Review

sustainability
Review
Bacterial Plant Biostimulants: A Sustainable Way towards
Improving Growth, Productivity, and Health of Crops
Basharat Hamid 1 , Muzafar Zaman 1 , Shabeena Farooq 1 , Sabah Fatima 1, *, R. Z. Sayyed 2, * ,
Zahoor Ahmad Baba 3 , Tahir Ahmad Sheikh 4 , Munagala S. Reddy 5, *, Hesham El Enshasy 6,7 , Abdul Gafur 8
and Ni Luh Suriani 9
1 Department of Environmental Science, University of Kashmir, Hazratbal,

Srinagar 190006, Jammu and Kashmir, India; basharat384@gmail.com (B.H.);
muzafarzaman@gmail.com (M.Z.); shabeenafarooq188@gmail.com (S.F.)
2 Department of Microbiology, PSGVP Mandal’s Arts, Science, and Commerce College,
Shahada 425409, Maharashtra, India
3 Division of Basic Science and Humanities, FOA, Wadura, Sher-e-Kashmir University of Agricultural Sciences
and Technology, Wadura 193201, Jammu and Kashmir, India; baba.zahoor@gmail.com
4 Division of Agronomy, FOA, Wadura, Sher-e-Kashmir University of Agricultural Sciences and Technology,
Wadura 193201, Jammu and Kashmir, India; tahirkmr@gmail.com
5 Asian PGPR Society for Sustainable Agriculture & Auburn Ventures, Department of Plant Pathology and
Entomology, Auburn University, Auburn, AL 36830, USA
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 (SRTA), New Borg Al-Arab, Alexandria 21934, Egypt
8
Sinarmas Forestry Corporate Research and Development, Perawang 28772, Indonesia; gafur@uwalumni.com
9 Biology Study Program, Mathematics and Natural Sciences Faculty, Udayana University,
Citation: Hamid, B.; Zaman, M.;
Bali 80361, Indonesia; niluhsuriani@unud.ac.id
* Correspondence: sabahfatima333@gmail.com (S.F.); sayyedrz@gmail.com (R.Z.S.); prof.m.s.reddy@gmail.com
Farooq, S.; Fatima, S.; Sayyed, R.Z.;
(M.S.R.)
Baba, Z.A.; Sheikh, T.A.; Reddy, M.S.;
El Enshasy, H.; Gafur, A.; et al.
Bacterial Plant Biostimulants: A
Abstract: This review presents a comprehensive and systematic study of the field of bacterial plant
Sustainable Way towards Improving biostimulants and considers the fundamental and innovative principles underlying this technology.
Growth, Productivity, and Health of Plant biostimulants are an important tool for modern agriculture as part of an integrated crop man-
Crops. Sustainability 2021, 13, 2856. agement (ICM) system, helping make agriculture more sustainable and resilient. Plant biostimulants
https://doi.org/10.3390/su13052856 contain substance(s) and/or microorganisms whose function when applied to plants or the rhizo-
sphere is to stimulate natural processes to enhance plant nutrient uptake, nutrient use efficiency,
Academic Editor: Domenico Ronga tolerance to abiotic stress, biocontrol, and crop quality. The use of plant biostimulants has gained
substantial and significant heed worldwide as an environmentally friendly alternative to sustainable
Received: 2 February 2021
agricultural production. At present, there is an increasing curiosity in industry and researchers about
Accepted: 1 March 2021
microbial biostimulants, especially bacterial plant biostimulants (BPBs), to improve crop growth
Published: 6 March 2021
and productivity. The BPBs that are based on PGPR (plant growth-promoting rhizobacteria) play
plausible roles to promote/stimulate crop plant growth through several mechanisms that include
Publisher’s Note: MDPI stays neutral
(i) nutrient acquisition by nitrogen (N2 ) fixation and solubilization of insoluble minerals (P, K, Zn),
with regard to jurisdictional claims in
published maps and institutional affil-
organic acids and siderophores; (ii) antimicrobial metabolites and various lytic enzymes; (iii) the
iations. action of growth regulators and stress-responsive/induced phytohormones; (iv) ameliorating abiotic
stress such as drought, high soil salinity, extreme temperatures, oxidative stress, and heavy metals
by using different modes of action; and (v) plant defense induction modes. Presented here is a
brief review emphasizing the applicability of BPBs as an innovative exertion to fulfill the current
Copyright: © 2021 by the authors.
food crisis.
Licensee MDPI, Basel, Switzerland.
This article is an open access article Keywords: abiotic stress; ethylene; jasomic acid; mineral solubilization; phytostimulants
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
Sustainability 2021, 13, 2856. https://doi.org/10.3390/su13052856 https://www.mdpi.com/journal/sustainability

Sustainability 2021, 13, 2856 2 of 24
1. Introduction
The global environment is changing continuously and the incidence of global warming
caused by extreme climatic events is also on the rise, consequently disturbing the world
ecosystems, including agro-ecosystems [1]. Such extreme changes in climate can affect
the quality and quantity of crops severely by inducing various environmental stresses
to crops, threatening food security worldwide [2]. An increase in global temperature,
atmospheric CO2 level, tropospheric O3 , and acid rains can cause multifarious chronic
stresses to plants, reducing their capability to respond in case of pathogen attacks [3].
Among these stresses, drought, water scarcity, and soil salinization are the most problematic
and complicated factors of agricultural losses resulting from human-induced climate
changes [4]. Fluctuations in temperature and rainfall variations are key indicators of
environmental stresses [5]. Elevated temperatures lead to an amplification of the rates of
respiration and evapotranspiration in crops, a higher infestation of pests, shifts in weed
flora patterns, and reduction in crop duration [6]. Water scarcity is also considered one
of the prime global issues that have direct effects on agricultural systems and according
to climate projections, its severity will increase in the future [7]. Water scarcity piercingly
influences a crop’s gaseous exchange capacity, causing the closure of stomata [8]. This
leads to the impairment of the evapotranspiration and photosynthetic activities of plants,
affecting overall biomass production [9]. Impaired evapotranspiration reductions also
affect the nutrient uptake ability of plants [8]. In semi-arid and arid climatic zones where
rainfalls are already less intense and sporadic, the damages caused by drought stress can
be exacerbated due to excessive accumulation of salts in soil [10].
Furthermore, the liberal use of inorganic fertilizers and pesticides to increase crop
productivity and meet the food requirement of the ever-growing human population, which
is projected to reach 9.7 billion by 2050, has severely affected the health of agro-ecosystems
and human beings. Confrontational challenges of improving agriculture production with
limited arable land rely on sustainable technologies. Several technical advances have been
suggested in the past three decades to increase the productivity of agricultural production
processes by reducing toxic agrochemical substances such as pesticides and fertilizers. An
emerging technology tackling these critical problems includes the creation of novel plant
biostimulants and successful methods for their application [11–15]. Plant biostimulants
differ from other agricultural inputs such as fertilizers and plant protection products
because they utilize different mechanisms and work regardless of the presence of nutrients
in the products. They also do not take any direct action against pests or diseases and
therefore complement the use of fertilizers and plant protection products. According to the
latest European Regulation (EU 2019/1009), a biostimulant is an EU fertilizer that seeks
to promote processes for plant feeding, regardless of the product’s nutrient quality, solely
to boost the following plant or plant rhizosphere characteristics: (i) increased nutrient
utilization efficiency, (ii) abiotic stress alleviation/tolerance, (iii) quality traits, and (iv) soil
or rhizosphere supply of stored nutrients [16,17]. Over the past decade, microbiome
research has changed our understanding of the complexity and composition of microbial
communities. The intense interest of industry and academics in biostimulants based on
live microbes has increased due to the reason that the growth and development of a plant
can be improved under field conditions more effortlessly than other biostimulants [18,19].
Biostimulants are not nutrients, but encourage the utilization of nutrients or help foster
plant growth or plants’ resistance/tolerance to various types of stresses [9,20]. Beneficial
plant fungi and bacteria can be considered the most promising microbial biostimulants [21].
The recent trend has underscored the fact that plants are not autonomous agents in their
environments but are associated with bacterial and fungal microorganisms, and that many
external and internal microbial interactions respond to biotic and abiotic stresses [22,23].
Therefore, biostimulants are gradually being incorporated into production systems to alter
physiological processes in plants to maximize productivity [24].
Bacterial plant biostimulants (BPBs) comprise a major category of plant biostimulants.
Plant growth-promoting rhizobacteria (PGPR) that colonize the plant rhizosphere are the
Sustainability 2021, 13, x FOR PEER REVIEW 3 of 26
Bacterial plant biostimulants (BPBs) comprise a major category of plant

biostimulants. Plant growth-promoting rhizobacteria (PGPR) that colonize the plant
most prominent
rhizosphere aregroup
the mostin this category
prominent [24].inThese
group PGPR improve
this category plant
[24]. These growth,
PGPR control
improve
plant
plant growth, control plant pathogens, improve nutrient and mineral uptake in plants,resis-
pathogens, improve nutrient and mineral uptake in plants, and increase plants’
tance
and to various
increase typesresistance
plants’ of biotic to
stresses
variousand tolerance
types of biotictowards
stressesabiotic stressestowards
and tolerance (Figure 1).
The representative
abiotic beneficial
stresses (Figure groups
1). The of PGPR-based
representative BPBs
beneficial include
groups of nitrogen-fixing
PGPR-based BPBs Rhizo-
bium, Azotobacter
include spp., Azospirillum
nitrogen-fixing Rhizobium, spp., Pseudomonas
Azotobacter spp., and Bacillus
spp., Azospirillum spp. [25,26]. The
spp., Pseudomonas
spp., and
present reviewBacillus spp.the
describes [25,26].
recentThe present concerning
knowledge review describes the BPBs
beneficial recentandknowledge
their role in
concerning beneficial BPBs and their role in improving crop health
improving crop health through various mechanisms. The article concludes by highlightingthrough various
mechanisms. The article concludes by highlighting the main findings
the main findings of an in-depth analysis of research articles published between 2015 andof an in-depth
analysis
2020, sorted of using
research articlesdatabases
different published such
between 2015 and
as Google 2020, Science
Scholar, sorted using different
direct, Pub Med,
databases such
Web of Science, etc.as Google Scholar, Science direct, Pub Med, Web of Science, etc.
Figure 1.1.The
Figure Thebeneficial
beneficialinfluence of PGPR
influence of PGPRon
oncrop
cropplants.
plants.
2. 2.
Global
GlobalMarket
Marketfor
forPGPR-Based Biostimulants
PGPR-Based Biostimulants
Biostimulants
Biostimulants are are emerging
emerging as as an
an essential
essentialcomponent
componentinin sustainable
sustainable agricultural
agricultural
practices.Instances
practices. Instances of of environmental
environmental hazards
hazardsandandsoil
soilcontamination
contamination from
frominjudicious
injudicious
andand excessiveapplication
excessive application of of chemical-based
chemical-based products
productsonon crops
cropshave been
have a key
been issue
a key for for
issue
thethe industryininrecent
industry recenttimes.
times. The global
globalbiostimulants
biostimulantsmarket
market size was
size estimated
was estimated at USD
at USD
1.74
1.74 billioninin2016,
billion 2016,and
andprojected
projected to
to expand
expandatata aCompound
Compound Annual
AnnualGrowth
GrowthRateRate
(CAGR)
(CAGR)
of of 10.2%
10.2% from
from 2017
2017 toto 2025.AArising
2025. risingfocus
focuson
onenhanced
enhancedproductivity,
productivity,coupled
coupled with
with rapid
rapid soil
soil degradation,
degradation, is likelyis tolikely
drivetothedrive
markettheover
market over theperiod.
the forecast forecastThe
period.
globalThe global
biostimulants
market size was estimated at USD 2.30 billion in 2019 and is expected to reachtoUSD
biostimulants market size was estimated at USD 2.30 billion in 2019 and is expected
reach USD 2.53 billion in 2020. The global biostimulants market is expected to grow at a
2.53 billion in 2020. The global biostimulants market is expected to grow at a compound
compound annual growth rate of 10.2% from 2017 to 2025 to reach USD 4.14 billion by
annual growth rate of 10.2% from 2017 to 2025 to reach USD 4.14 billion by 2025 [27].
2025 [27]. Although not all biostimulants are biological in nature [28], the bacteria are
Although not all biostimulants are biological in nature [28], the bacteria are ancestral
companions of a plant in all conditions. Moreover, according to the currently available
literature, less than 25% of the commercial products of biostimulants are microbial based [9].
Table 1 provides a list of some popular PGPR-based commercial biostimulants [29–31].
Although some formulations contain fungal associations, the preparations are mainly based
on PGPR.
Table 1. Examples of commercial PGPR-based plant biostimulants [29–31].
Commercial Products
PGPR Strains Target Crops for Use Target of Function
(Manufacturer)
FZB24® fl
Bacillus amyloliquefaciens and Ornamentals, vegetable Phosphate availability and
Rhizovital 42®
B. amyloliquefaciens sp. plantarum field crops protection against pathogens
(ABiTEP GmbH, Germany)
B. subtilis (IAB/BS/F1) and B.
polymyxa (IAB/BP/01);
Inomix® Biostimulant, Saccharomyces cerevisiae;
Plant growth promotion
Inomix® phosphore, and B. megaterium and P. fluorescens; and
Cereals increases root and shoot
Inomix® Biofertilisant Rhizobium leguminosarum,
weight, strong root system
(IAB (Iabiotec), Spain) Azotobacter vinelandii,
B. megaterium, and
Saccharomyces cerevisiae
Soil amelioration; produce
Azotobacter vinelandii,
BactoFil B10® plant growth-promoting
Azospirillum lipoferum, Dicotyledons (potato,
(AGRO.bio Hungary Kft., hormones auxin, gibberellins,
P. fluorescens, B. circulans, B. sunflower, rapeseed)
Hungary) and kinetin; N2 fixation; a
megaterium, and B. subtilis
biocontrol agent
Growth promotion via
nitrogen fixation, drought
Bio-Gold Pseudomonas fluorescens and All agricultural and
tolerance, control of root rot
(BioPower, Sri Lanka) Azotobacter chroococcum horticultural crops
and wilt diseases, phosphorus
solubilization
Cedomon® Highly effective against
(Lantmannen BioAgri AB, P. chlororaphis Barley and oats various types of
Sweden) seed-borne diseases
Rhizosum N
Phosphate availability,
Liquid PSA Azotoformans (N2 -fixing bacteria)
Wheat N2 fixation, plant
(Mapleton Agri Biotec Pty and Pseudomonas sp
growth promotion
Limited, Australia)
BactoFil A10® Azotobacter vinelandii, Azospirillum Increased soil nutrient content
Monocotyledons
(AGRO.bio Hungary Kft., brasilense, P. fluorescens, B. polymyxa, that results in plant
(cereals)
Hungary) and B. megaterium growth promotion
Agrobacterium radiobacter AR 39,
Fruits, vegetables,
Streptomyces sp. SB 14, and B.
Micosat F® Uno; and flowers Increased nutrient and water
subtilis BA 41
Micosat F® Cereali absorption, increases stress
(CCS Aosta Srl, Italy) Cereals, soybeans, tolerance and enhances ISR
Paenibacillus durus PD 76, B. subtilis
beet, tomatoes,
BR 62, and Streptomyces spp. ST 60
and sunflowers
Deciduous fruit trees,
horticultural brassicas,
Bioscrop BT16
cotton, citrus, Protection against
(Motivos Campestres, Bacillus thuringiensis var. kurstaki
cauliflower, olives, pests (beetles)
Portugal)
pepper, banana,
and tomato
Cucumber, lettuce, Growth promotion, quick
Amase®
Rhizobium, Azotobacter, Pseudomonas, tomato, pepper, production of the large and
(Lantmannen Bioagri,
Bacillus, and Chaetomium eggplant, cabbage, strong root system, and
Sweden)
and broccoli increases stress tolerance
PGA® Improved biomass
Bacillus sp. Fruits and vegetables
(Organica technologies, USA) accumulation, stress tolerance
Table 1. Cont.
Commercial Products
PGPR Strains Target Crops for Use Target of Function
(Manufacturer)
Azorhizobium caulinodens NAB38,
Azospirillum brasilense NAB317, Cereals, rapeseed, Growth promotion via
Nitroguard®
Azoarcus indigens NAB04, and and sugar nitrogen fixation
Bacillus sp.
Helps with nitrogen fixation
TwinN® Azospirillum brasilense NAB317,
and phosphorus solubilization
(Mapleton Agri Biotec Azoarcus indigens NAB04, and A.
and produces
Pty Ltd. Australia) caulinodens NAB38
growth-promoting hormones
Beet, sugarcane, and
Symbion® -N, vegetables
Rhizobium, Azotobacter, Promotion of plant growth,
Symbion® -P, and
Azospirillum, Acetobacter; improved root and shoot
Symbion® -K
B. megaterium var. phosphaticum; and weight, and a
(T. Stanes &
Frateuria aurantia stronger root system
Company Ltd., India)
Ceres® Field and Biocontrol agent
Pseudomonas fluorescens
(Biovitis, France) horticultural crops against pathogens
Nitrogen and phosphatic
Gmax® PGPR P. fluorescens, Azotobacter, nutrition, disease prevention
Field crops
(Greenmax AgroTech, India) and phosphobacteria and helps in plant
growth promotion.
3. Bacterial Plant Biostimulants, Beneficial Effects, and Mode of Action

Bacteria are known to interact with plants in all possible ways [32], including (i) con-
tinuum of symbiosis; (ii) bacteria niches extending from the substrate to the interior of cells,
which are called intermediate locations for rhizosphere and rhizoplane; (iii) associations
that are transient or lifelong; and (iv) functions that affect lots, including engagement in
biogeochemical cycles, the supply of nutrients, increased nutrient consumer efficiency,
induction of resistance, increased stress tolerance, plant growth regulators, and morpho-
genesis control. In this regard, a large amount of work presented in recent literature has a
sharp emphasis on potential applications of the bacterial association of plants largely as
agents for promoting plant growth and maintaining soil and crop health [33–36]. Plant
growth-promoting bacteria are generally associated with numerous (if not all) crop plant
species and are habitually present in varied environments. The most extensively inves-
tigated category of PGPB is the plant growth-promoting rhizobacteria (PGPR) primarily
colonizing the surfaces of roots and closely adhering to the soil interface, namely, the
rhizosphere. As overviewed by recent reviews [37–39], several PGPR can enter the root
interior, thereby establishing endophytic associations. Some of them can even surpass
the endodermis barrier, transcending from root cortex to vascular system, and afterward
thrive as endophytes (inside stem, tubers, leaves, and other organs). The extent of the
endophytic associations of host plant tissues (and/or organs) reflects the capability of these
bacteria to selectively acclimatize to various specific ecological niches [40,41]. As a result,
such intimate bacterial associations with host plants are formed with no damage to the
plant [42,43]. In regard to taxonomic, functional, and ecological diversity in developing
agriculture biostimulants, PGPR seize the most prominent place.
Although numerous soil bacteria were documented to help plant growth promotion
and production, the mode(s) of action by which the bacteria exhibit beneficial activities are
hardly understood. The molecular basis for association processes between bacteria and
crop plants that induce/stimulate physiological modifications is starting to be understood,
primarily because of the emerging approaches to “omics.” A varied number of pathways
have been employed to aid the acquisition of plant nutrients, including improved plant root
surface, phosphorus solubilization, nitrogen fixation, production of HCN, and development
of siderophores, which are further discussed under subsections [44]. PGPR differ and have
Although numerous soil bacteria were documented to help plant growth promotion
and production, the mode(s) of action by which the bacteria exhibit beneficial activities
are hardly understood. The molecular basis for association processes between bacteria
and crop plants that induce/stimulate physiological modifications is starting to be
Sustainability 2021, understood,
13, 2856 primarily because of the emerging approaches to “omics.” A varied number 6 of 24
of pathways have been employed to aid the acquisition of plant nutrients, including
improved plant root surface, phosphorus solubilization, nitrogen fixation, production of
HCN, and development of siderophores, which are further discussed under subsections
consequences
[44]. PGPR differ for all facets for
and have consequences of the plant life
all facets cycle:
of the plantpromoting
life cycle:growth and nutraceutical
promoting
values of plants, morphological and physiological development,
growth and nutraceutical values of plants, morphological and physiological stress responses (biotic
development, stress responses (biotic and abiotic), interactions of agro-ecosystems withand enhanced
and abiotic), interactions of agro-ecosystems with other species forms,
production.
other species forms, Numerous
and enhanced direct andNumerous
production. indirect mechanisms are involved
direct and indirect in the development of
mechanisms
these responses that are shown in Figure 2.
are involved in the development of these responses that are shown in Figure 2.
Figure 2. Mode ofFigure

action 2.
of Mode
PGPRof
onaction
the growth of crop
of PGPR plants.
on the growth of crop plants.
3.1. Plant Growth Promotion and Nutrient Acquisition

3.1. Plant Growth Promotion and Nutrient Acquisition
The modulation of bacterial behavior has tremendous potential for the procurement
The modulation
of nutrition for plants. of bacterial
PGPR formulations arebehavior has tremendous
a significant potential
biostimulant class, for the procurement of
as they
allow root growth, mineral availability, and efficiencies in the utilization of nutrients in as they allow
nutrition for plants. PGPR formulations are a significant biostimulant class,
root growth,
the crop rhizosphere mineral
to increase availability,
crop growth [45].and Many
efficiencies
PGPRinaretheknown
utilization of nutrients in the crop
to stimulate
rhizosphere to increase crop growth [45]. Many PGPR are known to stimulate phytohor-
phytohormone production through a combination of various mechanisms
mone production through a combination of various mechanisms [46–53] represented in
[46,47,48,49,50,51,52,53] represented in Table 2.
Table 2.
Table 2. Beneficial effects of reported PGPR biostimulants on different crops and their modes of action.
PGPR Biostimulant Crop Beneficial Effects Mode of Action References

Increased production of
Growth, biomass, and
Bacillus sp. Lettuce phytohormones and availability [46]
yield of plants
of nutrients
Azospirillum brasilense,
Gluconacetobacter Plant growth, crop Production of plant hormones and
diazotrophicus, Herbaspirillum Onion yield, and increased solubilization of nutrients that [47]
seropedicae, and number of bulbs cause uptake of nutrients
Burkholderia ambifaria
Bacillus pumilus, B. mojavensis,
Growth and production Synthesis of indole-3-acetic acid
B. Amyloliquefaciens, and Tomato [48]
and nutrient uptake N2 -fixation and P solubilization
P. putida.
Enhanced production of phenols,
PGPR (Bacillus subtilis) Tomato Improved fruit quality flavonoids, carotenoids, [49]
and antioxidants
N2 fixation involving many
Pseudomonas aeruginosa Wheat Nutrient uptake reactions and synthesis of [50]
organic acids
Enhanced germination,
Cucumber, Production of a substantial
Azospirillum brasilense (Sp7b root length, and weight;
lettuce, amount of phytohormones such [51]
and Sp245b) vigor index of
and tomato as IAA
germinating seeds
Phosphate solubilization and
Bacillus pumilus and Stimulated growth
Rice production of IAA, gibberellins, [52]
Pseudomonas pseudoalcaligenes and production
siderophores, and ACC utilization
Synthesis of indoleacetic acid
Maize, sorghum,
Biostimulated growth (IAA), nitric oxide, carotenoids,
Azospirillum brasilense wheat, barley, [53]
and production and numerous cell
and legumes
surface components
3.1.1. Phytohormone Stimulation

Auxins such as 3-Indole Acetic Acid (IAA) are involved in processes such as the germi-
nation of seeds, control processes for vegetative increase, and the establishment of lateral
or adventurous roots, and can mediate light and heavy reactions, photosynthesis biosyn-
thesis of metabolites, and stress tolerance [54]. It has been observed that PGPR produces
hormones that provide protection and wall-related transcription changes [55], induce long
roots, increase the biomass of roots, and reduce the density and dimensions of stomata [56],
in addition to activating auxin reaction genes that enhance plant development [21]. As IAA
producers, separate PGPR genera have been recognized, such as Rhizobium [57], Aeromonas
and Azotobacter [32], Bacillus [21], and Pseudomonas [58]. A great number of PGPR produce
cytokinins and gibberellins [59], although the roles of bacteria in the regulation of plant hor-
mones and the bacterial mechanism involved in their synthesis are largely not understood
yet. Some strains of PGPR can support relatively large quantities of gibberellins, which
contribute to increased growth in plants [60]. PGPR also regulate the proper amounts of
ethylene to maintain plant growth, as confirmed by previous studies [61].
3.1.2. Nitrogen
Nitrogen (N) is a very essential macronutrient needed for plant growth and devel-
opment, but it is not available to most plants due to its inertness. Atmospheric nitrogen
(N2 ) is converted into ammonia by PGPR by nitrogen fixation and this source of nitrogen
(ammonia) can be utilized by crop plants for productivity purposes [62]. The application of
N2 -fixing bacteria as growth enhancers has become known as one of the most effective and
environmentally feasible methods and concurrently replaces the use of inorganic nitrogen
fertilizers [63]. Biological nitrogen fixation (BNF) is accomplished by free-living microor-

ganisms such as Azotobacter, Azospirillum, Bacillus, Enterobacter, Pseudomonas, Burkholderia,
and Serratia, etc., and symbiotic or associated microorganisms such as Rhizobium, Bradyrhi-
zobium, and certain species of Azospirillum sp., which contribute fixed nitrogen to the
associated crop plants [64,65]. Moreover, a small group of woody non-legumes, known
as actinorheic plants, can also be colonized by diazotrophs belonging to the Frankia sp.,
which can induce the development of nitrogen-fixing root nodules. Leguminous inoculants
are the first example of industrial bacterial products in agriculture and are now the most
commonly used inoculants in agriculture [66]. Beginning in the early 21st century, interest
began rising around the mass production of commercial inoculants from wild, live N-fixing
bacteria, including Azoarcus sp., Burkholderia sp., Gluconacetobacter sp., and Diazotrophicus
sp. These free-living diazotrophs are more efficient in providing N to a wider variety of
crops than rhizobia. Azospirillum sp.-based commercial inoculants from small and medium-
sized businesses worldwide have improved the production yields of different cereal crops
effectively [67]. Other bacteria that do not primarily fix N2 have also shown increased N
in many plants possibly due to root growth enhancement, allowing plants to gain more
soil [68] and thus, increase the efficiency of nitrogen usage.
3.1.3. Phosphorus
Phosphorus is another essential macronutrient in metabolic and physiological pro-
cesses in plants such as photosynthesis, biological oxidation, and cell division [69], and
is also an important nutrient for crop growth and productivity. Chemical phosphorus
fertilizers are subjected to chemical fixation (in soil) with some other metal cations and
are lost by leaching, and their unavailability to plants limits their ability to perform these
crucial functions [70]. The application of stimulants that contain PGPR that are capable of
solubilizing insoluble phosphate by discharging organic acids increases the accessibility
of this element to crop plants, thereby improving soil fertility and productivity [71,72].
Numerous strains among bacterial genera including Pseudomonas, Rhizobium, Bacillus, and
Enterobacter are the most potent P-solubilizers. Phosphorus solubilizing bacteria (PSB) may
facilitate plants’ access to the non-labile phosphorus reserve by liberation of its recalcitrant
form and making it more accessible to crops by secreting organic acids and/or hydrochloric
ions. Likewise, PSB-manufactured phytase can release reactive phosphates from organic
compounds [73].
3.1.4. Potassium
Potassium is another fundamentally important macronutrient required for crop growth
and improvement owing to the rhizospheric deficiency of crops and consequently has
always been a major constraint in crop production [74,75]. The shortage of the solubilized
form of rhizospheric potassium is also because it tends to form insoluble complexes when
applied as an inorganic fertilizer. However, PGPR can solubilize insoluble potassium
through secretions of inorganic acids and by making it available to crop plants, thus im-
proving the agricultural productivity and health of crops [76,77]. Hence, they offer an
attractive option as biostimulators in place of conventional fertilizers. PGPR such as Bacil-
lus edaphicus, Acidothiobacillus sp., Ferrooxidans sp., Pseudomonas sp., Bacillus mucilaginosus,
Burkholderia sp., and Paenibacillus sp. have been known to release potassium in its available
form from potassium-bearing minerals in soils [78].
3.1.5. Micronutrients
Many strains of bacteria improve Fe (iron) availability by generating siderophores
or organic acids. The commercial preparation of the genus Acidithiobacillus ferrooxidans
developed and produced by AgriLife (India) [79] solubilizes Fe through the release of
organic acids [80]. Zinc is another crucial micronutrient that is needed in smaller quantities
for the healthy growth and improved production of crops. About 96–99% of the zinc
applied to crop plants is converted into an insoluble form that depends on soil type and
other physiological reactions [81]. Several bacteria strains increase Zn mobilization, thereby
increasing Zn uptake by plants and boosting the yield in many crops [82]. Although
the mechanisms involving Zn mobilizers still remain uncertain, they are more likely
similar to PSBs and Fe mobilizers and involve mainly the production of organic acids and
chelating agents.
3.2. Quality Improvement of Crop and Yield by Bacterial Plant Biostimulants

Plant biostimulants, which increase plant evolution, flowering, fruit forming, and crop
production, can provide a desirable and environmentally friendly agricultural moderniza-
tion [83]. A variety of living and non-living bacterial isolates such as Bacillus licheniformis,
Bacillus megaterium, Bacillus pumilus, Bacillus safensis, Microbacterium sp., Nocardia globerula,
Pseudomonas fluorescens, Pseudomonas fulva, Pseudoxanthomonas dajeonensis, Rhodococcus
coprophilus, Lactobacillus plantarum, Sphingopyxis macrogoltabida, Streptomyces sp., Bifidobac-
terium bifidus, Lactobacillus acidophilus, Lactobacillus sp., Lactobacillus buchneri, Lactobacillus
paraplantarum, Lactobacillus delbrueckii, and Lactobacillus pentosus have been reported to
increase concentrations of total carbohydrates, nutrients (magnesium, nitrogen, and phos-
phorus, etc.), pigments (such as chlorophyll, carotenoids), and antioxidant substances
and therefore improve plant quality, productivity, and yield [21,83,84]. As an example,
the impact on common bean plants cultivated under water stress shows substantial en-
hancement in the phenolic contents of the inoculated plants of four biostimulant products
with Bacillus subtilis in their formulations [84]. In addition, by inoculation of the Bacillus
subtilis CBR05 PGPR strain, the quality of tomatoes is known to improve for the carotenoid
profile (carotene and lycopene) [49]. The influence of the biopreparation containing some
bacterial species such as Streptomyces sp., Bacillus subtilis, and Pseudomonas fluorescens on
the growth enhancement of fruits through organic farming was reported as improving
the growth of sour cherry and apple trees [85]. The regulation of horticultural primary
and secondary metabolisms in microbial biostimulants culminates in the synthesis and
build-up of lipophilic as well as hydrophilic antioxidant molecules, also referred to as
phytochemicals [86,87]. Microbial biostimulant applications containing beneficial bacterial
cultures often improve fruit quality by suppressing diseases that may cause economic
loss [88].
3.3. Abiotic Stress Tolerance Induced by Bacterial Plant Biostimulants

Global climate change dictates that abiotic stresses, particularly nutrient deficiency,
salinity, drought, hypoxia, and heat stress, are responsible for 60–70% of yield deficit [14].
Under these situations, plant biostimulant application is suggested as an effective agro-
nomic method to improve tolerance to adverse soil and harsh environmental conditions
and to address the adverse effects of the suboptimal conditions on agricultural and hor-
ticulture crops [9]. Plant growth rhizobacteria (PGPR) can enhance plant reactions to
abiotic pressures (Figure 3), and promote physical, chemical, and biological activities [89]
through various mechanisms [90–100], as presented in Table 3. Much work has been done
on bacterial isolates that can be employed to promote the mitigation of abiotic stress in
various crops.
Sustainability 2021, 13, x FOR PEER REVIEW 11 of 26

3. Much work has been done on bacterial isolates that can be employed to promote the
mitigation of abiotic stress in various crops.
Figure 3. Illustration of abiotic stress tolerance induced by bacterial plant biostimulants.
Table 3. Influence of PGPR biostimulants on abiotic stress

stress tolerance
tolerance in
in various
various crop
crop plants.
plants.
PGPR Biostimulants CropCrop

Plants Type
TypeofofAbiotic
Abiotic Stress Mode of Action References
PGPR Biostimulants Mode of Action References
Plants Stress Ethylene mediation, reacive oxygen
Ethylene mediation,
species reacive oxygen
(ROS) accumulation, species
maintaining
(ROS) photosynthetic
accumulation, efficiency and ion
maintaining
Glutamicibacter sp. YD01 Rice Salt tolerance [90]
homeostasis, increasing expression of
Glutamicibacter sp. YD01 Rice Salt tolerance photosynthetic efficiency and ion homeostasis, [90]
stress-related genes, the activity of ACC
increasing expression of stress-related
oxidase, and acquisition of K genes,
+ the
activity of ACC oxidase, and acquisition of K+
Bacillus sp., Azospirillum
Bacillus Production of phytohormones and
lipoferum,sp., Azospirillum
Azospirillum Production of phytohormones and
Wheat Salt stress osmoregulators, and enzyme (ROS [91]
lipoferum,
brasilense,Azospirillum
and
Pseudomonas Wheat Salt stress osmoregulators,scavenging)
and enzyme activation
(ROS scavenging) [91]
brasilense, andstutzeri
Pseudomonas
activation
stutzeri Increased production of Abscisic acid
Gluconacetobacter Drought stressIncreased
(ABA), osmoprotectants
production (proline
of Abscisic and
acid (ABA),
Red rice [92]
Gluconacetobacter
diazotrophicus Pal5 Drought stress
alleviation glycine betaine) and e AT-hook motif
Red rice osmoprotectants (proline and glycine betaine)
nuclear-localized (AHLs)
[92]
diazotrophicus Pal5 alleviation
and e AT-hook motif nuclear-localized (AHLs)
Increased ABA production, enhanced
Gluconacetobacter Increased ABA production,
chlorophyll synthesis, andenhanced
increased
Gluconacetobacter Red rice Water stressalleviation
Water stress [93]
diazotrophicus Pal5 Red rice chlorophyll synthesis, and increased
trehalose and α-tocopherol trehalose
content [93]
diazotrophicus Pal5 alleviation
and α-tocopherol content in roots.
in roots.
Water/drought IncreasedIncreased
production of proline,
production trehalose
of proline,
Azospirillum spp. (Az19) Maize Water/drought [94]
Azospirillum spp. (Az19) Maize stressstress
alleviation trehalose
(glutamate) and (glutamate) and
glycine-betaine [94]
alleviation
Bacillus spp XT13, XT38, and Increased prolineglycine-betaine
content accompanied by
Maize Drought stress Increased proline content accompanied [95]
XT110 reduced Ascorbate Peroxidae (APX) and
Bacillus spp XT13, XT38, by reduced Ascorbate Peroxidae (APX)
Maize Drought stress [95]
and XT110 and glutathione reductase (GR)
activities, increased nutrient uptake
Table 3. Cont.
PGPR Biostimulants Crop Plants Type of Abiotic Stress Mode of Action References
Pseudomonas Salinity stress Exopolysaccharides, IAA, gibberellic
Sunflower [96]
entomophila (PE3) alleviation acid, and siderophores
Reduced chill injury, lipid peroxidation,
P. fragi, P. proteolytica, P.
and ice-nucleating activity
fluorescens, P. chloropaphis,
Bean Cold stress corresponding to ROS level, and [97]
and Brevibacterium
stimulation of apoplastic antioxidant
frigoritolerans
enzyme activities
Pseudochrobactrum
Wheat Cold stress Growth promotion and biocontrol [98]
kiredjianiae
Pseudomonasfluorescens Maize Heavy metal stress Production of IAA [99]
Production of siderophores, ammonia,
Azotobacter chroococcum Maize Heavy metal stress and 1-aminocyclopropane-1-carboxylate [100]
deaminase (ACCD)
3.3.1. Drought Stress

Recent attention has turned to the application of beneficial microorganisms that
mediate drought tolerance and improve plant water-use efficiency. These efforts have
been augmented due to technological advances in next-generation sequencing and micro-
biomics [101,102]. The application of plant growth-promoting rhizobacteria (PGPR) is con-
sidered a sustainable synergistic biological approach to cope with water deficiency in crop
production [103]. PGPR can impart tolerance to drought stress by releasing phytohormones,
volatile compounds, ACCD, exopolysaccharides, and antioxidants by regulating osmolytes
and stress-responsive genes and aggravating modifications in the roots [102–104].
3.3.2. Salinity Stress

Soil salinization accounts for more than 6% of global land, rendering 22% and 33%
of total cultivated and irrigated agrarian land, respectively, under stress that adversely
affects crop productivity [105]. By the year 2050, approximately 50% of arable area will be
under threat due to soil salinity, as it increases rapidly at the rate of 10% annually due to
numerous reasons including implausible irrigation practices, irrational fertilization, poor
drainage, and climate change [106,107].
PGPR can alleviate salinity stress in plants through many synergistic mechanisms
including osmotic regulation by prompting accumulation of osmolytes and signaling of
phytohormones, increasing nutrient uptake and attaining homeostasis of ions, and reducing
oxidative stress through enhanced antioxidant activity, volatile organic compounds (VOCs),
and photosynthesis amelioration [108,109].
3.3.3. Heat Stress

The prime alarming effect of climate change is the rise in global temperature and is
directly linked to crop productivity. High temperatures increase respiration and transpira-
tion rates, alter the allocation of photosynthates, and affect photosynthesis (particularly
C3 plants), thereby influencing plant physiology [110]. Intense heat can cause plant cell
protein denaturation or affect cell wall and membrane permeability [111]. PGPR help
mitigate the heat stress in plants through properties such as the production of osmolytes
and the reduction of carbon flux [112]. They can secrete several polysaccharides involved
in biofilm formation, covering root nodules that enhance the water retaining capability
of plant roots. PGPR, especially the heat-tolerant/evolved strains, possess the ability to
enhance the production of lipopolysaccharides (LPS) and exopolysaccharides (EPS) and
specific proteins known as heat shock proteins (HSPs) [113]. The application of ethylene
reducing bacteria, especially with ACC deaminase activity, can avoid the detrimental
effects of heat stress in plants [3].
3.3.4. Cold Stress

Cold stress is detrimental to plants, as it directly affects the rate of nutrient and water
uptake, which may lead to cell starvation, desiccation, and consequent death. Reduced
metabolism, which occurs in cold tension, results in photo inhibition, inhibition of the activ-
ity of photosystem II, and destabilization of the phosphorus lipid bilayers, thereby affecting
the normal architecture of cell membranes [44,114]. In harsh environments, psychrophilic
(cold-adapted) microorganisms can thrive and have possible resistance enhancement path-
ways that benefit plants [115]. Cold-adapted PGPR belong to various genera, including
Pseudomonas, Bacillus, Arthrobacter, Exiguobacterium, Paenibacillus, Providencia, and Serra-
tia. There are several attributes of psychrotolerant PGPR that make their application as
biostimulants beneficial in alleviating cold stress. These attributes include solubilization
of nutrients, Fe-chelating compounds, ACC deaminase production, IAA, and bioactive
compounds. In plants, cold tolerance can be imparted by PGPR through the enhanced
accumulation of carbohydrates, the regulation of stress-responsive genes for modulation
of osmolytes, and increasing specific proteins, including cold shock proteins (CSPs) [113].
In addition, the application of such biostimulants with the ability to outcompete the ice-
nucleating activity of microorganisms is becoming an effective method to overcome the
losses caused by cold/frost damage [3].
3.3.5. Heavy Metal Stress

Heavy metal stress due to hyperaccumulation of toxic metals, including Hg, As, Cd,
Pb, and Al, greatly decreases crop productivity. Their accumulation in the soil directly
affects its texture and pH, which consequently reduces crop growth by exerting negative
effects on several biological processes [116]. In plants, heavy metal stress shows both direct
effects, including cytoplasmic enzyme inhibitions and cell structure damage as well as
indirect consequences, including oxidative stress through several indirect mechanisms
(e.g., glutathione depletion or binding to proteins—sulf-hydryl (SH) groups) or inhibiting
anti-oxidative enzymes, inducing ROS-producing enzymes (e.g., Nicotinamide Adenine
Dinucleotide Phosphate Hydrogen (NADPH) oxidases) [117]. Heavy metal-tolerant PGPR
such as Pseudomonas, Bacillus, Methylobacterium, and Streptomyces can reduce the deleterious
effects of heavy metals and improve the growth and yield of crops. PGPR biostimulants
are very effective in alleviating the toxicity of heavy metals in plants. They reduce the
translocation of heavy metals to different parts of the plant by altering their mobilization
through chelation, precipitation, complexation, redox reactions, and adsorption [118,119].
Rhizospheric bacteria also release extracellular polymeric substances (EPS) [93] such as
polysaccharides, glycoprotein, lipopolysaccharide, and soluble peptide, which possess a
substantial quantity of anion binding sites to help in the removal or recovery of heavy
metals from the rhizosphere via biosorption. However, in highly contaminated sites, the
mobilization and consequent bioavailability of heavy metals in excess by siderophores,
organic acids, or through bioleaching remains debatable.
3.4. Disease Suppression/Defense against Plant Pathogens through Antagonism

Nowadays, the biological control of pathogens is managed by the activities of several
microbiomes. Additionally, PGPR are known to develop resistance to various diseases
through various direct or indirect mechanisms [120–128], shown in Table 4. The application
of bacterial biostimulants encourages the healthy growth of crops through the suppres-
sion of different plant pathogens and pests. The PGPR inhibition of microbial/pathogen
growth occurs synergistically through several chief mechanisms, including antibiosis,
volatile organic compound (VOC) production, extracellular enzymatic lysis, bacteriocin,
and siderophore-mediated inhibition [129].
Table 4. Influence of PGPR biostimulants on biotic stress resistance in different crop plants.
PGPR Biostimulants Crop Biotic Stress Mode of Action References

Bacillus cereus (PX35),
Serratia sp. XY21, and Tomato Root-knot nematodes Synergistic biocontrol [120]
Bacillus subtilis SM21
Extracellular-bioactive compounds
Pseudomonas aeruginosa LV Tomato Bacterial stem rot (phytoalexins, flavonoids, defensins, [121]
proteins, and phenolics)
Production of Cry1Ia δ-endotoxin,
Late blight agent and
stimulating transcription of jasmonate
B. subtilis 26DCryChS Potato damaged by Colorado [122]
reliant genes promoting transcription of
potato beetle larvae
salicylate reliant gene (PR1)
Lactobacillus plantarum Disease prevention in Antimicrobial metabolites (lactic acid)
PM411 and Lactobacillus Strawberry strawberry and production that disrupts pathogen’s [123]
plantarum TC92 kiwi fruit cell membranes
Production of defense enzymes such as
B. subtilis BS2 Tomato Tomato wilt peroxidase, polyphenol oxidase, [124]
chitinase, and phenylalanine
Bacillus safensis and
Cabbage Black rot IAA production [125]
Bacillus altitudinis
B. velezensis,
B. mojavensis, and Soybean Phytophthora root rot IAA production [126]
B. safensis
Bacillus cereu,
1-aminocyclopropane,1, carboxylic
B. subtilis BSV, and Ginger Blister blight [127]
acid production
B. subtilis BSP
B. cepacia GRB35 Ginger Soft rot in ginger Fungicide production [128]
3.4.1. Antibiosis
PGPR produce antibiotics that are the most significant antagonistic agents effective
against phytopathogens. Antibiotics produced by PGPR are known to have antimicro-
bial, antiviral, cytotoxic, insecticidal, antihelminthic, and phytotoxic (against weeds) ef-
fects [130,131]. Antibiotic production usually allows better competition between microbes
and thus enhances the efficiency of beneficial PGPR associations [132]. Numerous species
of Pseudomonas produce a broad range of antifungal antibiotics, including butyrolactones,
cepaciamide A, ecomycins, 2,4-diacetylphloroglucinol (2,4-DAPG), phenazines, pyrrol-
nitrin, pyocyanin, pyoluteorin, oomycin A, rhamnolipids, N-butylbenzene sulfonamide,
and viscosinamide [133]. Bacillus species also secrete a large variety of antibiotics, in-
cluding bacilysin, bacillaene, difficidin, mycobacillin, rhizocticins, sublancin, subtilintas
A, subtilosin A, etc. They also produce numerous lipopeptide biosurfactants, such as
bacillomycin, iturins, surfactin, etc. with antibiotic activity [134].
3.4.2. VOC Antagonism

In plants, VOCs help in the biocontrol of bacteria and fungi nematodes and also act
as elicitors of the induced systemic resistance against phytopathogens [135]. Several VOC
metabolites with antagonistic activities are secreted by PGPR. These include benzene, cyclo-
hexane, 2-(benzyloxy)-1-ethanamine, methyl, dodecane, decane, 1-(N-phenyl carbamyl)-2-
morpholinocyclohexene, benzene (1-methylnonadecyl), dotriacontane, 1-chlorooctadecane,
tetradecane, and 11-decyldocosane, although their type and quantities released vary among
different species [136]. Among VOCs, HCN produced by rhizospheric bacteria is known
to play an important function in the biocontrol of phytopathogens and pests [137]. Pseu-
domonas sp. synthesizing HCN can inhibit some pathogenic fungi [138]. HCN released by
P. chlororaphis O6 is known to show nematicidal activity [139]. In addition, VOCs (acetoin
and 2,3-Butanediol) secreted by Bacillus spp. are very effective fungal inhibitors [140]. In
addition to biological control, VOCs are associated with beneficial tradeoffs in attracting
pollinators via the mediation of communication signals [141].
3.4.3. Lysis by Extracellular Enzymes

Lytic enzymes produced by PGPR provide another effective mechanism for combating
pathogen attacks. Rhizobacteria release extracellular enzymes such as chitinase and β-1,3-
glucanase, which are involved in cell wall lysis, killing pathogens [142]. Since the fungal cell
wall is mainly composed of chitin and β-1,4-N-acetyl-glucosamine, rhizobacteria secreting
chitinase and β-1,3-glucanase are potent antifungals. For example, P. fluorescens LPK2 and
S. fredii KCC5 release β-glucanases and chitinases and suppress wilts caused by Fusarium
udum and F.oxysporum [133]. Bacteria with protease, lipase, and chitinolytic activities have
been reported to show insecticidal activity [143]. PGPR with ACC deaminase activity also
play a very important role in all types of stresses, including biocontrol.
3.4.4. Bacteriocins
Bacteriocins or bacterial toxins are narrow-spectrum antimicrobial peptides produced
by bacteria, including PGPR. Their production is another mechanism for eliminating
competitor strains that are narrow-spectrum, proteinaceous antibiotics that target and
kill related bacterial species [144]. Bacteriocins are produced by both Gram -negative
(colicins, S-piocins, microcins, etc.) as well as Gram -positive (nisin, helvecin, mersadicin,
etc.) bacteria [145]. The direct application of bacteriocins has shown promising results
under laboratory conditions against bacterial spot disease in tomato [146]. Typically,
bacteriocins are highly selective of their targets without affecting off-targets and provide a
safer substitute to field applications of chemicals [147].
3.4.5. Siderophores
Siderophores are the largest class of known compounds that can bind and transport,
or shuttle, iron (Fe). These low-molecular-weight coordination molecules are excreted by a
wide variety of fungi and bacteria to aid Fe assimilation [148]. Siderophore production by
PGPR is an indirect mechanism involving the reduction or prevention of destructive effects
caused by phytopathogens [149]. Siderophores possess an antagonistic effect and prevent
the escalation of other pathogenic bacteria and fungi in the plant’s rhizosphere [150]. Their
low molecular weight and ability to sequester Fe3+ ions in the rhizospheric zone makes
iron inaccessible to the plant pathogens, thus preventing their growth.
3.5. Induction of Systemic Resistance (ISR)

The first line of the defense system of plants is comprised of a precise surveillance
system that, by perceiving several elicitors, allows them to switch on plant defense mode
and reject potentially dangerous pathogens or microbes. The elicitors are small structures
referred to as pathogen/microbe-associated molecular patterns (PAMPs or MAMPs), which
are recognized by the pattern recognition receptors (PRRs) of the plant’s innate immune
system [151]. Similar to this innate mechanism, PGPR are also capable of stimulating the
defense system of their associated plants against pathogen attack through the induction of
systemic resistance (ISR) by SAR (system acquired resistance) and ISR (induced systemic
resistance) pathways [152]. Furthermore, PGPR can be exploited for the stimulation of
induced systemic tolerance (IST) against various abiotic stresses, including water scarcity,
drought, salinity, osmolyte stress, temperature extremes, heavy-metal stress, and mechan-
ical injuries [153] (Figure 4). Therefore, the application of multi-stress-resistant PGPR
biostimulants has become important for enhancing agricultural production, resolving
global climate change concerns and low annual crop yields, and combatting increasing
food demands [13].
recently as successfully inducing resistance against Magnaporthe oryzae [176] whereas
orfamide (at 25 μM concentration) is known as an elicitor of ISR against Cochliobolus
miyabeanus [177]. Accumulation of ROS following the inoculation of bacteria
Gluconacetobacter diazotrophicus has also been observed at the early stages of rice root
colonization. This study indicates that bacterial ROS-scavenging enzymes, glutathione
reductase, and superoxide dismutase help trigger a typical ISR plant defense response
against pathogens [178].
Figure 4. Types of induced resistance in plants by

by bacterial
bacterial biostimulants.
biostimulants.
3.5.3.
3.5.1. Induced
SystemicSystemic
AcquiredTolerance
Resistance (IST)
(SAR)
Similar
Systemictoacquired
ISR against biotic (SAR)
resistance stresses,
is athe defense responses
mechanism of inducedinduced
defense bythatdifferent
confers
PGPR to withstand
long-lasting protection abiotic
againststresses
a broad generally
spectrum involve highly regulated
of microorganisms. It ismechanisms,
an induced
including the regulation
immune mechanism of phytohormones,
found in plants with aROS broadaccumulation,
spectrum that EPSis(exopolysaccharide)
not specific to the
initial infection
production, [154] and can beactivity,
ACC-deaminase systematically expressed
the secretion of in all organsmetabolites,
secondary [155]. SAR requires
VOCs,
the salicylic acid (SA) signaling that accumulates within the infected
antioxidant machinery, and the activation of defense-related genes that lead to induced plant tissues after
pathogentolerance
systemic attack, which(IST)stimulates
and has been immune
well responses
documented suchbyas[153].
pathogenesis-related
Such responses (PR) also
gene expression
involve a web of andhighly
antimicrobial substance
coordinated plantencoding
hormones [156].
suchTheasSA signal transduction
abscisic acid (ABA),
requires activation
gibberellins of PR (pathogenesis-related)
(GA), ethylene (ET), auxins (indolegenes, aceticofacid,
which the NPR1
IAA), regulatory
cytokinins (CK),
(activator)acid
jasmonic protein
(JA),issalicylic
an essential gene that
acid (SA), and operates within the
brassinosteroids terminal
(BRs). Theseofplant
the SAR signal
hormones
pathway [157].
habitually act as the key signaling molecules triggering intricate signaling cascades that
SAR is generally
subsequently lead toactivated by pathogens
the stimulation or chemical stimuli;
of physiological however, some PGPR
and morphological are
changes,
also known to trigger the SA (salicylic acid)-dependent pathway through
eventually leading to tolerance or resistance of abiotic stresses [179]. Several molecular the production
of SA at the root surface [158]. Treatment of tomato plants with Bacillus amyloliquefaciens
(strain MBI600), which is an active component of the fungicide Serifel® , was shown to
produce antiviral action against Potato virus Y (PVY) and tomato spotted wilt virus (TSWS)
in tomato plants through the SA-dependent signaling pathway [159]. In another example,
leaf infiltration with Bacillus cereus (AR156), a PGPR was reported to enhance disease
resistance against Pst (P. syringae pv. tomato) in Arabidopsis through the activation of
a SAR pathway [160]. However, the salicylic acid released by rhizobacteria does not
necessarily need to mediate the SAR mechanism, as SA produced by rhizobacteria may
require siderophores for its assimilation [161].
3.5.2. Induced Systemic Resistance (ISR)

Induced systemic resistance (ISR) emerged as an important mechanism by which
selected plant growth-promoting bacteria and fungi in the rhizosphere enhanced defense
against a broad range of pathogens and insect herbivores [162]. ISR induction requires
components of the jasmonic acid (JA) signaling pathway followed by the ethylene signal-
ing pathway [163]. For many biological control agents, ISR has been recognized as the
mechanism that at least partly explains disease suppression. It is of significant importance
from an agronomic perspective for its effectiveness against a wide range of microbial
pathogens, nematodes, and insects that damage crops [164,165]. It was reported that the
PGPR Bacillus amyloliquefaciens induces systemic resistance in bean plants against aphids
through the production of higher contents of jasmonic acid [166]. The attack of insect
herbivores on plant roots and leaves imposes different selection pressures on plants, which
in turn produces contrasting responses in terms of gene expression and the production of
secondary metabolites and wound hormones [167]. PGPR-triggered ISR does not involve
severe defense-related gene changes and assists the plant in the induction of resistance
against various pathogens by the production of several extracellular metabolites that act
as elicitors [153]. Several PGPR metabolites include N-Acyl homoserine lactones [168],
siderophores [169], VOCs [170], rhamnolipids [171], and cyclic lipopeptides [172]. How-
ever, most of these elicitors have been identified from strains of Bacillus and Pseudomonas
sp. and elicitors from many other species remain mostly undiscovered.
These elicitors require higher µM concentrations to activate the immune responses
compared to MAMPs, indicating that they may not be sensed through high-affinity recep-
tors [173]. Quorum-sensing molecules such as acyl homoserine lactones produced by PGPR
represent novel elicitors of biotic stress resistance in plants. In a recent study, a halotolerant
plant growth-promoting bacterium, Staphylococcus equorum EN21, triggered ISR against
Pseudomonas syringae (pv. Tomato) through quorum quenching of acyl homoserine in Ara-
bidopsis and tomato plants [174]. ISR activity of the elicitor oxo-C14-HSL was observed in
tomato and wheat against Phytophthora infestans and Puccinia graminis f., respectively [175].
In monocots (such as rice) cyclic lipopeptides released by Pseudomonas are crucial in elic-
iting the ISR. For example, cyclic lipopeptides such as lokisin, endolysin, and white line
inducing principle (WLIP) were described recently as successfully inducing resistance
against Magnaporthe oryzae [176] whereas orfamide (at 25 µM concentration) is known as
an elicitor of ISR against Cochliobolus miyabeanus [177]. Accumulation of ROS following
the inoculation of bacteria Gluconacetobacter diazotrophicus has also been observed at the
early stages of rice root colonization. This study indicates that bacterial ROS-scavenging
enzymes, glutathione reductase, and superoxide dismutase help trigger a typical ISR plant
defense response against pathogens [178].
3.5.3. Induced Systemic Tolerance (IST)

Similar to ISR against biotic stresses, the defense responses induced by different PGPR
to withstand abiotic stresses generally involve highly regulated mechanisms, including
the regulation of phytohormones, ROS accumulation, EPS (exopolysaccharide) production,
ACC-deaminase activity, the secretion of secondary metabolites, VOCs, antioxidant ma-
chinery, and the activation of defense-related genes that lead to induced systemic tolerance
(IST) and has been well documented by [153]. Such responses also involve a web of highly
coordinated plant hormones such as abscisic acid (ABA), gibberellins (GA), ethylene (ET),
auxins (indole acetic acid, IAA), cytokinins (CK), jasmonic acid (JA), salicylic acid (SA),
and brassinosteroids (BRs). These plant hormones habitually act as the key signaling
molecules triggering intricate signaling cascades that subsequently lead to the stimulation
of physiological and morphological changes, eventually leading to tolerance or resistance
of abiotic stresses [179]. Several molecular studies have described that PGPR induce stress
tolerance (biotic as well abiotic) through crosstalk between various phytohormones and
the proper signaling network [180].
Different mechanisms of IST by several elicitors stimulated by inoculation of PGPR
have been also demonstrated for the mitigation of abiotic stresses [92,93]. Under the condi-
tions of salt stress, the inoculation of tomato by PGPR Sphingobacterium BHU-AV3 showing
whole plant protection through IST was due to reduced ROS levels, increased antioxidant
enzyme activities, and the multiple-isoform expression of superoxide dismutase (SOD),
polyphenol oxidase (PPO), and peroxidase (POD) in the plant roots [181]. In wheat, IST
was elicited by a halotolerant Aeromonas sp. (strains SAL17 and SAL21) via the production
of many acyl homoserine lactones (AHLs) to mitigate salt stress [182]. During heavy
metal stress, Pseudomonas SFP1, which is a metal-tolerant species, produces IAA [183].
It also secretes many enzymes for degradation of the cell wall that include chitinases,
cellulose, protease, glucanase, lipopolypeptides, and HCN, which provide inhibition to
plant pathogenic fungi, bacteria, and viruses, and also restrain nematodes [184]. Different
PGPR treatments known to induce systemic tolerance in wheat against abiotic stresses
including salinity, drought, heat, and cold have been well studied.
4. Conclusions
Feeding the world’s rising population is one of the biggest challenges, especially when
the agriculture system is facing a multitude of complex problems arising from changing
environments due to global climate change. This global phenomenon triggers and worsens
already existing abiotic stresses due to the shifting of normal climatic patterns such as water
budgets, resulting in frequent droughts, floods, salinization, and temperature extremes.
These problems become factors for shifting patterns of weeds and phytopathogens and
reduce the beneficial microbial population associated with plants that affect plant health
while leaving plants susceptible to biotic stress. Furthermore, to guarantee and ensure a
sufficient yield and the biocontrol of pests, agriculture is increasingly relying on chemical
fertilizers and pesticides, which unfortunately have a very negative environmental effect.
Therefore, in recent years, to establish environmentally sustainable alternatives to such
agrochemicals, the use of PGPR plant biostimulants (PBs) has attracted worldwide interest.
The PB market is rising rapidly, with an expected exponential growth rate in the near future.
PGPR-based BPBs have shown effectiveness in nutrition use, mitigation of abiotic/biotic
stress, and/or crop quality characteristics when applied to agricultural and horticultural
crop plants (fruits, vegetables, ornamental plants, and medicinal plants). PGPR make
soil elements such as iron, phosphorus, potassium, and zinc more available to plants
through the phytohormone regulation, production, and release of siderophores, organic
acids, and enzymes.
Furthermore, PGPR fight various abiotic and biotic stresses through a multitude of
mechanisms or a combination of an array of mechanisms such as phytohormone regula-
tion, signaling pathways, gene regulation and expression, secondary metabolites, VOCs,
bioactive compound enhancement, ROS enzyme activities, etc. However, detailed work
also needs to be carried out for an additional explanation of mechanisms related to plant–
microbe interactions, their bilateral “molecular dialogue,” and the “omics” approaches,
particularly under the synergistic pressures of abiotic and biotic stress under field condi-
tions. Such cognizance will expound on the development of new biostimulant formulations
and their implementation as an innovative solution to the current food crisis.
Funding: The authors extend their appreciation to Universiti Teknologi Malaysia (UTM) for project
Nos. 526 QJ130000.3609.02M43 and QJ130000.3609.02M39, and All Cosmos Industries Sdn. Bhd.
through project No. R.J130000.7344.4B200.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: All the supporting data is available in the manuscript.
Acknowledgments: The authors extend their appreciation to Universiti Teknologi Malaysia (UTM),
Malaysia and All Cosmos Industries Sdn. Bhd. for providing support to this study.
Conflicts of Interest: The authors declare no conflict of interest.
References
1. Ebert, A.W.; Engels, J.M. Plant Biodiversity and Genetic Resources Matter! Plants 2020, 9, 1706. [CrossRef]
2. Shahzad, A.; Ullah, S.; Dar, A.A.; Sardar, M.F.; Mehmood, T.; Tufail, M.A.; Shakoor, A.; Haris, M. Nexus on climate change:
Agriculture and possible solution to cope future climate change stresses. Environ. Sci. Pollut. Res. 2021, 7, 1–22.
3. Sangiorgio, D.; Cellini, A.; Donati, I.; Pastore, C.; Onofrietti, C.; Spinelli, F. Facing climate change: Application of microbial
biostimulants to mitigate stress in horticultural crops. Agronomy 2020, 10, 794. [CrossRef]
4. Del Buono, D. Can biostimulants be used to mitigate the effect of anthropogenic climate change on agriculture? It is time to
respond. Sci. Total. Environ. 2020, 751, 141763. [CrossRef]
5. Raza, A.; Razzaq, A.; Mehmood, S.S.; Zou, X.; Zhang, X.; Lv, Y.; Xu, J. Impact of climate change on crops adaptation and strategies
to tackle its outcome: A review. Plants 2019, 8, 34. [CrossRef]
6. Malhi, G.S.; Kaur, M.; Kaushik, P. Impact of Climate Change on Agriculture and Its Mitigation Strategies: A Review. Sustainability
2021, 13, 1318. [CrossRef]
7. Mancosu, N.; Snyder, R.L.; Kyriakakis, G.; Spano, D. Water scarcity and future challenges for food production. Water 2015,
7, 975–992. [CrossRef]
8. Kałużewicz, A.; Bosiacki, M.; Spiżewski, T. Influence of biostimulants on the content of macro-and micronutrients in broccoli
plants exposed to drought stress. J. Elem. 2018, 23, 287–296.
9. Bulgari, R.; Franzoni, G.; Ferrante, A. Biostimulants application in horticultural crops under abiotic stress conditions. Agronomy
2019, 9, 306. [CrossRef]
10. Daneshmand, H.; Alaghmand, S.; Camporese, M.; Talei, A.; Yeh, P.J.F.; Daly, E. Long-term impacts of partial afforestation on
water and salt dynamics of an intermittent catchment under climate change. Water 2020, 12, 1067. [CrossRef]
11. Bulgari, R.; Cocetta, G.; Trivellini, A.; Vernieri, P.; Ferrante, A. Biostimulants and crop responses: A review. Biol. Agric. Hort. 2015,
31, 1–17. [CrossRef]
12. Colla, G.; Rouphael, Y. Biostimulants in horticulture. Sci. Hortic. 2015, 196, 1–2. [CrossRef]
13. Yakhin, O.I.; Lubyanov, A.A.; Yakhin, I.A.; Brown, P.H. Biostimulants in plant science: A global perspective. Front. Plant Sci. 2017,
7, 2049. [CrossRef] [PubMed]
14. Rouphael, Y.; Colla, G. Synergistic biostimulatory action: Designing the next generation of plant biostimulants for sustainable
agriculture. Front. Plant Sci. 2018, 9, 1655. [CrossRef]
15. Chiaiese, P.; Corrado, G.; Colla, G.; Kyriacou, M.C.; Rouphael, Y. Renewable sources of plant biostimulation: Microalgae as a
sustainable means to improve crop performance. Front. Plant Sci. 2018, 9, 1782. [CrossRef]
16. Rouphael, Y.; Colla, G. Toward sustainable agriculture through plant biostimulants: From experimental data to practical
applications. Agronomy 2020, 10, 1461. [CrossRef]
17. E.U. Regulation of the European Parliament and the Council Laying Down Rules on the Making Available on the Market of EU
Fertilising Products and Amending Regulations (EC) No 1069/2009 and (EC) No. 1107/2009 and Repealing Regulation (EC) No
2003/2003. 2019. Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=OJ:L:2019:170:TOC (accessed on 11
January 2021).
18. Szczałba, M.; Kopta, T.; Gastoł,
˛ M.; S˛ekara, A. Comprehensive insight into arbuscular mycorrhizal fu ngi, Trichoderma spp. and
plant multilevel interactions with emphasis on biostimulation of horticultural crops. J. Appl. Microbiol. 2019, 127, 630–647.
[CrossRef] [PubMed]
19. Wozniak, E.; Blaszczak, A.; Wiatrak, P.; Canady, M. Biostimulant Mode of Action: Impact of Biostimulant on Whole-Plant Level.
In The Chemical Biology of Plant Biostimulants; Geelan, D., Xu, L., Eds.; Wiley Online Library: Hoboken, NJ, USA, 2020; pp. 205–227.
20. Brown, P.; Saa, S. Biostimulants in agriculture. Front. Plant Sci. 2015, 6, 671. [CrossRef]
21. Ruzzi, M.; Aroca, R. Plant growth-promoting rhizobacteria act as biostimulants in horticulture. Sci. Hort. 2015, 196, 124–134.
[CrossRef]
22. Vandenkoornhuyse, P.; Quaiser, A.; Le Van Duhamel, M.; Dufresne, A. The importance of the microbiome of the plant holobiont.
New Phytol. 2015, 206, 1196–1206. [CrossRef] [PubMed]
23. Ratiu, I.A.; Al-Suod, H.; Ligor, M.; Monedeiro, F.; Buszewski, B. Effects of growth conditions and cultivability on the content of
cyclitols in Medicago sativa. Int. J. Environ. Sci. Technol. 2020, 18, 33–48. [CrossRef]
24. Du Jardin, P. Plant biostimulants: Definition, concept, main categories and regulation. Sci. Hort. 2015, 196, 3–14. [CrossRef]
25. Lugtenberg, B. Principles of Plant-Microbe Interactions: Microbes for Sustainable Agriculture; Lugtenberg, B., Ed.; Springer: Cham,
Switzerland, 2015; pp. 1–15.
26. Rouphael, Y.; Colla, G. Biostimulants in Agriculture. Front. Plant Sci. 2020, 11, 40. [CrossRef]
27. Dunhamtrimmer.com. 2018. Available online: http://dunhamtrimmer.com/products-services (accessed on 11 January 2021).
28. Woo, S.L.; Pepe, O. Microbial consortia: Promising probiotics as plant biostimulants for sustainable agriculture. Front. Plant Sci.
2018, 9, 1801. [CrossRef]
29. Le Mire, G.; Nguyen, M.; Fassotte, B.; du Jardin, P.; Verheggen, F.; Delaplace, P.; Jijakli, H. Implementing biostimulants and
biocontrol strategies in the agroecological management of cultivated ecosystems. Biotechnol. Agron. Société Environ. 2016, 20, 1–15.
30. Aamir, M.; Rai, K.K.; Zehra, A.; Dubey, M.K.; Kumar, S.; Shukla, V.; Upadhyay, R.S. Microbial bioformulation-based plant
biostimulants: A plausible approach toward next generation of sustainable agriculture. In Microbial Endophytes; Woodhead
Publishing: Cambridge, UK, 2020; pp. 195–225.
31. Mishra, J.; Arora, N.K. Bioformulations for plant growth promotion and combating phytopathogens: A sustainable approach. In
Bioformulations: For Sustainable Agriculture; Springer: New Delhi, India, 2016; pp. 3–33.
32. Dellagi, A.; Quillere, I.; Hirel, B. Beneficial soil-borne bacteria, and fungi: A promising way to improve plant nitrogen acquisition.
J. Exp. Bot. 2020, 7, 4469–4479. [CrossRef] [PubMed]
33. 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]
34. Souza, R.D.; Ambrosini, A.; Passaglia, L.M. Plant growth-promoting bacteria as inoculants in agricultural soils. Genet. Mol. Biol.
2015, 38, 401–419. [CrossRef]
35. Santoyo, G.; Moreno-Hagelsieb, G.; Del Carmen Orozco-Mosqueda, M.; Glick, B.R. Plant growth-promoting bacterial endophytes.
Microbiol. Res. 2016, 183, 92–99. [CrossRef] [PubMed]
36. Patel, P.R.; Shaikh, S.S.; Sayyed, R.Z. Dynamism of PGPR in bioremediation and plant growth promotion in heavy metal
contaminated soil. Indian J. Exp. Biol. 2016, 54, 286–290.
37. Woźniak, M.; Gałazka,
˛ A.; Tyśkiewicz, R.; Jaroszuk-Ściseł, J. Endophytic Bacteria Potentially Promote Plant Growth by Synthesiz-
ing Different Metabolites and their Phenotypic/Physiological Profiles in the Biolog GEN III MicroPlateTM Test. Int. J. Mol. Sci.
2019, 20, 5283. [CrossRef]
38. Kabiraj, A.; Majhi, K.; Halder, U.; Let, M.; Bandopadhyay, R. Role of Plant Growth-Promoting Rhizobacteria (PGPR) for crop
stress management. In Sustainable Agriculture in the Era of Climate Change; Springer: Cham, Switzerland, 2020; pp. 367–389.
39. Papik, J.; Folkmanova, M.; Polivkova, M.; Suman, J.; Uhlik, O. The invisible life inside plants: Deciphering the riddles of
endophytic bacterial diversity. Biotechnol. Adv. 2020, 44, 107614. [CrossRef]
40. Miliute, I.; Buzaite, O.; Baniulis, D.; Stanys, V. Bacterial endophytes in agricultural crops and their role in stress tolerance: A
review. Zemdirb. Agric. 2015, 102, 465–478. [CrossRef]
41. Wemheuer, F.; Kaiser, K.; Karlovsky, P.; Daniel, R.; Vidal, S.; Wemheuer, B. Bacterial endophyte communities of three agricultural
important grass species differ in their response towards management regimes. Sci. Rep. 2017, 7, 1–13.
42. Liu, H.; Carvalhais, L.C.; Crawford, M.; Singh, E.; Dennis, P.G.; Pieterse, C.M.; Schenk, P.M. Inner plant values: Diversity,
colonization, and benefits from endophytic bacteria. Front. Microbiol. 2017, 8, 2552. [CrossRef]
43. Pii, Y.; Penn, A.; Gattullo, C.E.; Allegretta, I.; Terzano, R.; Crecchio, C.; Mimmo, T.; Cesco, S. The interactions between plant,
microorganism, and soil affect Fe acquisition in cucumber plants. Center Soil Ecol. 2015, 87, 45–52.
44. Sayyed, R.Z.; Arora, N.K.; Reddy, M.S. Rhizobacteria in Abiotic Stress Management. In Plant Growth Promoting Rhizobacteria for
Sustainable Stress Management; Springer Nature: Singapore, 2019; Volume 1, pp. 1–362.
45. Nguyen, M.L.; Spaepen, S.; du Jardin, P.; Delaplace, P. Biostimulant effects of rhizobacteria on wheat growth and nutrient uptake
depend on nitrogen application and plant development. Arch Agron. Soil Sci. 2019, 65, 58–73. [CrossRef]
46. Vetrano, F.; Miceli, C.; Angileri, V.; Frangipane, B.; Moncada, A.; Miceli, A. Effect of Bacterial Inoculum and Fertigation
Management on Nursery and Field Production of Lettuce Plants. Agronomy 2020, 10, 1477. [CrossRef]
47. Pellegrini, M.; Spera, D.; Ercole, C.; del Gallo, M. Allium cepa L. seed inoculation with a consortium of plant growth-promoting
bacteria: Effects on plant growth and development and soil fertility status and microbial community. Proceedings 2020, 6, 20.
48. He, Y.; Pantigoso, H.A.; Wu, Z.; Vivanco, J.M. Co-inoculation of Bacillus sp. and Pseudomonas putida at different development
stages acts as a biostimulant to promote growth, yield, and nutrient uptake of tomato. J. Appl. Microbiol. 2019, 127, 196–207.
[CrossRef]
49. Chandrasekaran, M.; Chun, S.C.; Oh, J.W.; Paramasivan, M.; Saini, R.K.; Sahayarayan, J.J. Bacillus subtilis CBR05 for Tomato
(Solanum lycopersicum) Fruits in South Korea as a Novel Plant Probiotic Bacterium (PPB): Implications from Total Phenolics,
Flavonoids, and Carotenoids Content for Fruit Quality. Agronomy 2019, 9, 838. [CrossRef]
50. Islam, S.; Akanda, A.M.; Prova, A.; Islam, M.T.; Hossain, M.M. Isolation and identification of plant growth-promoting rhizobac-
teria from cucumber rhizosphere and their effect on plant growth promotion and disease suppression. Front. Microbiol. 2016,
6, 1360. [CrossRef]
51. Mangmang, J.S.; Deaker, R.; Rogers, G. Optimal plant growth-promoting concentration of Azospirillum brasilense inoculated to
cucumber, lettuce, and tomato seeds varies between bacterial strains. Isr. J. Plant Sci. 2015, 62, 145–152. [CrossRef]
52. Jha, Y.; Subramanian, R.B. PGPR regulate the caspase-like activity, programmed cell death, and antioxidant enzyme activity in
paddy under salinity. Physiol. Mol. Biol. Plants 2014, 20, 201–207. [CrossRef] [PubMed]
53. Fibach-Paldi, S.; Burdman, S.; Okon, Y. Key physiological properties contributing to rhizosphere adaptation and plant growth
promotion abilities of Azospirillum Brasilense. FEMS Microbiol. Lett. 2012, 326, 99–108. [CrossRef]
54. Fahad, S.; Hussain, S.; Matloob, A.; Khan, F.A.; Khaliq, A.; Saud, S.; Hassan, S.; Shan, D.; Khan, F.; Ullah, N.; et al. Phytohormones
and plant responses to salinity stress: A review. Plant Growth Reg. 2015, 75, 391–404. [CrossRef]
55. Spaepen, S.; Bossuyt, S.; Engelen, K.; Marchal, K.; Vanderleyden, J. Phenotypical and molecular responses of Arabidopsis thaliana
roots as a result of inoculation with the auxin-producing bacterium Azospirillum brasilense. New Phytol. 2014, 201, 850–861.
[CrossRef] [PubMed]
56. Llorente, B.E.; Alasia, M.A.; Larraburu, E.E. Biofertilization with Azospirillum brasilense improves in vitro culture of Handroanthus
ochraceus, a forestry, ornamental and medicinal plant. New Biotechnol. 2016, 33, 32–40. [CrossRef] [PubMed]
57. Faruque, O.M.; Miwa, H.; Yasuda, M.; Fujii, Y.; Kaneko, T.; Sato, S.; Okazaki, S. Identification of Bradyrhizobium elkanii genes
involved in incompatibility with soybean plants carrying the Rj4 allele. Appl. Environ. Microbiol. 2015, 81, 6710–6717. [CrossRef]
[PubMed]
58. Hernández-León, R.; Rojas-Solís, D.; Contreras-Pérez, M.; del Carmen Orozco-Mosqueda, M.; Macías-Rodríguez, L.I.; Reyes-de la
Cruz, H.; Valencia-Cantero, E.; Santoyo, G. Characterization of the antifungal and plant growth-promoting effects of diffusible
and volatile organic compounds produced by Pseudomonas fluorescens strains. Biol. Control 2015, 81, 83–92. [CrossRef]
59. Gupta, G.; Parihar, S.S.; Ahirwar, N.K.; Snehi, S.K.; Singh, V. Plant growth-promoting rhizobacteria (PGPR): Current and prospects
for the development of sustainable agriculture. J. Microbiol. Biochem. Technol. 2015, 7, 096–102.
60. Jha, C.K.; Saraf, M. Plant growth-promoting rhizobacteria (PGPR): A review. J. Agric. Res. Dev. 2015, 5, 108–119.
61. Heydarian, Z.; Yu, M.; Gruber, M.; Glick, B.R.; Zhou, R.; Hegedus, D.D. Inoculation of soil with plant growth-promoting bacteria
producing 1-aminocyclopropane-1-carboxylate deaminase or expression of the corresponding acdS gene in transgenic plants
increases salinity tolerance in Camelina sativa. Front. Microbiol. 2016, 7, 1966. [CrossRef] [PubMed]
62. Bucao, D.S.; Yapit, R.H.; Gabriel, M.L.S. Biochemical Characterization of Microbials and Their Effects on the Growth and Yield of
Multiplier Onion (Allium ascalonicum L.) in Northwestern Philippines. In Plant Growth Promoting Rhizobacteria (PGPR): Prospects
for Sustainable Agriculture; Springer: Singapore, 2019; pp. 75–91.
63. Kumar, R.; Saurabh, K.; Kumawat, N.; Sundaram, P.K.; Mishra, J.S.; Singh, D.K.; Hans, H.; Krishna, B.; Bhatt, B.P. Sustaining
productivity through integrated use of microbes in agriculture. In Role of Microbial Communities for Sustainability; Springer:
Singapore, 2021; pp. 109–145.
64. Singh, M.; Dotaniya, M.L.; Mishra, A.; Dotaniya, C.K.; Regar, K.L.; Lata, M. Role of biofertilizers in conservation agriculture. In
Conservation Agriculture; Bisht, J., Meena, V., Mishra, P., Pattanayak, A., Eds.; Springer: Singapore, 2016; pp. 113–134. [CrossRef]
65. Thilakarathna, M.S.; Raizada, M.N. A meta-analysis of the effectiveness of diverse rhizobia inoculants on soybean traits under
field conditions. Soil. Bioland. Biochem. 2017, 105, 177–196. [CrossRef]
66. Ramakrishna, W.; Yadav, R.; Li, K. Plant growth-promoting bacteria in agriculture: Two sides of a coin. Appl. Soil. Ecol. 2019,
138, 10–18. [CrossRef]
67. Bashan, Y.; de-Bashan, L.E. Inoculant preparation, and formulations for Azospirillum spp. In Handbook for Azospirillum; Springer:
Cham, Switzerland, 2015; pp. 469–485.
68. Beattie, G.A. Microbiomes: Curating communities from plants. Nature 2015, 528, 340–341. [CrossRef] [PubMed]
69. Gupta, M.; Kiran, S.; Gulati, A.; Singh, B.; Tewari, R. Isolation and identification of phosphate solubilizing bacteria able to enhance
the growth and aloin-A biosynthesis of Aloe barbadensis Miller. Microbiol. Res. 2012, 167, 358–363. [CrossRef]
70. Sharma, S.B.; Sayyed, R.Z.; Trivedi, M.H.; Gobi, T.A. Phosphate Solubilizing Microbes: Sustainable Approach for Managing Phosphorus
Deficiency in Agricultural Soils; Springer Plus: Berlin/Heidelberg, Germany, 2013; Volume 2, p. 587.
71. Basu, A.; Prasad, P.; Das, S.N.; Kalam, S.; Sayyed, R.Z.; Reddy, M.S.; El Enshasy, H. Plant Growth Promoting Rhizobacteria (PGPR)
as Green Bioinoculants: Recent Developments, Constraints, and Prospects. Sustainability 2021, 13, 1140. [CrossRef]
72. Suleman, M.; Yasmin, S.; Rasul, M.; Yahya, M.; Atta, B.M.; Mirza, M.S. Phosphate solubilizing bacteria with glucose dehydrogenase
gene for phosphorus uptake and beneficial effects on wheat. PLoS ONE 2018, 13, 0204408. [CrossRef]
73. Bechtaoui, N.; Raklami, A.; Benidire, L.; Tahiri, A.I.; Göttfert, M.; Oufdou, K. Effects of PGPR co-inoculation on growth,
phosphorus nutrition and phosphatase/phytase activities of faba bean under different phosphorus availability conditions. Pol. J.
Environ. Stud. 2020, 29, 1557–1565. [CrossRef]
74. Nath, D.; Maurya, B.R.; Meena, V.S. Documentation of five potassium-and phosphorus-solubilizing bacteria for their K and
P-solubilization ability from various minerals. Biocatal. Agric. Biotechnol. 2017, 10, 174–181. [CrossRef]
75. Meena, V.S.; Meena, S.K.; Verma, J.P.; Kumar, A.; Aeron, A.; Mishra, P.K.; Bisht, J.K.; Pattanayak, A.; Naveed, M.; Dotaniya, M.L.
Plant beneficial rhizospheric microorganism (PBRM) strategies to improve nutrients use efficiency: A review. Ecol. Eng. 2017,
107, 8–32. [CrossRef]
76. Sindhu, S.S.; Parmar, P.; Phour, M.; Sehrawat, A. Potassium-solubilizing microorganisms (KSMs) and its effect on plant growth
improvement. In Potassium Solubilizing Microorganisms for Sustainable Agriculture; Springer: Berlin/Heidelberg, Germany, 2016;
pp. 171–185.
77. Bahadur, I.; Maurya, B.R.; Meena, V.S.; Saha, M.; Kumar, A.; Aeron, A. Mineral release dynamics of tricalcium phosphate
and waste muscovite by mineral-solubilizing rhizobacteria isolated from Indo-Gangetic plain of India. Geomicrobiol. J. 2017,
34, 454–466. [CrossRef]
78. Liu, J.; Aronsson, H.; Ulen, B.; Bergström, L. Potential phosphorus leaching from sandy topsoils with different fertilizer histories
before and after application of pig slurry. Soil. Use Manag. 2012, 28, 457–467. [CrossRef]
79. Mehnaz, S. An overview of globally available bioformulations. In Bioformulations: Sustainable Agriculture; Arora, N.K., Mehnaz, S.,
Balestrini, R., Eds.; Springer: Singapore, 2016; pp. 267–281.
80. Wei, Y.; Zhao, Y.; Shi, M.; Cao, Z.; Lu, Q.; Yang, T.; Fan, Y.; Wei, Z. Effect of organic acids production and bacterial community
on the possible mechanism of phosphorus solubilization during composting with enriched phosphate-solubilizing bacteria
inoculation. Biores. Technol. 2018, 247, 190–199. [CrossRef] [PubMed]
81. Schultz, N.; Pereira, W.; de Albuquerque Silva, P.; Baldani, J.I.; Boddey, R.M.; Alves, B.J.R.; Urquiaga, S.; Reis, V.M. Yield of
sugarcane varieties and their sugar quality grown in different soil types and inoculated with a diazotrophic bacteria consortium.
Plant Prod. Sci. 2018, 20, 366–374. [CrossRef]
82. Shakeel, M.; Rais, A.; Hassan, M.N.; Hafeez, F.Y. Root associated Bacillus sp. improves growth, yield, and zinc translocation for
basmati rice (Oryza sativa) varieties. Front. Microbiol. 2015, 6, 1286. [CrossRef]
83. Bhupenchandra, I.; Devi, S.H.; Basumatary, A.; Dutta, S.; Singh, L.K.; Kalita, P.; Bora, S.S.; Devi, S.R.; Saikia, A.; Sharma, P.; et al.
Biostimulants: Potential and Prospects in Agriculture. Int. Res. J. Pure Appl. Chem. 2020, 21, 20–35. [CrossRef]
84. Colla, G.; Nardi, S.; Cardarelli, M.; Ertani, A.; Lucini, L.; Canaguier, R.; Rouphael, Y. Protein hydrolysates as biostimulants in
horticulture. Sci. Hort. 2015, 196, 28–38. [CrossRef]
85. Grzyb, Z.S.; Paszt, L.S.; Piotrowski, W.; Malusa, E. The influence of mycorrhizal fungi on the growth of apple and sour cherry
maidens fertilized with different bioproducts in the organic nursery. J. Life Sci. 2015, 9, 221–228.
86. Drobek, M.; Frac, ˛ M.; Cybulska, J. Plant biostimulants: The importance of the quality and yield of horticultural crops and the
improvement of plant tolerance to abiotic stress—A review. Agronomy 2019, 9, 335. [CrossRef]
87. Fiorentino, N.; Ventorino, V.; Woo, S.L.; Pepe, O.; De Rosa, A.; Gioia, L.; Romano, I.; Lombardi, N.; Napolitano, M.; Colla, G.;
et al. Trichoderma-based biostimulants modulate rhizosphere microbial populations and improve N uptake efficiency, yield, and
nutritional quality of leafy vegetables. Front. Plant Sci. 2018, 9, 743. [CrossRef] [PubMed]
88. Caradonia, F.; Ronga, D.; Flore, A.; Barbieri, R.; Moulin, L.; Terzi, V.; Francia, E. Biostimulants and cherry rootstock increased
tomato fruit yield and quality in sustainable farming systems. Ital. J. Agron. 2020, 15, 121–131. [CrossRef]
89. Turan, M.; Yildirim, E.; Kitir, N.; Unek, C.; Nikerel, E.; Ozdemir, B.S.; Güneş, A.; Mokhtari, N.E.P. Beneficial role of plant
growth-promoting bacteria in vegetable production under abiotic stress. In Microbial Strategies for Vegetable Production; Zaidi, A.,
Khan, M., Eds.; Springer: Cham, Switzerland, 2017; pp. 151–166. [CrossRef]
90. Ji, J.; Yuan, D.; Jin, C.; Wang, G.; Li, X.; Guan, C. Enhancement of growth and salt tolerance of rice seedlings (Oryza sativa L.)
by regulating ethylene production with a novel halotolerant PGPR strain Glutamicibacter sp. YD01 containing ACC deaminase
activity. Acta Physiol. Plant. 2020, 42, 1–17. [CrossRef]
91. Ilyas, N.; Mazhar, R.; Yasmin, H.; Khan, W.; Iqbal, S.; Enshasy, H.E.; Dailin, D.J. Rhizobacteria isolated from saline soil induce
systemic tolerance in wheat (Triticum aestivum L.) against salinity stress. Agronomy 2020, 10, 989. [CrossRef]
92. Filgueiras, L.; Silva, R.; Almeida, I.; Vidal, M.; Baldani, J.I.; Meneses, C.H.S.G. Gluconacetobacter diazotrophicus mitigates
drought stress in Oryza sativa L. Plant Soil. 2019, 451, 57–73. [CrossRef]
93. Silva, R.; Filgueiras, L.; Santos, B.; Coelho, M.; Silva, M.; Estrada-Bonilla, G.; Meneses, C. Gluconacetobacter diazotrophicus
changes the molecular mechanisms of root development in Oryza sativa L. growing under water stress. Int. J. Mol. Sci. 2020,
21, 333. [CrossRef]
94. Garcia, J.E.; Maroniche, G.; Creus, C.; Suarez-Rodriguez, R.; Ramirez-Trujillo, J.A.; Groppa, M.D. In vitro PGPR properties and
osmotic tolerance of different Azospirillum native strains and their effects on growth of maize under drought stress. Microbiol. Res.
2017, 202, 21–29. [CrossRef] [PubMed]
95. Moreno-Galván, A.; Romero-Perdomo, F.A.; Estrada-Bonilla, G.; Meneses, C.H.S.G.; Bonilla, R.R. Dry-caribbean Bacillus spp.
strains ameliorate drought stress in maize by a strain-specific antioxidant response modulation. Microorganisms 2020, 8, 823.
96. Fatima, T.; Arora, N.K. Pseudomonas entomophila PE3 and its exopolysaccharides as biostimulants for enhancing growth, yield,
and tolerance responses of sunflower under saline conditions. Microbiol. Res. 2021, 244, 126671. [CrossRef]
97. Tiryaki, D.; Aydın, İ.; Atıcı, Ö. Psychrotolerant bacteria isolated from the leaf apoplast of cold-adapted wild plants improve the
cold resistance of bean (Phaseolus vulgaris L.) under low temperature. Cryobiology 2019, 86, 111–119. [CrossRef]
98. Qin, Y.; Fu, Y.; Kang, W.; Li, H.; Gao, H.; Vitalievitch, K.S.; Liu, H. Isolation and identification of a cold-adapted bacterium and its
characterization for biocontrol and plant growth-promoting activity. Ecol. Eng. 2017, 105, 362–369. [CrossRef]
99. Zerrouk, I.Z.; Benchabane, M.; Khelifi, L.; Yokawa, K.; Ludwig-Muller, J.; Baluska, F. Pseudomonas strain isolated from date-palm
rhizospheres improves root growth and promotes root formation in maize exposed to salt and aluminum stress. J. Plant Physiol.
2016, 191, 111–119. [CrossRef] [PubMed]
100. Rizvi, A.; Khan, M.S. Heavy metal-induced oxidative damage and root morphology alterations of maize (Zea mays L.) plants and
stress mitigation by metal tolerant nitrogen-fixing Azotobacter chroococcum. Ecotoxicol. Environ. Saf. 2018, 157, 9–20. [CrossRef]
101. Ngumbi, E.; Kloepper, J. Bacterial-mediated drought tolerance: Current and future prospects. Appl. Soil Ecol. 2016, 10, 109–125.
[CrossRef]
102. Vurukonda, S.S.K.P.; Vardharajula, S.; Shrivastava, M.; Ali, S.Z. Enhancement of drought stress tolerance in crops by plant
growth-promoting rhizobacteria. Microbiol. Res. 2016, 184, 13–24. [CrossRef]
103. Jochum, M.D.; McWilliams, K.L.; Borrego, E.J.; Kolomiets, M.V.; Niu, G.; Pierson, E.A.; Jo, Y.K. Bioprospecting plant growth-
promoting rhizobacteria that mitigate drought stress in grasses. Front. Microbiol. 2019, 10, 2106. [CrossRef] [PubMed]
104. Khan, I.; Samrah, A.A.; Ikram, R.; Rizwan, M.; Akhtar, N.; Yasmin, H.; Sayyed, R.Z.; Ali, S.; Ilyas, N. 24-Epibrassinolide regulated
antioxidants and osmolyte defense and endogenous hormones in two wheat varieties under drought stress. Physiol. Plantarum.
2020, 1–11. [CrossRef]
105. Abbas, R.; Rasul, S.; Aslam, K.; Baber, M.; Shahid, M.; Mubeen, F.; Naqqash, T. Halotolerant PGPR: A hope for the cultivation of
saline soils. J. King Saud Univ. Sci. 2019, 31, 1195–1201. [CrossRef]
106. 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] [PubMed]
107. Wen, W.; Timmermans, J.; Chen, Q.; van Bodegom, P.M. A Review of Remote Sensing Challenges for Food Security with Respect
to Salinity and Drought Threats. Remote Sens. 2021, 13, 6. [CrossRef]
108. Fazeli-Nasab, B.; Sayyed, R.Z. Plant growth-promoting rhizobacteria and salinity stress: A journey into the soil. In Plant Growth
Promoting Rhizobacteria for Sustainable Stress Management; Springer: Singapore, 2019; pp. 21–34.
109. Pan, J.; Peng, F.; Xue, X.; You, Q.; Zhang, W.; Wang, T.; Huang, C. The growth promotion of two salt-tolerant plant groups with
PGPR inoculation: A meta-analysis. Sustainability. 2019, 11, 378. [CrossRef]
110. Malhotra, S.K. Horticultural crops and climate change—A review. Indian J. Agric. Sci. 2017, 87, 12–22.
111. Pereira, F. Rhizobacteria as Bioprotectants against stress conditions. In Plant Growth Promoting Rhizobacteria for Sustainable Stress
Management; Springer: Singapore, 2019; pp. 157–177.
112. Canarini, A.; Dijkstra, F.A. Dry-rewetting cycles regulate wheat carbon rhizodeposition, stabilization, and nitrogen cycling. Soil
Biol. Biochem. 2015, 81, 195–203. [CrossRef]
113. Singh, J.; Singh, P.; Ray, S.; Rajput, R.S.; Singh, H.B. Plant growth-promoting rhizobacteria: Benign and useful substitute for
mitigation of biotic and abiotic stresses. In Plant Growth Promoting Rhizobacteria for Sustainable Stress Management; Springer:
Singapore, 2019; pp. 81–101.
114. Huang, S.; Zuo, T.; Ni, W. Important roles of glycine betaine in stabilizing the structure and function of the photosystem II
complex under abiotic stresses. Planta 2020, 251, 1–14. [CrossRef] [PubMed]
115. 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, 1–16. [CrossRef]
[PubMed]
116. Kang, S.M.; Asaf, S.; Khan, A.L.; Khan, A.; Mun, B.G.; Khan, M.A.; Gul, H.; Lee, I.J. Complete genome sequence of Pseudomonas
psychrotolerans CS51, a plant growth-promoting bacterium, under heavy metal stress conditions. Microorganisms 2020, 8, 382.
[CrossRef]
117. Mishra, J.; Singh, R.; Arora, N.K. Alleviation of heavy metal stress in plants and remediation of soil by rhizosphere microorganisms.
Front. Microbiol. 2017, 8, 1706. [CrossRef]
118. Hassan, T.U.; Bano, A.; Naz, I. Alleviation of heavy metals toxicity by the application of plant growth-promoting rhizobacteria
and effects on wheat grown in saline-sodic field. Int. J. Phytoremed. 2017, 19, 522–529. [CrossRef] [PubMed]
119. Khanna, K.; Jamwal, V.L.; Gandhi, S.G.; Ohri, P.; Bhardwaj, R. Metal resistant PGPR lowered Cd uptake and expression of metal
transporter genes with improved growth and photosynthetic pigments in Lycopersicon esculentum under metal toxicity. Sci. Rep.
2019, 9, 1–14. [CrossRef]
120. Niu, D.D.; Zheng, Y.; Zheng, L.; Jiang, C.H.; Zhou, D.M.; Guo, J.H. Application of PSX biocontrol preparation confers root-knot
nematode management and increased fruit quality in tomato under field conditions. Biocont. Sci. Technol. 2016, 26, 174–180.
[CrossRef]
121. Munhoz, L.D.; Fonteque, J.P.; Santos, I.M.O.; Navarro, M.O.P.; Simionato, A.S.; Goya, E.T.; Rezende, M.I.; Balbi-Peña, M.L.;
de Oliveira, A.G.; Andrade, G. Control of bacterial stem rot on tomato by extracellular bioactive compounds produced by
Pseudomonas aeruginosa LV strain. Cogent Food Agric. 2017, 31, 1282592. [CrossRef]
122. Sorokan, A.; Benkovskaya, G.; Burkhanova, G.; Blagova, D.; Maksimov, I. Endophytic Strain Bacillus subtilis 26DCryChS
Producing Cry1Ia Toxin from Bacillus thuringiensis Promotes Multifaceted Potato Defense against Phytophthora infestans (Mont.)
de Bary and Pest Leptinotarsa decemlineata Say. Plants 2020, 9, 1115. [CrossRef]
123. Daranas, N.; Badosa, E.; Francés, J.; Montesinos, E.; Bonaterra, A. Enhancing water stress tolerance improves fitness in biological
control strains of Lactobacillus plantarum in-plant environments. PLoS ONE 2018, 13, 0190931. [CrossRef]
124. Meena, M.; Zehra, A. Tomato: A model plant to study plant-pathogen interactions. Food Sci. Nutr. Technol. 2019, 4, 000171.
125. Liu, K.; Garrett, C.; Fadamiro, H.; Kloepper, J.W. Induction of systemic resistance in Chinese cabbage against black rot by plant
growth-promoting rhizobacteria. Biol. Control. 2016, 99, 8–13. [CrossRef]
126. Zehra, A.; Meena, M.; Dubey, M.K.; Aamir, M.; Upadhyay, R.S. Synergistic effects of plant defense elicitors and Trichoderma
harzianum on enhanced induction of antioxidant defense system in tomato against Fusarium wilt disease. Bot. Stud. 2017, 58, 44.
[CrossRef] [PubMed]
127. Goutam, J.; Singh, R.; Vijayaraman, R.S.; Meena, M. Endophytic fungi: Carrier of potential antioxidants. In Fungi and Their Role in
Sustainable Development: Current Perspectives; Gehlot, P., Singh, J., Eds.; Springer: Singapore, 2018; pp. 539–551.
128. Dinesh, R.; Anandaraj, M.; Kumar, A.; Bini, Y.K.; Subila, K.P.; Aravind, R. Isolation, characterization, and evaluation of multi-trait
plant growth-promoting rhizobacteria for their growth-promoting and disease suppressing effects on ginger. Microbiol. Res. 2015,
173, 34–43. [CrossRef] [PubMed]
129. Sayyed, R.Z. Rhizobacteria in Biotic Stress Management. In Plant Growth Promoting Rhizobacteria for Sustainable Stress Management;
Springer Nature: Singapore, 2019; Volume 2, pp. 1–419.
130. Ulloa-Ogaz, A.L.; Muñoz-Castellanos, L.N.; Nevárez-Moorillón, G.V. Biocontrol of phytopathogens: Antibiotic production as a
mechanism of control. In The Battle Against Microbial Pathogens: Basic Science, Technological Advances, and Educational Programs;
Méndez-Vilas, A., Ed.; Formatex Research Center: Badajoz, Spain, 2015; pp. 305–309.
131. Fernando, W.; Nakkeeran, S.; Zhang, Y.; Savchuk, S. Biological control of Sclerotinia Sclerotiorum (lib.) de Bary by Pseudomonas and
Bacillus species on canola petals. Crop. Prot. 2018, 26, 100–107. [CrossRef]
132. Sharma, S.; Kumar, V.; Tripathi, R.B. Isolation of phosphate solubilizing microorganism (PSMs) from the soil. J. Microbiol. Bitechnol.
Res. 2017, 1, 90–95.
133. Ramadan, E.M.; AbdelHafez, A.A.; Hassan, E.A.; Saber, F.M. Plant growth-promoting rhizobacteria and their potential for
biocontrol of phytopathogens. Afr. J. Microbiol. Res. 2016, 10, 486–504.
134. Wang, X.; Mavrodi, D.V.; Ke, L.; Mavrodi, O.V.; Yang, M.; Thomashow, L.S.; Zhang, N.; Weller, D.M.; Zhang, J. Biocontrol and
plant growth-promoting activity of rhizobacteria from Chinese fields with contaminated soils. Microb. Biotechnol. 2015, 8, 404–418.
[CrossRef] [PubMed]
135. Raza, W.; Yousaf, S.; Rajer, F.U. Plant growth-promoting activity of volatile organic compounds produced by biocontrol strains.
Sci. Lett. 2016, 4, 40–43.
136. Kanchiswamy, C.N.; Malnoy, M.; Maffei, M.E. Chemical diversity of microbial volatiles and their potential for plant growth and
productivity. Front. Plant Sci. 2015, 6, 151. [CrossRef]
137. Sindhu, S.S.; Sharma, R. Amelioration of biotic stress by application of rhizobacteria for agriculture sustainability. In Plant Growth
Promoting Rhizobacteria for Sustainable Stress Management; Springer: Singapore, 2019; pp. 111–168.
138. Suryadi, Y.; Susilowati, D.N.; Fauziah, F. Management of plant diseases by PGPR-mediated induced resistance with special refer-
ence to tea and rice crops. In Plant Growth Promoting Rhizobacteria for Sustainable Stress Management; Springer: Berlin/Heidelberg,
Germany, 2019; pp. 65–110.
139. Kang, B.R.; Anderson, A.J.; Kim, Y.C. Hydrogen cyanide produced by Pseudomonas chlororaphis o6 exhibits nematicidal activity
against Meloidogyne Hapla. Plant Pathol. J. 2018, 34, 35–43. [CrossRef]
140. Santoro, M.V.; Bogino, P.C.; Nocelli, N.; Cappellari, L.R.; Giordano, W.F.; Banchio, E. Analysis of plant growth-promoting effects
of Fluorescent Pseudomonas strains isolated from Mentha piperita rhizosphere and effects of their volatile organic compounds on
essential oil composition. Front. Microbiol. 2016, 7, 1085. [CrossRef]
141. Liu, H.; Brettell, L.E. Plant defense by VOC-induced microbial priming. Trends Plant Sci. 2019, 24, 187–189. [CrossRef]
142. Goswami, D.; Thakker, J.N.; Dhandhukia, P.C. Portraying mechanics of plant growth-promoting rhizobacteria (PGPR): A review.
Cogent Food Agric. 2016, 2, 1–19. [CrossRef]
143. Rakshiya, Y.S.; Verma, M.K.; Sindhu, S.S. Efficacy of antagonistic soil bacteria in the management of subterranean termites
(Isoptera). Res. Environ. Life Sci. 2016, 9, 949–955.
144. Rooney, W.M.; Grinter, R.W.; Correia, A.; Parkhill, J.; Walker, D.C.; Milner, J.J. Engineering bacteriocin-mediated resistance against
the plant pathogen Pseudomonas syringae. Plant Biotechnol. J. 2020, 18, 1296–1306. [CrossRef]
145. Zimina, M.; Babich, O.; Prosekov, A.; Sukhikh, S.; Ivanova, S.; Shevchenko, M.; Noskova, S. Overview of global trends in
classification, methods of preparation and application of bacteriocins. Antibiotics 2020, 9, 553. [CrossRef] [PubMed]
146. Príncipe, A.; Fernandez, M.; Torasso, M.; Godino, A.; Fischer, S. Effectiveness of tailocins produced by prin in controlling the
bacterial-spot disease in tomatoes caused by Xanthomonas vesicatoria. Microbiol. Res. 2018, 213, 94–102. [CrossRef] [PubMed]
147. Rooney, W.M.; Chai, R.; Milner, J.J.; Walker, D. Bacteriocins targeting Gram-negative phytopathogenic bacteria: Plantibiotics of
the future. Front. Microbiol. 2020, 11, 2283. [CrossRef]
148. Riaz, U.; Murtaza, G.; Anum, W.; Samreen, T.; Sarfraz, M.; Nazir, M.Z. Plant Growth-Promoting Rhizobacteria (PGPR) as
biofertilizers and biopesticides. In Microbiota and Biofertilizers; Springer: Cham, Switzerland, 2021; pp. 181–196.
149. Reed, S.C.; Yang, X.; Thornton, P.E. Incorporating phosphorus cycling into global modeling efforts: A worthwhile, tractable
endeavor. New Phytol. 2015, 208, 324–329. [CrossRef]
150. Sayyed, R.Z.; Ilyas, N.; Tabassum, B.; Hashem, A.; Abd Allah, E.F.; Jadhav, H.P. Plausible role of plant growth-promoting
Rhizobacteria in future climatic scenario. In Enviromet Biotechnology: For Sustainable Future; Sobti, R., Arora, N., Kothari, R., Eds.;
Springer: Singapore, 2019; pp. 175–197.
151. Abdul Malik, N.A.; Kumar, I.S.; Nadarajah, K. Elicitor and receptor molecules: Orchestrators of plant defense and immunity. Int.
J. Mol. Sci. 2020, 21, 963. [CrossRef] [PubMed]
152. Maithani, D.; Singh, H.; Sharma, A. Stress alleviation in plants using SAR and ISR: Current views on stress signaling network. In
Microbes and Signaling Biomolecules Against Plant Stress; Springer: Singapore, 2021; pp. 7–36.
153. 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. [PubMed]
154. David, L.; Kang, J.; Dufresne, D.; Zhu, D.; Chen, S. Multi-Omics Revealed Molecular Mechanisms Underlying Guard Cell
Systemic Acquired Resistance. Int. J. Mol. Sci. 2021, 22, 191. [CrossRef] [PubMed]
155. Nishad, R.; Ahmed, T.; Rahman, V.J.; Kareem, A. Modulation of Plant Defense System in Response to Microbial Interactions.
156. Shaikh, S.S.; Sayyed, R.Z.; Reddy, M.S. Plant growth-promoting rhizobacteria: An eco-friendly approach for sustainable
agroecosystem. In Plant, Soil, and Microbes; Springer: Cham, Switzerland, 2016; pp. 181–201.
157. Backer, R.; Rokem, J.S.; Ilangumaran, G.; Lamont, J.; Praslickova, D.; Ricci, E.; Subramanian, S.; Smith, L.D. Plant growth-
promoting rhizobacteria: Context, mechanisms of action, and roadmap to the commercialization of biostimulants for sustainable
agriculture. Front. Plant Sci. 2018, 9, 1473. [CrossRef]
158. Choudhary, D.K.; Prakash, A.; Johri, B.N. Induced systemic resistance (ISR) in plants: Mechanism of action. Ind. J. Microbiol. 2007,
47, 289–297. [CrossRef]
159. Beris, D.; Theologidis, I.; Skandalis, N.; Vassilakos, N. Bacillus amyloliquefaciens strain MBI600 induces salicylic acid-dependent
resistance in tomato plants against Tomato spotted wilt virus and Potato virus Y. Sci. Rep. 2018, 8, 1–11. [CrossRef] [PubMed]
160. Niu, D.; Wang, X.; Wang, Y.; Song, X.; Wang, J.; Guo, J.; Zhao, H. Bacillus cereus AR156 activates PAMP-triggered immunity
and induces a systemic acquired resistance through a NPR1-and SA-dependent signaling pathway. Biochem. Biophys. Res. 2016,
469, 120–125. [CrossRef] [PubMed]
161. Bukhat, S.; Imran, A.; Javaid, S.; Shahid, M.; Majeed, A.; Naqqash, T. Communication of plants with microbial world: Exploring
the regulatory networks for PGPR mediated defense signaling. Microb. Res. 2020, 23, 126486. [CrossRef] [PubMed]
162. Zebelo, S.; Song, Y.; Kloepper, J.W.; Fadamiro, H. Rhizobacteria activates (+)-δ-cadinene synthase genes and induces systemic
resistance in cotton against beet armyworm (Spodoptera exigua). Plant Cell Environ. 2016, 39, 935–943. [CrossRef]
163. Khoshru, B.; Mitra, D.; Khoshmanzar, E.; Myo, E.M.; Uniyal, N.; Mahakur, B.; Mohapatra, P.K.D.; 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]
164. Rashid, M.H.O.; Chung, Y.R. Induction of systemic resistance against insect herbivores in plants by beneficial soil microbes. Front.
Plant Sci. 2017, 8, 1816. [CrossRef]
165. Mhatre, P.H.; Karthik, C.; Kadirvelu, K.; Divya, K.L.; Venkatasalam, E.P.; Srinivasan, S.; Ramkumar, G.; Saranya, C.; Shanmu-
ganathan, R. Plant growth-promoting rhizobacteria (PGPR): A potential alternative tool for nematodes bio-control. Biocatal. Agric.
Biotechnol. 2018, 17, 119–128. [CrossRef]
166. Serteyn, L.; Quaghebeur, C.; Ongena, M.; Cabrera, N.; Barrera, A.; Molina-Montenegro, A.M.; Francis, F.; Ramírez, C.C. Induced
Systemic Resistance by a Plant Growth-Promoting Rhizobacterium Impacts Development and Feeding Behavior of Aphids.
Insects 2020, 11, 234. [CrossRef] [PubMed]
167. Johnson, S.N.; Erb, M.; Hartley, S.E. Roots under attack: Contrasting plant responses to below- and aboveground insect herbivory.
New Phytologist. 2016, 210, 413–418. [CrossRef] [PubMed]
168. Schikora, A.; Schenk, S.T.; Hartmann, A. Beneficial effects of bacteria plant communication based on quorum sensing molecules
of the N-acyl homoserine lactone group. Plant Mol. Biol. 2016, 90, 605–612. [CrossRef] [PubMed]
169. Kramer, J.; Özkaya, Ö.; Kümmerli, R. Bacterial siderophores in community and host interactions. Nat. Rev. Microbiol. 2020,
18, 152–163. [CrossRef]
170. Kang, S.M.; Shahzad, R.; Bilal, S.; Khan, A.L.; Park, Y.G.; Lee, K.E.; Asaf, S.; Khan, M.A.; Lee, I.-J. Indole-3-acetic-acid and ACC
deaminase producing Leclercia adecarboxylata MO1 improves Solanum lycopersicum L. growth and salinity stress tolerance by
endogenous secondary metabolites regulation. BMC Microbiol. 2019, 19, 80. [CrossRef] [PubMed]
171. Monnier, N.; Furlan, A.; Botcazon, C.; Dahi, A.; Mongelard, G.; Cordelier, S. Rhamnolipids from Pseudomonas aeruginosa are
elicitors triggering Brassica napus protection against Botrytis cinerea without physiological disorders. Front. Plant Sci. 2018,
9, 1170. [CrossRef]
172. Mejri, S.; Siah, A.; Coutte, F.; Magnin-Robert, M.; Randoux, B.; Tisserant, B.; Krier, F.; Jacques, P.; Reignault, P.; Halama, P.
Biocontrol of the wheat pathogen Zymoseptoria tritici using cyclic lipopeptides from Bacillus subtilis. Environ. Sci. Pollut. Res.
2018, 25, 29822–29833. [CrossRef] [PubMed]
173. Pršić, J.; Ongena, M. Elicitors of plant immunity triggered by beneficial bacteria. Front. Plant. Sci. 2020, 11, 1675. [CrossRef]
[PubMed]
174. Vega, C.; Rodríguez, M.; Llamas, I.; Béjar, V.; Sampedro, I. Silencing of Phytopathogen Communication by the Halotolerant PGPR
Staphylococcus Equorum Strain EN21. Microorganisms 2020, 8, 42. [CrossRef]
175. Hernández-Reyes, C.; Schenk, S.T.; Neumann, C.; Kogel, K.H.; Schikora, A. N-acyl-homoserine lactones-producing bacteria
protect plants against plant and human pathogens. Microb. Biotechnol. 2014, 7, 580–588. [CrossRef] [PubMed]
176. Omoboye, O.O.; Oni, F.E.; Batool, H.; Yimer, H.Z.; De Mot, R.; Höfte, M. Pseudomonas cyclic lipopeptides suppress the rice blast
fungus Magnaporthe oryzae by induced resistance and direct antagonism. Front. Plant Sci. 2019, 10, 901. [CrossRef]
177. Ma, Z.; Ongena, M.; Höfte, M. The cyclic lipopeptide orfamide induces systemic resistance in rice to Cochliobolus miyabeanus but
not to Magnaporthe oryzae. Plant Cell Rep. 2017, 36, 1731–1746. [CrossRef] [PubMed]
178. Alquéres, S.; Meneses, C.; Rouws, L.; Rothballer, M.; Baldani, I.; Schmid, M.; Hartmann, A. The bacterial superoxide dismutase
and glutathione reductase are crucial for endophytic colonization of rice roots by Gluconacetobacter diazotrophicus PAL5. Mol. Plant
Microbe Interact. 2013, 26, 937–945. [CrossRef] [PubMed]
179. Nephali, L.; Piater, L.A.; Dubery, I.A.; Patterson, V.; Huyser, J.; Burgess, K.; Tugizimana, F. Biostimulants for plant growth and
mitigation of abiotic stresses: A metabolomics perspective. Metabolites 2020, 10, 505. [CrossRef]
180. Khan, N.; Bano, A.; Ali, S.; Babar, M.A. Crosstalk amongst phytohormones from plant and PGPR under biotic and abiotic stresses.
Plant Growth Regul. 2020, 90, 189–203. [CrossRef]
181. Vaishnav, A.; Singh, J.; Singh, P.; Rajput, R.S.; Singh, H.B.; Sarma, B.K. Sphingo bacterium sp. BHU-AV3 Induces Salt Tolerance in
tomato by enhancing antioxidant activities and energy metabolism. Front. Microbiol. 2020, 11, 443. [CrossRef] [PubMed]
182. Nawaz, M.S.; Arshad, A.; Rajput, L.; Fatima, K.; Ullah, S.; Ahmad, M.; Imran, A. Growth-Stimulatory Effect of Quorum Sensing
Signal Molecule N-Acyl-Homoserine Lactone-Producing Multi-Trait Aeromonas spp. on Wheat Genotypes Under Salt Stress.
183. Saif, S.; Khan, M.S. Assessment of toxic impact of metals on proline, antioxidant enzymes, and biological characteristics of
Pseudomonas aeruginosa inoculated Cicer arietinum grown in chromium and nickel-stressed sandy clay loam soils. Environ.
Monit. Assess. 2018, 190, 1–18. [CrossRef] [PubMed]
184. Abd El-Daim, I.A.; Bejai, S.; Meijer, J. Bacillus velezensis 5113 Induced Metabolic and Molecular Reprogramming during Abiotic
Stress Tolerance in Wheat. Sci. Rep. 2019, 9, 16282. [CrossRef]

Review

Uploaded by

Copyright:

Available Formats

Review

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Review

Uploaded by

Copyright:

Available Formats

sustainability

1 Department of Environmental Science, University of Kashmir, Hazratbal,

Sustainability 2021, 13, 2856. https://doi.org/10.3390/su13052856 https://www.mdpi.com/journal/sustainability

Sustainability 2021, 13, 2856 3 of 24

Bacterial plant biostimulants (BPBs) comprise a major category of plant

Table 1. Examples of commercial PGPR-based plant biostimulants [29–31].

3. Bacterial Plant Biostimulants, Beneficial Effects, and Mode of Action

Figure 2. Mode ofFigure

3.1. Plant Growth Promotion and Nutrient Acquisition

PGPR Biostimulant Crop Beneficial Effects Mode of Action References

3.1.1. Phytohormone Stimulation

fertilizers [63]. Biological nitrogen fixation (BNF) is accomplished by free-living microor-

3.2. Quality Improvement of Crop and Yield by Bacterial Plant Biostimulants

3.3. Abiotic Stress Tolerance Induced by Bacterial Plant Biostimulants

Sustainability 2021, 13, 2856 10 of 24

Figure 3. Illustration of abiotic stress tolerance induced by bacterial plant biostimulants.

Table 3. Influence of PGPR biostimulants on abiotic stress

PGPR Biostimulants CropCrop

3.3.1. Drought Stress

3.3.2. Salinity Stress

3.3.3. Heat Stress

3.3.4. Cold Stress

3.3.5. Heavy Metal Stress

3.4. Disease Suppression/Defense against Plant Pathogens through Antagonism

PGPR Biostimulants Crop Biotic Stress Mode of Action References

3.4.2. VOC Antagonism

3.4.3. Lysis by Extracellular Enzymes

3.5. Induction of Systemic Resistance (ISR)

Figure 4. Types of induced resistance in plants by

3.5.2. Induced Systemic Resistance (ISR)

3.5.3. Induced Systemic Tolerance (IST)

You might also like