Received: 11 June 2020 | Revised: 28 July 2020 | Accepted: 2 August 2020

DOI: 10.1002/jobm.202000370

REVIEW

PGPR‐mediated induction of systemic resistance and

physiochemical alterations in plants against the pathogens:
Current perspectives

Mukesh Meena1,2 | Prashant Swapnil2,3 | Kumari Divyanshu2 |

Sunil Kumar2 | Harish4 | Yashoda Nandan Tripathi2 | Andleeb Zehra2 |
Avinash Marwal5 | Ram Sanmukh Upadhyay2

1
Laboratory of Phytopathology and
Microbial Biotechnology, Department of Abstract
Botany, Mohanlal Sukhadia University, Plant growth‐promoting rhizobacteria (PGPR) are diverse groups of plant‐
Udaipur, Rajasthan, India
2
associated microorganisms, which can reduce the severity or incidence of
Centre of Advanced Study in Botany,
Institute of Science, Banaras Hindu disease during antagonism among bacteria and soil‐borne pathogens, as well as
University, Varanasi, India by influencing a systemic resistance to elicit defense response in host plants.
3
Department of Botany, Acharya Narendra An amalgamation of various strains of PGPR has improved the efficacy by
Dev College, University of Delhi,
enhancing the systemic resistance opposed to various pathogens affecting the
New Delhi, India
4
Plant Biotechnology Laboratory,
crop. Many PGPR used with seed treatment causes structural improvement of
Department of Botany, Mohanlal the cell wall and physiological/biochemical changes leading to the synthesis of
Sukhadia University, Udaipur, Rajasthan, proteins, peptides, and chemicals occupied in plant defense mechanisms. The
India
5
major determinants of PGPR‐mediated induced systemic resistance (ISR) are
Department of Biotechnology, Vigyan
Bhawan—Block B, New Campus, lipopolysaccharides, lipopeptides, siderophores, pyocyanin, antibiotics 2,4‐
Mohanlal Sukhadia University, Udaipur, diacetylphoroglucinol, the volatile 2,3‐butanediol, N‐alkylated benzylamine,
Rajasthan, India
and iron‐regulated compounds. Many PGPR inoculants have been commer-
Correspondence cialized and these inoculants consequently aid in the improvement of crop
Mukesh Meena, Laboratory of growth yield and provide effective reinforcement to the crop from disease,
Phytopathology and Microbial
Biotechnology, Department of Botany,
whereas other inoculants are used as biofertilizers for native as well
Mohanlal Sukhadia University, Udaipur, as crops growing at diverse extreme habitat and exhibit multifunctional
Rajasthan 313001, India. plant growth‐promoting attributes. A number of applications of PGPR
Email: mukeshmeenamlsu@gmail.com
and mukeshmeenabhu@gmail.com formulation are needed to maintain the resistance levels in crop plants.
Several microarray‐based studies have been done to identify the genes,
which are associated with PGPR‐induced systemic resistance. Identifica-
tion of these genes associated with ISR‐mediating disease suppression and
biochemical changes in the crop plant is one of the essential steps in

Abbreviations: ABA, abscisic acid; ACC, 1‐aminocyclopropane‐1‐carboxylate; AFP, antifreeze protein; AM, arbuscular mycorrhiza; AMF,
arbuscular mycorrhizal fungi; APX, ascorbate peroxidise; CAT, catalase; CS, cold stress; EPS, exopolysaccharides; FC, field capacity; GA,
gibberellic acid; GPX, guaiacol peroxidise; HCN, hydrogen cyanide; IAA, indole‐3‐acetic acid; ISR, induced systemic resistance; JA, jasmonic
acid; MDA, malondialdehyde; NCS, noncold stress; PAL, phenylalanine ammonia‐lyase; PGPMs, plant growth‐promoting microorganisms;
PGPR, plant growth‐promoting rhizobacteria; POD, peroxidase; PPO, polyphenol peroxidase; PR protein, pathogenesis‐related proteins; ROS,
reactive oxygen species; SA, salicylic acid; SAR, systemic acquired resistance; SOD, superoxide dismutase; VOC, volatile organic compound.

J Basic Microbiol. 2020;1–34. www.jbm-journal.com © 2020 Wiley‐VCH GmbH | 1

2 | MEENA ET AL.

understanding the disease resistance mechanisms in crops. Therefore, in

this review, we discuss the PGPR‐mediated innovative methods, focusing
on the mode of action of compounds authorized that may be significant in
the development contributing to enhance plant growth, disease resistance,
and serve as an efficient bioinoculants for sustainable agriculture. The
review also highlights current research progress in this field with a special
emphasis on challenges, limitations, and their environmental and eco-
nomic advantages.

KEYWORDS
ACC‐deaminase, biocontrol, fertilizers, germination, plant defense, plant growth‐promoting
rhizobacteria, reactive oxygen species

1 | INTRODUCTION fertilizers and poses human and environmental hazards

The most important nutrition‐related problem is food
insecurity, which causes serious effects on the health of
millions of people [1,2]. The rates of food insecurity have
been increased by more than one‐third since 2007 in the
United States. This food insecurity can be defined either
in terms of availability of food or the availability of un-
healthy food. In the last few decades, modern agricultural
processes indiscriminately promotes the use of fertilizers,
predominantly nitrogenous and phosphorus to monitor
the considerable pollution of soil, water, and air. Che-
mical fertilizers have both positive and negative effects on
the growth of plants as well as the soil. Nowadays,
farmers are using higher nutrient‐containing chemical
fertilizers extensively [2]. The excessive use of these fer-
tilizers (chemicals) exerts detrimental effects on soil mi-
croorganisms, soil fertility, as well as pollutes the
environment [1,2]. The long‐term use of these fertilizers
leads to a decline in soil pH. Acidification of soil is caused
by a number of factors such as acidic precipitation and
the deposition of acidifying particles or gases (nitric acid,
sulfur dioxide, and ammonia). Mostly, soil acidification
in agricultural land is caused by the application of urea
and ammonium‐based fertilizers and the growth of le-
gumes [3]. Acidification also causes the loss of ex-
changeable bases (exchangeable form of the bases like
calcium [Ca], magnesium [Mg], potassium [K], and so-
dium [Na], which are expressed as milligram equivalents
per 100 g of soil), thus making them unavailable to crops
and reduces the crop productivity results and a decline in
crop yields [4]. To preclude this problem and achieve
higher productivity, farmers have become more depen-
dent on chemical sources of nitrogen and phosphorus.
Moreover, apart from being costly, the production of
chemical fertilizers reduces nonrenewable resources,
such as oil and natural gas, used to produce these
[3,4]. However, crop plants were frequently exposed to
various biotic and abiotic stresses, which decrease the
grain yield as well as other physiological functions of
plants.
Plant growth and their productivity rely on the re-
lationship with associated rhizosphere microbes [5].
These rhizosphere protists‐bacterial interactions re-
mobilize the essential nutrients for plant uptake. Protists
are an essential component of the soil microbiome except
for plants, fungi, and animals. They play very important
roles in the understanding of the eukaryotic evolution
and biogeography of microbes, as well as are considered
as consumers of bacteria, fungi, and other eukaryotes in
microbial food webs and also regulate the populations
and shape of the communities [6]. To overcome these
problems, farmers can use plant growth‐promoting rhi-
zobacteria (PGPR) in the agricultural fields. The PGPR
are soil‐borne bacteria that aggressively colonize the
plant root and benefit the plant in multiple ways. PGPR
greatly revitalize the soil quality and plant growth, and
enhance agricultural productivity in many parts of the
world [5,6]. They have positive effects on plant nutrition
and root development, whereas negative effects on the
harmful microbial process. PGPR produces siderophores,
phytohormones such as cytokinins, gibberellins, indole‐
3‐acetic acid (IAA), and protect the plant from pathogens
through several mechanisms (Figure 1). PGPR also helps
in nitrogen (N2) fixation and provide ammonium for the
plants (Figure 1), as well as contributes toward plant
growth promotion through direct and indirect mechan-
isms. Direct mechanism includes phosphate solubiliza-
tion and mineralization of organic compounds,
production of phytohormones (biofertilizers) like IAA,
abscisic acid (ABA), ethylene (ET), and auxins, and ni-
trogen fixation [7]. Indirect mechanism shows antag-
onistic activity against phytopathogen through the
MEENA ET AL. | 3

F I G U R E 1 A comprehensive diagrammatic appearance of positive and negative interaction of plant growth‐promoting

rhizobacteria‐mediated plant growth promotion and disease suppression

production of secondary metabolites, siderophore pro- reacting to specific biotic or chemical stimuli [18,19].
duction, induction of disease resistance, and fungicidal Induced resistance can be classified into two basic
products [7] (Figure 1). Thus, the PGPR suggests an ap- forms: (a) Systemic acquired resistance (SAR), and
proach to enhance the crop productivity and sustainable (b) ISR. In both these forms, plant defense response is
environment for the future generation. The region of the
soil where the plant's root interacts with a range of mi-
crobes such as bacteria, fungi, and several other parasites
is known as rhizospheric soil, and many complex biolo-
gical and physiological interactions occur in rhizospheric
soil. Among these microbes, rhizobacteria that are cap-
able of promoting growth mainly includes members of
bacterial phyla such as Actinobacteria, Bacteroidetes,
Cyanobacteria, Firmicutes, and Proteobacteria with
Pseudomonas spp. and Bacillus spp. as their re-
presentative members [8–10]. They may control plant
health by suppressing infectious diseases [11,12]. Every
plant protects itself from pathogen attack by their innate
defense mechanisms. Figure 2 shows the elicitation of
induced systemic resistance (ISR) by microorganisms and
their counterparts through various mechanisms. Some-
times, these mechanisms fail when a virulent pathogen
attacks the plant and tries to evade the resistive reactions
of the plant [13,14]. Pathogenic and nonpathogenic mi- F I G U R E 2 Elicitation of induced systemic resistance (ISR)
crobes trigger different types of defense response [15–17]. by microbial apparatus or their counterparts. The diminutive
The incidence of disease can be drastically reduced if the molecules or several other chelating complexes may work as
defense mechanisms are induced appropriately before the elicitors for ISR stimulation. The root exudates, such as organic
pathogen's attack. Induced resistance is thus a state of acids, attract certain positive beneficial microbes for host
enhanced defensive capacity developed by a plant colonization and provide initial priming for disease suppression
4 |
preconditioned by a prior infection or treatment, which
helps in developing resistance against subsequent ex-
posure to the same pathogen or parasite [19,20]. Using
PGPR, some defense genes have been found to be asso-
ciated with ISR and these are induced by PGPR volatile
compounds without the organisms being in contact with
the roots such as 3‐hydroxy‐2‐butanone and (2R,3R)‐2,3‐
butanediol from Bacillus spp. [21].
ISR is phenotypically similar to SAR as they both
reduce the disease severity caused by the pathogen. They
both only differ in the signaling compounds involved
against different pathogens. For example, in wild‐type
tobacco plants, salicylic acid (SA) accumulation is es-
sential for the mechanism of SAR, whereas transgenic
tobacco plants do not show SAR expressions because of
having salicylate hydroxylase gene of Pseudomonas puti-
da, which causes constitutive expression of nahG gene
[22]. ISR by Pseudomonas fluorescens WCS417r has been
shown to be independent of SA accumulation in trans-
genic Arabidiopsis thaliana, which constitutively ex-
presses nahG gene, but a response to ethylene or
jasmonic acid (JA) is essential for the expression of
ISR [23,24].
SAR that depends upon SA‐signaling and is marked
by overexpression of pathogenesis‐related (PR) pro-
teins, is generally induced by biotrophic pathogens
[25,26]. On the contrary, PGPR, triggered by ISR, do
not involve severe changes in defense‐related genes
expression but rather defense priming [27,28]. Upon
pathogens or herbivores attack, the defense of PGPR‐
primed plants is more strongly activated, and this re-
sponse is dependent on a functional JA pathway
[21,29]. Most of the colonizing rhizobacteria have
adopted ISR as a mechanism for disease suppression in
disease‐suppressive soils [30,31]. Frequently, the defi-
nition of suppressive soil from Baker and Cook [32] is
“soils in which the pathogens do not establish or per-
sist, establishes but causes little or no damage, or es-
tablishes and causes disease for a while but thereafter
the disease is less important, although the pathogen
may persist in the soil.” Therefore, suppressive soils are
characterized by a diminutive level of disease estab-
lishment although a virulent pathogen and susceptible
host are present [33,34]. However, it is not easy to
define the term “suppressive soil” because there are
several types of suppressiveness acting in the rhizo-
sphere. Several studies have shown that a consortium
of microbes governs the disease suppression in such
soils. Many bacterial taxa like Pseudomonas, Azospir-
illum, Gluconacetobacter, Bulkholderia, Comamonas,
and Sphingomonadaceae have been detected as a pre-
valent microflora in suppressive soil than conducive
soil using 16S rRNA taxonomic microarray [35].
MEENA ET AL.
2 | M E C H A N I S M OF
PHYSIOLOGICAL CHANGES IN
T H E H O S T P L AN T S A N D DI S E A SE
SUPPRESSION BY PGPR
Root hairs and lateral roots play vital roles in
colonization with PGPR [36,37]. Soluble proteins N‐
ethylmaleimide‐sensitive‐factor attachment protein re-
ceptor (SNARE) was found effective in transportation,
fusion of membranes of cargo‐containing small shuttles,
and referred to as vesicles, which target membranes in
both exocytic and endocytic pathways [38]. Syntaxin of
plant proteins (SYP), such as SYP123 and SYP132, and
SNARE proteins were reported to be expressed specifi-
cally in the root hairs and were found to play roles in the
correct localization and dispersion of defense‐related
proteins such as PRP3 (proline‐rich protein 3) in the cell
wall, thus establishing an effective plant defense against
diseases [39]. The defense genes such as PR1, PDF1.2,
MYB72, and MYC2 showed manifold expression on ISR‐
priming [40,41]. The transgenic plants, which show an
overexpression of SYP123, have the ability to increase the
expression of ISR‐priming genes as compared with wild‐
type plants in response to rhizobacteria Pseudomonas
spp. [39,42].
The nahG gene‐containing plants do not show the
accumulation of SA or PR, and also development of SAR
when attacked by a necrotizing pathogen [43,44]. Bacillus
cereus AR156, a PGPR, showed ISR to Pseudomonas
syringae pv. tomato (Pst) in Arabidopsis, which is de-
pendent upon SA‐signaling pathway and NPR1, but not
on JA and ET [45]. Infiltration of Arabidopsis leaf with
AR156‐activated SAR along with PR1 protein activation
and reactive oxygen species (ROS) burst. SAR is triggered
by AR156 in jar1 or ein2 mutants but not in NahG
transgenic and NPR1‐mutant plants. In another study, JA
signaling was found to be involved in providing im-
munity to tomato plants infected by a fungal pathogen
Botrytis cinerea [46]. In this study, Micromonospora,
which is a Gram‐positive bacterium isolated from
surface‐sterilized nodules of alfalfa (Medicago sativa) and
inoculated in the root of tomato (Solanum lycopersicum)
cause leaf reduction infected by B. cinerea. Through gene
expression analysis, it has been cleared that jasmonate‐
regulated defense priming was strongly induced in the
presence of Micromonospora. This was further proved by
using JA‐deficient line def1 defense‐impaired tomato
mutants which were incapable of displaying a long‐term
induced resistance to Micromonospora spp. inocula-
tion [47].
The applications of PGPR avoid the use of chemical
fertilizer and synthetic pesticides through the improve-
ment of plant growth and yield and induction of systemic
MEENA ET AL.
resistance [48]. Bano and Muqarab [48] demonstrated
that the application of PGPR prevent the use of chemical
fertilizer and synthetic pesticides through the enhance-
ment of plant growth and yield, and induction of sys-
temic resistance. Bano and Muqarab [48] investigated
that the role of the PGPR, P. putida and Rothia sp., used
to overcome the loss in tomato yield caused by Spo-
doptera litura (an insect). An infestation of tomato with
S. litura reduced the dry weight of shoots and roots by
46% and 22%, respectively [48]. When surface‐sterilized
seeds of tomato were inoculated for 48 h with P. putida
and Rothia sp., it was found that the effects of S. litura
infestation were ameliorated and resulted in 60% and 40%
increment in plant biomass and their yield, respectively,
over infested plants [48]. This PGPR defense mechanism
enhance the proline accumulation, antioxidative enzyme
activities, and stimulation of protease activities and
polyphenol oxidases, and also increase the phenolic
contents, proteins, and chlorophyll [48]. In another
study, a bacterial isolate CDP‐13 isolated from Capparis
decidua plant, which was identified as Serratia marces-
cens by 16S rRNA gene sequence analysis, was found to
exhibit significant PGPR traits [49]. CDP‐13 was found to
be halophilic as it showed an increase in growth at higher
salt concentration (up to 6% NaCl). Inoculation of the
wheat plant under salinity stress (150–200 mM) with S.
marcescens augmented its growth. Varied concentrations
(20–75%) of some osmoprotectants (proline, mal-
ondialdehyde [MDA], total soluble sugar, total protein
content, and IAA) in plants were regulated on the ap-
plication of CDP‐13, indicating its potential role in en-
abling plants to tolerate salt stressors [49]. CDP‐13
bacterial isolate's ability to confer ISR in host plants was
illustrated by the reduction in the disease severity caused
by the fungal infection [49]. There are many PGPR
available in the rhizosphere, which suppress or reduce
the host plant diseases and increase plant growth and
development (Table 1).
3 | P GP R ‐ MEDIATED
B I O C H E M I C A L AN D
P H Y S I OL O G I C A L CH A N G E S I N
THE HOST PLANTS
3.1 | PGPR‐mediated biochemical
changes in crop plants
The plant growth‐promoting microorganisms (PGPMs)
increased phenol (42%) and flavonoid (26%) contents in
the root of the rice plants treated with Trichoderma as-
perellum, whereas lignin content was increased approxi-
mately by 300% and 200% in the plant treated with T.
| 5
asperellum and P. fluorescens, respectively [82]. Plants
inoculated with P. fluorescens showed the K+ions con-
centration increment, whereas concentration of Na+ ions
decreased in shoots under high salt concentrations [83].
In plants treated with PGPR, the concentration of proline
increased in shoots under salt stress conditions [83].
Common bean (Phaseolus vulgaris L.), in a symbiotic
association with Rhizobium leguminoserum bv. phaseoli,
represents one of the world's most important sources of
dietary protein after soybean and groundnut [84,85]. The
beneficial microorganisms colonize the rhizospheric re-
gion of the plants and provide support to the plant
against drought by producing exopolysaccharides (EPS),
phytohormones, volatile compounds, inducing accumu-
lation of osmolytes and antioxidants [86]. The 1‐
aminocyclopropane‐1‐carboxylate (ACC) deaminase
produced by the microorganism (Ochrobactrum pseudo-
grignonense RJ12, Pseudomonas sp. RJ15, and Bacillus
subtilis RJ46) supports drought stress tolerance by reg-
ulating the ethylene level in plants [87].
Plants treated with dual or individual inoculation of
arbuscular mycorrhizal fungi (AMF) and PGPR, the
growth of the plant enhanced and reduced the nematodes
infection. While AMF and PGPR increase the phenolic
contents (28%), defensive enzymes such as peroxidase,
polyphenol oxidase, and superoxide dismutase (SOD), on
the contrary, significantly reduce MDA and hydrogen
peroxide (H2O2) concentrations [88]. In plants treated
with PGPR, under the drought and salinity stress, some
metabolic changes have been observed in agricultural
crop species such as wheat [88], tobacco [89], Brassica
juncea [90], soybean [91] tomatoes, bell peppers, cu-
cumbers [92], barley [93], and black gram [94]. Moreover,
PGPR promotes the growth and productivity of plants by
synthesis of different phytohormones like auxins and
cytokinins [95].
3.1.1 | Plant–microbe interaction:
Hormonal type changes
ACC is a precursor of ethylene, which actively partici-
pates in the development of plant, both negatively (pa-
thogens) and positively (plant growth‐promoting and
symbiotic bacteria). Both ACC and ethylene play a vital
role in the regulation of bacterial colonization by mod-
ulating plant immune responses and symbiotic programs.
In both the plant hosts and its bacterial community, the
impact of ethylene and ACC develop new strategies to
increase plant growth and protection [96]. In the root,
ACC‐deaminase metabolizes the ACC into α‐
ketoglutarate and ammonia and it can check ethylene
production level and promote plant growth [97]. The crop
6 | MEENA ET AL.

T A B L E 1 Table showing the various host plants, their diseases and various PGPR, which are involved in plant growth and development
by suppressing/reducing the disease

PGPR Host plant Disease Mechanism References

Bacillus safensis Chinese Black rot IAA production [50]
Bacillus altitudinis cabbage
Bacillus velezensis
Fictibacillus solisalsi
Bacillus mojavensis
Lysinibacillus macroides
Pseudomonas sp. Eucalyptus Mini‐cutting rot IAA production [51,52]
Bacillus subtilis
Pseudomonas fulva
B. velezensis Soyabean Phytophthora root rot IAA production [53–55]
B. mojavensis and Phytophthora
B. safensis stem rot
B. subtilis
B. altitudinis
Pseudomonas putida Cucumber Fusarium wilt IAA production [56,57]
Serratia marcescens
Pseudomonas sp. strain WCS Carnation Fusarium wilt Phytolexins production [54,58,59]
Pseudomonas yuorescens Rice Rice sheath blight Talc‐based formulation [60,61]
P. yuorescens strain 97 Beans Halo blight Induced systemic resistance [62]
P. putida strain 89B‐27 Cucumber Bacterial wilt Induced systemic resistance [63]
S. marcescens strain 90‐166
P. yuorescens strain CHAO Tobacco Tobacco necrosis virus In vitro production of salicylic acid to acquired [64,65]
induces systemic acquired resistance
Brevibacterium iodinum Pepper Gray leaf‐spot disease Biofertilization and phytostimulation [66]
KUDC1716
Burkholderia cepacia BRB 21 Black pepper Root rot Greenhouse study to promote chemical [67]
regulatory system
Pseudomonas fluorescens Pf1 Tea Blister blight 1‐aminocyclopropane‐1‐carboxylic acid [68,69]
Bacillus cereus production
B. subtilis BSV
B. subtilis BSP
P. putida 89B‐27 Cucumber Anthracnose Induced systemic resistance [70]
Serratia marcescens 90‐166
P. fluorescens strain 4 Chickpea Collar rot Fungicide and phenolic acid synthesis [71,72]
Pseudomonas aeruginosa
P. fluorescens Sugar beet Preemergence Secondary metabolite production and cell wall‐ [73]
damping‐off degrading enzyme activity
Bacillus spp. Kale Black rot incidence Production of peptide antibiotics [74]
Cabbage
P. fluorescens PF15 Tomato Fusarium wilt Induced systemic resistance [75,76]
P. putida PP27
Pseudomonas protegens Wheat Rhizoctonia root rot Production of a cyclic lipopeptide [77]
Pseudomonas chlororaphis
B. cepacia GRB35 Ginger Soft rot in ginger Fungicide production (B. amyloliquefaciens [78]
Bacillus amyloliquefaciens GRB35 and S. marcescens GRB68)
GRB58
MEENA ET AL.
TABLE 1 (Continued)
PGPR Host plant Disease
S. marcescens GRB68
S. marcescens GRB91
P. aeruginosa
Bacillus sp. strain L81 Arabidopsis Foliar disease
Arthrobacter oxidans thaliana
strain BB1
B. subtilis BS2 Tomato Tomato wilt
Abbreviations: IAA, indole‐3‐acetic acid; PGPR, plant growth‐promoting rhizobacteria.
plants treated with PGPR produce the ACC‐deaminase,
which may have relatively high root growth due to less
ethylene production and more resistance to various
stresses [87,96,98–101]. The stress‐responsive hormones
abscisic acid (ABA) content in control plants were found
94% and 145% higher under drought and salinity stress,
respectively, as compared to PGPR‐treated plants. This
suggested that the downregulation of ABA response by
Burkholderia cepacia, Acinetobacter calcoaceticus, and
Promicromonospora sp. treatments [102]. In plants trea-
ted with B. cepacia, A. calcoaceticus, and Promicromo-
nospora sp. the quantity of SA increased 0.7‐ to 1.4‐fold
higher than the untreated (control) plants under the
salinity and drought stress conditions [102]. With respect
to gibberellic acid (GA4), the PGPR‐treated plants have a
higher amount of GAs as compared to the untreated
plants under the different abiotic stress conditions such
as salinity and drought [102]. In the wheat plant, the
selected pseudomonas strains such as Pseudomonas jes-
senii R62 and Pseudomonas synxantha R81 enhanced the
phosphate solubilization, auxin production, siderophores,
and 2,4‐diacetylphloroglucinol (2,4‐DAPG) [103–106].
Growth enhanced in drought‐tolerant and sensitive
cultivars of rice with PGPR consortia containing
P. synxantha R81, P. jessenii R62, and Arthrobacter
nitroguajacolicus strain YB5 and YB3 [105].
3.1.2 | Effect of PGPR on the oxidative
stress enzymes
The activity of antioxidative enzymes catalase (CAT),
peroxidase (POD), and polyphenol peroxidase (PPO) was
found to be higher in salinity and drought‐treated cu-
cumber plants as compared to plants treated with the
PGPR under the same stress conditions [102,107]. Under
the cold stress (CS), wheat and barley plants showed
| 7
Mechanism References
Induced systemic resistance [79]
Induced the activities of defense‐related [80,81]
enzymes such as peroxidase, polyphenol
oxidase, chitinase, and phenylalanine
ammonia‐lyase and phenolics
higher activity of antioxidative enzymes such as SOD,
POD, and CAT as compared to noncold stress (NCS)
condition plants, but in the association with PGPR
(R. terrigena) the activity of SOD was found lowest (6 kg
B/ha) for NCS condition and higher with R. terrigena in
CS condition [108]. PGPR change the values of SOD,
POD, and CAT as well as decline the value of H2O2 in
both CS and NCS conditions [109,110]. Vigna radiata
under the salt stress also showed the upregulation of
antioxidative enzymes and protect the plants by scaven-
ging overproducing ROS [111]. Peanut plants treated
with halotolerant bacteria such as Klebsiella, Pseudomo-
nas, Agrobacterium, and Ochrobactrum showed an in-
crease in nitrogen (N2) content up to 76% as compared to
untreated peanut plants under salinity [112].
Water stress is the most important abiotic stress,
which limits the plant growth and their yield, and can be
controlled by PGPR that reduces the water stress by sti-
mulating resistance of the host [113]. Plant under the
water‐stressed condition showed a reduction in the ac-
tivity of ascorbate peroxidase (APX) and guaiacol perox-
idase (GPX), but PGPR‐associated water‐stressed plants
showed higher activity of GPX and APX, significantly
[114,115]. The antioxidant activity and photosynthetic
pigment were increased by the treatment of rhizobacteria
under the water stress condition compared to the un-
treated plant (control). The CAT enzyme activity sig-
nificantly increased when the plant was treated by
Pseudomonades sp. under water stress condition [86]. The
activity of GPX, APX, and chlorophyll contents was in-
creased in the basil plants treated with PGPR [114,115].
PGPR strains (SJ04, WCS417r, and GB03)‐treated pep-
permint plant (Mentha piperina), showed an increase in
the emission of volatile organic compounds (VOCs) as
compared to untreated plants, whereas treatment with
combination of PGPR such as WCS417r + SJ04, and
GB03 + SJ04 showed maximum emission of VOCs.
8 |
The phenylalanine ammonia lyase (PAL) enzyme activity
and phenolic compounds increased in leaves of pepper-
mint plants treated with PGPR as compared to non-
inoculated plants [116]. In chickpea, (Cicer arietinum)
synthesis of phenolic acids (gallic, ferulic, chlorogenic,
and cinnamic acid), salicylic acid, as well as total phe-
nolic compounds, was induced when treated with two
PGPR strains, namely, P. fluorescens Pf4 and Pseudomo-
nas aeruginosa Pag [117].
In PGPR‐inoculated plants such as maize showed
increased contents of proline, sugar, and free amino
acids, and decreased protein and starch contents under
the drought stress condition as compared to control
plants [118]. The inoculated seedling of maize plants
lowers the activities of different antioxidant enzymes
such as APX, CAT, and GPX, compared to the untreated
seedling of maize plants under drought stress conditions
[119]. The tomato plant treated with PGPR (Leifsonia xyli
SE134) stimulated total polyphenol and flavonoid con-
tent, but reduced SOD activity strongly and also inhibited
the Cu content, whereas it increased the phosphorus and
iron content under elevated Cu stress condition [120].
PGPR (Bacillus megaterium TRS 4) enhanced the activ-
ities of several defensive enzymes such as POD, PAL,
chitinase, β‐1,3‐glucanase, as well as total phenols in tea
plants [121]. The isolates of Bacillus weihenstephanensis
(TSB4), B. cereus (CLB2), B. subtilis (TSB5), B. cereus
(TSB4D), and B. licheniformis (TSB4) have the ability to
produce the plant growth hormones like IAA and GA
and trigger the defense enzymatic activity of total phenol,
POD, PPO, and PAL following M. incognita infestation
both under glasshouse and field conditions [122]. In
plants (wheat) treated with PGPR in combination with
compost and minerals, applying drought stress with
PGPR triggered the accumulation of soluble sugar and
proline content in plants [123].
The wheat seedling treated with PGPR (Klebsiella sp.
SBP‐8), showed the enhancement of the proline, soluble
sugar, total protein content, and various antioxidative en-
zymes like SOD, CAT, and POX, compared to the untreated
wheat seedling [124]. The concentration of proline, abscisic
acid, auxin, gibberellin and cytokinine content increased in
maize plant treated with the P. fluorescens under drought
condition [125]. Tomato (Lycopersicon esculentum Mill.) cv.
anakha inoculated with phosphate‐solubilizing bacteria
(Bacillus polymyxa), also revealed the increase of proline
content under the drought stress condition [126,127]. In the
wheat plants, P. aeruginosa CPSB1 has been considered as
PGPR, which ameliorated the metal stress by reducing
proline content, antioxidative enzymes, and MDA content
[128]. The Enterobacter spp. strain SBP‐6 has been also used
as PGPR to reduce salt stress by having the ability of IAA
production, phosphate solubilization, siderophore, NH3,
MEENA ET AL.
and ACC‐deaminase production, which are essential for
plant growth [129].
Under salinity, P23 strain involved in the protection
of rice seedling by reducing the production of ethylene
and ROS to enhance seed germination [130]. The PGPR
P. fluorescens enhanced the growth of Catharanthus ro-
seus plant by the production of ajmalicine (mono-
terpenoid indole alkaloid) under the drought stress [131].
Inoculation of Enterobacter cloacae HSNJ4, promotes the
growth of canola seedlings and improves salt tolerance by
increasing the production of IAA, proline accumulation,
and vice versa the ethylene synthesis [132]. The in-
oculation of rhizobacteria such as Burkholderia pyrroci-
nia (R‐46) + P. fluorescens (R‐55) and T. asperellum (Ta:
mixture of strains T‐06, T‐09, T‐12, and T‐52) increase the
flavonoid content, whereas the treatments of Ta and R‐55
increases the lignin synthesis [82].
3.2 | PGPR‐mediated physiological
changes in crop plants
The growth rates of the plants such as wheat with in-
oculation of the plant growth‐promoting bacteria, by
increasing the physiological process through the in-
creases in the root and shoot length, and total fresh
weight of the plants under the salt stress condition
compared to the untreated wheat plant [133,134]. The
inoculation of PGPR such as Azospirillum brasilense
strain Az39 and Bradirhizobium japonicum strain E109
enhance the level of phytohormones such as IAA, gib-
berellic acid (GA3), zeatin (Z), and plant growth reg-
ulators at the early growth stage of seedlings of the corn
(Zea mays L.) and soyabean (Glycine max L.) by con-
trolling the photoperiod and increasing the seed ger-
mination and number of nodules per plant [135]. The
inoculation of Bacillus methylotrophicus KE2 in the se-
same plants showed the synthesis of the higher amount
of physiological components such as photosynthetic
pigments, sugar, malic acid, amino acid, total poly-
phenol, and a decline in the level of stress hormones
such as salicylic acid and abscisic acid in shoot and pods
of the sesame plants [136]. It also increases the vegeta-
tive and reproductive phases of the sesame plants [137].
Physiological changes such as an increase in the pho-
tosynthesis process and a decrease in the transpiration
rate and no effect on ABA content were observed with
the inoculation of the Phyllobacterium brassicacearum
STM196 under drought stress condition compared to the
normal condition that represents a significant added
value to drought response strategy of Arabidopsis [108].
The inoculation of silica (Si) improved the whole phy-
siological growth and the yield of mung bean also
MEENA ET AL.
increased under saline condition. When the plant had
the combined effect of PGPR such as Bacillus drentensis
and Si 2 kg/ha, it reduced the stomatal conductance,
transpiration rate, relative water content, total chlor-
ophyll content, and carotenoid content [138].
The higher photosynthesis rate in PGPMs (containing
bacteria, yeast, mycorrhiza, and trichoderma‐beneficial
species) was observed in inoculated soybean (Glycine max
[L.] Merr.) plants as compared to control (noninoculated)
plants at the beginning of flowering [135]. Under this
experiment, it has been observed that the maximal PS‐II
photochemical efficiency was found in the inoculated
plant as compared to the control plant. Thus, PGPMs
positively affect plant growth and seed production [139].
The emission of ethylene reduced when the red pepper
plant was treated with the Pseudomonas freder-
iksbergensis compared to the noninoculated plant under
saline stress conditions. It also regulated the antioxidant
enzymes and decreased hydrogen ion concentra-
tion [140].
When the wheat (Triticum aestivum) plants were
treated with salt‐tolerant bacteria (halophilic bacterium)
Serratia sp. SI‐12, it improved salt tolerance and in-
creased shoot biomass under the salt stress condition [.
When the maize plants were treated with B. megaterium,
it was observed that it controlled the physiological pro-
cesses such as water potential and stomatal opening by
increasing the root hydrolic conductivity and transpira-
tion rate under the saline‐stress condition, and increased
the expression of plasma membrane aquaporin proteins
[142]. Similarly, when the pepper plant was inoculated
with the A. brasilense and Pantoeadispersa under the
salinity, it showed enhancement in stomatal conductivity
and photosynthesis, but no change in chlorophyll content
and photochemical efficiency of PS‐II as compared to
untreated plant [143].
When the wheat plants were treated with nitrogen‐
fixing bacteria (A. brasilense Sp245), they showed in-
creased lateral root growth, root hair development,
higher water content, and greater grain yield than the
untreated plants under the water stress condition
[144,145]. When the wheat plant was treated with the
IAA‐producing Azospirillum spp., it improved the
drought tolerance capacity by enhancing the root growth
and formation of lateral roots [146]. During the cold ac-
climation or hardening, many crop plants showed phy-
siological changes by increasing the sugar, proline, and
anthocyanine content in the crop plants [147]. Rhizo-
bacteria often changed in the phytohormones signaling
[148]. When Arabidopsis plant was treated with Phyllo-
bacterium brassicacearum STM196, it showed changes in
the auxin distribution within its roots, and finally showed
lateral root growth [149].
| 9
4 | D E T ER M I N AN T S O F P GP R
IMPARTING I SR
4.1 | Mechanism of crop protection
against biotic stress
PGPR strains like Pseudomonas, Bacillus, Rhizobium,
Azospirillum, and so forth show their efficacy in crop
protection through various mechanisms including
synthesis of siderophore, antibiotics, enzymes, and ISR
applications [150]. Figure 3 shows a broad range me-
chanisms and widespread route of PGPR in the soil,
whereas different environmental factors (both biotic and
abiotic) have affected the beneficiary aspects of microbe‐
mediated growth promotion. Singh and Jha [124] re-
ported that rhizospheric bacterial isolate SBP‐9 isolated
from Sorghum bicolor showed the response against sali-
nity stress and fungal pathogen Fusarium graminearum
in wheat plant. During stress, PGPR further increases
plant growth and plant tolerance through various me-
chanisms. Pseudomonas and Bacillus spp. are known to
suppress the blister blight disease on tea plant and sig-
nificantly raise the tea yield [68]. Siderophore and anti-
biotic production are known to protect the plant from
phytopathogenic infections [151]. Figure 4 points out the
mechanism of plant growth promotion through
phosphate‐solubilizing bacteria. These bacteria convert
insoluble phosphate into soluble phosphate and increase
the growth of plants. These bacteria also secrete plant
growth regulators such as cytokinins, gibberellins, ACC‐
deaminase, IAA, and so forth; as well as biological con-
trol of phytopathogens like antibiotics, siderophores,
hydrogen cyanide (HCN), and EPS to promote plant
growth (Figure 4). PGPR strain individually and along
with consortia are known to increase the yield and
growth of Chinese cabbage and enhance ISR against
black rot caused by Xanthomonas campestris pv. cam-
pestris [50]. Antibiotics such as phenazines are known to
block the electron transport in phytopathogen micro-
organisms, by reducing their disease‐causing ability
[152]. Albicidin is another antibiotic known to obstruct
the replication of phytopathogen [153].
4.1.1 | Enzymes production by PGPR
Cappuccino and Sherman [154] described that many
PGPR produced several enzymes such as amylase, cel-
lulase, pectinase, and protease, which degrade the cell
wall of harmful microorganisms and hence reduces the
biotic stress. The fungal pathogen is also degraded by the
destruction of cell wall component by the enzymes, for
example, chitinase, β‐1,3‐glucanase, proteases, and
10 | MEENA ET AL.

F I G U R E 3 A wide range of mechanisms and comprehensive route of plant growth‐promoting rhizobacteria (PGPR) in the soil.
The solid arrows (sky blue color) point out the mutual interaction and correlation of each mechanism with other groups. The
environmental factors (both abiotic and biotic) have an effect on the whole beneficiary aspects of microbe‐mediated growth
promotion. PGPR further increase plant growth and plant tolerance to biotic and abiotic stresses by diverse action mechanisms

produced by PGPR [155]. Extracellular chitinase and la-
minarinase enzymes synthesized by Pseudomonas stutzeri
are known to degrade mycelia of Fusarium solani [156].
Frankowski et al. [157] studied that the production of
chitinase enzyme through Serratia plymuthica C48 re-
stricted the germ tube elongation and spore germination
in B. cinerea.
4.1.2 | HCN/siderophore/IAA
production
HCN, siderophores, and phytohormones such as IAA are
amid the main compounds, which play a considerable
impact in plant–microbe interaction and microbe–
microbe interaction. HCN is a gaseous secondary meta-
bolite commonly synthesized from the rhizospheric
pseudomonas to repress the root metabolism and growth
[158]. Ahmad et al. [159] reported that the Pseudomonas
and Bacillus strains have more potential for HCN pro-
duction, that is, 88.89% and 50%, respectively. The pro-
duction of HCN by certain fluorescent pseudomonads
may involved in the suppression of root pathogen.
Voisard et al. [160] reported that P. fluorescens CHA0
secretes antibiotics, siderophores and HCN, but
suppression of black rot of tobacco disease caused by the
pathogenic fungus Thielaviopsis basicola becomes visi-
ble predominantly due to production of HCN.
Microorganism synthesized an iron‐chelating, low
molecular weight compound known as siderophore [161]
that checks the pathogenic microorganism's growth by
preventing the availability of iron by binding to the freely
available form of iron (Fe2+) in the rhizosphere [159].
PGPR produce siderophores to competitively acquire
ferric ions under the iron‐limiting conditions [162–164].
However, de Villegas et al. [165] reported that increased
iron concentration in the environment has a negative
effect on the siderophore production. In their experi-
ment, the increases of Fe (III) concentration (>10 µM)
have an adverse impact on siderophore production by P.
aeruginosa.
It has been reported that PGPR improve plant growth
and development by secreting the phytohormones. Vik-
ram et al. [166] reported that 30 isolated phosphate so-
lubilizing bacteria (PSB) have the ability to produce both
IAA and GA, and observed that IAA produced by the PSB
strains, ranging from 1.1 to 28.0 μg/25 ml broth and GA
ranged from 0.6 to 9.8 µg/25 ml broth. Similarly, Fatima
et al. [167] exposed that the strains WPR‐51, WPR‐42,
and WM‐3 belonging to Azotobacter and Azospirillum
MEENA ET AL.
FIGURE 4 Diagramatic representation of the mechanism of plant growth promotion through phosphate‐solubilizing bacteria
produced IAA ranging from 19.4 to 30.2 µg/ml. Karnwal
[168] demonstrated that P. fluorescens AK1 and P. aeru-
ginosa AK2 have the capability to produce IAA in the
presence and absence of tryptophan and revealed
that both strains have enhanced indole production
ability with a concurrent increase in tryptophan
concentration.
4.1.3 | Antibiotic production
Antibiotic synthesis by PGPR shows an antagonistic ac-
tivity against the phytopathogens [169]. Antibiotics are
the heterogeneous organic low molecular weight com-
pound [170]. Phenazines, phloroglucinols, pyoluteorin,
pyrrolnitrin, cyclic lipopeptides, and HCN are the six
classes of antibiotic compounds [152]. In in vitro condi-
tion, PGPR synthesize various antibiotics that are known
| 11
to prevent the phytopathogenic growth over the host
plant [171]. Among the various PGPR, B. subtilis is the
genus that has the ability to produce a wide range of
antibiotics and can check the growth of approximately
23 types of plant pathogens [172,173]. Antibiotic pro-
duction through bacterial system also signifies the me-
tabolic activity of the organism, as the metabolic activity
depends on the various environmental factors like pH,
temperature, and other various physiological and phy-
siochemical conditions [174–176]; however, the activity
of antibiotics is also resistant to the various ranges of
temperatures and pH [177]. DAPG, phenazine‐1‐
carboxylic acid, pyoluterin, viscosinamide, xantho-
baccin, oomycin A kanosamine, zwittermycin A, tensin,
tropolone, oomycin A, and cyclic lipopeptides are a few
antibiotic compounds, which are known to check the
phytopathogenecity [173–175,178–184]. Table 2 shows
the production of antibiotics by various strains of PGPR.
12 | MEENA ET AL.

4.1.4 | Secondary metabolites synthesized by the shikimate pathway initiate from

Bottone and Peluso [199] reported that Bacillus strains
produce more than 100 secondary metabolite compounds
against phytopathogenic microorganisms. Narasimhan
et al. [200] provided a strategy to increase the microbial
biomass in the rhizosphere for using the natural sec-
ondary metabolites exuded by the wild‐type plants.
Through the establishment of Arabidopsis–Pseudomonas
spp. rhizosphere model, various secondary metabolites of
plants were exuded inadequatelly for the establishment
of rhizosphere specificity of the rhizobacterial strains to
compete for metabolizing phenylpropanoids. Further-
more, they indicated, in cases where the pollutant‐
degrading microbes are not known to use secondary
metabolites, such characteristics could be introduced into
them using Under drought stress genetic engineering
methods. Similarly, Chekol et al. [201] reported that
switchgrass and reed canarygrass successfully increased
the activity of microbial dehydrogenase after the de-
gradation of the high level of Aroclor 1248, a kind of
polychlorinated biphenyl. Tryptophan biosynthesis re-
quired a five‐step reaction encoded by trp genes en-
hanced by the metabolic node chorismate. Chorismate is
phosphoenolpyruvate and erythrose 4‐phosphate, which
is a common pathway for the biosynthesis of many sec-
ondary metabolites and aromatic amino acids [202,203].
Iturin A is a secondary metabolite synthesized after the
logarithmic phase [203]. HCN is known to prevent
the root growth of phytopathogens [158]. Phytoalexins
are the secondary metabolites that are lipophilic in nat-
ure and are not specific in their antifungal activity
[204–207]. Some other metabolites have also been
reported such as pyoluteorin [208] and auxofuran [209].
4.2 | Mechanism of crop protection
under abiotic stresses
Water stress, waterlogging, salinity, drought, high and
low temperature, heavy metal stress, and mechanical
wounding are some examples of stresses, which come
under abiotic stress [210]. Abiotic stresses are also the
major factors that reduce agricultural productivity as well
as physiology and biological health of plants. Table 3
shows the different mechanisms of PGPR, which are
engaged in amelioration of diverse abiotic stress

TABLE 2 Antibiotic production by various plant growth‐promoting rhizobacteria (PGPR) strains

PGPR strain Antibiotics Stress References

Pseudomonas fluorescens
BL915
Bacillus amyloliquefaciens
FZB42
Pseudomonads
Fluorescent pseudomonads
Bacillus spp.
Bacillus subtilis AU195
B. subtilis BBG100
B. subtilis QST713
Bacillus cereus UW85
Agrobacterium radiobacter
Lysobacter sp. SB‐K88
Paenibacillus sp. 300
Streptomyces sp. 385
Bacillus cepacia
Pyrrolnitrin (PRN) In vitro bacterial and fungal stress [185]
Bacillomycin D, fengycin, surfactin In vitro fungal stress [186]
2,4‐diacetylphloroglucinol (2,4‐DAPG), Soil‐borne plant pathogens in field [187]
phenazine conditions
Pyoluteorin (PLT), 2,4‐DAPG, PRN, phenazine‐ In vitro abiotic (oxygen, temperature, [181]
1‐carboxyclic acid, 2‐ hydroxy phenazines, specific carbon, nitrogen sources, and
phenazine‐1‐carboxamide microelements) and biotic (bacteria and
fungi) stress
Polymyxin, circulin, colistin, bacillomycin, In vitro fungal and bacterial [188–190]
plipastatins A and B
Bacillomycin D In vitro fungal [191]
Mycosubtilin In vitro yeasts and pathogenic fungi [192]
Iturin A In vitro fungal stress [193]
Zwittermicin A (aminopolyol), kanosamine In vitro fungal stress [194,195]
(aminoglycoside)
Agrocin 84 Bacterial stress in field conditions [196]
Xanthobaccin A In vitro fungal stress [183]
β‐1,3‐glucanase Fungal stress in pot conditions [197,198]
MEENA ET AL.
tolerances in host plants. Ethylene is known to facilitate
the plant's normal physiological functions such as fruit
ripening, seed germination, and root development
[258,259]. Excessive secretion of ethylene leads to adverse
affect to the plants like inhibition of root elongation, leaf
senescence, and abscission. The PGPR isolate containing
ACC‐deaminase enzyme lowers the ACC level and
hence the ethylene amount by breaking ACC into
α‐ketobutyrate and ammonia [260]. Figure 5 shows a
schematic representation of the ACC‐deaminase me-
chanism produced from rhizobacteria, which promote
plant growth in association with IAA.
4.2.1 | Salt stress
Accumulation of a high amount of salt (NaCl) in the soil
makes the soil unproductive and infertile, which results
in poor yield and causes economic as well as agricultural
losses. Salt stress causes oxidative damage to the plant,
which consequently negatively affects the root coloniza-
tion, mycorrhizal colonization, and rhizobial nodulation
[224,261]. High NaCl concentration in the root zone re-
gion causes osmotic pressure and hence creates hin-
drance in water absorption and necessary nutritional ions
uptake by root [262]. Gamalero et al. [263] reported that
the plant treated with PGPR strain containing ACC‐
deaminase enzyme (lower ethylene level) can survive
under the saline condition to some extent. Thuan et al.
[264] reported that the PGPR strain of Enterobacter and
Pseudomonas produces ACC‐deaminase and IAA, and
facilitated the growth of cowpea under salt stress. De
novo synthesis of osmolytes, alanine, glycine, glutamic
acid, serine, threonine, and aspartic acid in the cytosol of
P. fluorescens MSP‐393 are known to respond against salt
stress and facilitate the plant growth under saline en-
vironment [265]. Kim et al. [266] reported that the PGPR‐
containing antioxidative enzymes facilitate the plant
growth in saline environment by removing the H2O2
from the salt‐stressed root regions [267]. P. fluorescens
strain REN1 contains the ACC‐deaminase enzyme, hence
reduce the amount of ethylene, and enhance the rice
seedling by elongation and endophytic colonization in
the root of rice. Mayak et al. [226] studied that PGPR
strain Achromobacter piechaudii raised the fresh and dry
weight of tomato seedling grown under the saline en-
vironment and also reduced the ethylene level in the
tomato plant. Zafar‐ul‐Hye et al. [268] also studied the
effects of the two Pseudomonas species on maize plant
alone as well as combined with fertilizer, and reported an
increase in root–shoot length, fresh, and dry weight as
well as advanced and increased growth in the saline en-
vironment. Bal et al. [221] worked on ACC‐deaminase
| 13
containing isolates Alcaligens spp., Bacillus spp., and
Ochrobactrum spp., which enhance the rice seedling and
seed germination under saline condition.
4.2.2 | Heavy metal stress
Soil contaminated by heavy metals is absorbed by the
roots of the plant and diffused to the different parts of
plants, which consequently disturbs the plant's metabolic
activity as well as deteriorate the plant development
[269,270]. When plants are exposed to heavy metal stress
or other abiotic stresses the endogenous ethylene level
increases [259,271–273]. Pseudomonas koreensis AGB‐1
isolated from Miscanthus sinensis is effective against
metal toxicity and contains heavy metal marker genes in
their genome [274]. The PGPR exhibit various strategies
such as biosorption, complexion, uptake and efflux, pre-
cipitation, and intracellular assimilation for plant
protection against heavy metal toxicity [274]. Phytor-
emediation is one of the eco‐friendly, effective, and
low‐cost ways against heavy metal contamination as it is
accompanied by plants, and the plants make the soil free
from contamination by absorption of contamination in-
volving chemical, physical, as well as biological processes
[275–278].
Phytoextraction is also an eco‐friendly and in-
expensive way for the exclusion of heavy metal toxicity
from the soil through plants [279]. Phytoextraction is also
a part of phytoremediation. Application of triton X‐100
and Sinorhizobium sp. Pb002 together elevate the phy-
toextraction capability of B. juncea plant for lead ab-
sorption [280]. Plociniczak et al. [281] reported that
Brevibacterium casei MH8a not only enhance the phy-
toextraction ability of white mustard plant but also en-
hance the growth promotion as it shows ammonia
production, HCN production, IAA production, and ACC‐
deaminase activity. Burd et al. [98] have reported that
Kluyvera ascorbata SUD165 shows siderophore and ACC‐
deaminase activity as well as enhance the seedling of
tomato and canola plants and rescue the plant from
nickel toxicity. Jiang et al. [282] reported that paddy and
tomato plants inoculated with PGPR strain Burkholderia
sp. J62, enhanced the uptake of the heavy metals like lead
(Pb) and cadmium (Cd) in the plant, and also elevated
the growth promotion of plant as J62 produced IAA,
siderophore, and showed ACC‐deaminase activity.
4.2.3 | Water stress
Declination in the relative water content of the leaves
shows the water status in the plant [283–285]. Creus et al.
14 | MEENA ET AL.

TABLE 3 Representative list of PGPR strains and their various mechanisms involved in amelioration of different abiotic stress
tolerances in host plants

Action mechanism PGPR involved Host plant Stress References

Enhanced activity of 1‐aminocyclopropane‐1‐ Bacillus cereus AR156 Cucumber Drought [211]
carboxylate (ACC) deaminase Bacillus subtilis SM21
Serratia sp. XY21
Azospirillum lipoferum Wheat Drought [146]
Achromobacter Sunflower Drought [212]
xylosoxidans (SF2)
Bacillus pumilus (SF3)
Proteus penneri (Pp1) Maize Drought [213]
Pseudomonas aeruginosa (Pa2)
Alcaligenes faecalis (AF3)
Pseudomonas fluorescens biotype Pea Drought [214]
G (ACC‐5)
P. fluorescens (ACC‐14)
P. putida biotype A (Q‐7)
Burkholderia phytofirmans PsJN Maize Drought [215]
Enterobacter sp. FD17
B. subtilis B26 Imothy Drought [216]
Klebsiella sp. IG3 Wheat Drought [217]
Enterobacter ludwigii IG 10,
Flavobacterium sp. IG 15
Citrobacter freundii—J118 Tomato Drought [218]
P. putida NBRIRA Chickpea Drought [219]
Bacillus amyloliquefaciens
NBRISN13
Bacillus licheniformis K11 Pepper Drought [220]
Alcaligens spp. Rice Salinity [221]
Bacillus spp.
Ochrobactrum spp.
Pseudomonas Rice Salinity [222]
Acinetobacter (two strains) Wheat Salinity [223]
P. aeruginosa
Staphylococcus saprophyticus
B. cereus
Enterobacter hormaechei
Pantoae agglomerans
A. faecalis
Arthrobacter protophormiae Pea Salinity [224]
P. fluorescens Groundnut Salinity [68]
Brevibacterium iodinum Red pepper Salinity [225]
B. licheniformis
Zhihengliuela alba
Achromobacter piechaudi Tomato Moisture [226]
B. phytofirmans PsJN Grapevine Low temperature [227]
P. putida Canola Low temperature [228]
Phytohormone production Bacillus megaterium Trifolium Drought [229]
Glomus sp.
Azospirillum brasilense Sp245 Arabidopsis Osmotic stress [230]
A. lipoferum Maize Drought [231]
Pseudomonas aurantiaca, Wheat Salinity [232]
Pseudomonas extremorientalis
MEENA ET AL. | 15

TABLE 3 (Continued)

Action mechanism PGPR involved Host plant Stress References

B. subtilis Platycladus Drought [233]
orientalis
P. putida H‐2‐3 Soybean Drought [102]
Production and intracellular accumulation of A. brasilense Az39 Rice Osmotic stress [135]
osmolyte Rhizobium and Pseudomonas Maize Salinity [234]
A. brasilense Maize Drought [125,235]
P. fluorescens
B. subtilis GB03 Arabidopsis Drought [236]
Pseudomonas pseudoalcaligenes Rice Salinity [237]
Bacillus spp. Maize Drought [238]
Exopolysaccharide (EPS) production Pantoea agglomerans Wheat Drought [239]
Rhizobium sp. Sunflower Drought [240]
P. putida P45 Sunflower Drought [119]
EPS‐producing bacteria Maize Salinity [241]
Induction of antioxidative enzymes and Bradyrhizobium japonicum Soybean Salinity [242]
improved antioxidant position Serratia proteamaculans
Piriformospora indica Barley Salinity [243]
Pseudomonas mendocina Lettuce Drought [244]
Glomus intraradices
P. mendocina Lettuce Salinity [245]
Sinorhizobium meliloti Medicago Salinity [246]
Ion homeostasis A. brasilense Maize Salinity [247]
A. brasilense Pepper Osmotic stress [143]
Pantoea dispersa
B. subtilis Arabidopsis Salinity [248]
Improved nutrient and water uptake Azospirillum sp. Wheat Drought [249]
AM Fungi Sorghum Salinity, drought [250]
Pseudomonas monteilii Basil Abiotic stress [251]
Cronobacter dublinensis
Bacillus spp.
Production of volatile compounds B. subtilis Arabidopsis Drought, salinity [252,253]
Induction of stress reliever genes and Paenibacillus polymyxa Arabidopsis Drought [254]
proteins thaliana
Bacterial endophytes Sugarcane Drought [255]
Paraphaeosphaeria quadriseptata Arabidopsis Drought [256]
Pseudomonas sp. AMK‐P6 Sorghum Heat stress [257]
B. licheniformis Pepper Drought [220]

[144] reported that PGPR A. brasilense Sp245‐treated
wheat plant under drought condition showed higher
grain yield and mineral quality, higher Mg, K, and Ca
content and higher relative water content were also ob-
served as compared to the nontreated wheat plant.
Arzanesh et al. [146] reported that wheat plant treated
with Azospirillum lipoferum AZ45 showed high grain
yield as well as showed various plant growth‐promoting
traits like ACC‐deaminase production, nitrogen fixation,
and auxin production under water stress condition in
comparison to the nontreated control plant, similarly, the
other Azospirillum strain, A. lipoferum AZ9 showed
siderophore production and found to be the most potent
strain under drought condition. Under drought stress
condition, A. thaliana treated with Paenibacillus poly-
myxa showed the expression of drought‐responsive gene
ERD15 (early responsive gene to dehydration) and ab-
scisic acid‐responsive gene [254]. Wang et al. [211]
16 | MEENA
F I G U R E 5 A schematic illustration viewing mechanism of ACC‐deaminase produced from rhizobacteria, which facilitates plant
growth in association with IAA. ACC, 1‐aminocyclopropane‐1‐carboxylate; IAA, indole‐3‐acetic acid; SAM, S‐adenosyl methionine
examined the combined effect of the three PGPR strains
(B. cereus AR156, B. subtilis SM21, and Serratia sp. XY21)
on cucumber plant under nonirrigated conditions and
found healthy and green leaves, appropriate chlorophyll
amount, less leaf monodehydroascorbate content, better
SOD activity, hence better growth promotion as com-
pared to the nontreated plants. Gagné‐Bourque et al.
[216], investigated the effect of PGPR strain B. subtilis
B26 on Timothy (Phleum pratense L.) plant under
drought stress condition and found higher photosynth-
esis efficiency, improved root and shoot biomass, and
better stomatal conductivity as compared to the control
plant. Naveed et al. [215] have studied the efficacy of the
two PGPR isolates Burkholderia phytofirmans strain PsJN
and Enterobacter sp. FD17 over the maize plant, exposed
to water‐stress condition, and concluded that the treated
plant showed an increase in the leaf surface area, pho-
tosynthetic efficiency, root and shoot biomass as well as
enhancement in the chlorophyll content as compared to
control plant. In this treatment, PsJN was found to be
more potent than Enterobacter sp. FD17. Sarma et al.
[286] reported that PGPR strain P. aeruginosa GGRJ21
isolated from the rhizosphere of mung bean. Then, after
treatment on mung bean plant it boosts the different
drought stress‐responsive genes, that is, dehydration re-
sponsive element binding protein (DREB2A), catalase
(CAT1), and dehydrin (DHN), as well as raise the yield,
and also promote the root–shoot length and other phy-
siological characters. Zahir et al. [214] have studied the
ET AL.
effect of ACC‐deaminase containing P. fluorescens bio-
type G (ACC‐5) on pea plant at the lowest soil moisture
level and found to be the most potent and promising
strain under drought condition. Arshad et al. [287] stu-
died the effect of ACC‐deaminase containing Pseudomo-
nas sp. bacteria on pea plant under drought condition,
and reported that the treated plant showed a better grain
yield, delayed the pod ripening as well as decreased the
triple response effect on pea plant, and showed a pro-
mising effect against the drought response effects.
5 | A P P L I C AT I O N S OF P G P R
5.1 | PGPR are used for recovering soil
nutrients
PGPR strains produce phytase enzyme to solubilize the
inorganic and organic phosphate present in the soil and
make it available to the plants. Therefore, they have an
effective role in biofertilization using various mechan-
isms such as phosphate solubilization, nitrogen fixation,
and IAA production [288].
5.1.1 | Phosphate solubilization
After nitrogen, the second most important nutrient for
plant growth is phosphorus (P). The insoluble forms of P
MEENA ET AL.
are present abundantly in both inorganic and organic forms
in the soils [289]. Only two soluble forms of P are absorbed
by the plants: (a) monobasic (H2PO4−) and (b) diabasic
(HPO42−) ions [290]. Inositol phosphate, phosphotriesters,
and phosphomonesters are the insoluble forms of P [291].
Some phosphate‐solubilizing microorganisms (PSM) such
as Azotobacter, Bacillus, Beijerinckia, Burkholderia, En-
terobacter, Erwinia, Flavobacterium, Microbacterium, Pseu-
domonas, Rhizobium, and Serratia have the capability to
convert the unavailable form of P into available forms for
the plants in place of chemical phosphatic fertilizers [290].
However, these PSM can be used alone or with a combi-
nation of other beneficial rhizospheric microorganisms
[292]. The solubilizing ability of P can be processed in terms
of solubilization index (SI) [293–295].
Colony diameter + Holozone diameter
SI = .
Colony diameter
5.1.2 | Nitrogen (N2) fixation
The atmospheric N2 can be converted into usable form by
different mechanisms. Biological N2 fixation governed by
some nitrogen‐fixing microorganisms convert the unu-
sable form of nitrogen to usable form such as ammonia
by nitrogenase enzyme at mild temperatures [296]. These
nitrogen‐fixing microorganisms are also an alternative to
chemical fertilizers [297]. Nitrogen‐fixing organisms can
be symbiotic or nonsymbiotic [298]. Symbiotic nitrogen
fixers are associated with leguminous or nonleguminous
plants, whereas nonsymbiotic nitrogen‐fixing organisms
are Nostoc, Anabaena, Azospirillum, Gluconoacetobacter,
Azotobacter, Azocarus, and diazotrophicus [290]. Non-
leguminous plants associated with nitrogen‐fixing or-
ganisms are known as diazotrophs, which has the
capability to interact (nonobligatory) with the host plants
[299]. Nitrogen fixation is carried out by nitrogenase
enzyme and it requires 16 mol of adenosine triphosphate
for one mole of reduced nitrogen [291].
Fan et al. [300] reported that the treatment of a
combination of PGPR strains Bacillus amyloliquefaciens
IN937a and Bacillus pumilus T4 increased plant height,
shoot dry weight, and shoot N uptake compared to
without inoculation of PGPR. Meanwhile, the addition of
PGPR in the soil enhances the shoot P uptake in the
treatments when compared to without PGPR [300]. A
similar type of study was reported by Adesemoye et al.
[301], in which addition of a combination of PGPR
strains B. amyloliquefaciens IN937a and B. pumilus T4
into the soil at 75% fertilizer rate (0.188 g N/kg) produces
similar tomato yield to that at 100% fertilizer rate. It has
been reported that PGPR formulation LS256 increased
the yields of pepper and tomato [302]. Vessey [303] also
| 17
reported that mechanisms of PGPR included N2 fixation,
enhancing the nutrient's availability in rhizosphere soil,
and supporting additional beneficial plant growth‐
promoting bacteria or amalgamation of these
mechanisms.
5.2 | PGPR role in seed germination by
producing various growth hormones
PGPR strains, by producing IAA, gibberellic acid, and
cytokinin promote seed germination rates, root growth,
leaf area, chlorophyll content, magnesium content, ni-
trogen content, protein content, hydraulic activity, tol-
erance to drought, shoot and root weights, and delayed
leaf senescence [304]. Different strains of rhizobacteria
either individual or in combined form can produce phy-
tohormones like IAA. They have the ability to produce
23.02 µg/ml IAA in tomato plants [305]. It can sig-
nificantly enhance the height of plants, their radical vo-
lume, the diameter of stem, dry biomass, and fruit yield.
The production of IAA can be increased by the stimula-
tion of cell division and cell differentiation, which results
in increasing biomass [306]. The production of IAA does
not affect enzymatic activities such as ACC‐deaminase
activity [307]. Shah et al. [308] reported that IAA pro-
duction in P. fluorescens and P. putida helps in growth‐
promoting mechanism and cultivation productivity.
Shaukat et al. [309] reported that Pseudomonas spp. and
Azotobacter spp. had a vital effect on seedling growth and
germination of Z. mays. Similarly, Gholami et al. [310]
showed that seedling germination of Z. mays enhanced
when inoculated with growth‐promoting rhizobacteria.
Likewise, Nuncio‐Orta et al. [311] recently reported that
Azotobacter increased the seed germination of Capsicum
annum. In elucidating this, it can be affirmed that in the
process of seed germination there is the participation of
some enzymes like hydrolytic enzyme, in the presence of
growth‐promoting rhizobacteria, activities were more
rapidly than observed with the control treatment (with-
out fertilizer) and consequently, the seed germination
and percentage of this treatment is evaluated more with
control treatment [312]. It has been reported that the
positive effects of growth‐promoting rhizobacteria were
found in the seed germination of wheat and rice [313].
Delshadi et al. [314] showed that the use of biofertilizers,
separately or in combination, increased the seed germi-
nation of Onobrychis sativa L., and also according to the
results, it appears that these fertilizers at 0.7 FC (field
capacity) and the FC levels were effective in increasing
the plant's growth.
PGPR strains have the potential role of toleration
during various stress conditions by producing various
18 | MEENA
stress tolerance phytohormones like ACC‐deaminase,
IAA production [233,315], which hinder the plant
growth under various biotic conditions. Plants absorb
ACC‐deaminase, produced by PGPR which helps to
convert ACC into ammonia and α‐ketobutyrate that re-
duce the ethylene levels, ultimately decrease the stress.
Under various abiotic stress conditions, such as heat,
salinity, drought etc., PGPR strains helps in accumulation
of trehalose sugar that forms a gel‐like mat which prevent
cells from dehydration [235,315].
5.3 | PGPR used as a biocontrol agent
There are many PGPR strains having a potential role and
are used for controlling many plant diseases by secreting
many compounds like phenazine, pyoluteorin, DAPG,
viscosinamide, and tensin, which are frequently detected
having disease‐suppressing activity. These bacteria are
Pseudomonas, Azospirillium, Azotobacter, Bacillus, En-
terobacter, Paenibacillus, and Streptomyces [316,317].
Rhizobacteria can restrain the growth of many phyto-
pathogens through various ways such as competing for
nutrients and space, producing lytic enzymes, bacter-
iocins, antibiotics, and siderophores [318,319].
5.4 | PGPR used as an antibiotic source
The production of antibiotics is the most effective an-
tagonistic activity to suppress the growth of phyto-
pathogens [152,317]. Therefore, antibiotics play a
significant role in disease management, that is, it can be
used as biocontrol agents [318,319]. Some PGPR strains
produce B group vitamins like pantothenic acid, thia-
mine, riboflavin, and biotin that are absorbed by plant
roots and help in plant growth promotions [288,320].
Strains of PGPR produce several antibiotics, for instance,
kanosamine, 2,4‐DAPG, Martínez‐Viveros oligomycin A,
butyrolactones, xanthobaccin phenazine‐1‐carboxylic
acid, pyrrolnitrin, zwittermycin A, and viscosinamide
[321]. These antibiotics are used as the broad‐spectrum
antibiotic, antibacterial, and antihelmintic, which are
effective against the control of plant pathogens [322–324].
The strains including Rhizobium leguminosarum bv. tri-
folii, R. leguminosarum bv. viciae, Rhizobium meliloti,
Rhizobium trifolii, Sinorhizobium meliloti, and B. japoni-
cum have been accounted to produce antibiotics and
enzymes related to cell wall degradation, which can
hamper the phytopathogens [320,325,326].
The bacterial strain of P. fluorescens BL915 is involved in
the production of antibiotics identified as pyrrolnitrin, which
have the capability to inhibit the deterioration of Rhizoctonia
ET AL.
solani. 2,4‐DAPG is an extensively studied antibiotic involved
in the membrane destruction of Pythium spp. [327]. Bene-
duzi et al. [328] reported that Pseudomonas spp. synthesizes
phenazine that has antagonistic activity against Fusarium
oxysporum. There are many Bacillus spp., which produced
antibiotics like circulin, polymyxin, and colistin that are ac-
tively involved in the growth inhibition of pathogenic fungi
as well as Gram‐negative and ‐positive bacteria. B. subtilis
produces antibiotics like fengycin and iturins, which inhibit
the growth of Podosphaera fusca fungus [190,329]. Bacterial
siderophores and antibiotics suppress the phytopathogens
and considered as significant agronomical factors which
played vital roles in antagonism and led to obtained induced
resistance. They might be useful in formulating new in-
oculants, as eco‐friendly biological control [330].
5.5 | PGPR strains produce antifreeze
proteins (AFPs)
Psychrophilic or psychrotolerant PGPR strains of bacteria
secrete AFPs and they have ice nucleation activity, which
helps in forming ice crystal outside of the bacterium,
these properties of bacteria help to promote plant growth
in agriculture under harsh cold temperature [331,332].
The arctic PGPR P. putida GR 12‐2 secretes an AFP that
increases its survival at subzero temperature. Expression
of afpA gene of P. putida in E. coli yielded an intracellular
72 kDa protein that exhibited lower levels of antifreeze
and ice nucleation activities. The AfpA sequence was the
most similar to cell wall‐associated proteins and less si-
milar to ice nucleation proteins [333,334].
5.6 | PGPR can be used for
phytoremediation
Plants are not able to tolerate very heavy metal stress
conditions, bacteria are competent to neutralize the
heavy metal toxicity by binding with their negatively
charged functional group, and this process is known as
biosorption [335,336]. Phytoremediation is a process in
which PGPR colonize the root of the plants and helps in
mobilization of contaminates in the form of consortia,
enhance the detoxification of contaminants, and also
increase the plant biomass and grain yields [337].
5.7 | PGPR affect ethylene level in
plants
Ethylene is a plant hormone that affects plant growth and
development through several ways such as inhibiting root
MEENA ET AL.
elongation, promoting root initiation, control various
processes like the ripening of the fruits, abscission of
leaves, promoting flower wilting, leaves senescence, ac-
tivating the synthesis of other plant hormones, stimu-
lating seed germination, inhibiting Rhizobia sp. nodule
formation, inhibiting mycorrhizae‐plant interaction, and
responding to both biotic and abiotic stresses
[260,338,339]. The synthesis of ethylene follows three
successive enzymatic processes such as methionine is
converted to S‐adenosyl methionine (SAM) followed by
the formation of ACC. ACC oxidase enzyme increases the
production of ethylene by ACC in roots in different plant
tissues [340]. Furthermore, at higher concentrations,
ethylene persuades the cellular processes and defoliation,
which furthermore leads to the inhibition of stem and
root growth together with premature senescence, which
ultimately results in deprived crop performance [341].
Ethylene precursor aminocyclopropane‐1‐carboxylate
(ACC), synthesized by plants in response to exposure to
several types of environmental stress, such as drought,
flooding, cold, high temperature, extreme light, presence
of toxic heavy metals and organic pollutants, radiations,
wounding, high salt, insect predation, various pathogen
infection including fungi, bacteria, and viruses [291,342]
(Figure 4). To improve the growth and stress tolerance,
ACC‐deaminase producing bacteria considered as a pos-
sible biological approach in plants by decreasing the en-
dogenous level of ethylene [343]. During salt stress
conditions PGPR produces ACC‐deaminase, which low-
ers ethylene level in plants [226]. PGPR degrades ACC in
the rhizosphere, which could restrain the deteriorating
cycle and renovate a healthy root system that would
withstand environmental stress, and the ACC‐deaminase
enzyme engaged in the key mechanism of ethylene uti-
lization [344]. Ahmad et al. [345] demonstrated that
ACC‐deaminase producing strains (Rhizobium and
Pseudomonas) can enlarge the growth, development,
physiology, and quality of mung beans under salt‐affected
environments.
5.8 | PGPR help to cope up under
salinity stress condition
Under salinity stress condition plant growth is retarded by
ion imbalance and nutrient absorption, therefore, to over-
come this problem, some strains of PGPR such as Klebsiella
sp. enhance salinity tolerance and promote plant growth in
Avena sativa [346]. Under salinity conditions, Bacillus
megatertum strain inoculated into maize roots enhanced
the capacity of the root by absorbing the water [142].
Similarly, Gond et al. [347] reported that the capacity of the
maize root to absorb water in saline conditions had
| 19
enhanced when maize roots were inoculated with Pantoea
agglomerans. Now, bacteria that can be cultivated under
hypersaline conditions will be more efficient to colonize
the rhizosphere root and external places of the roots to
perform at high salinity conditions.
Gonzalez et al. [348] showed that A. brasilense im-
proves the salt tolerance of the jojoba plant during in
vitro rooting. Derived from the findings obtained, A.
brasilense can diminish the adverse effects of saline
conditions on the jojoba rooting. This finding suggests
that the bacteria attenuate salinity's effect on the rooting
capability of the jojoba plant, which suggests that A.
brasilense has higher plant tolerance to salt stress. Like-
wise, Fasciglione et al. [349] used Azospirillum to de-
monstrate the growth of lettuce under salt‐stressed
conditions and found that Azospirillum sp. inoculated
lettuce showed not only improved and better quality but
also extended storage life.
5.9 | PGPR strains are used for
environmental cleaning
Petroleum oil is one of the energy sources worldwide. Dur-
ing the transportation process, oil spills and leakage occurs
due to the hydrophobic nature of hydrocarbons. It happens
due to the slow process of degradation, which can be over-
come by some strains of PGPR such as Pseudomonas sp.
ITRH25, Pantoea sp. BTRH7, Burkholderia sp. PsJN [350],
Mycobacterium frederiksbergense, and Acinetobacter sp. [351]
that help in the degradation of these hydrocarbons [337]. Soil
rhizobacteria also have the ability to influence metal solu-
bility by altering heavy metal speciation in the rhizosphere.
Several studies have proved the functions of mycorrhiza in
the soil during metal speciation by increasing host plant
tolerance against excessive heavy metals. The study showed
speciation of copper (Cu), zinc (Zn), and Pb altered sig-
nificantly in the rhizosphere of arbuscular mycorrhiza (AM)
infected and non‐infected maize in comparison to bulk soil.
The maximum alter was exchangeable to Cu that enhanced
by 26% and 43% in AM‐noninfected and infected rhizo-
sphere, respectively, than in bulk soil [352]. Pseudomonas
rhizophila S211 showed high performance in solubilization
of chemical pesticides and emerged as a potential agent for
environmental bioremediation [353].
6 | C HALLE NGE S I N PGPR
6.1 | Selection of specific strain
Selection of appropriate PGPR strains from thousands of
root‐colonizing bacteria is a tedious process. Therefore,
20 | MEENA
an appropriate technique is needed for the screening and
selection of specific PGPR strains to perform successful
experiments. Bergey's Manual of Determinative Bacter-
iology is the primary method used for screening of new
isolates on the basis of morphology, physiology, and
biochemical basis. New isolates will be considered on the
basis of soil type, climatic adaptability, and the screening
assay, which will enhance the crop yield and disease
management [8,354]. The most common method for
quantification of root‐colonizing bacteria is dilution‐plate
counting and even in sterile conditions, it can be used
effectively in gnotobiotic systems [355,356].
6.2 | Challenges in products registration
and patent filing
Registration of biocontrol agents (BCAs) should be relaxed
by the environmental protection agencies and to promote
biocontrol agents either by agencies or universities to
strengthen the organization for effective products. In addi-
tion, the documentation and regulatory procedures for
product registration are extremely intricate and need sig-
nificant levels of expertise. The registration process of BCAs
in the European Union or any other union is extensive,
difficult, and complicated. For marketable delivery, the
product must be manufactured on a commercial level,
preserved for storage, and formulated to confirm bio-
compatibility. These processes may be patented for large‐
scale use. Although, apart from a high number of patents
there are only a small number of patents that have mate-
rialized in a register for the agricultural application [357].
6.3 | Challenges in PGPR propagation in
field condition
Food and Agriculture Organization reported that the
population of the world in 2025 will be nearly 8.5 × 109.
This increment will require additional agricultural pro-
duction of ~2.4 × 109 t/year without any doubt [357]. So,
there is a need to deliver PGPR directly to the field. PGPR
potential is different in laboratory and greenhouse but it
is difficult to regain their viability and biological activity
in field condition. Propagation of rhizobacteria also de-
pends on plant type and climatic conditions [358].
6.4 | Challenges in product
commercialization
Formulation of biopesticide development needed good
infrastructure, formulation, field trials, production,
ET AL.
commercialization of products, storage and scale‐up the
products, product registration, and regulatory matters. A
lot of efforts are lost during bioformulation of effective
biopesticide, which needed multidisciplinary approaches
and development, rarely all the range of expertise exist in
the same organization [358].
6.5 | Challenges in biopesticide delivery
and their quality
The major challenge in promoting biopesticides as
chemical pesticides is the lack of profiling of biopesti-
cides, which showed the weakness of the associated
policy network, limited resources, capabilities, and not
having trust between regulators and producers. There
is a lack in the delivery of biopesticide that depends on
understanding the use of products and also improving
the delivery as per the performance of the products
[359]. Multinational companies have to invest in large
scale production of the biopesticides to maintain their
quality, stability and also to improve their shelf‐life
rather than small scale production which cause the
inoculums contamination [291,357,360,361]. As the
environmental safety is a global concern, we need to
bring awareness among the farmers, government
agencies, manufacturers, policymakers, and specially,
the common men to switch‐over to biopesticides from
the chemical pesticides for the pest management
requirements.
6.6 | Challenges in understanding the
microbial niche and their interaction
Plant root exudates that are carbohydrates and chemical
signaling are important factors in rhizobacteria coloni-
zation responsible for signaling mechanisms. For
screening of effective biocontrol agents, it is important to
understand the interaction of rhizobacteria, pathogen,
and plant‐bacteria niche. Plant microbiome plays very
important roles in the development of hosts and their
health [362]. The plant microbiome at the rhizospheric
level showed a reservoir of microorganisms with adverse
ability against pathogens. In this respect, the isolation,
identification, and characterization of the microbiome
with biocontrol potential with the ability of adaptation in
a complex niche like the rhizosphere, which constitutes
an attractive strategy regarding disease management
[363]. PGPR strains produce different extracellular me-
tabolites that elicit the ISR defense mechanism. PGPR
strains have to cope with fluctuating environmental
conditions [358,364].
MEENA ET AL.
7 | BIOSAFETY OF PGPR
For sustainable agriculture, PGPR are considered as
reasonable candidates. It is very important that these
microbes do not cause any harmful effects on environ-
ments as well as human health. Therefore, now it is time
to incorporate new strategies or methods for the selection
of PGPR to study the biosafety risks and understand the
loss of biological material for both environment and
humans [365]. Richmond and McKinney [366] published
guidelines regarding the usage of microorganisms in a
range of biosafety classes. So, biosafety levels (BSL) are
made for the classification of usable microorganisms
under the different categories of risk. According to the
World Health Organization [367], the classification of
communicable agents is divided into four risk group le-
vels based on pathogenicity to the health of humans,
their transmission mode, and the availability of treat-
ments. BSL‐1 refers to a low‐risk group including non-
pathogenic organisms, which are not infectious and
considered as a safe laboratory. BSL‐2 refers to infectious
microorganisms, which cause infection in human beings.
So special handling training is required at this level. The
vaccines and treatments are available to control the
pathogen infection at this level. BSL‐3 refers to low‐
community and high‐individual risk, which includes
lethal infectious microorganisms and have easy disper-
sion property. At this level, specialized equipment is
required to prevent containment of microorganisms.
BSL‐4 refers to high‐community and ‐individual risk,
which is caused by high‐risk groups of microorganisms,
and for these infections, no vaccines and treatments are
available [368]. It requires special training to handle
these microorganisms and should follow the institutional
policy to stop the trouble‐free access of BSL‐4.
8 | FU TURE PROS PE CTI V E
IN P GPR
The biological control microbial inoculants, combined
with PGPR, have the potential for a huge market share
worldwide with a growth rate of 15%, annually. Their
commercialization is dependent on advancements and
improvements in interdisciplinary research with the
large‐scale production, product marketing, and formula-
tion methods [369]. Due to global climate changes and
rising population that lead to demand of increasing
agricultural yields; for that purpose, PGPR are safest so-
lution for increasing productivity [358]. As growing po-
pulation size and climate change leads to food insecurity,
to fulfill the food demands by using biocontrol agents,
PGPR will be required to increase soil fertility in a
| 21
sustainable developmental manner. For this purpose,
researchers need to be focussed on molecular and bio-
technology approaches to enhance the soil fertility, pa-
thogen, and pest control by using rhizoengineering
[366–369]. Major macronutrients for plant growth are
nitrogen, phosphorus, and potassium but there are less
research work on potassium as essential macronutrient.
Therefore, researchers should be allowed to work on
potassium solubilization essential nutrients. The practical
inoculant formulation of the PGPR used as biofertilizers
to increase crop productivity [370,371]. Focusing on na-
noagriculture, through nanofertilizers, which have un-
ique properties and are more effective as compared to
ordinary fertilizers by reducing nitrogen loss due to
leaching, emissions, and long‐term persistence in the soil
[372–376]. PGPR encapsulated in gold, silver, and aluminum
using nanosized fertilizers increase the soil fertility by
decreasing the 90% loss of conventional PGPR fertilizers.
These nanofertilizers emerged as more eco‐friendly as com-
pared to chemical fertilizers [121,377–383]. Environmental
barriers and adverse conditions interfere in PGPR's efficacy.
To overcome this problem, strain mixing and biotechnology
approaches will be needed.
9 | C O NC L U S I O N S
To enhance crop productivity, there are certain varieties
of PGPR strains available, which belong to Bacillus,
Azospirillium, Azotobacter, Enterobacter, Acinetobacter,
Rhizobium, Burkholderia, Beijerinckia, Erwinia, Alcali-
genes, Arthrobacter, Flavobacterium, and Serratia and are
used worldwide. These PGPR stimulate plant growth
promotion and increase plant biomass of many agri-
cultural crop species, for example, tomato, wheat, to-
bacco, bell peppers, mustard, and cucumbers. The
beneficial effects of PGPR can be owed to their potential
to secrete biologically active secondary metabolites in-
cluding phytohormones and siderophore production.
These phytohormone‐generating PGPR can be applied to
enhance crop productivity and their organization will
decline the negative impacts of salinity and short‐range
drought phases. However, some examples of PGPR‐
secreting phytohormones exist, whereas the functions of
gibberellins‐producing PGPR have been inadequately
understood.
PGPR inoculants have attracted more attention all
over the world by having positive responses under con-
trolled (greenhouse and laboratory) conditions; more-
over, their results under open conditions are
unpredictable. So, these PGPR must be proliferated arti-
ficially to optimize their capability and biological activity
under field applications. In the future, research will be
22 | MEENA
needed to optimize favorable growth conditions and in-
crease shelf‐life of the PGPR products, which are not
phytotoxic to plants, abide adverse environmental con-
ditions, high productivity, and cost‐effective PGPR pro-
ducts for the agricultural farmers.
ACKNOWLEDGMEN TS
Authors are highly grateful to the authorities of respective
departments for support in doing this study. This study was
supported by Startup Research Grant (UGC Faculty
Research Promotion Scheme; FRPS) and sustained by
Mohanlal Sukhadia University, Udaipur, Rajasthan, India.
Authors are thankful to Principal and Head of the
Department of Botany, Acharya Narendra Dev College,
University of Delhi, New Delhi, India for providing neces-
sary facilities during this study.
CONFLICT OF INTERESTS
The authors declare that there are no conflict of interests.
ORCID
Mukesh Meena http://orcid.org/0000-0002-6336-1140
Prashant Swapnil https://orcid.org/0000-0001-
7932-5913
Harish https://orcid.org/0000-0002-9883-7014
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How to cite this article: Meena M, Swapnil P,
Divyanshu K, et al. PGPR‐mediated induction of
systemic resistance and physiochemical alterations
in plants against the pathogens: Current
perspectives. J Basic Microbiol. 2020;1–34.
https://doi.org/10.1002/jobm.202000370