B.; Sayyed, R.Z.; Trivedi, M.H.; Gobi, T.A. Phosphate solubilizing microbes: Sustainable approach for managing phosphorus deficiency in agricultural soils. Springerplus 2013, 2, 587. [Google Scholar] [CrossRef] [Green Version]
  16. Vessey, J.K. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 2003, 255, 571–586. [Google Scholar] [CrossRef]
  17. Anli, M.; Baslam, M.; Tahiri, A.; Raklami, A.; Symanczik, S.; Boutasknit, A.; Ait-El-Mokhtar, M.; Ben-Laouane, R.; Toubali, S.; Ait Rahou, Y.; et al. Biofertilizers as strategies to improve photosynthetic apparatus, growth, and drought stress tolerance in the date palm. Front. Plant Sci. 2020, 11, 516818. [Google Scholar] [CrossRef]
  18. Dong, L.; Li, Y.; Xu, J.; Yang, J.; Wei, G.; Shen, L.; Ding, W.; Chen, S. Biofertilizers regulate the soil microbial community and enhance Panax ginseng yields. Chin. Med. 2019, 14, 20. [Google Scholar] [CrossRef] [Green Version]
  19. Atieno, M.; Herrmann, L.; Nguyen, H.T.; Phan, H.T.; Nguyen, N.K.; Srean, P.; Than, M.M.; Zhiyong, R.; Tittabutr, P.; Shutsrirung, A.; et al. Assessment of biofertilizer use for sustainable agriculture in the Great Mekong Region. J. Environ. Manag. 2020, 275, 111300. [Google Scholar] [CrossRef]
  20. Dineshkumar, R.; Kumaravel, R.; Gopalsamy, J.; Sikder, M.N.A.; Sampathkumar, P. Microalgae as bio-fertilizers for rice growth and seed yield productivity. Waste Biomass Valorization 2018, 9, 793–800. [Google Scholar] [CrossRef]
  21. Mahanty, T.; Bhattacharjee, S.; Goswami, M.; Bhattacharyya, P.; Das, B.; Ghosh, A.; Tribedi, P. Biofertilizers: A potential approach for sustainable agriculture development. Environ. Sci. Pollut. Res. 2017, 24, 3315–3335. [Google Scholar] [CrossRef] [PubMed]
  22. Zandi, P.; Basu, S.K. Role of plant growth-promoting rhizobacteria (PGPR) as biofertilizers in stabilizing agricultural ecosystems. In Organic Farming for Sustainable Agriculture; Nandwani, D., Ed.; Springer: Cham, Switzerland, 2016; pp. 71–87. [Google Scholar] [CrossRef]
  23. 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, 1–10. [Google Scholar] [CrossRef] [Green Version]
  24. Ritika, B.; Utpal, D. Biofertilizer, a way towards organic agriculture: A review. Afr. J. Microbiol. Res. 2014, 8, 2332–2343. [Google Scholar] [CrossRef] [Green Version]
  25. Borkar, S.G. Microbes as Bio-Fertilizers and Their Production Technology, 1st ed.; WPI Publishing: New York, NY, USA, 2015. [Google Scholar]
  26. Kumar, S.M.; Reddy, C.G.; Phogat, M.; Korav, S. Role of bio-fertilizers towards sustainable agricultural development: A review. J. Pharm. Phytochem. 2018, 7, 1915–1921. [Google Scholar]
  27. Itelima, J.; Bang, W.J.; Onyimba, I.A.; Sila, M.D.; Egbere, O.J. Bio-fertilizers as key player in enhancing soil fertility and crop productivity: A review. J. Microbiol. Biotechnol. Rep. 2018, 2, 22–28. [Google Scholar]
  28. Singh, J.S.; Pandey, V.C.; Singh, D.P. Efficient soil microorganisms: A new dimension for sustainable agriculture and environmental development. Agric. Ecosyst. Environ. 2011, 140, 339–353. [Google Scholar] [CrossRef]
  29. Sun, B.; Bai, Z.; Bao, L.; Xue, L.; Zhang, S.; Wei, Y.; Zhang, Z.; Zhuang, G.; Zhuang, X. Bacillus subtilis biofertilizer mitigating agricultural ammonia emission and shifting soil nitrogen cycling microbiomes. Environ. Int. 2020, 144, 105989. [Google Scholar] [CrossRef]
  30. Backer, R.; Rokem, J.S.; Ilangumaran, G.; Lamont, J.; Praslickova, D.; Ricci, E.; Subramanian, S.; Smith, D.L. Plant growth-promoting rhizobacteria: Context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front. Plant Sci. 2018, 9, 1473. [Google Scholar] [CrossRef] [Green Version]
  31. Mahajan, A.; Gupta, R.D. Bio-fertilizers: Their kinds and requirement in India. In Integrated Nutrient Management (INM) in a Sustainable Rice—Wheat Cropping System; Mahajan, A., Gupta, R.D., Eds.; Springer: Dordrecht, The Netherlands, 2009; pp. 75–100. [Google Scholar]
  32. Meena, M.; Swapnil, P.; Divyanshu, K.; Kumar, S.; Tripathi, Y.N.; Zehra, A.; Marwal, A.; Upadhyay, R.S. PGPR-mediated induction of systemic resistance and physiochemical alterations in plants against the pathogens: Current perspectives. J. Basic Microbiol. 2020, 60, 828–861. [Google Scholar] [CrossRef]
  33. Timmusk, S.; Kim, S.-B.; Nevo, E.; Abd El Daim, I.; Ek, B.; Bergquist, J.; Behers, L. Sfp-type PPTase inactivation promotes bacterial biofilm formation and ability to enhance wheat drought tolerance. Front. Microbiol. 2015, 6, 387. [Google Scholar] [CrossRef] [Green Version]
  34. Bharti, N.; Pandey, S.S.; Barnawal, D.; Patel, V.K.; Kalra, A. Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci. Rep. 2016, 6, 34768. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Sharma, S.; Kulkarni, J.; Jha, B. Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Front. Microbiol. 2016, 7, 1600. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Timmusk, S.; Abd El-Daim, I.A.; Copolovici, L.; Tanilas, T.; Kännaste, A.; Behers, L.; Nevo, E.; Seisenbaeva, G.; Stenström, E.; Niinemets, Ü. Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: Enhanced biomass production and reduced emissions of stress volatiles. PLoS ONE 2014, 9, e96086. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Schütz, L.; Gattinger, A.; Meier, M.; Müller, A.; Boller, T.; Mäder, P.; Mathimaran, N. Improving crop yield and nutrient use efficiency via biofertilization—A global meta-analysis. Front. Plant Sci. 2018, 8, 2204. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. De la Fuente Cantó, C.; Simonin, M.; King, E.; Moulin, L.; Bennett, M.J.; Castrillo, G.; Laplaze, L. An extended root phenotype: The rhizosphere, its formation and impacts on plant fitness. Plant J. 2020, 103, 951–964. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  39. Kalam, S.; Das, S.N.; Basu, A.; Podile, A.R. Population densities of indigenous Acidobacteria change in the presence of plant growth promoting rhizobacteria (PGPR) in rhizosphere. J. Basic Microbiol. 2017, 57, 376–385. [Google Scholar] [CrossRef]
  40. Buée, M.; de Boer, W.; Martin, F.; van Overbeek, L.; Jurkevitch, E. The rhizosphere zoo: An overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 2009, 321, 189–212. [Google Scholar] [CrossRef]
  41. Dutta, S.; Podile, A.R. Plant Growth Promoting Rhizobacteria (PGPR): The bugs to debug the root zone. Crit. Rev. Microbiol. 2010, 36, 232–244. [Google Scholar] [CrossRef]
  42. Khoshru, B.; Mitra, D.; Khoshmanzar, E.; Myo, E.M.; Uniyal, N.; Mahakur, B.; Mohapatra, P.K.; Panneerselvam, P.; Boutaj, H.; Alizadeh, M.; et al. Current scenario and future prospects of plant growth-promoting rhizobacteria: An economic valuable resource for the agriculture revival under stressful conditions. J. Plant Nutr. 2020, 43, 3062–3092. [Google Scholar] [CrossRef]
  43. Ahemad, M.; Kibret, M. Mechanisms and applications of plant growth promoting rhizobacteria: Current perspective. J. King Saud Univ. Sci. 2014, 26, 1–20. [Google Scholar] [CrossRef] [Green Version]
  44. Parray, J.A.; Jan, S.; Kamili, A.N.; Qadri, R.A.; Egamberdieva, D.; Ahmad, P. Current perspectives on plant growth-promoting rhizobacteria. J. Plant Growth Regul. 2016, 35, 877–902. [Google Scholar] [CrossRef]
  45. Vejan, P.; Abdullah, R.; Khadiran, T.; Ismail, S.; Nasrulhaq Boyce, A. Role of plant growth promoting rhizobacteria in agricultural sustainability - A review. Molecules 2016, 21, 573. [Google Scholar] [CrossRef] [PubMed]
  46. Kalam, S.; Basu, A.; Podile, A.R. Functional and molecular characterization of plant growth promoting Bacillus isolates from tomato rhizosphere. Heliyon 2020, 6, e04734. [Google Scholar] [CrossRef] [PubMed]
  47. Swarnalakshmi, K.; Yadav, V.; Tyagi, D.; Dhar, D.W.; Kannepalli, A.; Kumar, S. Significance of plant growth promoting rhizobacteria in grain legumes: Growth promotion and crop production. Plants 2020, 9, 1596. [Google Scholar] [CrossRef] [PubMed]
  48. Gopalakrishnan, S.; Sathya, A.; Vijayabharathi, R.; Varshney, R.K.; Gowda, C.L.L.; Krishnamurthy, L. Plant growth promoting rhizobia: Challenges and opportunities. 3 Biotech 2015, 5, 355–377. [Google Scholar] [CrossRef] [Green Version]
  49. Bhattacharyya, P.N.; Jha, D.K. Plant growth-promoting rhizobacteria (PGPR): Emergence in agriculture. World J. Microbiol. Biotechnol. 2012, 28, 1327–1350. [Google Scholar] [CrossRef]
  50. Vaikuntapu, P.R.; Dutta, S.; Samudrala, R.B.; Rao, V.R.V.N.; Kalam, S.; Podile, A.R. Preferential promotion of Lycopersicon esculentum (tomato) growth by plant growth promoting bacteria associated with tomato. Indian J. Microbiol. 2014, 54, 403–412. [Google Scholar] [CrossRef] [Green Version]
  51. Goswami, D.; Thakker, J.N.; Dhandhukia, P.C. Portraying mechanics of plant growth promoting rhizobacteria (PGPR): A review. Cogent Food Agric. 2016, 2, 1127500. [Google Scholar] [CrossRef]
  52. Ankati, S.; Podile, A.R. Understanding plant-beneficial microbe interactions for sustainable agriculture. J. Spices Aromat. Crop. 2018, 27, 93–105. [Google Scholar] [CrossRef] [Green Version]
  53. Ahmad, F.; Ahmad, I.; Khan, M.S. Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol. Res. 2008, 163, 173–181. [Google Scholar] [CrossRef]
  54. Niu, X.; Song, L.; Xiao, Y.; Ge, W. Drought-tolerant plant growth-promoting rhizobacteria associated with foxtail millet in a semi-arid agroecosystem and their potential in alleviating drought stress. Front. Microbiol. 2018, 8, 2580. [Google Scholar] [CrossRef] [PubMed]
  55. De Lima, B.C.; Moro, A.L.; Santos, A.C.P.; Bonifacio, A.; Araujo, A.S.F.; de Araujo, F.F. Bacillus subtilis ameliorates water stress tolerance in maize and common bean. J. Plant Interact. 2019, 14, 432–439. [Google Scholar] [CrossRef] [Green Version]
  56. Bresson, J.; Varoquaux, F.; Bontpart, T.; Touraine, B.; Vile, D. The PGPR strain Phyllobacterium brassicacearum STM196 induces a reproductive delay and physiological changes that result in improved drought tolerance in Arabidopsis. New Phytol. 2013, 200, 558–569. [Google Scholar] [CrossRef] [PubMed]
  57. Figueiredo, M.V.B.; Burity, H.A.; Martínez, C.R.; Chanway, C.P. Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl. Soil Ecol. 2008, 40, 182–188. [Google Scholar] [CrossRef]
  58. Yang, J.; Kloepper, J.W.; Ryu, C.M. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 2009, 14, 1–4. [Google Scholar] [CrossRef]
  59. Ilyas, N.; Mumtaz, K.; Akhtar, N.; Yasmin, H.; Sayyed, R.Z.; Khan, W.; El Enshasy, H.A.; Dailin, D.J.; Elsayed, E.A.; Ali, Z. Exopolysaccharides producing bacteria for the amelioration of drought stress in wheat. Sustainability 2020, 12, 8876. [Google Scholar] [CrossRef]
  60. Mayak, S.; Tirosh, T.; Glick, B.R. Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol. Biochem. 2004, 42, 565–572. [Google Scholar] [CrossRef]
  61. Bharti, N.; Yadav, D.; Barnawal, D.; Maji, D.; Kalra, A. Exiguobacterium oxidotolerans, a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J. Microbiol. Biotechnol. 2013, 29, 379–387. [Google Scholar] [CrossRef]
  62. Marulanda, A.; Azcón, R.; Chaumont, F.; Ruiz-Lozano, J.M.; Aroca, R. Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 2010, 232, 533–543. [Google Scholar] [CrossRef]
  63. Fasciglione, G.; Casanovas, E.M.; Quillehauquy, V.; Yommi, A.K.; Gõ Ni, M.G.; Roura, S.I.; Barassi, C.A. Azospirillum inoculation effects on growth, product quality and storage life of lettuce plants grown under salt stress. Sci. Hortic. 2015, 195, 154–162. [Google Scholar] [CrossRef]
  64. Sagar, A.; Sayyed, R.Z.; Ramteke, P.W.; Sharma, S.; Marraiki, N.; Elgorban, A.M.; Syed, A. ACC deaminase and antioxidant enzymes producing halophilic Enterobacter sp. PR14 promotes the growth of rice and millets under salinity stress. Physiol. Mol. Biol. Plants 2020, 26, 1847–1854. [Google Scholar] [CrossRef] [PubMed]
  65. Verma, P.; Yadav, A.N.; Khannam, K.S.; Kumar, S.; Saxena, A.K.; Suman, A. Molecular diversity and multifarious plant growth promoting attributes of Bacilli associated with wheat (Triticum aestivum L.) rhizosphere from six diverse agro-ecological zones of India. J. Basic Microbiol. 2016, 56, 44–58. [Google Scholar] [CrossRef] [PubMed]
  66. Srivastava, S.; Bist, V.; Srivastava, S.; Singh, P.C.; Trivedi, P.K.; Asif, M.H.; Chauhan, P.S.; Nautiyal, C.S. Unraveling aspects of Bacillus amyloliquefaciens mediated enhanced production of rice under biotic stress of Rhizoctonia solani. Front. Plant Sci. 2016, 7, 587. [Google Scholar] [CrossRef] [Green Version]
  67. De Vasconcellos, R.L.F.; Cardoso, E.J.B.N. Rhizospheric streptomycetes as potential biocontrol agents of Fusarium and Armillaria pine rot and as PGPR for Pinus taeda. Biocontrol 2009, 54, 807–816. [Google Scholar] [CrossRef]
  68. Gowtham, H.G.; Hariprasad, P.; Nayak, S.C.; Niranjana, S.R. Application of rhizobacteria antagonistic to Fusarium oxysporum f. sp. lycopersici for the management of Fusarium wilt in tomato. Rhizosphere 2016, 2, 72–74. [Google Scholar] [CrossRef]
  69. Khan, N.; Mishra, A.; Nautiyal, C.S. Paenibacillus lentimorbus B-30488 r controls early blight disease in tomato by inducing host resistance associated gene expression and inhibiting Alternaria solani. Biol. Control 2012, 62, 65–74. [Google Scholar] [CrossRef]
  70. Reshma, P.; Naik, M.K.; Aiyaz, M.; Niranjana, S.K.; Chennappa, G.; Shaikh, S.S.; Sayyed, R.Z. Induced systemic resistance by 2,4-diacetylphloroglucinol positive fluorescent Pseudomonas strains against rice sheath blight. Indian J. Exp. Biol. 2018, 56, 207–212. [Google Scholar]
  71. Chen, Q.; Liu, S. Identification and characterization of the phosphate-solubilizing bacterium Pantoea sp. S32 in reclamation soil in Shanxi, China. Front. Microbiol. 2019, 10, 2171. [Google Scholar] [CrossRef] [Green Version]
  72. Pii, Y.; Mimmo, T.; Tomasi, N.; Terzano, R.; Cesco, S.; Crecchio, C. Microbial interactions in the rhizosphere: Beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol. Fertil. Soils 2015, 51, 403–415. [Google Scholar] [CrossRef]
  73. Castillo-Aguilar, C.; Garruña, R.; Zúñiga-Aguilar, J.J.; Guzmán-Antonio, A.A. PGPR inoculation improves growth, nutrient uptake and physiological parameters of Capsicum chinense plants. Phyton Int. J. Exp. Bot. 2017, 86, 199–204. [Google Scholar] [CrossRef]
  74. Almaghrabi, O.A.; Abdelmoneim, T.S.; Albishri, H.M.; Moussa, T.A. Enhancement of maize growth using some plant growth promoting rhizobacteria (PGPR) under laboratory conditions. Life Sci. J. 2014, 11, 764–772. [Google Scholar]
  75. Nezarat, S.; Gholami, A. Screening plant growth promoting rhizobacteria for improving seed germination, seedling growth and yield of maize. Pak. J. Biol. Sci. 2009, 12, 26–32. [Google Scholar] [CrossRef] [PubMed]
  76. Rana, A.; Saharan, B.; Joshi, M.; Prasanna, R.; Kumar, K.; Nain, L. Identification of multi-trait PGPR isolates and evaluating their potential as inoculants for wheat. Ann. Microbiol. 2011, 61, 893–900. [Google Scholar] [CrossRef]
  77. Cassán, F.D.; Lucangeli, C.D.; Bottini, R.; Piccoli, P.N. Azospirillum spp. metabolize [17,17-2H2] gibberellin A20 to [17,17-2H2] gibberellin A1 in vivo in dy rice mutant seedlings. Plant Cell Physiol. 2001, 42, 763–767. [Google Scholar] [CrossRef] [Green Version]
  78. Tahir, H.A.S.; Gu, Q.; Wu, H.; Raza, W.; Hanif, A.; Wu, L.; Colman, M.V.; Gao, X. Plant growth promotion by volatile organic compounds produced by Bacillus subtilis SYST2. Front. Microbiol. 2017, 8, 171. [Google Scholar] [CrossRef] [Green Version]
  79. Barnawal, D.; Bharti, N.; Pandey, S.S.; Pandey, A.; Chanotiya, C.S.; Kalra, A. Plant growth-promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression. Physiol. Plant. 2017, 161, 502–514. [Google Scholar] [CrossRef] [Green Version]
  80. Jang, J.H.; Woo, S.Y.; Kim, S.H.; Khaine, I.; Kwak, M.J.; Lee, H.K.; Lee, T.Y.; Lee, W.Y. Effects of increased soil fertility and plant growth-promoting rhizobacteria inoculation on biomass yield, energy value, and physiological response of poplar in short-rotation coppices in a reclaimed tideland: A case study in the Saemangeum area of Korea. Biomass Bioenergy 2017, 107, 29–38. [Google Scholar] [CrossRef]
  81. Islam, S.; Akanda, A.M.; Prova, A.; Islam, M.T.; Hossain, M.M. Isolation and identification of plant growth promoting rhizobacteria from cucumber rhizosphere and their effect on plant growth promotion and disease suppression. Front. Microbiol. 2016, 6, 1360. [Google Scholar] [CrossRef] [Green Version]
  82. Ahmad, M.; Zahir, Z.A.; Asghar, H.N.; Asghar, M. Inducing salt tolerance in mung bean through coinoculation with rhizobia and plant-growth promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylate deaminase. Can. J. Microbiol. 2011, 57, 578–589. [Google Scholar] [CrossRef]
  83. Pandey, S.; Ghosh, P.K.; Ghosh, S.; De, T.K.; Maiti, T.K. Role of heavy metal resistant Ochrobactrum sp. and Bacillus spp. strains in bioremediation of a rice cultivar and their PGPR like activities. J. Microbiol. 2013, 51, 11–17. [Google Scholar] [CrossRef]
  84. Khan, N.; Bano, A. Role of plant growth promoting rhizobacteria and Ag-nano particle in the bioremediation of heavy metals and maize growth under municipal wastewater irrigation. Int. J. Phytoremediat. 2016, 18, 211–221. [Google Scholar] [CrossRef] [PubMed]
  85. Das, A.J.; Kumar, R. Bioremediation of petroleum contaminated soil to combat toxicity on Withania somnifera through seed priming with biosurfactant producing plant growth promoting rhizobacteria. J. Environ. Manag. 2016, 174, 79–86. [Google Scholar] [CrossRef] [PubMed]
  86. Kalam, S.; Basu, A.; Ankati, S. Plant root-associated biofilms in bioremediation. In Biofilms in Plant and Soil Health; Ahmad, I., Husain, F.M., Eds.; John Wiley & Sons, Ltd.: Chichester, UK, 2017; pp. 337–355. [Google Scholar]
  87. Patel, P.; Shaikh, S.; Sayyed, R. Dynamism of PGPR in bioremediation and plant growth promotion in heavy metal contaminated soil. Indian J. Exp. Biol. 2016, 54, 286–290. [Google Scholar] [PubMed]
  88. Sayyed, R.Z.; Patel, P.R.; Shaikh, S.S. Plant growth promotion and root colonization by EPS producing Enterobacter sp. RZS5 under heavy metal contaminated soil. Indian J. Exp. Biol. 2015, 53, 116–123. [Google Scholar] [PubMed]
  89. Banchio, E.; Xie, X.; Zhang, H.; Paré, P.W. Soil bacteria elevate essential oil accumulation and emissions in sweet basil. J. Agric. Food Chem. 2009, 57, 653–657. [Google Scholar] [CrossRef]
  90. Ordookhani, K.; Sharafzadeh, S.; Zare, M. Influence of PGPR on growth, essential oil and nutrients uptake of sweet basil. Adv. Environ. Biol. 2011, 5, 672–677. [Google Scholar]
  91. Etesami, H.; Maheshwari, D.K. Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: Action mechanisms and future prospects. Ecotoxicol. Environ. Saf. 2018, 156, 225–246. [Google Scholar] [CrossRef]
  92. Mahdi, I.; Fahsi, N.; Hafidi, M.; Allaoui, A.; Biskri, L. Plant growth enhancement using rhizospheric halotolerant phosphate solubilizing bacterium Bacillus licheniformis QA1 and Enterobacter asburiae QF11 isolated from Chenopodium quinoa willd. Microorganisms 2020, 8, 948. [Google Scholar] [CrossRef]
  93. Etesami, H.; Alikhani, H.A.; Mirseyed Hosseini, H. Indole-3-acetic acid and 1-aminocyclopropane-1-carboxylate deaminase: Bacterial traits required in rhizosphere, rhizoplane and/or endophytic competence by beneficial bacteria. In Bacterial Metabolites in Sustainable Agroecosystem; Maheshwari, D.K., Ed.; Springer: Cham, Switzerland, 2015; pp. 183–258. [Google Scholar]
  94. Umesha, S.; Singh, P.K.; Singh, R.P. Microbial biotechnology and sustainable agriculture. In Biotechnology for Sustainable Agriculture: Emerging Approaches and Strategies; Singh, R.L., Mondal, S., Eds.; Woodhead Publishing: Cambridge, UK, 2018; pp. 185–205. [Google Scholar]
  95. Gouda, S.; Kerry, R.G.; Das, G.; Paramithiotis, S.; Shin, H.-S.; Patra, J.K. Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiol. Res. 2018, 206, 131–140. [Google Scholar] [CrossRef]
  96. Khatoon, Z.; Huang, S.; Rafique, M.; Fakhar, A.; Kamran, M.A.; Santoyo, G. Unlocking the potential of plant growth-promoting rhizobacteria on soil health and the sustainability of agricultural systems. J. Environ. Manag. 2020, 273, 111118. [Google Scholar] [CrossRef]
  97. Oleńska, E.; Małek, W.; Wójcik, M.; Swiecicka, I.; Thijs, S.; Vangronsveld, J. Beneficial features of plant growth-promoting rhizobacteria for improving plant growth and health in challenging conditions: A methodical review. Sci. Total Environ. 2020, 743, 140682. [Google Scholar] [CrossRef] [PubMed]
  98. Beneduzi, A.; Ambrosini, A.; Passaglia, L.M.P. Plant growth-promoting rhizobacteria (PGPR): Their potential as antagonists and biocontrol agents. Genet. Mol. Biol. 2012, 35, 1044–1051. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  99. Glick, B.R. Plant growth-promoting bacteria: Mechanisms and applications. Scientifica 2012, 2012, 963401. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  100. Glick, B.R. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol. Res. 2014, 169, 30–39. [Google Scholar] [CrossRef] [PubMed]
  101. Singh, I. Plant growth promoting rhizobacteria (PGPR) and their various mechanisms for plant growth enhancement in stressful conditions: A review. Eur. J. Biol. Res. 2018, 8, 191–213. [Google Scholar] [CrossRef]
  102. Kumar, A.; Bahadur, I.; Maurya, B.R.; Raghuwanshi, R.; Meena, V.S.; Singh, D.K.; Dixit, J. Does a plant growth promoting rhizobacteria enhance agricultural sustainability? J. Pure Appl. Microbiol. 2015, 9, 715–724. [Google Scholar]
  103. Berg, G.; Köberl, M.; Rybakova, D.; Müller, H.; Grosch, R.; Smalla, K. Plant microbial diversity is suggested as the key to future biocontrol and health trends. Fems Microbiol. Ecol. 2017, 93, 50. [Google Scholar] [CrossRef]
  104. Sayyed, R.Z.; Seifi, S.; Patel, P.R.; Shaikh, S.S.; Jadhav, H.P.; El Enshasy, H. Siderophore production in groundnut rhizosphere isolate, Achromobacter sp. RZS2 influenced by physicochemical factors and metal ions. Environ. Sustain. 2019, 2, 117–124. [Google Scholar] [CrossRef]
  105. García-Fraile, P.; Menéndez, E.; Rivas, R. Role of bacterial biofertilizers in agriculture and forestry. Aims Bioeng. 2015, 2, 183–205. [Google Scholar] [CrossRef]
  106. Vacheron, J.; Desbrosses, G.; Bouffaud, M.L.; Touraine, B.; Moënne-Loccoz, Y.; Muller, D.; Legendre, L.; Wisniewski-Dyé, F.; Prigent-Combaret, C. Plant growth-promoting rhizobacteria and root system functioning. Front. Plant Sci. 2013, 4, 356. [Google Scholar] [CrossRef] [Green Version]
  107. Timmusk, S.; Behers, L.; Muthoni, J.; Muraya, A.; Aronsson, A.C. Perspectives and challenges of microbial application for crop improvement. Front. Plant Sci. 2017, 8, 49. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  108. Soumare, A.; Diedhiou, A.G.; Thuita, M.; Hafidi, M.; Ouhdouch, Y.; Gopalakrishnan, S.; Kouisni, L. Exploiting biological nitrogen fixation: A route towards a sustainable agriculture. Plants 2020, 9, 1011. [Google Scholar] [CrossRef] [PubMed]
  109. Ferguson, B.J.; Mens, C.; Hastwell, A.H.; Zhang, M.; Su, H.; Jones, C.H.; Chu, X.; Gresshoff, P.M. Legume nodulation: The host controls the party. Plant. Cell Environ. 2019, 42, 41–51. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  110. García-Fraile, P.; Menéndez, E.; Celador-Lera, L.; Díez-Méndez, A.; Jiménez-Gómez, A.; Marcos-García, M.; Cruz-González, X.A.; Martínez-Hidalgo, P.; Mateos, P.F.; Rivas, R. Bacterial probiotics: A truly green revolution. In Probiotics and Plant Health; Kumar, V., Kumar, M., Sharma, S., Prasad, R., Eds.; Springer: Singapore, 2017; pp. 131–162. [Google Scholar]
  111. Dal Cortivo, C.; Ferrari, M.; Visioli, G.; Lauro, M.; Fornasier, F.; Barion, G.; Panozzo, A.; Vamerali, T. Effects of seed-applied biofertilizers on rhizosphere biodiversity and growth of common wheat (Triticum aestivum L.) in the field. Front. Plant Sci. 2020, 11, 72. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  112. Aloo, B.N.; Makumba, B.A.; Mbega, E.R. Plant growth promoting rhizobacterial biofertilizers for sustainable crop production: The past, present, and future. Preprints 2020, 2020090650. [Google Scholar] [CrossRef]
  113. Adeleke, R.A.; Raimi, A.R.; Roopnarain, A.; Mokubedi, S.M. Status and prospects of bacterial inoculants for sustainable management of agroecosystems. In Biofertilizers for Sustainable Agriculture and Environment; Giri, B., Prasad, R., Wu, Q.-S., Varma, A., Eds.; Springer: Cham, Switzerland, 2019; pp. 137–172. [Google Scholar]
  114. Mustafa, S.; Kabir, S.; Shabbir, U.; Batool, R. Plant growth promoting rhizobacteria in sustainable agriculture: From theoretical to pragmatic approach. Symbiosis 2019, 78, 115–123. [Google Scholar] [CrossRef]
  115. Mącik, M.; Gryta, A.; Frąc, M. Biofertilizers in agriculture: An overview on concepts, strategies and effects on soil microorganisms. In Advances in Agronomy; Sparks, D.L., Ed.; Academic Press Inc.: Cambridge, MA, USA, 2020; Volume 162, pp. 31–87. [Google Scholar]
  116. Artyszak, A.; Gozdowski, D. The effect of growth activators and plant growth-promoting rhizobacteria (PGPR) on the soil properties, root yield, and technological quality of sugar beet. Agronomy 2020, 10, 1262. [Google Scholar] [CrossRef]
  117. Uribe, D.; Sánchez-Nieves, J.; Vanegas, J. Role of microbial biofertilizers in the development of a sustainable agriculture in the Tropics. In Soil Biology and Agriculture in the Tropics; Dion, P., Ed.; Springer: Berlin/Heidelberg, Germany, 2010; pp. 235–250. [Google Scholar]
  118. Mehnaz, S. An overview of globally available bioformulations. In Bioformulations: For Sustainable Agriculture; Arora, N., Mehnaz, S., Balestrini, R., Eds.; Springer: New Delhi, India, 2016; pp. 268–281. [Google Scholar]
  119. Sessitsch, A.; Mitter, B. 21st century agriculture: Integration of plant microbiomes for improved crop production and food security. Microb. Biotechnol. 2015, 8, 32–33. [Google Scholar] [CrossRef]
  120. Cardinale, M.; Ratering, S.; Suarez, C.; Zapata Montoya, A.M.; Geissler-Plaum, R.; Schnell, S. Paradox of plant growth promotion potential of rhizobacteria and their actual promotion effect on growth of barley (Hordeum vulgare L.) under salt stress. Microbiol. Res. 2015, 181, 22–32. [Google Scholar] [CrossRef]
  121. Amara, U.; Khalid, R.; Hayat, R. Soil bacteria and phytohormones for sustainable crop production. In Bacterial Metabolites in Sustainable Agroecosystem; Maheshwari, D.K., Ed.; Springer: Cham, Switzerland, 2015; pp. 87–103. [Google Scholar] [CrossRef]
  122. Kamilova, F.; Okon, Y.; Deweert, S.; Horal, K. Commercialization of microbes: Manufacturing, inoculation, best practice for objective field testing, and registration. In Principles of Plant-Microbe Interactions: Microbes for Sustainable Agriculture; Lugtenberg, B., Ed.; Springer: Cham, Switzerland, 2015; pp. 319–327. [Google Scholar] [CrossRef]
  123. Thomas, L.; Singh, I. Microbial biofertilizers: Types and applications. In Biofertilizers for Sustainable Agriculture and Environment; Giri, B., Prasad, R., Wu, Q.S., Varma, A., Eds.; Springer: Cham, Switzerland, 2019; pp. 1–19. [Google Scholar]
  124. Arora, N.K.; Khare, E.; Maheshwari, D.K. Plant growth promoting rhizobacteria: Constraints in bioformulation, commercialization, and future strategies. In Plant Growth and Health Promoting Bacteria; Maheshwari, D., Ed.; Springer: Berlin/Heidelberg, Germany, 2010; pp. 97–116. [Google Scholar]
  125. Du Jardin, P. Plant biostimulants: Definition, concept, main categories and regulation. Sci. Hortic. 2015, 196, 3–14. [Google Scholar] [CrossRef] [Green Version]
  126. Barea, J.M. Future challenges and perspectives for applying microbial biotechnology in sustainable agriculture based on a better understanding of plant-microbiome interactions. J. Soil Sci. Plant Nutr. 2015, 15, 261–282. [Google Scholar] [CrossRef]
  127. Parnell, J.J.; Berka, R.; Young, H.A.; Sturino, J.M.; Kang, Y.; Barnhart, D.M.; Dileo, M.V. From the lab to the farm: An industrial perspective of plant beneficial microorganisms. Front. Plant Sci. 2016, 7, 1110. [Google Scholar] [CrossRef] [PubMed]
  128. Ndeddy Aka, R.J.; Babalola, O.O. Effect of bacterial inoculation of strains of Pseudomonas aeruginosa, Alcaligenes feacalis and Bacillus subtilis on germination, growth and heavy metal (Cd, Cr, and Ni) uptake of Brassica juncea. Int. J. Phytoremediat. 2016, 18, 200–209. [Google Scholar] [CrossRef]
  129. Kumar, A.; Verma, H.; Singh, V.K.; Singh, P.P.; Singh, S.K.; Ansari, W.A.; Yadav, A.; Singh, P.K.; Pandey, K.D. Role of Pseudomonas sp. in sustainable agriculture and disease management. In Agriculturally Important Microbes for Sustainable Agriculture; Meena, V.S., Mishra, P.K., Bisht, J.K., Pattanayak, A., Eds.; Springer: Singapore, 2017; Volume 2, pp. 195–215. [Google Scholar]
  130. Malusà, E.; Pinzari, F.; Canfora, L. Efficacy of biofertilizers: Challenges to improve crop production. In Microbial Inoculants in Sustainable Agricultural Productivity; Singh, D.P., Singh, H.B., Prabha, R., Eds.; Springer: New Delhi, India, 2016; pp. 17–40. [Google Scholar]
  131. Dangi, S.R.; Tirado-Corbalá, R.; Gerik, J.; Hanson, B.D. Effect of long-term continuous fumigation on soil microbial communities. Agronomy 2017, 7, 37. [Google Scholar] [CrossRef] [Green Version]
  132. Bashan, Y.; de-Bashan, L.E.; Prabhu, S.R.; Hernandez, J.P. Advances in plant growth-promoting bacterial inoculant technology: Formulations and practical perspectives (1998–2013). Plant Soil 2014, 378, 1–33. [Google Scholar] [CrossRef] [Green Version]
Sustainability 13 01140 g001 550
Figure 1. Main overview of interactions between plant growth promoting rhizobacteria (PGPR), plants, and pathogens. PGPRs directly promote plant growth by improving nutrient acquisition by the plant and growth augmentation via regulating phytohormone levels. The indirect effects of PGPRs include suppression of phytopathogens and inducing systemic resistance in plants against a wide range of pathogenic microbes.
Figure 1. Main overview of interactions between plant growth promoting rhizobacteria (PGPR), plants, and pathogens. PGPRs directly promote plant growth by improving nutrient acquisition by the plant and growth augmentation via regulating phytohormone levels. The indirect effects of PGPRs include suppression of phytopathogens and inducing systemic resistance in plants against a wide range of pathogenic microbes.
Sustainability 13 01140 g001
Sustainability 13 01140 g002 550
Figure 2. Global biofertilizer market share by product typology (nitrogen-fixing and phosphate-solubilizing microbe-based biofertilizers and others). Market data of 2012 (left panel) and 2017 (right panel) respectively compiled from Timmusk et al. [107] and Soumare et al. [108].
Figure 2. Global biofertilizer market share by product typology (nitrogen-fixing and phosphate-solubilizing microbe-based biofertilizers and others). Market data of 2012 (left panel) and 2017 (right panel) respectively compiled from Timmusk et al. [107] and Soumare et al. [108].
Sustainability 13 01140 g002
Sustainability 13 01140 g003 550
Figure 3. Size and distribution of the global biofertilizer market in USD million per region. The area of each circle is proportional to the size of the biofertilizer market (in USD million) in the specific region. Data compiled from Soumare et al. [108].
Figure 3. Size and distribution of the global biofertilizer market in USD million per region. The area of each circle is proportional to the size of the biofertilizer market (in USD million) in the specific region. Data compiled from Soumare et al. [108].
Sustainability 13 01140 g003
Sustainability 13 01140 g004 550
Figure 4. Constraints in the utilization, production, and commercialization of PGPR-based biofertilizers.
Figure 4. Constraints in the utilization, production, and commercialization of PGPR-based biofertilizers.
Sustainability 13 01140 g004
Sustainability 13 01140 g005 550
Figure 5. A roadmap for commercializing PGPR-based biofertilizers.
Figure 5. A roadmap for commercializing PGPR-based biofertilizers.
Sustainability 13 01140 g005
Table
Table 1. An overview of the benefits of plant growth promoting rhizobacteria (PGPR) inoculation to plants.
Table 1. An overview of the benefits of plant growth promoting rhizobacteria (PGPR) inoculation to plants.
Benefits of PGPR Inoculation to PlantsPGPR Strain(s)Tested Plant(s)Reference(s)
Tolerance to drought stressPseudomonas fluorescens DR11, Enterobacter hormaechei DR16, Pseudomonas migulae DR35, Bacillus subtilis, Achromobacter piechaudii ARV8, Phyllobacterium brassicacearum, Paenibacillus polymyxa, Rhizobium tropici, Azospirillum brasilenseFoxtail millet (Setaria italica L.), Maize (Zea mays L.), Bean (Phaseolus vulgaris L.), Arabidopsis thaliana, Tomato (Lycopersicum esculentum Mill cv. F144), Pepper (Capsicum annuum L. cv. Maor), Wheat (Triticum aestivum L.)[36,54,55,56,57,58,59]
Tolerance to salinity stressBacillus pumilus, Exiguobacterium oxidotolerans, Bacillus megaterium, Azospirillum sp., Achromobacter piechaudii, Eneterobacter sp. PR14Brahmi (Bacopa monnieri L.), Maize (Zea mays L.), Lettuce (Lactuca sativa L.), Tomato (Lycopersicum esculentum Mill.), Rice (Oryza sativa cv. Sahbhagi), Sorghum (Sorghum bicolor), Finger Millets (Eleusine coracana)[60,61,62,63,64]
Tolerance to biotic stress (biocontrol) Paenibacillus xylanexedens, Bacillus amyloliquefaciens, Streptomyces sp., Ochrobacttrum intermedium, Paenibacillus lentimorbus, Pseudomonas spp.Wheat (Triticum aestivum L.), Rice (Oryza sativa), Pine (Pinus taeda L.), Tomato (Lycopersicum esculentum Mill.)[65,66,67,68,69,70]
Increased nutrient absorption Pantoea sp. S32, Paenibacillus polymyxa Rice (Oryza sativa L.), Habanero pepper (Capsicum chinense)[71,72,73]
Seed germination enhancementSerratia marcences, Pseudomonas fluorescens, Azospirillum lipoferum, Pseudomonas putida, Bacillus subtilis, Providencia sp., Brevundimonas diminutaMaize (Zea mays L.), Wheat (Triticum aestivum L.)[74,75,76]
Biostimulation by phytohormone(s) productionAzospirillum lipoferum, Bacillus subtilis, Arthrobacter protophormiae, Dietzia natronolimnaea, Bacillus sp.Rice (Oryza sativa L.), Tomato (Solanum lycopersicum L.), Wheat (Triticum aestivum L.)[46,77,78,79]
Soil fertility enhancementBacillus subtilis, Bacillus cereus, Rhizobium spp.Poplar (Populus sp.), Mung bean (Vigna radiata L.)[80,81,82]
Bioremediation of heavy metals and pollutantsOchrobactrum sp., Bacillus spp., Pseudomonas spp., Pseudomonas fluorescens, Bacillus cereus, Alcaligenes feacalis RZS2, Pseudomonas aeruginosa RZS3, Enterobacter sp. RZS5 Rice (Oryza sativa L.), Groundnut (Arachis hypogaea), Maize (Zea mays L.), Ashwagandha (Withania somnifera)[83,84,85,86,87,88]
Modulation of plant secondary metabolitesBacillus subtilis, Azotobacter chroococcum, Pseudomonas putida, Bacillus pumilus, Exiguobacterium oxidotoleransBasil (Ocimum basilicum), Brahmi (Bacopa monnieri L.)[89,90]
Table
Table 2. An overview of globally available PGPR-based biofertilizer products.
Table 2. An overview of globally available PGPR-based biofertilizer products.
Type of BiofertilizerName of BiofertilizerPGPR Strain(s)Manufacturer’s CountryMarket RegionReference(s)
Nitrogen fixerNitragin Gold® RhizobiaUSANorth America[110]
Cell-Tech®RhizobiaUSANorth America[110]
TagTeam®Rhizobia, Penicillium bilaiiUSANorth America[110]
Custom N2Paenibacillus polymyxaUSANorth America[110]
Nodulator®Bradyrhizobium japonicumCanadaNorth America[110]
Nodulator® PROBacillus subtilis, Bradyrhizobium japonicumCanadaNorth America[110]
Bioboots®Delftia acidovorans, Bradyrhizobium sp.CanadaNorth America[105,110]
Azofer® Azospirillum brasilenseMexicoNorth America[110]
Rhizofer®Rhizobium etliMexicoNorth America[110]
Nitrofix® Azospirillum sp.CubaNorth America[105,110]
Rhizosum N®Azotobacter vinelandii, Rhizophagus irregularisSpainEurope[110,111]
Rhizosum AquaAzospirillum sp.SpainEurope[105,110]
Legume Fix Rhizobium sp., Bradyrhizobium japonicumUKEurope[112,113]
BactoFil® A10Azospirillum brasilense, Azotobacter vinelandii, Bacllius megateriumHungaryEurope[112]
BactoFil® SoyaBradyrhizobium japonicumHungaryEurope[114]
Phylazonit MAzotobacter chroococcum, Bacillus megateriumHungaryEurope[115]
Azotobacterin®Azospirillum brasilense B-4485Russia Europe[105,110]
AzoterAzotobacter chroococcum, Azospirillum brasilense, Bacillus megateriumSlovakiaEurope[116]
TwinN®Azorhizobium sp., Azoarcus sp., Azospirillum sp.AustraliaAsia-Pacific[113]
TripleN®Azorhizobium spp., Azoarcus spp., Azospirillum spp.AustraliaAsia-Pacific[111]
Bio-NAzospirillum spp.Philippines, AustraliaAsia-Pacific[112,117]
BioGro®Pseudomonas fluorescens / putida, Klebsiella pneumoniae, Citrobacter freundii VietnamAsia-Pacific[117]
Mamezo®RhizobiaJapanAsia-Pacific[105,110]
Agrilife NitrofixAzotobacter chroococcum, A. vinelandii, Acetobacter diazotrophicus, Azospirillum lipoferum, Rhizobium japonicumIndiaAsia-Pacific[118]
Ajay AzospirillumAzospirillum sp.IndiaAsia-Pacific[112]
Symbion NAzospirillum sp., Rhizobium sp., Acetobacter sp., Azotobacter sp.IndiaAsia-Pacific[115]
Zadspirillum Azospirillum brasilenseArgentinaSouth America[112]
Rizo-LiqBradyrhizobium sp., Mesorhizobium ciceri, Rhizobium spp.ArgentinaSouth America[112,113]
Nodulest 10Bradyrhizobium japonicumArgentinaSouth America[118]
Rizo-Liq TopBradyrhizobium japonicumArgentinaSouth America[113]
BiAgro 10®Bradyrhizobium japonicumArgentina, Brazil, BoliviaSouth America[117]
Dimargon®Azotobacter chroococcumColombia South America[117]
NitrasecRhizobium sp.UruguaySouth America[112]
BiofixRhizobiaKenyaAfrica[112,113]
NodumaxBradyrhizobium spp.NigeriaAfrica[112,113]
Azo-NAzospirillum brasilense, A. lipoferumSouth AfricaAfrica[113]
Azo-N PlusAzospirillum brasilense, A. lipoferum, Azotobacter chroococcumSouth AfricaAfrica[113]
Phosphate solubilizerFosforina®Pseudomonas fluorescensCubaNorth America[117]
Rhizosum PK®Bacillus megaterium, Frateuria aurantia, Rhizophagus irregularisSpainEurope[110,111]
PhosphobacterinBacillus megaterium var. phosphaticumRussiaEurope[31]
CataPultBacillus spp., Glomus intraradices AustraliaAsia-Pacific[118]
Symbion van PlusBacillus megateriumIndiaAsia-Pacific[112]
P Sol BPseudomonas striata, Bacillus polymyxa, B. megateriumIndiaAsia-Pacific[115,118]
CBFBacillus mucilaginosus, B. subtilisChinaAsia-Pacific[117]
Bio Phos®Bacillus megateriumSri LankaAsia-Pacific[115,118]
Potassium solubilizerRhizosum K Frateuria aurantiaSpainEurope[105,110]
K Sol BFrateuria aurantiaIndiaAsia-Pacific[118]
Zinc solubilizerBiozink®PGPR consortiaIndiaAsia-Pacific[110]
Zn Sol BThiobacillus thiooxidansIndiaAsia-Pacific[118]
PhytostimulatorEVL Coating®PGPR consortiaCanadaNorth America[105]
Amase®Pseudomonas azotoformansSwedenEurope[114,118]
Bio GoldAzotobacter chroococcum, Pseudomonas fluorescensSri LankaAsia-Pacific[115,118]
Bioativo PGPR consortiaBrazilSouth America[112]
BiocontrolCedomon®Pseudomonas chlororaphisSwedenEurope[114]
Cedress®Pseudomonas chlororaphisSwedenEurope[114]
Cerall®Pseudomonas chlororaphisSwedenEurope[114]
BiotilisBacillus subtilisIndiaAsia-Pacific[118]
SoilfixBrevibacillus laterosporus, Paenibacillus chitinolyticusSouth AfricaAfrica[112]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Basu, A.; Prasad, P.; Das, S.N.; Kalam, S.; Sayyed, R.Z.; Reddy, M.S.; El Enshasy, H. Plant Growth Promoting Rhizobacteria (PGPR) as Green Bioinoculants: Recent Developments, Constraints, and Prospects. Sustainability 2021, 13, 1140. https://doi.org/10.3390/su13031140

AMA Style

Basu A, Prasad P, Das SN, Kalam S, Sayyed RZ, Reddy MS, El Enshasy H. Plant Growth Promoting Rhizobacteria (PGPR) as Green Bioinoculants: Recent Developments, Constraints, and Prospects. Sustainability. 2021; 13(3):1140. https://doi.org/10.3390/su13031140

Chicago/Turabian Style

Basu, Anirban, Priyanka Prasad, Subha Narayan Das, Sadaf Kalam, R. Z. Sayyed, M. S. Reddy, and Hesham El Enshasy. 2021. "Plant Growth Promoting Rhizobacteria (PGPR) as Green Bioinoculants: Recent Developments, Constraints, and Prospects" Sustainability 13, no. 3: 1140. https://doi.org/10.3390/su13031140

APA Style

Basu, A., Prasad, P., Das, S. N., Kalam, S., Sayyed, R. Z., Reddy, M. S., & El Enshasy, H. (2021). Plant Growth Promoting Rhizobacteria (PGPR) as Green Bioinoculants: Recent Developments, Constraints, and Prospects. Sustainability, 13(3), 1140. https://doi.org/10.3390/su13031140

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop