sustainability

Review
Plant Growth Promoting Rhizobacteria (PGPR) as Green
Bioinoculants: Recent Developments, Constraints,
and Prospects
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;
anirbanbasu99@gmail.com
2 Department of Botany, Indira Gandhi National Tribal University, Amarkantak 484887, India;
prasadpriyanka696@gmail.com (P.P.); subha.bunu@igntu.ac.in (S.N.D.)
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; prof.m.s.reddy@gmail.com
6 Institute of Bioproduct Development (IBD), Universiti Teknologi Malaysia (UTM), Skudai, Johor Bahru 81310,
Malaysia; henshasy@ibd.utm.my
7 City of Scientific Research and Technology Applications, Alexandria 21934, Egypt
* Correspondence: sadaf2577@gmail.com (S.K.); sayyedrz@gmail.com (R.Z.S.)

Abstract: The quest for enhancing agricultural yields due to increased pressure on food produc-
tion 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
Citation: Basu, A.; Prasad, P.; Das, eco-friendly manner. They contain living or dormant microbes, which are applied to the soil or used
S.N.; Kalam, S.; Sayyed, R.Z.; Reddy,
for treating crop seeds. One of the foremost candidates in this respect is rhizobacteria. Plant growth
M.S.; El Enshasy, H. Plant Growth
promoting rhizobacteria (PGPR) are an important cluster of beneficial, root-colonizing bacteria thriv-
Promoting Rhizobacteria (PGPR) as
ing in the plant rhizosphere and bulk soil. They exhibit synergistic and antagonistic interactions
Green Bioinoculants: Recent
with the soil microbiota and engage in an array of activities of ecological significance. They promote
Developments, Constraints, and
Prospects. Sustainability 2021, 13,
plant growth by facilitating biotic and abiotic stress tolerance and support the nutrition of host plants.
1140. https://doi.org/10.3390/ Due to their active growth endorsing activities, PGPRs are considered an eco-friendly alternative to
su13031140 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
Received: 24 December 2020 has several pros and cons. Application of potential biofertilizers that perform well in the laboratory
Accepted: 18 January 2021 and greenhouse conditions often fails to deliver the expected effects on plant development in field
Published: 22 January 2021 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
Publisher’s Note: MDPI stays neutral to promote sustainable agriculture.
with regard to jurisdictional claims in
published maps and institutional affil-
Keywords: biofertilizer; bioinoculant; PGPR; rhizosphere; sustainable agriculture
iations.

1. Introduction
Copyright: © 2021 by the authors.
The advent of the Green Revolution in the latter part of the twentieth century triggered
Licensee MDPI, Basel, Switzerland.
a worldwide boom in the agriculture sector. By introducing new high-yielding seed
This article is an open access article
varieties and increasing the use of synthetic fertilizers, pesticides, and other agrochemicals,
distributed under the terms and
the Green Revolution contributed significantly to enhanced plant productivity and crop
conditions of the Creative Commons
Attribution (CC BY) license (https://
yields [1]. The global agricultural landscape has drastically changed since then. Rampant
creativecommons.org/licenses/by/
overuse of synthetic agrochemicals for enhancing crop productivity has deteriorated the
4.0/). biological and physicochemical health of the arable soil, leading to a declining trend

Sustainability 2021, 13, 1140. https://doi.org/10.3390/su13031140 https://www.mdpi.com/journal/sustainability

Sustainability 2021, 13, 1140 2 of 20

in agricultural productivity across the globe over the past few decades [2–4]. 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 manipula-
tion 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 [10–12]. 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 micro-
bial formulations to fertilize agricultural crops [13–15]. The use of efficient plant growth
promoting rhizobacteria (PGPR) as biofertilizers and biological control agents is deliber-
ated as a suitable substitute for minimizing the use of synthetic agrochemicals in crop
production [16–19]. 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 sub-
stance 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]. Dineshku-
mar 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 pro-
vide 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 [21–24]. 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 hor-
mones [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 [27–29].
The microbial inoculants possess several advantages over their chemical counter-
parts [30–32]. 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 [8,33–36]. Vari-
ous microbial taxa have been commercially used as efficient biofertilizers, based on their
Sustainability 2021, 13, 1140 3 of 20

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 colo-
nized 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 emer-
gence of seedlings [45–50]. Reported PGPRs include members of the genera Acinetobacter,
Aeromonas, Agrobacterium, Allorhizobium, Arthrobacter, Azoarcus, Azorhizobium, Azospirillum,
Azotobacter, Bacillus, Bradyrhizobium, Burkholderia, Caulobacter, Chromobacterium, Delftia, En-
terobacter, Flavobacterium, Frankia, Gluconacetobacter, Klebsiella, Mesorhizobium, Micrococcus,
Paenibacillus, Pantoea, Pseudomonas, Rhizobium, Serratia, Streptomyces, Thiobacillus, and oth-
ers [16,43,44,46,51–53]. 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 com-
munities.
Sustainability 2021, 13, 1140 4 of 20

Table 1. An overview of the benefits of plant growth promoting rhizobacteria (PGPR) inoculation to plants.

Benefits of PGPR
PGPR Strain(s) Tested Plant(s) Reference(s)
Inoculation to Plants
Pseudomonas fluorescens DR11, Foxtail millet (Setaria italica L.),
Enterobacter hormaechei DR16, Maize (Zea mays L.), Bean
Pseudomonas migulae DR35, Bacillus (Phaseolus vulgaris L.), Arabidopsis
Tolerance to drought stress subtilis, Achromobacter piechaudii ARV8, thaliana, Tomato (Lycopersicum [36,54–59]
Phyllobacterium brassicacearum, esculentum Mill cv. F144), Pepper
Paenibacillus polymyxa, Rhizobium tropici, (Capsicum annuum L. cv. Maor),
Azospirillum brasilense Wheat (Triticum aestivum L.)
Brahmi (Bacopa monnieri L.),
Maize (Zea mays L.), Lettuce
Bacillus pumilus, Exiguobacterium
(Lactuca sativa L.), Tomato
oxidotolerans, Bacillus megaterium,
Tolerance to salinity stress (Lycopersicum esculentum Mill.), [60–64]
Azospirillum sp., Achromobacter piechaudii,
Rice (Oryza sativa cv. Sahbhagi),
Eneterobacter sp. PR14
Sorghum (Sorghum bicolor), Finger
Millets (Eleusine coracana)
Paenibacillus xylanexedens, Bacillus Wheat (Triticum aestivum L.), Rice
Tolerance to biotic stress amyloliquefaciens, Streptomyces sp., (Oryza sativa), Pine (Pinus taeda L.),
[65–70]
(biocontrol) Ochrobacttrum intermedium, Paenibacillus Tomato (Lycopersicum
lentimorbus, Pseudomonas spp. esculentum Mill.)
Rice (Oryza sativa L.), Habanero
Increased nutrient absorption Pantoea sp. S32, Paenibacillus polymyxa [71–73]
pepper (Capsicum chinense)
Serratia marcences, Pseudomonas fluorescens,
Seed germination Azospirillum lipoferum, Pseudomonas putida, Maize (Zea mays L.), Wheat
[74–76]
enhancement Bacillus subtilis, Providencia sp., (Triticum aestivum L.)
Brevundimonas diminuta
Azospirillum lipoferum, Bacillus subtilis, Rice (Oryza sativa L.), Tomato
Biostimulation by
Arthrobacter protophormiae, Dietzia (Solanum lycopersicum L.), Wheat [46,77–79]
phytohormone(s) production
natronolimnaea, Bacillus sp. (Triticum aestivum L.)
Bacillus subtilis, Bacillus cereus, Rhizobium Poplar (Populus sp.), Mung bean
Soil fertility enhancement [80–82]
spp. (Vigna radiata L.)
Ochrobactrum sp., Bacillus spp.,
Rice (Oryza sativa L.), Groundnut
Pseudomonas spp., Pseudomonas fluorescens,
Bioremediation of heavy (Arachis hypogaea), Maize (Zea
Bacillus cereus, Alcaligenes feacalis RZS2, [83–88]
metals and pollutants mays L.), Ashwagandha (Withania
Pseudomonas aeruginosa RZS3, Enterobacter
somnifera)
sp. RZS5
Bacillus subtilis, Azotobacter chroococcum,
Modulation of plant Basil (Ocimum basilicum), Brahmi
Pseudomonas putida, Bacillus pumilus, [89,90]
secondary metabolites (Bacopa monnieri L.)
Exiguobacterium oxidotolerans

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 multi-
faceted 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 mecha-
nisms of PGPR action and their specific contribution to plant growth promotion have been
reviewed comprehensively [30,41–44,47–49,51,52,93–102]. 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).
Sustainability 2021, 13, 1140 5 of 20

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.

Direct modes of PGPR action include improving plant nutrition by providing phy-
tonutrients 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 sub-
stances (like hydrogen cyanide, siderophores, antibiotics, and antimicrobial metabolites)
and lytic enzymes (like chitinases, glucanases, and proteases), and inducing systemic resis-
tance 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].
Sustainability 2021, 13, 1140 6 of 20

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].

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.

Figure 3. Size and distribution of the global biofertilizer market in USD million per region. The area of each circle is propor-
tional to the size of the biofertilizer market (in USD million) in the specific region. Data compiled from Soumare et al. [108].
Sustainability 2021, 13, 1140 7 of 20

Table 2. An overview of globally available PGPR-based biofertilizer products.

Type of Manufacturer’s
Name of Biofertilizer PGPR Strain(s) Market Region Reference(s)
Biofertilizer Country
Nitragin Gold® Rhizobia USA North America [110]
Cell-Tech® Rhizobia USA North America [110]
Rhizobia,
TagTeam® USA North America [110]
Penicillium bilaii
Paenibacillus
Custom N2 USA North America [110]
polymyxa
Bradyrhizobium
Nodulator® Canada North America [110]
japonicum
Bacillus subtilis,
Nodulator® PRO Bradyrhizobium Canada North America [110]
japonicum
Delftia acidovorans,
Bioboots® Canada North America [105,110]
Bradyrhizobium sp.
Azospirillum
Azofer® Mexico North America [110]
brasilense
Rhizofer® Rhizobium etli Mexico North America [110]
Nitrofix® Azospirillum sp. Cuba North America [105,110]
Azotobacter
vinelandii,
Rhizosum N® Spain Europe [110,111]
Rhizophagus
Nitrogen fixer irregularis
Rhizosum Aqua Azospirillum sp. Spain Europe [105,110]
Rhizobium sp.,
Legume Fix Bradyrhizobium UK Europe [112,113]
japonicum
Azospirillum
brasilense,
BactoFil® A10 Azotobacter Hungary Europe [112]
vinelandii, Bacllius
megaterium
Bradyrhizobium
BactoFil® Soya Hungary Europe [114]
japonicum
Azotobacter
Phylazonit M chroococcum, Hungary Europe [115]
Bacillus megaterium
Azospirillum
Azotobacterin® Russia Europe [105,110]
brasilense B-4485
Azotobacter
chroococcum,
Azoter Azospirillum Slovakia Europe [116]
brasilense, Bacillus
megaterium
Azorhizobium sp.,
TwinN® Azoarcus sp., Australia Asia-Pacific [113]
Azospirillum sp.
Azorhizobium spp.,
TripleN® Azoarcus spp., Australia Asia-Pacific [111]
Azospirillum spp.
Sustainability 2021, 13, 1140 8 of 20

Table 2. Cont.

Type of Manufacturer’s
Name of Biofertilizer PGPR Strain(s) Market Region Reference(s)
Biofertilizer Country
Philippines,
Bio-N Azospirillum spp. Asia-Pacific [112,117]
Australia
Pseudomonas
fluorescens / putida,
BioGro® Klebsiella Vietnam Asia-Pacific [117]
pneumoniae,
Citrobacter freundii
Mamezo® Rhizobia Japan Asia-Pacific [105,110]
Azotobacter
chroococcum, A.
vinelandii,
Acetobacter
Agrilife Nitrofix diazotrophicus, India Asia-Pacific [118]
Azospirillum
lipoferum,
Rhizobium
japonicum
Ajay Azospirillum Azospirillum sp. India Asia-Pacific [112]
Azospirillum sp.,
Rhizobium sp.,
Symbion N India Asia-Pacific [115]
Acetobacter sp.,
Azotobacter sp.
Nitrogen fixer Azospirillum
Zadspirillum Argentina South America [112]
brasilense
Bradyrhizobium sp.,
Mesorhizobium
Rizo-Liq Argentina South America [112,113]
ciceri, Rhizobium
spp.
Bradyrhizobium
Nodulest 10 Argentina South America [118]
japonicum
Bradyrhizobium
Rizo-Liq Top Argentina South America [113]
japonicum
Bradyrhizobium Argentina, Brazil,
BiAgro 10® South America [117]
japonicum Bolivia
Azotobacter
Dimargon® Colombia South America [117]
chroococcum
Nitrasec Rhizobium sp. Uruguay South America [112]
Biofix Rhizobia Kenya Africa [112,113]
Bradyrhizobium
Nodumax Nigeria Africa [112,113]
spp.
Azospirillum
Azo-N brasilense, A. South Africa Africa [113]
lipoferum
Azospirillum
brasilense, A.
Azo-N Plus lipoferum, South Africa Africa [113]
Azotobacter
chroococcum
Sustainability 2021, 13, 1140 9 of 20

Table 2. Cont.

Type of Manufacturer’s
Name of Biofertilizer PGPR Strain(s) Market Region Reference(s)
Biofertilizer Country
Pseudomonas
Fosforina® Cuba North America [117]
fluorescens
Bacillus megaterium,
Frateuria aurantia,
Rhizosum PK® Spain Europe [110,111]
Rhizophagus
irregularis
Bacillus megaterium
Phosphobacterin Russia Europe [31]
var. phosphaticum
Phosphate
solubilizer Bacillus spp.,
CataPult Australia Asia-Pacific [118]
Glomus intraradices
Symbion van Plus Bacillus megaterium India Asia-Pacific [112]
Pseudomonas striata,
P Sol B Bacillus polymyxa, India Asia-Pacific [115,118]
B. megaterium
Bacillus
CBF mucilaginosus, China Asia-Pacific [117]
B. subtilis
Bio Phos® Bacillus megaterium Sri Lanka Asia-Pacific [115,118]
Potassium Rhizosum K Frateuria aurantia Spain Europe [105,110]
solubilizer K Sol B Frateuria aurantia India Asia-Pacific [118]
Biozink® PGPR consortia India Asia-Pacific [110]
Zinc solubilizer Thiobacillus
Zn Sol B India Asia-Pacific [118]
thiooxidans
EVL Coating® PGPR consortia Canada North America [105]
Pseudomonas
Amase® Sweden Europe [114,118]
azotoformans
Phytostimulator Azotobacter
chroococcum,
Bio Gold Sri Lanka Asia-Pacific [115,118]
Pseudomonas
fluorescens
Bioativo PGPR consortia Brazil South America [112]
Pseudomonas
Cedomon® Sweden Europe [114]
chlororaphis
Pseudomonas
Cedress® Sweden Europe [114]
chlororaphis

Biocontrol Pseudomonas
Cerall® Sweden Europe [114]
chlororaphis
Biotilis Bacillus subtilis India Asia-Pacific [118]
Brevibacillus
laterosporus,
Soilfix South Africa Africa [112]
Paenibacillus
chitinolyticus

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
Sustainability 2021, 13, 1140 10 of 20

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).

Figure 4. Constraints in the utilization, production, and commercialization of PGPR-based biofertilizers.

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 PG-
PRs 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 rhi-
zobacteria do not possess the same mechanisms of action for plant growth promotion [121].
Several Gram-negative rhizobacteria are known to exhibit biocontrol potential. The con-
Sustainability 2021, 13, 1140 11 of 20

straint 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 unavail-
ability 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
Sustainability 2021, 13, 1140 12 of 20

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.
Sustainability 2021, 13, 1140 13 of 20

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 biofertiliz-
ers [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 biofertiliz-
ers 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) speci-
fied 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 microorgan-
isms start interacting with other microbiota in the rhizosphere and begin colonizing
the rhizosphere.
Sustainability 2021, 13, 1140 14 of 20

(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].

Figure 5. A roadmap for commercializing PGPR-based biofertilizers.

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
Sustainability 2021, 13, 1140 15 of 20

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, In-
dia, 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.
[CrossRef]
2. Pingali, P.L. Green revolution: Impacts, limits, and the path ahead. Proc. Natl. Acad. Sci. USA 2012, 109, 12302–12308. [CrossRef]
[PubMed]
3. Yang, X.; Fang, S. Practices, perceptions, and implications of fertilizer use in East-Central China. Ambio 2015, 44, 647–652.
[CrossRef] [PubMed]
4. Bishnoi, U. Agriculture and the dark side of chemical fertilizers. Environ. Anal. Ecol. Stud. 2018, 3, EAES.000552.2018. [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. [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. [CrossRef]
7. Liu, J.; Ma, K.; Ciais, P.; Polasky, S. Reducing human nitrogen use for food production. Sci. Rep. 2016, 6, 30104. [CrossRef]
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. [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. [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. [CrossRef]
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. [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. [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. [CrossRef]
[PubMed]
Sustainability 2021, 13, 1140 16 of 20

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. [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. [CrossRef]
16. Vessey, J.K. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 2003, 255, 571–586. [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. [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. [CrossRef]
19. Atieno, M.; Herrmann, L.; Nguyen, H.T.; Phan, H.T.; Nguyen, N.K.; Srean, P.; Than, M.M.; Zhiyong, R.; Tittabutr, P.; Shut-
srirung, A.; et al. Assessment of biofertilizer use for sustainable agriculture in the Great Mekong Region. J. Environ. Manag. 2020,
275, 111300. [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. [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. [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. [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. [CrossRef]
24. Ritika, B.; Utpal, D. Biofertilizer, a way towards organic agriculture: A review. Afr. J. Microbiol. Res. 2014, 8, 2332–2343. [CrossRef]
25. Borkar, S.G. Microbes as Bio-Fertilizers and Their Production Technology, 1st ed.; WPI Publishing: New York, NY, USA, 2015.
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.
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.
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. [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. [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. [CrossRef]
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.
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. [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. [CrossRef]
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. [CrossRef]
[PubMed]
35. Sharma, S.; Kulkarni, J.; Jha, B. Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Front. Micro-
biol. 2016, 7, 1600. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [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. [CrossRef]
Sustainability 2021, 13, 1140 17 of 20

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. [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. [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. [CrossRef]
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. [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. [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. [CrossRef] [PubMed]
47. Swarnalakshmi, K.; Yadav, V.; Tyagi, D.; Dhar, D.W.; Kannepalli, A.; Kumar, S. Significance of plant growth promoting rhizobacte-
ria in grain legumes: Growth promotion and crop production. Plants 2020, 9, 1596. [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. [CrossRef]
49. Bhattacharyya, P.N.; Jha, D.K. Plant growth-promoting rhizobacteria (PGPR): Emergence in agriculture. World J. Microbiol.
Biotechnol. 2012, 28, 1327–1350. [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.
[CrossRef]
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. [CrossRef]
52. Ankati, S.; Podile, A.R. Understanding plant-beneficial microbe interactions for sustainable agriculture. J. Spices Aromat. Crop.
2018, 27, 93–105. [CrossRef]
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. [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. [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. [CrossRef]
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. [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. [CrossRef]
58. Yang, J.; Kloepper, J.W.; Ryu, C.M. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 2009, 14, 1–4.
[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. [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. [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. [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. [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.
[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. [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. [CrossRef] [PubMed]
Sustainability 2021, 13, 1140 18 of 20

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. [CrossRef]
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. [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. [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. [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.
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. [CrossRef]
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. [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. [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.
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. [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. [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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [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.
[CrossRef]
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. [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. [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. [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. [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.
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. [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. [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. [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.
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. [CrossRef]
Sustainability 2021, 13, 1140 19 of 20

92. Mahdi, I.; Fahsi, N.; Hafidi, M.; Allaoui, A.; Biskri, L. Plant growth enhancement using rhizospheric halotolerant phosphate solubi-
lizing bacterium Bacillus licheniformis QA1 and Enterobacter asburiae QF11 isolated from Chenopodium quinoa willd. Microorganisms
2020, 8, 948. [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.
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.
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. [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. [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. [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. [CrossRef] [PubMed]
99. Glick, B.R. Plant growth-promoting bacteria: Mechanisms and applications. Scientifica 2012, 2012, 963401. [CrossRef] [PubMed]
100. Glick, B.R. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol. Res. 2014, 169, 30–39.
[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. [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.
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. [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.
[CrossRef]
105. García-Fraile, P.; Menéndez, E.; Rivas, R. Role of bacterial biofertilizers in agriculture and forestry. Aims Bioeng. 2015, 2, 183–205.
[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. [CrossRef]
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. [CrossRef] [PubMed]
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. [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. [CrossRef] [PubMed]
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.
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. [CrossRef] [PubMed]
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. [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.
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. [CrossRef]
115. Macik,
˛ M.; Gryta, A.; Frac,
˛ 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.
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. [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.
Sustainability 2021, 13, 1140 20 of 20

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.
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. [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. [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. [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. [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.
124. Arora, N.K.; Khare, E.; Maheshwari, D.K. Plant growth promoting rhizobacteria: Constraints in bioformulation, commercial-
ization, and future strategies. In Plant Growth and Health Promoting Bacteria; Maheshwari, D., Ed.; Springer: Berlin/Heidelberg,
Germany, 2010; pp. 97–116.
125. Du Jardin, P. Plant biostimulants: Definition, concept, main categories and regulation. Sci. Hortic. 2015, 196, 3–14. [CrossRef]
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. [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. [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.
[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.
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.
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. [CrossRef]
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. [CrossRef]