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Plant Growth-Promoting Rhizobacteria: Diversity and Applications
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Chapter 6
Plant Growth-Promoting Rhizobacteria:
Diversity and Applications
Maya Verma, Jitendra Mishra, and Naveen Kumar Arora
Contents
Introduction 130
PGPR Diversity 131
Roles of PGPR in Rhizosphere 134
Growth-Enhancing Activities 134
Nutrient Uptake 135
Phytohormone Production 138
Production of Volatile Organic Compounds (VOCs) 139
Biocontrol Activities 140
Competition 140
Production of Metabolites 141
Induced Systemic Resistance (ISR) and Systemic Acquired Resistance (SAR) 142
Abiotic Stress Management 143
Soil Renovation 144
Diverse Applications of PGPR 146
Biofertilizers 146
Biopesticides 148
Future Roles of PGPR 150
Conclusion 151
References 152
Abstract The rhizosphere is the region around plant roots where maximum micro-
bial activities occur. In the rhizosphere both beneficial and harmful activities of
microorganisms affect plant growth and development. The mutualistic rhizospheric
bacteria which improve the plant growth and health are known as plant growth-
promoting rhizobacteria (PGPR). They are of much importance due to their ability
to help the plant in diverse manners. PGPR such as Pseudomonas, Bacillus,
Azospirillum, Azotobacter, Arthrobacter, Achromobacter, Micrococcus,
Enterobacter, Rhizobium, Agrobacterium, Pantoea, and Serratia are now very well
known. Application of PGPR as bioinoculants/bioformulations is found to be very
M. Verma · J. Mishra · N. K. Arora (*)

Department of Environmental Microbiology, School for Environmental Sciences, Babasaheb
Bhimrao Ambedkar University, Lucknow, Uttar Pradesh, India
e-mail: nkarora_net@rediffmail.com
© Springer Nature Singapore Pte Ltd. 2019 129

R. C. Sobti et al. (eds.), Environmental Biotechnology: For Sustainable Future,
https://doi.org/10.1007/978-981-10-7284-0_6
130 M. Verma et al.
effective in enhancing crop productivity in a sustainable way. The use of PGPR in

agriculture is also ecologically important as the synthetic chemicals used in agricul-
ture are a severe threat to agroecosystems.
Keywords Rhizosphere · PGPR · Bioinoculants · Agriculture · Agroecosystem
Introduction
In soil, there is a region around plant’s root known as rhizosphere (Hiltner 1904).
Rhizosphere has diverse number of microorganisms which are 10–100 times higher
in comparison with bulk soil (Weller and Thomashow 1994). These rhizospheric
microbes have been found to have beneficial, harmful, or neutral impact on plant’s
health (Whipps 2001; Bais et al. 2006). However PGPR, which show beneficial
effect on their host plant, are of prime importance. The term PGPR was coined by
Kloepper and Schroth (1978). Among all the rhizospheric bacteria, about 2–5% are
considered as PGPR (Antoun and Kloepper 2001). PGPR have three main features:
(i) root colonization ability, (ii) high survivability and multiplicity in root surround-
ings helping in plant growth promotion, and (iii) inhibition of phytopathogens
(Lugtenberg et al. 2001; Gamalero et al. 2004). Currently diverse types of bacterial
genera are considered as PGPR (Lucy et al. 2004; Adesemoye et al. 2008; Saharan
and Nehra 2011; Tailor and Joshi 2014). On the basis of their relationship with the
plants, PGPR have been divided into two major groups: symbiotic and free-living
(Khan 2005; Hayat et al. 2010). Pseudomonas and Bacillus are widely reported as
free-living whereas rhizobia as symbiotic plant growth promoters (Podile and
Kishore 2006).
As the PGPR live in close association with plant roots, they also improve soil
quality (Haghighi et al. 2011). Plant growth stimulation by PGPR involves multiple
mechanisms (Martinez-Viveros et al. 2010). However, few activities are very com-
mon among certain bacteria, and others might be species specific (Schwachtje et al.
2012). PGPR play fundamental roles in physiology and development of plants by
influencing various activities (Arora et al. 2013; Arora 2015; Kundan et al. 2015;
Gouda et al. 2018). They directly enhance plant growth by the process of nitrogen
fixation (Islam et al. 2013), phytohormone production (auxins, cytokinins, gibberel-
lins, ethylene, abscisic acid) (Glick et al. 1995; Vacheron et al. 2013; Maheshwari
et al. 2015), mineral (phosphorus, iron, zinc, potassium, and sulfur) solubilization
(Rodríguez et al. 2006; Delvasto et al. 2009), and siderophore, enzyme, and organic
acid production (Sayyed et al. 2005; Ahemad and Kibret 2014). Indirect growth
promotion is mainly due to their biocontrol activities attributed to antibiotic produc-
tion, iron chelation, cyanide production, induced resistance, synthesis of extracel-
lular enzymes, and competition for niches within the rhizosphere (Beneduzi et al.
2012; Ramadan et al. 2016). In addition to these activities, PGPR also have a role in
the management of abiotic stress conditions such as nutrient deficiency, salinity,
drought, floods, and extreme temperatures (Da Mota et al. 2008; Arzanesh et al.
2011; Arora et al. 2012; Asari 2015; Tewari and Arora 2016) and removal of various
6 Plant Growth-Promoting Rhizobacteria: Diversity and Applications 131
pollutants (heavy metals, organic pollutants) by the process of phyto- and rhizore-
mediation (Wani et al. 2007; Ma et al. 2011; Kong and Glick 2017; Mishra et al.
2017a). PGPR thus can be used in the enhancement of crop productivity in stressed
soils as well as for the bioremediation of such habitats.
Application of PGPR on different crops has shown a notable success. These
crops include cereals (Lucas et al. 2009; Qaisrani et al. 2014; Majeed et al. 2015;
Karnwal 2017), oil crops (Shahid et al. 2012; Tewari and Arora 2014; Sharifi 2017),
pulses (Khare and Arora 2010; Pérez-Montaño et al. 2013; Kumari et al. 2018), and
vegetables (Loganathan et al. 2014; Moustaine et al. 2017). Studies indicate that
PGPR increase seed germination, seedling vigor, seed emergence, root and shoot
growth, total biomass of the plants, seed weight, flowering, and yields (Van Loon
et al. 1998; Spaepen et al. 2009; Ahmad et al. 2013; Korir et al. 2017).
Plant productivity is governed by various climatic conditions and increases
under suitable conditions, but unfortunately various types of negative changes are
occurring in global climate due to anthropogenic activities. Various adverse effects
are generated due to climate change which cause degenerative impacts on global
vegetation including crop productivity. Climate change is also a threat causing
reduction in soil microbial diversity (Bradford et al. 2008; Ladau et al. 2017). Due
to climate change, various abiotic stresses have developed which reduce the crop
production. PGPR can work as suitable agents to combat the impact of abiotic
stresses caused by climate changes. Hence, PGPR inoculation is emerging as a very
effective method for enhancing crop production not only for our current food
requirements but for future needs as well. In this review we have discussed about
the diversity of rhizospheric bacteria and the plant growth-promoting (PGP) mecha-
nisms along with their important roles in agriculture. Some future potential uses of
PGPR in enhancing crop productivity and combating global warming are also
projected.
PGPR Diversity
The rhizospheric region of plants harbors diverse types of PGPR. Different plants
can have specific dominant PGPR genera and species. Root microbiome of plants
depends on various environmental (biotic and abiotic) factors such as root type,
plant species, plant age, soil type (Campbell 1985), and type of plant species (geno-
types) (Lareen et al. 2016). Exudates secreted by plant roots are the most important
factors responsible for high microbial diversity in rhizospheric region. On the basis
of their functions and taxonomical status, PGPR have been categorized in many
groups. According to Tilak et al. (2005), PGPR strains widely belong to five main
taxa: Actinobacteria, Bacteroidetes, Cyanobacteria, Firmicutes, and Proteobacteria.
It is reported that most commonly studied PGPR of these taxa are Azospirillum,
Azotobacter, Bacillus, Enterobacter, Gluconacetobacter, Paenibacillus,
Pseudomonas, Rhizobium, and Serratia (Bhattacharyya and Jha 2012; Arora 2015).
According to Gray and Smith (2005), PGPR are divided into four categories based
132 M. Verma et al.
on their association level with plant root: (i) those living in the root vicinity, (ii) liv-
ing on the root surface (rhizoplane-colonizing bacteria), (iii) residing in root tissue
(spaces between cortical cells), and (iv) living inside cells of specialized root struc-
tures or nodules. Broadly on the basis of these associations, PGPR can be separated
into two major groups: (i) extracellular (ePGPR) or rhizospheric and (ii) intracel-
lular or endophytic (iPGPR) (Vessey 2003; Gray and Smith 2005; Martinez-Viveros
et al. 2010; Santoyo et al. 2016).
ePGPR cause enhancement in plant growth by various mechanisms and are
known as efficient producers of various secondary metabolites which work as potent
PGP agents (Gray and Smith 2005). These free-living rhizobacteria, e.g.,
Achromobacter, Acetobacter, Alcaligenes, Arthrobacter, Azospirillum, Azotobacter,
Azomonas, Bacillus, Beijerinckia, Clostridium, Corynebacterium, Derxia,
Enterobacter, Herbaspirillum, Klebsiella, Pseudomonas, Rhodospirillum,
Rhodopseudomonas, Serratia, and Xanthobacter, have great agricultural impor-
tance (Prithiviraj et al. 2003; Bhattacharyya and Jha 2012).
Among all ePGPR, Bacillus and Pseudomonas are more abundant because of
their outstanding root-colonizing and PGP abilities (Sivasakthi et al. 2014). Bacillus
is known as very versatile and an important PGPR having many physiological char-
acters to survive in extreme environmental conditions (Shafi et al. 2017). Their abil-
ity to form endospore, multilayered cell wall, stress resistance, and secretion of
diverse secondary metabolites (peptide antibiotics, peptide signal molecules, extra-
cellular enzymes) are of importance (Gutiérrez-Mañero et al. 2001; Kumar et al.
2011). Many members of Bacillus and Bacillus-derived genera (BBDG) of phylum
Firmicutes are associated with different plants and show various PGP attributes
(Yadav et al. 2017). Among all the reported bacilli, Bacillus and Paenibacillus are
highly explored members of the PGPR group (Choudhary and Johri 2008) followed
by Alicyclobacillus, Aneurinibacillus, Virgibacillus, Solibacillus, and Gracilibacillus
isolated from different crop plants (Yadav et al. 2016). Pseudomonas is also ubiqui-
tous in soil and rhizosphere and one of the dominant PGPR genus with diverse traits
(Sivasakthi et al. 2014). Fluorescent pseudomonads are considered as most effective
and metabolically and physiologically diverse group of bacteria showing fast growth
rate with simple and diverse nutrients (Lugtenberg and Dekkers 1999; Lata et al.
2002). Fluorescent pseudomonads are known as efficient biocontrol agents because
of their ability to produce various types of metabolites against phytopathogens
(Khare and Arora 2011; Mishra et al. 2012; Tewari and Arora 2014; Mishra and
Arora 2018). The most studied members of this group are P. fluorescens, P. putida,
P. aeruginosa, P. chlororaphis, P. aureofaciens, and P. syringe (Tewari and Arora
2016; Dorjey et al. 2017).
Actinomycetes are also known as potential group of PGPRs and mainly reported
as biocontrol agents against diverse phytopathogens (Merzaeva and Shirokikh 2006;
Franco-Correa et al. 2010). Actinobacteria are well known for their ability to pro-
duce secondary metabolites and plant growth regulators (Sathya et al. 2017).
Besides biocontrol Actinobacteria are also able to mobilize minerals and metals in
various crops (He et al. 2010; Sathya et al. 2016). Streptomyces, Actinomadura,
Microbispora, Micromonospora, Nocardia, Nonomuraea, Mycobacterium, Frankia,
Actinoplanes, Saccharopolyspora, and Verrucosispora are common genera of

actinomycetes reported in soil and rhizosphere (Vijayabharathi et al. 2016). Some
Actinobacteria such as Arthrobacter, Agromyces, Corynebacterium, Mycobacterium,
Micromonospora, Propionibacteria, and Streptomyces are also reported as nitrogen-
fixing endophytes (Sellstedt and Richau 2013). Some other important ePGPR are
from among Cyanobacteria, Proteobacteria, and Firmicutes which include
Anabaena, Nostoc, Azotobacter, Azospirillum, Beijerinckia, and Clostridium
(Steenhoudt and Vanderleyden 2000; Duc et al. 2009). These are mainly free-living
nitrogen fixers present in soil (Zhan and Sun 2012).
iPGPR exist inside plant cells, in specialized nodular structures. Rhizobia and
Frankia are known as the most explored members of this group (Figueiredo et al.
2011; Gopalakrishnan et al. 2015). These two groups of bacteria can symbiotically
fix atmospheric nitrogen with higher plants and are widely studied as symbiotic
plant growth promoters (Ahemad and Kibret 2014). Rhizobia are a very broad
group of phenotypically heterogeneous Gram-negative, aerobic, non-sporulating,
rod-shaped bacteria (Tak et al. 2017; Rao et al. 2018). Rhizobia show various PGP
activities, but biological nitrogen fixation (BNF) is most important (Dardanelli et al.
2010; Arora et al. 2017). Rhizobia are known as legume symbionts with 238 species
and 18 genera, belonging to 3 different classes: α- proteobacteria (Rhizobium,
Mesorhizobium, Bradyrhizobium, Azorhizobium, Ensifer (formerly Sinorhizobium),
Methylobacterium, Devosia, Microvirga, Ochrobactrum, Phyllobacterium, Shinella,
Allorhizobium, Pararhizobium, Aminobacter, Blastobacter, Photorhizobium), ß-
proteobacteria (Burkholderia and Cupriavidus (formerly Ralstonia)), and
ϒ-proteobacteria (Pseudomonas) (Berrada and Fikri-Benbrahim 2014; Shamseldin
et al. 2017). Frankia forms root nodules in 200 species of non-leguminous woody
plants (24 genera of angiosperms in 8 different families) (Welsh et al. 2009; Franche
et al. 2011). Nitrogen-fixing cyanobacteria such as Nostoc, Anabaena, Calothrix,
Aulosira, Tolypothrix, Fischerella, and Chlorogloeopsis also have the ability to col-
onize different tissues of plants including Bryophyta, Pteridophyta, gymnosperms,
and angiosperms (Bergman et al. 2007; Santi et al. 2013; Mus et al. 2016).
Besides these, some rhizobacteria live inside plant roots with more intimacy and
are categorized as root endophytes (Schulz and Boyle 2006). Endophytic bacteria
are an important group of PGPR and now considered as more effective in compari-
son with rhizospheric bacteria (Coutinho et al. 2015; Asaf et al. 2017). Endophytes
belong to various bacterial phyla (Acidobacteria, Actinobacteria, Ascomycota,
Bacteroidetes, Basidiomycota, Deinococcus-Thermus, and Firmicutes) (Suman
et al. 2016). Dominant bacterial genera which are endophytes are Achromobacter,
Bacillus, Burkholderia, Enterobacter, Herbaspirillum, Micrococcus,
Microbacterium, Pantoea, Pseudomonas, and Streptomyces (Ryan et al. 2008;
Verma et al. 2013; Suman et al. 2016). Some researchers also consider rhizobia as
endophytes. Diversity of various PGP bacterial endophytes are explored and applied
for higher crop production (Rosenblueth and Martínez-Romero 2006; Liu et al.
2017).
134 M. Verma et al.
Roles of PGPR in Rhizosphere
PGPR perform various beneficial activities to promote plant growth and health
(Fig. 6.1). These mechanisms can be divided into four major activities: (i) growth-
enhancing activities, (ii) biocontrol activities, (iii) management of abiotic stresses,
and (iv) soil renovations by rhizoremediation (García-Fraile et al. 2015).
Growth-Enhancing Activities
PGPR enhance the plant growth by several mechanisms, and these work as direct
benefits to the plant (Table 6.1) (Bhattacharyya and Jha 2012; Arora 2015).
Fig. 6.1 Plant growth

promoting activities of
PGPR
Table 6.1 Direct mechanisms and PGPR used

Mechanism PGPR Crops References
Nitrogen Symbiotic Rhizobium and Legumes, e.g., Lucas-Garcia et al.
fixation allied genera Soybeans, Peanut, (2004), Vargas et al.
Chickpea etc. (2010), Laranjo et al.
(2014), and Abd-Alla
et al. (2017)
Frankia Higher Agiospermic Crannell et al. (1994),
plants (Actinorhizal Santi et al. (2013), Diagne
plants), e.g., Alnus, et al. (2013), and Ballhorn
Casurina et al. (2017)
Free- Cyanobacteria, Cereals, e.g., Wheat, Steenhoudt and
living Azotobacter, Rice, Maize Vanderleyden (2000),
Azospirillum, Cassán et al. (2009), and
Beijerinckia Shariatmadari et al. (2013)
Phosphate Pseudomonas, Any crops Mamta et al. (2010),
solubilisation Bacillus, Rhizobium Schoebitz et al. (2013),
and Oteino et al. (2015)
Iron sequestration Alcaligenes, Any crops Gamit and Tank (2014)
Pseudomonas, and Aznar and Dellagi
Bacillus (2015)
Zinc solubilisation Burkholderia, Any crops Goteti et al. (2013), Vaid
Pseudomonas, et al. (2014), and
Bacillus Sunithakumari et al.
(2016)
Potassium Bacillus, Any crops Bagyalakshmi et al.
solubilisation Pseudomonas (2012), Parmar and
Sindhu (2013), and
Prajapati and Modi (2016)
Phytohormone Bacillus, Rhizobium, Any crops Khare and Arora (2010),
production Pseudomonas Reetha et al. (2014), and
Pandya and Desai (2014)
Nutrient Uptake
Nitrogen (N) is among the most vital nutrients essential for plant growth. In the
atmosphere, nitrogen is present in very large amounts (78%) but remains unavail-
able for the direct uptake by the plant. Diazotrophic microorganisms, particularly
bacteria and archaea, can fix atmospheric dinitrogen (N2) through the BNF process
(Dixon and Kahn 2004). Nitrogen-fixing microorganisms change nitrogen to ammo-
nia by using a complex enzyme system known as nitrogenase (Postgate 1998; Leigh
2002). Nitrogen-fixing bacteria are of two types: symbiotic (rhizobia and Frankia)
(Ahemad and Khan 2012) and nonsymbiotic (Cyanobacteria, Azospirillum,
Azotobacter, Gluconacetobacter, Azoarcus) (Bhattacharyya and Jha 2012; Roper
and Gupta 2016). Among all nitrogen fixers, root nodule-associated rhizobia are
most studied and exploited. It is reported that in agricultural systems rhizobia are
annually able to fix 180 × 106 tonnes of nitrogen through BNF process at global
136 M. Verma et al.
level (Postgate 1998; Sahgal and Johri 2003) which causes efficient increment in the
productivity and quality of crops (Herridge et al. 2008; Krapp et al. 2011). It is also
estimated that the cost of total nitrogen fixed by BNF process is equivalent to US $
160–180 billion (Rajwar et al. 2013). Due to this (BNF) outstanding property, rhi-
zobia are being used as biofertilizers to enhance crop production in several coun-
tries (Mia and Shamsuddin 2010; Arora et al. 2017). In this regard, Yadegari et al.
(2010) reported that on inoculation of Rhizobium phaseoli, growth and yield of
Phaseolus vulgaris are increased due to high nitrogen fixation. Similarly Sarr et al.
(2015) also worked on the enhanced growth, nitrogen fixation, and increased nodu-
lation of cowpea by application of Bradyrhizobium strains.
Phosphorus (P) is the second major nutrient required for plant growth and devel-
opment and present at levels of 400–1200 mg/kg of soil (Begon et al. 1990; Khan
et al. 2007). Most of the soils are deficient in P due to its high fixation rate in
insoluble forms (Batjes 1997; Kravchenko et al. 2004), and very less amount (1 mg
or less) of P is in soluble form hence in general is not available for plant uptake
(Khan et al. 2009). It is reported that only 5% or less of total P present in soil is
available for plant uptake. PGPR solubilize these insoluble compounds by acidifica-
tion, chelation, exchange reactions, and gluconic acid production which make the P
uptake process by plants very easy (Rodriguez et al. 2004; Chung et al. 2005; Khan
et al. 2009; Coutinho et al. 2012; Li et al. 2017). Phosphate-solubilizing bacteria
(PSB) help in phosphate uptake by the plants due to one or more aforesaid mecha-
nisms. PSB belong to various genera such as Azotobacter, Bacillus, Beijerinckia,
Burkholderia, Enterobacter, Erwinia, Flavobacterium, Microbacterium,
Pseudomonas, Rhizobium, and Serratia (Bhattacharyya and Jha 2012). PSB enhance
the plant growth and yield such as Oteino et al. (2015) reported that phosphate-
solubilizing Pseudomonas strain increased the growth of Pisum sativum L. by pro-
ducing gluconic acid. Similarly, Demissie et al. (2013) and Gusain et al. (2015)
reported the enhanced plant growth and phosphate uptake in faba bean and rice,
respectively. Recently, Li et al. (2017) also worked on the growth promotion of
maize plants by inoculation of PSB isolates (Paenibacillus, Pseudomonas, and
Sphingomonas). Besides P uptake, PSB also enhance the plant growth by stimulat-
ing BNF (Ahmad et al. 2008; Zaidi et al. 2009).
Apart from N and P, PGPR also influence the uptake of other nutrients such as
potassium (K), zinc (Zn), iron (Fe), and sulfur (S) (Peix et al. 2001; Wu et al. 2005;
Adesemoye et al. 2008; Lukkani and Reddy 2014). K is also a very important nutri-
ent, essential for the growth and development of plants. However, more than 90% of
K in the soil exists in insoluble forms (micas, illite, and orthoclases) (Li et al. 2006;
Bahadur et al. 2016). PGPR such as Pseudomonas, Burkholderia, Acidithiobacillus,
Bacillus, and Paenibacillus are known to solubilize K for plant uptake mainly by
excreting organic acids (Rogers et al. 1998; Parmar and Sindhu 2013). Han and Lee
(2005) reported the increased K uptake, photosynthesis, and yield of eggplant grown
on K-limited soils by inoculation of K-solubilizing bacteria. According to
Bagyalakshmi et al. (2012), K-solubilizing bacteria caused high productivity of tea
plants by enhancing nutrient uptake efficiency. Shanware et al. (2014) and Etesami
et al. (2017) reported the detail about the mechanism, occurrence, and functions of
potassium-solubilizing rhizobacteria.
Zn is an essential micronutrient for plant growth, but according to FAO it is esti-
mated that about 50% of lands are Zn deficient due to fixed forms of Zn compounds
(FAO 2002; Review 2008). PGPR help plants to mobilize the fixed form of Zn
compound and its easy uptake (Iqbal et al. 2010; Hussain et al. 2015). Several bacte-
rial genera are now considered as Zn solubilizers which include Bacillus,
Pseudomonas, Rhizobium, Burkholderia, Acinetobacter, Mycobacterium,
Stenotrophomonas, Enterobacter, and Xanthomonas (Vaid et al. 2014; Naz et al.
2016). PGPR solubilize Zn by various mechanisms such as excretion of organic
acids (2-ketogluconic acid and gluconic acid), protein extrusion, and production of
chelating agents (Nahas 1996; Seshadre et al. 2002). Goteti et al. (2013) observed
enhanced nutrient uptake and growth of maize plants when inoculated with
Zn-solubilizing bacteria. Shakeel et al. (2015) also recorded that root-associated
Bacillus sp. enhanced Zn translocation toward grains of rice varieties, basmati-385
and super basmati, and also increased total yields by 22–49% and 18–47%, respec-
tively. Zinc-solubilizing PGPR have a very important role in agriculture and food
security (Shaikh and Saraf 2017).
Fe is the fourth most abundant and essential element present in the soil and works
as an essential nutrient for all forms of life on earth. Iron is spatially distributed in
soils with 0.2% to 55% (20,000–550,000 mg/kg), but in the aerobic environment, Fe
occurs in insoluble hydroxides and oxyhydroxide form, which is generally inacces-
sible to both plants and microorganisms (Rajkumar et al. 2010). In low Fe condi-
tions, certain bacteria produce siderophores as low-molecular mass Fe chelators
(Miethke and Marahiel 2007). Siderophore-producing PGPR help in Fe uptake by
the plants through formation of a ferric-siderophore complex even at very low con-
centrations (Podile and Kishore 2006; Dimkpa et al. 2009; Boiteau et al. 2016).
Bacterial genera Pseudomonas, Burkholderia, Enterobacter, and Grimontella are
reported as efficient siderophore producers, while Klebsiella, Stenotrophomonas,
Rhizobium, Herbaspirillum, and Citrobacter are also known to be siderophore pro-
ducers (De Souza et al. 2015; Arora and Verma 2017). In this context, Sharma et al.
(2013) reported that iron content of rice grains is increased on treatments with strain
of P. putida. In another study, Wang et al. (2017) observed the enhanced iron uptake
by Arabidopsis thaliana plants on inoculation with B. amyloliquefaciens. Detailed
information about the application of bacterial siderophores is described by Ali and
Vidhale (2013) and Saha et al. (2016).
S is also an essential nutrient for plant growth and taken up by plants mainly in
the form of sulfate and sulfur dioxide (Marschner 2012). A major part of S (95%) is
unavailable (bound with organic complex) for plant uptake, and only 5% is avail-
able (Kertesz and Mirleau 2004). Sulfur-oxidizing PGPR can be used to convert
unavailable S into available form for direct uptake by the plants (Gahan and
Schmalenberger 2014). Currently PGPR have gained much attention in agriculture
138 M. Verma et al.
to fulfil the sulfur requirements of plants (Salimpour et al. 2010; Anandham et al.
2014). Grayston and Germida (1991) reported that sulfur-oxidizing PGP isolates
stimulate canola growth by enhancing mineral nutrient uptake. Awad et al. (2011)
reported that onion growth, yield, and nutrient content were increased on inocula-
tion with sulfur-oxidizing bacteria. Similar work was also done by Eslamyan et al.
(2013) who reported that on inoculation with P. fluorescens, growth of rapeseed
cultivars is increased due to high S uptake.
Phytohormone Production
Phytohormones act as chemical messengers and enhance plant growth by affecting

all the major activities such as formation and development of various parts of plants
mainly leaves and flowers and ripening of fruits (Khalid et al. 2006). There are sev-
eral PGPR which show phytohormone production ability and influence the physio-
logical processes of plants to facilitate their growth by regulating hormonal balance
(Patten and Glick 2002; Asghar et al. 2004; Boiero et al. 2007; Maheshwari et al.
2015). PGPR can control the production of hormones such as indole acetic acid
(IAA), abscisic acid (ABA), cytokinins, gibberellins, and ethylene (Kudoyarova
et al. 2015). Among all, IAA is reported as quantitatively most abundant and
secreted by several bacterial genera including Azospirillum, Bacillus, Pseudomonas,
and Rhizobium (Arora 2013; Islam et al. 2015). It is reported that more than 80% of
the rhizospheric bacterial strains are able to produce auxins (Khalid et al. 2004;
Hayat et al. 2010). The biosynthesis of IAA depends on various environmental fac-
tors such as pH, carbon, and precursor concentration (Spaepen et al. 2009). IAA
plays a very important role in rhizobacteria-plant interactions (Spaepen and
Vanderleyden 2011) and promotes the plant growth mainly by stimulating the devel-
opment of root system (Khare and Arora 2010; Tewari and Arora 2013). Mohite
(2013) reported the enhanced growth of wheat plant due to inoculation of IAA-
producing strains of Bacillus and Lactobacillus. Etesami et al. (2015) observed the
enhanced growth of rice crop on inoculation with IAA producing rhizospheric and
endophytic bacteria. Recently Pérez-Fernández and Alexander (2017) also reported
that IAA-producing strains significantly enhanced the plant biomass, flower, pod,
and seed production along with nitrogen content in Cicer arietinum. Vidhyasekaran
(2015) reported that auxin also controls various plant defense-signaling pathways
by affecting other plant hormone activities, e.g., cytokinin, abscisic acid, ethylene,
jasmonate, and salicylic acid.
PGPR are also known to produce cytokinins which have major role in root initia-
tion, cell division, cell enlargement and increase the root surface area of plants by
enhanced formation of adventitious roots (Werner et al. 2003; Salamone et al. 2005).
Cytokinins mainly affect the leaf growth by delaying the senescence or aging of
plant tissues (Kundan et al. 2015). Some bacterial genera, e.g., Azotobacter,
Rhizobium, Pantoea, Rhodospirillum, Pseudomonas, Bacillus, and Paenibacillus,
are reported to produce cytokinins (Salamone et al. 2001; Glick 2012). In a study
Ortíz-Castro et al. (2009) reported that cytokinin-producing Bacillus megaterium

promote biomass production of Arabidopsis thaliana plant. Hussain and Hasnain
(2009) reported enhanced growth in cucumber on inoculation with
cytokinin-
producing bacterial extract. Selvakumar et al. (2016) reported that
cytokinin-producing osmotolerant strains (Citricoccus zhacaiensis and B. amyloliq-
uefaciens) enhance the growth of tomato under irrigation-deficit conditions.
Gibberellins (GA) are a class of phytohormones that commonly result in modifi-
cations of plant morphology by extension of plant tissues, particularly stem tissues
(Salisbury 1994). In bacteria, they act as signaling factors toward the host plant
(Bottini et al. 2004). GA production by PGPR induces growth promotion in plants
(Piccoli et al. 1997; Gutiérrez-Mañero et al. 2001; Kang et al. 2014). It is also
reported that GA interact with other phytohormones which modify the plant hor-
monal balance and affect plant growth (Bömke and Tudzynski 2009). Bottini et al.
(2004) stated that gibberellin-producing bacteria have potential to enhance the
growth and yields of crops. Kang et al. (2014) reported that gibberellin-producing
PGP strain Leifsonia soli (SE134) has efficient potential to enhance the biomass,
hypocotyl, and root lengths of cucumber seeds in comparison with control.
Ethylene is a gaseous phytohormone that controls the plant growth and develop-
ment (Abeles et al. 1992; Khalid et al. 2006). It is also important to induce different
physiological changes in plants by performing various activities such as inhibition
of root elongation and auxin transport which promotes senescence and abscission of
various organs and fruit ripening (Glick et al. 2007; Cassán et al. 2014). Besides
regulating plant growth, ethylene has also been recognized as a stress hormone
(Saleem et al. 2007). Ethylene production also regulates other important plant
growth functions such as seed germination, seedling establishment, development of
root hair, formation of adventitious roots, nodulation, flower and leaf senescence,
and leaf and fruit abscission (Kucera et al. 2005; Bakshi et al. 2015). Corbineau
et al. (2014) reported that ethylene production breaks seed dormancy and regulates
seed germination. Ribaudo et al. (2006) reported that ethylene produced by
Azospirillum brasilense promotes root hair development in tomato plants.
Production of Volatile Organic Compounds (VOCs)
It has recently been reported that some rhizobacteria promote plant growth by
releasing VOCs (Ping and Boland 2004; Ortíz-Castro et al. 2009; Tahir et al. 2017).
These compounds are of diverse types and very helpful for PGPR to communicate
with each other and their host plants (Peñuelas et al. 2014). VOCs include various
compounds such as 2, 3-butanediol, acetoin, terpenes, and jasmonates. The synthe-
sis of bioactive VOCs is considered to be a strain-specific phenomenon. These
VOCs can act as signaling molecules in plant-microbe interactions and elicit the
plant responses mainly when generated at sufficient concentrations (Ryu et al. 2003;
Reddy et al. 2014). Gutierrez-Luna et al. (2010) observed that VOC emission by
140 M. Verma et al.
PGPR can modulate both plant growth promotion and root system architecture of A.
thaliana plant. Similarly Tahir et al. (2017) reported that volatile compounds pro-
duced by Bacillus subtilis play a very significant role in growth promotion of tomato
plants by regulating biosynthesis of phytohormones.
Biocontrol Activities
Several phytopathogens cause severe diseases in crops and reduce crop yields.
Contamination of food grains with phytopathogens is also considered to diminish
quality of food and responsible for high economic losses (Guo et al. 2013).
Biocontrol of phytopathogens by using natural organisms is an effective method to
treat plant diseases in an eco-friendly manner without causing harm to the environ-
ment (Compant et al. 2005; Fatima et al. 2009). Hence application of biocontrol
appears as a more beneficial and profitable approach in comparison with synthetic
chemicals. Biocontrol PGPR are reported to control plant diseases caused by vari-
ous types of pathogens and pests such as bacteria, fungi, protozoa, viruses, nema-
todes, and insects (de Bruijn et al. 2007; Raaijmakers et al. 2010).
Biological control of phytopathogens by PGPR is boon to modern as well as
conventional agriculture. Currently various strains of PGPR in genera Agrobacterium,
Arthrobacter, Azoarcus, Azotobacter, Azospirillum, Bacillus, Burkholderia,
Caulobacter, Chromobacterium, Enterobacter, Erwinia, Flavobacterium,
Klebsiella, Micrococcus, Rhizobium, Pantoea, Pseudomonas, and Serratia are
being used to control the diseases of agriculturally important crops (Ahemad and
Kibret 2014; Figueroa-López et al. 2016). Pseudomonas and Bacillus are very pref-
erential among them because they are aggressive colonizers of the rhizosphere and
have broad-spectrum antagonistic activities (Weller et al. 2002; Ahmad et al. 2008;
Khare and Arora 2011; García-Gutiérrez et al. 2013; Arora and Mishra 2016; Mishra
and Arora 2018). PGPR show various biocontrol activities against phytopathogens
such as competition for nutrients, antagonism by production of various metabolites
(antibiotics, hydrolytic enzymes, cyanide, siderophores), and induction of systemic
resistance (Table 6.2) (Siddiqui 2006; Lugtenberg and Kamilova 2009;
Ramyasmruthi et al. 2012; Mishra et al. 2017b). These aforesaid mechanisms are
not only very efficient to control phytopathogens, but they also act in synergistic
manner to resist the plants against pathogens (Jha et al. 2011).
Competition
PGPR control the growth of pathogens by creating competitive environments for

nutrient uptake by them and cause the reduction in nutrient availability around the
host plant. This competition between pathogens and non-pathogens is responsible
to control the phytopathogen population (Pal and Gardener 2006). Rabosto et al.
Table 6.2 Indirect mechanisms and PGPR used

Mechanisms PGPR Crops References
Competition Enterobacter, Any crops, e.g., Raaijmakers and Weller (2001),
Pseudomonas, Wheat, Rice, Kageyama and Nelson (2003),
Bacillus Tomato and Liu et al. (2013)
Enzyme Bacillus, Any crops, e.g., Singh et al. (1999), Kishore
production Pseudomonas, Cucumber, Grape, et al. (2005), Arora et al. (2008),
Serratia Peanut and Kejela et al. (2016)
Antibiotic Pseudomonas, Any crops, e.g., Hill et al. (1994), Mishra and
production Bacillus, Tobacco, Cotton, Arora (2012), and Dhanya and
Agrobcaterium, Cabbage, Mung Adeline (2014)
Pantoea bean
HCN Pseudomonas, Any crops e. g. Reetha et al. (2014), and Nandi
production Bacillus, Burkholderia Wheat, Barley et al. (2015)
Siderophore Rhizobium, Any crops, e.g., Arora et al. (2001), Omidvari
production Pseudomonas, Groundnut, et al. (2010), Mishra and Arora
Bacillus Chickpea, Capsicum (2011), and Rais et al. (2017)
ISR and SAR Pseudomonas, Any crops, e.g., Press et al. (1997), Reitz et al.
Serratia, Bacillus, Cucumber, Tobacco (2002), Meziane et al. (2005),
Rhizobium Bean, Tomato Pal and Gardener (2006), and
Tahir et al. (2017)
(2006) studied that Bacillus sp. showed antagonistic activity against Botrytis cine-
rea creating competition for nutrients. Similarly, Haidar et al. (2016) reported the
biocontrol activity of antagonistic bacteria by creating competitive environments
for fungal pathogens. Siderophore production is very important for this type of
interaction in which siderophore-producing bacteria suppress the growth of patho-
gens by creating iron-limiting conditions in soil (Arora et al. 2001; Sayyed et al.
2008; Verma et al. 2011). Siderophores work as antagonistic metabolites for biocon-
trol of phytopathogens which helps bacteria to rapidly colonize around the plant
root (Keel et al. 1989; Loper and Buyer 1991; Haas and Défago 2005). According
to Hofte et al. (1992), siderophore (salicylic acid, pyochelin, and pyoverdine) pro-
duction causes disease suppression by limiting the supply of essential trace minerals
for pathogens in rhizosphere. Yu et al. (2011) reported that the siderophore-
producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium
wilt and promotes the growth of pepper plant. Recently Kotasthane et al. (2017) also
reported that siderophore-producing Pseudomonas strain controls the collar rot dis-
ease of chickpea plant.
Production of Metabolites
Production of metabolites is one of the potent and broad-spectrum mechanisms of

biocontrol (Mishra and Arora 2018). Besides siderophore, PGPR also produce many
other antagonistic compounds against pathogens such as (i) volatile compounds,
142 M. Verma et al.
e.g., hydrogen cyanide, aldehydes, alcohols, ketones, and sulfides, and (ii) nonvola-
tile compounds, e.g., polyketides (diacetylphloroglucinol (DAPG) and mupirocin)
and heterocyclic nitrogenous compounds such as derivatives of phenazines (pyocya-
nin, phenazine-1-carboxylic acid (PCA), phenazine-1-carboxamide (PCN), and
hydroxy phenazines) (De Souza et al. 2003). Meyer et al. (2016) reported that
DAPG-producing P. fluorescens is used for biocontrol of Meloidogyne incognita
and Fusarium oxysporum. In this context, recently Mishra and Arora (2018) and
Shahid et al. (2018) reported the detail information about the secondary metabolites
produced by pseudomonads for effective biocontrol activities. Exopolysaccharide
(EPS) production has also very promising role in growth enhancement of plants by
performing biocontrol activities. EPS control plant diseases by protecting their root
against phytopathogenic attacks (Noumavo et al. 2016). In this regard, Tewari and
Arora (2014) reported that EPS-producing Pseudomonas strain enhances the yield
of sunflower crop by protecting it from the attack of a pathogen, Macrophomina
phaseolina. Recently, Tewari and Arora (2018) reported role of salicylic acid
(SA) produced by fluorescent pseudomonads in biocontrol of fungal phytopatho-
gens. Khare et al. (2018) suggested the role of biologically active peptides known as
peptaibols, in inhibition of phytopathogen, Fusarium oxysporum.
Several biocontrol PGPR show antagonistic activity against phytopathogens by
causing lysis of their cell wall which is performed by secreting various hydrolytic
enzymes such as chitinases, glucanases, proteases, and lipases (Maksimov et al.
2011; Jadhav and Sayyed 2016). These enzymes are extracellular and hydrolytic
and cause the digestion or deformation of cell wall components of fungi (Aeron
et al. 2011). Hydrolytic enzymes producing bacteria are also used in combination
with other biocontrol agents, leading to a synergistic inhibitory effect against phy-
topathogens (Someya et al. 2007). Arora et al. (2007) and Saraf et al. (2014) reported
chitinase and glucanase production by Bacillus and Pseudomonas sp. as growth
suppressor of filamentous fungi both in laboratory and field conditions. Figueroa-
López et al. (2016) also observed the antagonistic activity of rhizospheric bacteria
against Fusarium verticillioides by producing various hydrolytic enzymes (gluca-
nases, proteases, or chitinases) for disease control in maize plant.
I nduced Systemic Resistance (ISR) and Systemic Acquired

Resistance (SAR)
ISR and SAR activate chemical and physical defense mechanisms of the host plant
by an inducer (chemical or microorganism) (Pieterse et al. 2014). However, induc-
tion of host defenses can be local and/or systemic in nature, depending on the type,
source, and number of stimuli or signaling compounds (Van Loon 2007). ISR is
triggered by PGPR and starts in the root and then spreads to the other plant parts
(Ramos-Solano et al. 2008). Various chemical elicitors are produced by PGPR
strains such as lipopolysaccharides (LPS), siderophores, cyclic lipopeptides, DAPG,
homoserine lactones, and volatiles (acetoin and 2, 3-butanediol) (Lugtenberg and
Kamilova 2009; Pieterse et al. 2014). ISR is mainly elicited by ethylene and jas-
monic acid signaling in the plant (Van Loon 2007). Several PGPR strains among
Pseudomonas, Bacillus, Serratia, and Azospirillum have been reported as ISR
inducers (Bakker et al. 2013). Zhang et al. (2002) observed the role of SA in ISR
elicited by PGPR against blue mold of tobacco. Boukerma et al. (2017) evaluated
that P. fluorescens (PF15) and P. putida (PP27) have potency to protect tomato
plants against Fusarium wilt by ISR. In contrast, SAR is typically activated by
necrotic pathogenic bacteria and the molecule that typically leads to the expression
of pathogenesis-related (PR) proteins such as SA. These PR proteins include
enzymes some of which may act directly to lyse invading cells, reinforce cell wall
boundaries to resist infections, or induce localized cell death (Beneduzi et al. 2012).
Abiotic Stress Management
Abiotic stresses are the major constraints that are affecting the soil quality as well as
productivity of the crops (Grayson 2013). According to the Food and Agriculture
Organization (FAO), it is estimated that due to abiotic stresses, 30% land will
degrade in the next 25 years and it will reach up to 50% by the year 2050 (Wang
et al. 2003). PGPR can support plants to resist against various types of stresses to
ameliorate their effect (Lugtenberg and Kamilova 2009; Egamberdieva 2012).
Stress-tolerant PGP inoculants work as cost-effective tools to improve production of
crops in a hostile environment (Nadeem et al. 2010; Tewari and Arora 2015). PGPR
can induce abiotic stress tolerance in plants by imposing physical and chemical
changes which is known as “induced systemic tolerance” (IST) (Yang et al. 2009).
PGPR like Achromobacter, Azotobacter, Azospirillum, Acetobacter, Bacillus,
Chryseobacterium, Flavobacterium, Enterococcus, Klebsiella, Pseudomonas,
Rhizobium, Serratia, and Paenibacillus are being used for ameliorating various
stresses in diverse habitats (Rabie and Almadini 2005; Egamberdieva 2012). Arora
et al. (2012) recommend that the use of such bioproducts is helpful to combat the
soil stress with high crop production. It is reported by various workers that applica-
tion of PGPR in stressed soils reduces their harmful effects by regulating the pro-
duction of various metabolites such as phytohormones, antioxidants, enzymes, and
EPS (Raghavendra et al. 2010; Kong et al. 2014; Arora and Mishra 2016).
Salinity stress is a major issue, affecting more than 900 million hectares (ha) land
around the globe (Khan and Panda 2008). Salinity causes alkalization of soil; hence
soil nutrients become unavailable for plant leading to nutrient stress (Maheshwari
et al. 2012a). Application of PGPR in saline soil can be helpful for reducing the
impact of salinity along with plant growth promotion (Ilangumaran and Smith 2017).
EPS production is known to be a potential trait for salinity stress amelioration. EPS
production by rhizobacteria is helpful for effective survival of plant under salinity
stress in rhizospheric soil by inducing osmotolerance activity (Grover et al. 2010;
Upadhyay et al. 2011). EPS production by salt-tolerant PGPR causes high accumu-
lation of soil particles around plant roots with high water retention activity along
144 M. Verma et al.
with nutrients and facilitates the plant growth in saline soil (Roberson and Firestone
1992; Paul and Lade 2014). Due to this activity, physiological properties of soils and
metabolic properties of crops increase, leading to higher crop p roductivity with
improved quality. In this regard, Qurashi and Sabri (2012) reported that salt-tolerant
PGP strains have the ability to enhance plant growth by secreting large amount of
EPS under high salinity. Tewari and Arora (2016) also reported the enhanced yield
of sunflower under salinity stress on inoculation with EPS-producing Pseudomonas
sp. An enzyme, 1-aminocyclopropane-1-carboxylate (ACC) deaminase produced by
PGPR, plays an important role in stress management by acting as regulator for phy-
tohormone ethylene (Glick 2014; Saikia et al. 2018). It cleaves ACC (immediate
precursor of ethylene) in the biosynthetic pathway for ethylene in plants (Glick et al.
1998). In this context Saleem et al. (2007) and Glick (2014) reported that ACC pro-
ducing PGPR can contribute to growth promotion efficiently in stressful soil condi-
tions when inoculated on plants. In another study Habib et al. (2016) worked on
ACC deaminase producing PGPR and their effect on reduction of salinity stress in
okra plant through reactive oxygen species (ROS)-scavenging enzyme activity.
Temperature is an important abiotic factor for plant growth, but exposure at very
high or very low temperatures is harmful. Cold-tolerant and heat-tolerant PGPR are
recently being used to ameliorate the adverse effects of temperature on plants
(Hoflich and Kuhn 1996; Meena et al. 2015). Ali et al. (2011) reported the effect of
thermotolerant PGPR inoculation on the growth of wheat under heat stress.
According to Mishra et al. (2012), cold-tolerant bioinoculants are also useful in
stress management. Drought is also reported as a major stress for crop production
(Glick 2004). Drought stress can be ameliorated by using various drought-tolerant
PGPR including Azotobacter, Azospirillum, Bacillus, Rhizobium, and Serratia
(Vurukonda et al. 2016). Sandhya et al. (2009) used the EPS-producing PGPR to
promote the growth of sunflower crop under drought stress. Kaushal and Wani
(2016) recommended the use of PGPR to combat the drought stress problems in
drylands. Flooding is also one of the major abiotic stresses that works as a limiting
factor for crop growth (Normile 2008). It is reported that on an average flooding
affects 140 million people per year around the globe (WDR 2003). Chakraborty
et al. (2013) reported the water stress amelioration and high yield of wheat crop by
using osmotic stress-tolerant bacteria. Similarly, Tewari and Arora (2016) reviewed
the effect of flooding stress on soybean production and their amelioration by using
PGPR. According to Tewari and Arora (2013), application of microbes to amelio-
rate soil abiotic stresses is easier and beneficial in comparison with developing
stress-tolerant crops. PGPR are now being used as efficient and inexpensive tools to
ameliorate the soil stresses (Batool et al. 2014; Gontia-Mishra et al. 2016).
Soil Renovation
Presently it is estimated that a large portion of the land around the globe is wasted
due to soil erosion and degradation problems. According to Riadh et al. (2010), out
of the world’s 5.2 billion ha of dryland agriculture, 3.6 billion ha is affected by the
problems of erosion and soil degradation. Soil properties and fertility depend on the
combination of various biotic and abiotic factors. Richness and diversity of micro-
bial communities in soil and their activity work as a major indicator of soil health
(fertility) (Griffiths and Philippot 2012; De Souza et al. 2015). In low-quality
pollutant-contaminated soil, microbial load and nutrients are very less, and PGPR
inoculation improves physicochemical as well as biological properties (Sahoo et al.
2013; Bhardwaj et al. 2014). Several methods have been developed for pollutant
removal, but microbes have emerged as successful solution for bioremediation due
to their high sensitivity, tolerance, and the sequestration ability (Burd et al. 2000;
Amora-Lazcano et al. 2010). The role of PGPR in pollutant degradation is very use-
ful for plants to grow as natural vegetation at a contaminated site (Pérez-Montaño
et al. 2014). It is reported that use of PGPR can be extensively applied for crop
improvement along with contaminant removal in deteriorating soils (Huang et al.
2005; Yang et al. 2009). Several researchers reported that on application of PGPR,
high crop production and metal removal takes place simultaneously in polluted
environment (Zhuang et al. 2007; Romeh and Hendawi 2014; Khan and Bano
2016). This bioremediation technology (rhizoremediation) is now being used for the
removal of pollutants such as pesticides, polyaromatic hydrocarbons, heavy metals,
and other toxic wastes (Bhalerao 2012; Hansda et al. 2014; Bisht et al. 2015).
Efficiency of rhizoremediation process is controlled by various factors such as pol-
lutant type and their bioavailability, plant variety and diversity and activity of
microbes, and environmental conditions (Wenzel 2009). In this regard, Okon et al.
(2014) worked on the bioremediation of palm oil mill effluent polluted soil and their
effect on the growth of Amaranthus hybridus L. They reported that the crop growth
in polluted soil can be upgraded by using bioproducts. It is also studied that PGPR
are used for rhizoremediation of petroleum compounds in soil along with the growth
of various plants such as cotton, ryegrass, tall fescue, and alfalfa (Tang et al. 2010).
Heavy metals are present in soils as contaminants (Gadd 2010) with concentra-
tion ranging from 1 to 100,000 mg/kg in typical soil (Long et al. 2002). Metal con-
tamination from soil can be removed mainly by geo-active action of soil microbes
(Mishra et al. 2017a). Metal-mobilizing PGPR remediate heavy metals from soil
and perform multiple functions, e.g., soil quality improvement, plant growth
enhancement, detoxification, and metal removal from soil (Hassan et al. 2016;
Mishra et al. 2017a). PGPR enhance rhizoremediation of metals through various
mechanisms such as acidification, chelation, complexation, precipitation, and redox
reactions by producing various metabolites, e.g., organic acids, siderophores, exo-
polymers, and biosurfactants (Ma et al. 2011; Ma et al. 2016). According to Pires
et al. (2017) Bacillus, Pseudomonas, and Arthrobacter are considered as predomi-
nant genera of the bacterial population in metal-contaminated sites. Abou-Shanab
et al. (2006) reported that application of certain rhizobacteria can increase the
uptake of nickel (Ni) from soils by changing its phase. Wani and Khan (2010)
worked on chromium (Cr) toxicity and reported its reduced uptake in roots, shoots,
and grains of Cicer plant on application of Bacillus strain. In the same year, Dary
et al. (2010) worked on the application of PGPR for remediation of copper (Cu),
cadmium (Cd), and lead (Pb) with increased biomass of Lupinus plant. Pinter et al.
146 M. Verma et al.
(2017) observed that on the application of arsenic (As)-tolerant PGPR (B.

licheniformis, Micrococcus luteus, and P. fluorescens), grapevine biomass is
increased. Zn-tolerant rhizobia from Zn mining soil is reported as growth promoter
of Leucaena leucocephala in contaminated soil (Rangel et al. 2017). Cu-resistant
Kocuria sp. is also reported as potential PGPR isolated from the dry tailing of cop-
per mine (Hansda et al. 2017). Ma et al. (2015) studied that PGP strains of Bacillus
sp. are able to mobilize high amount of metals. Rhizoremediation, thus, can be a
very important and low input biotechnology of the future for cleaning contaminated
soils off pollutants and simultaneously enhancing their productivity.
Diverse Applications of PGPR
PGPR are essential components of soil and for crop management. PGPR play sig-
nificant role in solving the problems related to soil stress, soil fertility, soil degrada-
tion, and plant growth (Glick 2010). Generally PGPR have been used as biofertilizers
or biopesticides (Vessey 2003; Zahir et al. 2004; Arora et al. 2016a; Vandenberghe
et al. 2017), but in the future these useful microbes can be used to play various other
roles in sustaining the agroecosystems.
Biofertilizers
Biofertilizers are playing crucial role in enhancing crop productivity and quality in
present-day agriculture (Mahanty et al. 2016). Currently biofertilizers are also
termed as biostimulants. Biostimulants are considered as any substance (of biologi-
cal origin) or microorganism or their combinations applied to plants, seeds, or soil
to enhance nutrient uptake efficiency, stress tolerance activation, and crop quality
improvement (du Jardin 2015). Biofertilizers/biostimulants are formulated products
of one or more microorganisms which promote plant growth by colonizing the rhi-
zosphere or inner parts of plants (Vessey 2003; Malusá and Vassilev 2014).
Biofertilizers work as important components of integrated nutrient management in
soil and nourish the plant by playing a very active role in nutrient cycling between
soil, plant roots, and microorganisms (Abdel Ghany et al. 2013; Vejan et al. 2016).
Globally biofertilizers have been commercially used in agriculture since more
than 120 years when “Nitragin” was launched (Nobbe and Hiltner 1896). Rhizobia-
based bioinoculants are commercially available since more than 100 years now
(Bashan 1998; Arora et al. 2017). According to BCC research (2014), it is estimated
that total fertilizer market has 5% share of biofertilizers and more than 150 microbe-
based products are registered for agricultural purposes. Currently various types of
biofertilizers are used in agriculture: nitrogen fixers, phosphate solubilizers, potash
solubilizers, and others (Zn, boron, S solubilizers). Among all the biofertilizers,
nitrogen fixers (Rhizobium, Azospirillum, Azotobacter, Azoarcus, and c yanobacteria)
Fig. 6.2 Market shares of

various types of
biofertilizers at global
level. (Research Nester
2018)
Nitrogen fixers Phosphate solubilizers

Potash mobilizers Others (Zinc,Boron, Sulfur solubilizers)
and phosphate solubilizers (B. megaterium, Pseudomonas sp.) have wide c ommercial
applications at global level (Mishra and Das 2014) (Fig. 6.2). Zn-, K-, and S-based
biofertilizers are also emerging as important bioinoculants to overcome their defi-
ciency in plants (Khatibi 2011; Shaikh and Saraf 2017). It is reported that biofertil-
izers increase the crop yield by up to 10–40% by improving uptake of various
nutrients such as proteins, amino acids, vitamins, nitrogen, etc. (Bhardwaj et al.
2014). Nitrogenous biofertilizers can increases up to 15–25% of total crop yield by
adding 20–200 kg N/ha/year, while PSB-based biofertilizers can increase 10–20%
crop yield by solubilizing about 30–50 kg phosphate/ha/year (AgriInfo.in 2015).
Although various types of biofertilizers are commercially available in the global
market, rhizobia-based inoculants have the largest market share estimated at approx-
imately 78%, while phosphate solubilizers and other bioinoculants have 15% and
7% shares respectively (Owen et al. 2015; Transparency Market Research 2017). It
is reported that various other nitrogen-fixing products are also used at large scale
which are based on Azospirillum, Azotobacter, and Gluconacetobacter species
(Parnell et al. 2016). Phytohormone-producing biofertilizers are also globally used
for sustainable agriculture mainly as growth regulators of plants (Narula et al. 2006;
Maheshwari et al. 2015). According to Nadeem et al. (2014), biofertilizers for high
nutrient uptake have wide applicability in global market, but growth regulator-based
biofertilizers need more concern for their commercialization. Currently, the require-
ment and growth of fertilizers, mainly biofertilizer market in all regions of the world
(Fig. 6.3), are increasing to fulfil the food requirements at global level. It is reported
that the biofertilizer market was valued at USD 946.6 million in 2015 (marketsand-
markets.com 2016). This market is projected to grow at a cumulative annual growth
rate (CAGR) of 14.08% from 2016 to 2022 to reach USD 2305.5 million (market-
sandmarkets.com 2016).
148 M. Verma et al.
Fig. 6.3 Market share of

biofertilizers in various
regions of world. (BCC
Research 2014)
North America Latin America

Europe Asia Pacific Rest of the World (ROW)
Biopesticides
Various plant diseases are responsible for the loss of approximately one-third of the
crop yields at global level (Lugtenberg et al. 2002). According to Lugtenberg
(2015), approximately 25% of the crop yield is lost every year due to diseases
caused by phytopathogens around the globe. To overcome this problem, PGPR with
biocontrol traits are used as biopesticides. Biopesticides are also attracting attention
to manage several pests and weeds (Kumar and Singh 2015). The global market for
pesticides has 2.5% contribution of biopesticides (marketsandmarkets 2014).
Biopesticides are of various types including living organisms, their products (phy-
tochemicals, microbial products), and byproducts (semiochemicals) (Dutta 2015).
Microbial biopesticides contribute in global biopesticide market with 30% share
(Thakore 2006; Cawoy et al. 2011). Although first commercial biopesticide
“Sporeine” based on Bacillus thuringiensis (Bt) was used in France in 1938, effec-
tive development and commercialization of microbial biopesticides was started by
the development and registration of “Thuricide,” as first registered commercial
product of B. thuringiensis in 1961. Biopesticides are target-specific, eco-friendly,
and effective solutions for the eradication of phytopathogenic diseases (Gupta and
Dikshit 2010; Kumar and Singh 2015). Biopesticides are used to protect various
crops (cereals, legumes, fruits, flowers, and ornamentals) from phytopathogenic
diseases. Presently biopesticides are gaining much attention and used as better alter-
natives of chemicals all over the world (Mishra et al. 2015).

various types of
biopesticides. (CPL
Business Consultants
2010)
Bacterial Viral
Fungal Others (nematodes)
In the global market, bacterial biopesticides have higher share in comparison

with other microbe-based products (Fig. 6.4). Most of the bacterial strains exploited
as biopesticides belong to the genera Bacillus and Pseudomonas (Fravel 2005).
Among various biopesticides, Bacillus-based products are considered as very popu-
lar and have been widely used (Schallmey et al. 2004). The most successful bacte-
rial biopesticides are B. thuringiensis (Bt) based which represent about 95% of total
market of biocontrol products (Bravo et al. 2011). Bt is specifically used for insect
pest control (Sanchis and Bourguet 2008). Other species of Bacillus used as biopes-
ticides are B. subtilis, B. licheniformis, and B. pumilus (Ongena and Jacques 2008).
Pseudomonas is also used as efficient and popular biopesticide (Ganeshan and
Kumar 2006). Among all Pseudomonas sp., fluorescent pseudomonads are reported
as important biopesticides in crop protection (Wilson et al. 1992; Fravel 2005).
Besides Bacillus and Pseudomonas, some other bacterial genera being used as
biopesticides are Agrobacterium, Azospirillum, Burkholderia, and Streptomyces,
which are commercially available in the market (Nakkeeran et al. 2005). Currently
biopesticides are being used all over the world, and their market share by geographi-
cal region is shown in Fig. 6.5. According to global market report of BCC research,
the total sale of biopesticide was $1.2 billion in 2008 and $1.6 billion in 2009 (BCC
Research 2010). According to PR Newswire (2017), the global biopesticide market
reached $3.7 billion in 2015 and nearly $4.0 billion in 2016. The market is projected
to gain at a CAGR of 14.1% from 2016 to 2021 and should reach $7.7 billion by
2021 (PR Newswire 2017).
150 M. Verma et al.

biopesticides in various
regions of world. (BCC
Research 2014)
North America Latin America

Europe Asia Pacific ROW
Future Roles of PGPR
To fulfil the food requirements of the growing world population, there is a need of a
suitable, economic, and beneficial approach which should not have side effects on
the environment. For the safe and sustainable agricultural future, there is a need to
produce sufficient amount of food crops with three main parameters: disease resis-
tance, stress tolerance, and high nutrient content (Arora et al. 2016a). PGPR appli-
cation can be an effective method for approaching this goal. PGPR impart a very big
role in increasing crop productivity by various beneficial processes, e.g., biofertil-
ization, biocontrol, bioremediation, and biofortification, which are important to
achieve agricultural sustainability for a better future (Rana et al. 2015; Shaikh and
Saraf 2017). Although PGPR are being used for crop production, their contribution
either as biofertilizers or biopesticides is very less at global level, hence by applying
various advanced techniques such as genomics, proteomics, metabolomics, and
nanotechnology, we can improve upon bioinoculant technology for better and reli-
able products (Vejan et al. 2016; Gouda et al. 2018). Various issues related with
plant-microbe interactions require more concern for better future approaches such
as advanced culture techniques for microbes (independent culture techniques),
diversity analysis of microbes, study of mechanism and genetic constructions of
plants and microbes, and the interaction of PGPR with plants at metabolic and
molecular levels. Some advanced inoculation methods can also be used for improv-
ing crop productivity, and in this regard Arora and Mishra (2016) suggested the
application of secondary metabolite-based formulations for high crop productivity.
Similarly, Timmusk et al. (2017) suggested that implementation of metabolomics of
microbiomes has potent capability to advance the quality and applications of bioin-
oculants in agriculture. Recently, Mitter et al. (2017) reported a new technique to
inoculate bioinoculants in plants: inoculating flowers to develop progeny seeds
which modify plant microbiomes and characters as per requirements. It is also sug-
gested that the integrated use of PGPR with other organic farming techniques
(Maheshwari et al. 2012b; Nazir et al. 2017) and seed biopriming techniques
(Mahmood et al. 2016) can also be focused for high crop productivity. Only explo-
ration and selection of efficient PGPR is not sufficient but also their proper registra-
tion, regulation, and effective delivery system are required (Arora et al. 2016b).
There is necessity to attract the farmers toward bioinoculants by selecting suitable
and reliable products; hence we can gain their faith in agrobiologicals.
Climate change is responsible for various problems and global warming is one of
them. Global warming causes reduction in crop production by causing hormonal
imbalances which has negative impacts on agriculture and global food security
(Lobell and Gourdji 2012). Global warming is increasing due to high emission of
carbon dioxide (CO2) in the atmosphere (Anderson et al. 2016). Soil systems work
as the largest sink of CO2, but due to high human interference, their deterioration
takes place which leads to the high release of CO2 in the atmosphere causing
enhanced global warming (Salam and Noguchi 2005). It is suggested by various
researchers that applications of microbial inoculants in agricultural crop produc-
tions can be used as sustainable tool to overcome the negative effect of climate
change as well as global warming (Dimkpa et al. 2009; Tewari and Arora 2013). It
is reported that maximum parts (90%) of plant biomass are derived from CO2 assim-
ilation by photosynthetic activity (Long et al. 2006) and photosynthetic rate of
plants is increased upon the application of biofertilizers (PGPR) (Mia and
Shamsuddin 2010; Mahanty et al. 2016). Hence it can be concluded that due to
PGPR inoculation, plants consume more CO2 which reduce the atmospheric CO2
level and global warming (Pendall et al. 2004; Nie et al. 2015). According to Nie
et al. (2015), the rate of microbial respiratory carbon loss is also reduced on the
application of PGPR which decreases global warming. Higher application of micro-
bial inoculants in agriculture minimizes the chemical load which also reduces the
risk of global warming. It is also reported that stress-tolerant PGPR significantly
help to maintain the soil fertility and reclamation of wastelands (Hrynkiewicz and
Baum 2011; Mishra et al. 2017b). It can be considered that due to the reclamation
of wastelands, sinks of CO2 are increased that cause reduction of atmospheric CO2
and global warming.
Conclusion
Extension of agriculture services in an eco-friendly manner is a key issue in present-

day era of increasing population and climate change. To attain surplus agricultural
production, farmers are still dependent on synthetic chemicals. However, indiscrim-
inate use of these harmful chemicals has only raised the problems. Soil microbes are
152 M. Verma et al.
always considered as chief components of soil fertility. In this context the use of
PGPR for enhancing plant growth, preventing deadly diseases, alleviating abiotic
and biotic stresses, and restoring soil health can be very useful. PGPR-based prod-
ucts such as biofertilizers and biopesticides are already being used at the global
level and found to be suitable alternatives to dangerous chemicals. There is a need
to explore PGPR now for purposes such as stress management, bioremediation, and
combating climate change (global warming). In recent years, considerable develop-
ments are visible in the field of plant-microbe interactions affirming their role in
solving key environmental problems. However, in agroecosystems, contribution of
PGPR is not fully exploited in accordance with economic and social needs. The
possibilities for their wide application in agriculture can increase by the advent of
newer techniques. A number of PGPR strains showing multifarious plant beneficial
activities are now known, but very few have been formulated in the form of bioin-
oculants. Hence a strong perspective focused on their extended use in remediation
of soil problems and diverse applicability in agroecosystems is required.
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Plant Growth-Promoting Rhizobacteria: Diversity and Applications

Chapter · January 2019

Maya Verma Jitendra Mishra

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Maya Verma, Jitendra Mishra, and Naveen Kumar Arora

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© Springer Nature Singapore Pte Ltd. 2019 129

effective in enhancing crop productivity in a sustainable way. The use of PGPR in

Keywords Rhizosphere · PGPR · Bioinoculants · Agriculture · Agroecosystem

Actinoplanes, Saccharopolyspora, and Verrucosispora are common genera of

Roles of PGPR in Rhizosphere

Fig. 6.1 Plant growth

Table 6.1 Direct mechanisms and PGPR used

Phytohormones act as chemical messengers and enhance plant growth by affecting

Ortíz-Castro et al. (2009) reported that cytokinin-producing Bacillus megaterium

Production of Volatile Organic Compounds (VOCs)

PGPR control the growth of pathogens by creating competitive environments for

Table 6.2 Indirect mechanisms and PGPR used

Production of metabolites is one of the potent and broad-spectrum mechanisms of

I nduced Systemic Resistance (ISR) and Systemic Acquired

Abiotic Stress Management

(2017) observed that on the application of arsenic (As)-tolerant PGPR (B.

Diverse Applications of PGPR

Fig. 6.2 Market shares of

Nitrogen fixers Phosphate solubilizers

Fig. 6.3 Market share of

North America Latin America

Fig. 6.4 Market share of

In the global market, bacterial biopesticides have higher share in comparison

Fig. 6.5 Market share of

North America Latin America

Future Roles of PGPR

Extension of agriculture services in an eco-friendly manner is a key issue in present-­

Asari, S. Y. (2015). Studies on plant-microbe interaction to improve stress tolerance in plants

Egamberdieva, D. (2012). Pseudomonas chlororaphis: A salt-tolerant bacterial inoculant for plant

Glick, B. R. (2012). Plant growth-promoting bacteria: Mechanisms and applications. Scientifica

Merzaeva, O. V., & Shirokikh, I. G. (2006). Colonization of plant rhizosphere by actinomycetes of

Nahas, E. (1996). Factors determining rock phosphate solubilization by microorganisms isolated

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Roles of PGPR in Rhizosphere

Production of Volatile Organic Compounds (VOCs)

I nduced Systemic Resistance (ISR) and Systemic Acquired

Abiotic Stress Management

Diverse Applications of PGPR

Future Roles of PGPR

Extension of agriculture services in an eco-friendly manner is a key issue in present-