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Current Perspectives on Plant GrowthPromoting Rhizobacteria
Javid A.Parray, Sumira Jan, Azra

N.Kamili, Raies A.Qadri, Dilfuza
Egamberdieva & Parvaiz Ahmad
Journal of Plant Growth Regulation
ISSN 0721-7595
J Plant Growth Regul
DOI 10.1007/s00344-016-9583-4
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Author's personal copy

DOI 10.1007/s00344-016-9583-4
Current Perspectives on Plant Growth-Promoting Rhizobacteria

Javid A. Parray1 Sumira Jan2 Azra N. Kamili1 Raies A. Qadri3
Dilfuza Egamberdieva4 Parvaiz Ahmad5
Received: 22 October 2015 / Accepted: 23 December 2015

Springer Science+Business Media New York 2016
Abstract The rhizosphere of plant species is an inimitable ecosystem that harbors an extensive range of
microbes. Research in the wide areas of rhizosphere
biotechnology highlighting new bioinoculants has received
ample attention during recent past, and suitable expertises
have been developed. However, the global recognition of
such technologies by farmers is still overwhelmed with
doubts owing to limited shelf-life and efficiency of the
products which demonstrate discrepancies. This review
illustrates plant growth-promoting rhizobacteria with
detailed emphasis on nutrient acquisition and potential
roles in conferring tolerance against abiotic stresses. The
review demonstrates the recent research in the field of
genomic and proteomic analysis, where systematic characterization of potentially effective rhizobacteria is being
carried out by screening the extensive bacterial gene pool
based on modern molecular tools. The review concludes by
emphasizing the efforts made in the proteomics field which
could compensate for understanding of prompt evolution in
& Parvaiz Ahmad

parvaizbot@yahoo.com
1
Center for Research and Development (CORD), University of

Kashmir, Srinagar, Jammu and Kashmir, India
ICAR- Central Institute of Temperate Horticulture, Rangreth,

Srinagar, Jammu and Kashmir, India
Department of Biotechnology, University of Kashmir,

Srinagar, Jammu and Kashmir, India
Department of Microbiology and Biotechnology, Faculty of

Biology and Soil Science, National University of Uzbekistan,
Tashkent, Uzbekistan
Department of Botany, S.P. College, Srinagar,

Jammu and Kashmir, India
microbe-derived and plant-derived protein and metabolite

substitute that activates vulnerability or resistance.
Keywords Plant growth-promoting rhizobacteria
(PGPR) Abiotic stress Tolerance Genomic analysis
Proteomic analysis Salinity
Introduction
The term rhizosphere comes from Greek word rhiza
meaning root and is used to illustrate the fraction of soil in
which growth of microbes is influenced by the existence of
the root system (Hiltner 1904). The rhizosphere bacteria, the
so-called rhizobacteria, can be broadly categorized as those
having symbiotic relationships with plants but not contributing to the soil profile. These are free living and directly
related with the root surface or inhabit inside the roots such as
endophytic bacteria (Kloepper and Beauchamp 1992). When
the existence of rhizobacteria assists in plant growth, those
rhizobacteria are defined as plant growth-promoting rhizobacteria (PGPR) (Kloepper and others 2004). To exert
their advantageous effects in the root system, bacteria must
be rhizosphere competent, that is, capable of competing with
other rhizospheric microbes for nutrients secreted by the root
and for sites that can be occupied on the root (Hao and others
2012b; Kim and others 2012). Moreover, PGPR have an
innate characteristic property of associating with other
microbes like arbuscular mycorrhizal fungi (AMF) to form a
tripartite interaction, which promotes plant growth. Along
with the soil microbes other than AMF, PGPR are apt to
manipulate both plant growth and plantAMF relationships
mostly via indirect mechanisms through an increase in soil
nutrient availability (Ghignone and others 2012; Pii and
others 2015), whereas their direct effect on plant growth is
123

still under debate (Glick 2012). Nevertheless, few studies

have assessed the effects of either AMF or other plant
growth-promoting microorganisms on plant metabolic
pathways, and most that have been conducted under controlled greenhouse conditions in sterilized natural media as a
control (Lekberg and Koide 2014; Glaeser and others 2015)
have analyzed only target compounds (Walker and others
2011; Salvioli and others 2015).
In this context, there is ongoing research aimed at
investigating an extensive variety of rhizobacteria possessing novel beneficial qualities like heavy metal detoxification
(Barea and others 2013a), pesticide degradation/tolerance
(Carvalhais and others 2013), salinity tolerance (Bashan and
others 2014), biocontrol of phytopathogens and insects (Pii
and others 2015) together with plant growth-promoting traits
for instance, phytohormone (Barea and others 2013b;
Lugtenberg 2015; Parray and others 2013, 2015), siderophore (Bakker and others 2013), 1-aminocyclopropane-1carboxylate, hydrogen cyanate (HCN), and ammonia production, and nitrogenase activity (Olivares and others 2013;
Barea and Richardson 2015), and phosphate solubilization
(Browne and others 2013; Barea and others 2013a). This
review focuses on rhizospheric microbes that are advantageous for the plant.
In this review, we commence with the mechanisms
including direct and indirect strategies employed by specialized beneficial rhizobacteria to influence plant growth
positively. We will follow up the review with emphasis on
the potential role of PGPR in conferring tolerance to plants
under various stresses. Currently, the advancement and
expansion of molecular techniques present more precise
information of bacteria in their innate environment
assembling more elicit scenarios of microbial ecology and
producing new-fangled issues about the functions of bacteria in the rhizosphere. Progress in genomics including
whole genome sequencing of various PGPR strains helps
us develop our perceptive of the microbial communities at
an advanced upshot. This review provides an outline of the
current awareness on the study of the bacterial community
in the rhizosphere via modern molecular techniques,
relating the preconception of conventional molecular
techniques, subsequent generation sequencing platforms
and post-genomics techniques. The review will conclude
with impending succession for further progress in PGPR
through the advancement in proteomics.
PGPR and Their Potential in Improving Plant

Tolerance
In a natural environment, most of the mechanisms used by
PGPR for growth enhancement are common, whereas under
stress conditions, some strains may not be able to perform
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efficiently due to their inability to survive and compete in the

harsh environment. However, certain PGPR strains not only
tolerate stress conditions but also have the ability to promote
plant growth under stressful environments.
Heavy Metal
Accumulation of heavy metals in the soil environment and
their uptake by both plant growth-promoting rhizobacteria
and plants is a matter of environmental concern. For survival in a metal stressed environment, plant growth-promoting rhizobacteria have evolved several mechanisms by
which they can immobilize, mobilize, or transform metals
rendering them inactive to tolerate the uptake of heavy
metal ions (Ting 2015).
The rhizospheric soil zone is an imperative territory for
microbes including bacteria, fungi, algae, and protozoa (Hao
and others 2012a). Plant cells are closely associated with
microbial cells that expand as bio film over the root surface
generating signal molecules and resulting in a phenomenon
defined as quorum sensing (Daniels and others 2004). This
ability of microbes to sense the surrounding environment
plays an imperative role in nutrient efficiency and can
counteract the deleterious effects of heavy metals on plants.
Some of the rhizospheric microbes can directly degrade the
organic as well as inorganic pollutants via their diverse
dilapidation traits like volatilization, transformation and
rhizodegradation, EPS sequestration, metal complexation,
and enzymatic detoxification (Gadd 2010; Tangahu and
others 2011; Pavel and others 2013). Moreover, some PGPR
have the potential to reduce ethylene levels, resulting in
enhanced plant growth. This can be ascribed to ACC
deaminase, which hydrolyzes ACC, the biosynthetic precursor for ethylene in plants, into ammonia and a-ketobutyrate (Ullah and others 2015a). PGPR increase the
phytoextraction ability of plants by improving heavy metal
mobility and increasing their bioavailability through the
release of chelating agents, acidification, phosphate solubilization, and redox changes (Ullah and others 2015b). An
extensive range of PGPR has been identified as most efficient candidates in phytoremediation (Glick 2010). Jing and
others (2014) isolated Enterobacter sp. 192 and Klebsiella
sp., strains which were later inoculated with Brassica napus
L. for heavy metal accumulation. The strains not only
improved the growth of Brassica napus L. but also resulted
in bioaccumulation of Cd, Pb and Zn. Yong and others
(2014) enhanced the efficiency of phytoremediation of
heavy metals through the development of a recombinant
strain KT2440-spPCS. This strain was developed through
the cloning of phytochelatin synthase (PCS) genes from
Schizosaccharomyces pombe expressed in Pseudomonas
putida KT2440. The recombinant strain KT2440-spPCS
exhibited enhanced resistance to Hg, Cd, and Ag, and a 3- to

5-fold increase in Cd accumulation, which led to an increase

in the efficiency of phytoremediation of heavy metals. In
addition, engineered bacteria resulted in significantly 221
enhanced germination and growth of wheat, which indicates
that Pseudomonas putida KT2440 222 uses symbiosis for
enhanced phytoremediation of heavy metals. Some PGPR
produce organic acids, for example, gluconic, oxalic, and
citric acids, which play an imperative role in mobilization
and solubilization and complexation of heavy metals (Rajkumar and others 2012; Ullah and others 2015a, b). In
addition, biosurfactants are integral metabolites produced by
PGP bacteria that have the potential to improve metal
mobilization and phytoremediation. These biosurfactants
released by PGP bacteria enhance metal solubility and
bioavailability via metal complexation (Rajkumar and others 2012). Microbes can activate metal translocation through
biomethylation, which can result in volatilization. Several
PGPR can mediate the methylation of Pb, Hg, Se, As, Tn,
and Sn. These bacteria can transfer a methyl group to the
metals, resulting in volatile methylated metal compounds
that can easily excavate the soil zone (Bolan and others
2014). Several PGPR act as bio control agents by producing
antimicrobial metabolites like HCN, pyrrolnitrin, phenazines, pyoluteorin, 2,4-diacetylphloroglucinol, tensin, and
viscosinamide (Ahemad and Kibret 2014). On the whole,
these PGPR bacteria modulate plantsoil chemistry, which
in turn pave the way towards the phytoremediation process.
Salinity
Soil salinity is an important limiting factor for agricultural
crops especially in arid and semi-arid regions of the world.
Although many technologies have been implicated in the
improvement of salt tolerance, only PGPR-elicited plant
tolerance against salt stress has been previously studied.
Yang and others (2009) reported reduced ethylene content
in tomato seedlings thriving under high salinity by application of Achromobacter piechaudii, indicating that bacterial ACC deaminase was functional. A. piechaudii, which
produces ACC, increased the growth of tomato seedlings
by as much as 66 % in the presence of high salt contents.
Zhang and others (2010) demonstrated induced systemic
tolerance to osmotic stress when Arabidopsis was inoculated with the beneficial soil bacterium Bacillus subtilis (strain GB03). Moreover, Bacillus subtilis (strain
GB03) produced a blend of volatile organic compounds
like 2,3-butanediol and its precursor 3-hydroxy-2-butanone, which are known to promote plant growth (Farag
and others 2013). Among the 600 Arabidopsis genes isolated by transcriptome analysis, transcriptional expression
of high-affinity K? TRANSPORTER 1 (HKT1), which
controls Na? import in roots, was decreased. HKT1 has
been shown to adjust Na? and K? levels differentially,
depending on the plant tissue. Exposure of an athkt1

mutant to bacterial VOCs not only resulted in typical salt
stress phenotypes, such as stunting, but also led to the
inhibition of seedling growth. Transcriptional validation
revealed that bacterial volatile organic compounds (VOCs)
down-regulated HKT1 expression in roots but upregulated
it in shoot tissues, thereby orchestrating lower Na? levels
in the whole plant. Furthermore, there is no difference in
induced systemic tolerance (IST) to salt stress in the Na?export mutant salt overly sensitive3 (sos3), suggesting that
HKT1 functions in shoots to retrieve Na? from the xylem,
thereby facilitating shoot-to-root Na? recirculation. Overall, plant perception of bacterial VOC causes a tissuespecific regulation of HKT1 that controls Na? homeostasis
under salt stress (Yang and others 2009). Jha and Subramanian (2014) reported a defensive response of two rootassociated
bacteria Pseudomonas
pseudoalcaligenes and Bacillus pumilus in the salt-sensitive rice cultivar
GJ17. This study demonstrated PGPR can modulate lipid
peroxidation and superoxide dismutase activity in the saltsensitive GJ17 cultivar thriving in saline soils. This
research report confirmed that the inoculation of paddy
(Oryza sativa) with bacteria could enhance salt tolerance
via reduced toxicity through reactive oxygen species by
reducing the plant cell membrane index, cell caspase-like
protease activity, and programmed cell death and consequently leading to improved cell viability.
Under stress conditions, plant growth is also affected by
nutritional imbalances. For example, in saline conditions,
an elevated level of sodium (Na?) not only disturbs the
uptake of other nutrients but also causes specific ion toxicity
(Ashraf and Harris 2013). Certain PGPR strains also have
the ability to protect plants from the harmful effects of high
Na? concentrations in a saline soil environment (Suarez and
others 2015; Baha and Bekki 2015; Younesi and Moradi
2014). Several researchers have demonstrated the positive
effect of rhizobacteria in terms of alleviating the negative
impact of salinity on crop growth under laboratory as well
as field conditions (Ashraf and others 2013). One of the
common hypotheses employed in most of the studies conducted under salinity stress was the lowering of ethylene
levels by the ACC deaminase activities of PGPR. These
studies conducted under both controlled and natural environments showed that inoculation with PGPR containing
ACC deaminase significantly increased plant growth and
yield compared to that of controls. Yue and others (2007)
have shown that inoculation with Klebsiella oxytoca (Rs-5)
containing ACC deaminase enhanced the absorption of
major nutrients such as N, P, K, and Ca and promoted plant
growth by mitigating the negative effects of salt stress. The
inoculation with Pseudomonas spp. improved the growth of
eggplant by decreasing the uptake of Na? and enhancing the
activities of antioxidant enzymes under salinity stress
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conditions (Fu and others 2010). According to this study,

regulation of mineral uptake and increase in antioxidant
enzyme activities may be the two key mechanisms involved
in alleviation of salt stress. Although PGPR can enhance
plant growth under normal as well as stress conditions,
however, they have a differential potential for improving
plant growth and development. Egamberdiyeva (2007)
reported three PGPR isolates P. alcaligenes PsA15, Bacillus polymyxa BcP26 and Mycobacterium phlei MbP18 are
capable of tolerating intense temperature and high salt
concentrations conferring tolerance to plants under arid and
saline soils such as calcisol. In addition, Yao and others
(2010) demonstrated improved growth and germination in
cotton under saline conditions when inoculated with P.
putida Rs 198. Likewise, Upadhyay and others (2011)
reported co-inoculation with B. subtilis and Arthrobacter
sp. could alleviate the adverse effects of soil salinity on
wheat growth with an increase in dry biomass, total soluble
sugars, and proline content. Nia and others (2012) showed
that inoculation with saline-adapted Azospirillum strains
resulted in increased salinity tolerance and higher grain
productivity of wheat plants. Similarly, Ramadoss and
others (2013) reported inoculation with halotolerant bacterial strains including Halobacillus sp. and B. halodenitrificans can ameliorate salt stress and increase grain yield and
growth of wheat. Intensive selection of halotolerant
bioinoculants could lead to development of salt tolerant
crops which could advance the research towards bioengineering of susceptible plant lines.
Drought
Drought stress limits the growth and productivity of crops,
particularly in arid and semi-arid areas (Shanker and others
2014). Early studies on induced systemic tolerance to drought
reported that inoculation with the PGPR Bacillus licheniformis K11 enhanced the drought tolerance of pepper (Lim
and Kim 2013). Another PGPR strain, Achromobacter piechaudii ARV8, which produces 1-aminocyclopropane-1carboxylate (ACC) deaminase, conferred induced systemic
tolerance to drought stress in pepper (Capsicum annuum L.)
and tomato (Solanum lycopersicum L.) plants (Mayak and
others 2004). Under stress conditions, including drought, the
plant hormone ethylene endogenously regulates plant homeostasis and results in reduced root and shoot growth (Glick and
others 2007). The rhizobia are sensitive to drought stress,
resulting in a significant decrease of N2 fixation when faced
with low soilwater content. Under drought stress, co-inoculation of bean (Phaseolus vulgaris L.) with Rhizobium
tropici and two strains of P. polymyxa resulted in increased
plant height, shoot dry weight, and nodule number (Figueiredo and others 2011). Interestingly, the effect on IST and
increased nodule number was greater when a mixture of two
123
strains of P. polymyxa was applied than a single strain, suggesting some synergistic effects from the use of strain mixtures. Investigations into how drought stress affects plant
hormone balance revealed an increase in abscisic acid (ABA)
content in the leaves, indicating that reduction of endogenous
cytokinin levels magnifies ABA content, eliciting stomata
closure (Figueiredo and others 2008). It will be interesting to
determine whether cytokinin produced by P. polymyxa affects
ABA signaling of plants or rhizobia-elicited nodulation
(Figueiredo and others 2008). Co-inoculation of lettuce
(Lactuca sativa L.) with the PGPR Pseudomonas mendocina
and arbuscular mycorrhizal fungi (Glomus intraradices or G.
mosseae) augmented an antioxidant catalase under severe
drought conditions, suggesting that they can be used in
inoculants to alleviate the oxidative damage elicited by
drought (Kohler and others 2009).
PGPR strains are not only effective for improving plant
growth under salinity stress but are also helpful for
enhancing plant growth and development under heavy
metals, flooding, and drought stress (Glick and others
2007). Sandhya and others (2009) demonstrated that rhizobacteria having the ability to produce exopolysaccharides can be used effectively for enhancing drought
resistance in sunflower plants. Figueiredo and others
(2008) evaluated the effect of co-inoculation with Paenibacillus polymyxa and Rhizobium tropici on growth,
nitrogen content, and nodulation of common bean
(Phaseolus vulgaris L.) under a water-deficit environment.
The results showed that co-inoculation enhanced plant
growth, nitrogen content, and nodulation of bean under
drought stress compared to uninoculated controls. To
commercialize the PGPR inocula, the effectiveness of
PGPR has also been evaluated in the field. In a field trial,
under water stress conditions, PGPR inoculation enhanced
the proline, chlorophyll, and water content of basil (Ocimum basilicum L.) under stress conditions (Heidari and
Golpayegani 2012). The PGPR were not only effective
under water stress conditions but also proved helpful for
enhancing plant growth under salinity stress. Cohen and
others (2015) reported the positive changes in drought
affected Arabidopsis when inoculated with Azospirillum
brasilense Sp 245 strain. The authors demonstrated altered
root architecture, stimulated photosynthetic and photoprotective pigments and retarded water loss in correlation with
enhanced ABA levels. Overall, PGPR alleviate effects of
drought stress on plants via rhizobacterial-induced drought
endurance and resilience (RIDER) encompassing both
physiological and biochemical modulations. Several
RIDER methods include alterations in phytohormonal
levels, antioxidant defense, bacterial exopolysaccharides
(EPS), and numerous metabolites that contribute to osmotic
adjustment including sugars, polyamines, and amino acids.
In addition, a specific set of volatile organic compounds

(VOCs) and proteins like heat-shock proteins (HSPs) and

dehydrins play an imperative role in acquirement of
drought tolerance. Assortment, assessment, and relevance
of drought-stress-tolerant PGPRs to crops can help surmount productivity limits in drylands.
Mechanism of Action of PGPR

According to Kloepper and Schroth (1981), PGPR-mediated plant growth promotion occurs by the alteration of the
whole microbial community in the rhizosphere niche
through the production of various substances (Kloepper
and Schroth 1981). Generally, PGPR promote plant growth
directly by either facilitating resource acquisition like
nitrogen, phosphorus, and essential minerals via biological
nitrogen fixation, phosphate solubilization, and iron
sequestration by siderophore, respectively, or modulating
plant hormone levels such as auxins, gibberellins (GAs),
cytokinins (CK), and nitric oxide (NO), or indirectly with
rhizosphere competition, induced systemic resistance
(ISR), and biosynthesis of stress-related phytohormones
like jasmonic acid (JA), cadaverine (Cad), or the ethylene
catabolism-related enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase. In current years, it has been
evident that root colonization definitely is requisite for
various biocontrol mechanisms, for instance, antibiosis
(Chin-A-Woeng and others 1998) and CNN (competition
for nutrients and niches) (Kamilova and others 2005;
Validov and others 2009). One of the possible reasons may
be due to the production of exopolysaccharides. The
exopolysaccharides so produced reduce Na? uptake in the
plant by binding it and also by biofilm formation (Khodair
and others 2008; Qurashi and Sabri 2012).
Direct Mechanisms
Direct PGPR enhance plant growth in the absence of
pathogens. In accordance with Vessey (2003), soil bacterial
species in the plant rhizosphere which grow in, on, or
around plant tissues stimulate plant growth by a plethora of
mechanisms. In addition to providing the mechanical
support and facilitating water and nutrient uptake, microbial activity in the rhizosphere affects rooting patterns and
the supply of available nutrients to plants (Fig. 1).
Nutrient Acquisition
A fraction of these plant-derived small organic molecules
is further metabolized by microorganisms in the vicinity as
carbon and nitrogen sources, and some microbe-oriented
molecules are subsequently re-taken up by plants for
growth and development (Kang and others 2010).
Nitrogen Fixation
Biological N2 fixation (BNF) refers to conversion of
nitrogen to ammonia by nitrogen fixing microorganisms
using a complex enzyme system known as nitrogenase
(Kim and Rees 1994). In fact, BNF accounts for approximately two-thirds of the nitrogen fixed globally. Nitrogen
fixing organisms are generally categorized as (a) symbiotic
N2 fixing bacteria including members of the family rhizobiaceae which form symbioses with leguminous plants (for
example, rhizobia) (Ahemad and Khan 2012a; Zahran
2001) and non-leguminous trees (for example, Frankia),
and (b) non-symbiotic (free living, associative, and endophytes) nitrogen fixing form such as cyanobacteria (Anabaena,
Nostoc),
Azospirillum,
Azotobacter,
Gluconacetobacter diazotrophicus, and Azoarcus (Bhattacharyya and Jha 2012). However, non-symbiotic nitrogen
fixing bacteria provide only a small amount of the fixed
nitrogen that the bacterially associated host plant requires
(Glick 2012). Plant growth-promoting rhizobacteria that fix
N2 in non-leguminous plants are also called diazotrophs
capable of forming a non-obligate interaction with host
plants (Glick and others 1999). Most biological nitrogen
fixation is carried out by the activity of molybdenum
nitrogenase, which is found in all diazotrophs (Bishop and
Jorerger 1990). In addition to Rhizobia spp., a number of
free-living bacteria, for example, Azospirillum spp., are
also able to fix nitrogen and provide it to plants (Wisniewski-Dye and others 2015). However, it is generally
believed that free-living bacteria provide only a small
amount of the fixed nitrogen that the bacterially associated
host plant requires. Nitrogenase (nif) genes required for
nitrogen fixation include structural genes, genes involved
in activation of the Fe protein, iron molybdenum cofactor
biosynthesis, electron donation, and regulatory genes
required for the synthesis and function of the enzyme
(Bruto and others 2014). In diazotrophic (nitrogen fixing)
bacteria, nif genes are typically found in a cluster of around
2024 kb with seven operons encoding 20 different proteins (Glick 2012).
Phosphate Solubilization
Phosphorus (P), the second most important plant growthlimiting nutrient after nitrogen, is abundantly available in
soils in both organic and inorganic forms (Khan and others
2009). This low availability of phosphorous to plants is
because the majority of soil P is found in insoluble forms,
whereas plants absorb it only in two soluble forms, the
monobasic (H2PO4) and the diabasic (H2PO4) ions (Bhattacharyya and Jha 2012). To overcome P deficiency in
soils, there are frequent applications of phosphatic fertilizers in agricultural fields. Plants absorb low amounts of
123

Fig. 1 Schematic
representation of PGPR and
their beneficial effects on plant
metabolomics
applied phosphatic fertilizers, and the rest are rapidly

converted into insoluble complexes in the soil (Mckenzie
and Roberts, 1990). But regular application of phosphate
fertilizers is not only costly but is also environmentally
undesirable (Kaur and Reddy 2014). This has led to a
search for an ecologically safe and economically reasonable option for improving crop production in low P soils. In
this context, organisms coupled with phosphate-solubilizing activity, often termed phosphate-solubilizing microorganisms (PSM), may provide the available forms of P to
the plants and hence a viable substitute to chemical phosphatic fertilizers (Khan and others 2006). Of the various
PSM(s) inhabiting the rhizosphere, phosphate-solubilizing
bacteria (PSB) are considered as promising biofertilizers
because they can supply plants with P from sources
otherwise poorly available by various mechanisms (Zaidi
and others 2009). Bacterial genera like Azotobacter,
Bacillus, Beijerinckia, Burkholderia, Enterobacter, Erwinia, Flavobacterium, Microbacterium, Pseudomonas, Rhizobium, and Serratia are reported as the most significant
phosphate-solubilizing bacteria (Bhattacharyya and Jha
2012; Yadav and others 2014). Rhizobacteria can solubilise
inorganic P sources and enhance growth and yield of crop
plants. Examples of some widely reported P solubilising
microbial species intimately associated with a large number of agricultural crops like potato, tomato, wheat, and
radish are Azotobacter chroococcum (Kumar and others
2001), Bacillus circulans and Cladosporium herbarum
123
(Singh and Kapoor 1999), Bradyrhizobium japonicum

(Antoun and others 1998), Enterobacter agglomerans (Kim
and others 1998), Pseudomonas chlororaphis and P. putida
(Cattelan and others 1999), and Rhizobium leguminosarum
(Chabot and others 1998). The ability of PGPRs to solubilize mineral phosphate, therefore, has been of immense
interest to agricultural microbiologists since it can enhance
the availability of phosphorus for effective plant growth.
PGPRs have been recorded to solubilize precipitated
phosphates to plants, representing a possible mechanism of
plant growth promotion under field conditions (Verma and
others 2001; Guo and others 2015). Synthesis of organic
acids by rhizosphere microorganisms could be the possible
reason for solubilization of inorganic P sources (Barea and
Richardson 2015). Unfortunately, because of variable
results, the commercial application of phosphate-solubilizing PGPB has been quite limited. In fact, the most
consistent positive effects of applying phosphate-solubilizing bacteria are seen when these bacteria are co-inoculated with bacteria with other physiological capabilities
such as fixation, or with mycorrhizal or non-mycorrhizal
fungi (Rojas and others 2001; Ghosh and others 2014).
Siderophore Production
Iron is a vital nutrient for almost all forms of life. All
microorganisms known hitherto, with the exception of
certain lactobacilli, essentially require iron (Neilands

1995). In the aerobic environment, iron occurs principally

as Fe3? and is likely to form insoluble hydroxides and
oxyhydroxides, thus making it generally inaccessible to
both plants and microorganisms (Rajkumar and others
2010). Commonly, bacteria acquire iron by the secretion of
low-molecular mass iron chelators referred to as siderophores which have high association constants for complexing iron (Ahmed and Holmstrom 2014). Most of the
siderophores are water soluble and can be divided into
extracellular siderophores and intracellular siderophores.
Generally, rhizobacteria differ regarding siderophore crossutilizing ability; some are proficient in using siderophores
of the same genus (homologous siderophores), whereas
others can utilize those produced by other rhizobacteria of
different genera (heterologous siderophores) (Khan and
others 2009). In both Gram-negative and Gram-positive
rhizobacteria, iron (Fe3?) in Fe3?-siderophore complexes
on bacterial membranes is reduced to Fe2? which is further
released into the cell from the siderophore via a gating
mechanism linking the inner and outer membranes. During
this reduction process, the siderophore may be destroyed/
recycled (Rajkumar and others 2010; Neilands 1995).
Thus, siderophores act as solubilizing agents for iron from
minerals or organic compounds under conditions of iron
limitation (Indiragandhi and others 2008). Not only iron
but also siderophores form stable complexes with other
heavy metals that are of environmental concern, such as Al,
Cd, Cu, Ga, In, Pb, and Zn, as well as with radionuclides
including U and Np (Neubauer and others 2000). Binding
of the siderophore to a metal increases the soluble metal
concentration (Rajkumar and others 2010). Hence, bacterial siderophores help alleviate the stresses imposed on
plants by high soil levels of heavy metals. Plants assimilate
iron from bacterial siderophores by means of different
mechanisms, for instance, chelation and release of iron, the
direct uptake of siderophore-Fe complexes, or by a ligand
exchange reaction (Schmidt 1999). Numerous studies of
plant growth promotion vis-a-vis siderophore-mediated Feuptake as a result of siderophore-producing rhizobacterial
inoculations have been reported (Rajkumar and others
2010). For example, Crowley and Kraemer (2007) revealed
a siderophore-mediated iron transport system in oat plants
and inferred that siderophores produced by rhizosphere
microorganisms deliver iron to oats, which have mechanisms for using Fe-siderophore complexes under ironlimited conditions. Similarly, the Fe-pyoverdine complex
synthesized by Pseudomonas fluorescens C7 was taken up
by Arabidopsis thaliana plants, leading to an increase of
iron inside plant tissues and to improved plant growth
(Vansuyt and others 2007). Recently, Sharma and others
(2003) assessed the role of the siderophore-producing
Pseudomonas strain GRP3 on iron nutrition of Vigna
radiata. After 45 days, the plants showed a decline in
chlorotic symptoms and iron chlorophyll a and chlorophyll

b content increased in strain GRP3-inoculated plants
compared to controls. Different PGPR strains of Rhizobium
meliloti have been reported to produce siderophores (Arora
and others 2001) in iron stress conditions and therefore
added an advantage to exclude the pathogen,
Macrophomina phaseolina, causing charcoal rot of
groundnut. Some bacterial strains that do not employ any
other means of biocontrol can act as biocontrol agents
using the siderophores that they produce. In this case,
siderophores from PGPB can prevent some phytopathogens
from acquiring a sufficient amount of iron, thereby limiting
their ability to proliferate (Rajkumar and others 2010).
Phytohormone Production
PGPR can alter root architecture and promote plant
development with the production of different phytohormones like IAA, gibberellic acid, and cytokinins (Kloepper
and others 2007). Several PGPR as well as some pathogenic, symbiotic, and free-living rhizobacterial species are
reported to produce IAA and gibberellic acid in the rhizospheric soil and therefore play significant roles in
increasing the root surface area and number of root tips in
many plants (Han and others 2005). Similarly, significant
shoot growth in maize and rice dwarf mutants was promoted by gibberellin-like substances excreted by Azospirillum spp. (Boiero and others 2007). Microbial synthesis of
the phytohormone auxin (indole-3-acetic acid/indole acetic
acid/IAA) has been known for a long time. It is reported
that 80 % of microorganisms isolated from the rhizosphere
of various crops possess the ability to synthesize and
release auxins as secondary metabolites. Generally, IAA
secreted by rhizobacteria interferes with many plant
developmental processes because the endogenous pool of
plant IAA may be altered by the acquisition of IAA that has
been secreted by soil bacteria (Glick 2012; Spaepen and
others 2007). Evidently, IAA also acts as a reciprocal
signaling molecule affecting gene expression in several
microorganisms. Consequently, IAA plays a very important role in rhizobacteriaplant interactions (Spaepen and
Vanderleyden 2011). Moreover, down-regulation of IAA
as signaling is associated with plant defense mechanisms
against a number of phytopathogenic bacteria as evidenced
in enhanced susceptibility of plants to the bacterial
pathogen by exogenous application of IAA or IAA produced by the pathogen (Spaepen and Vanderleyden 2011).
IAA has been implicated in virtually every aspect of plant
growth and development, as well as defense responses.
This diversity of function is reflected by the extraordinary
complexity of the IAA biosynthetic, transport, and signaling pathways (Santner and others 2009). Generally, IAA
affects plant cell division, extension, and differentiation;
123

stimulates seed and tuber germination; increases the rate of

xylem and root development; controls processes of vegetative growth; initiates lateral and adventitious root formation; mediates responses to light, gravity and
florescence; and affects photosynthesis, pigment formation,
biosynthesis of various metabolites, and resistance to
stressful conditions. IAA produced by rhizobacteria likely
interferes with the above physiological processes of plants
by changing the plant auxin pool. Moreover, bacterial IAA
increases root surface area and length, and therefore provides the plant greater access to soil nutrients. Also, rhizobacterial IAA loosens plant cell walls and as a result
facilitates an increasing amount of root exudation that
provides additional nutrients to support the growth of rhizosphere bacteria (Glick 2012). Thus, rhizobacterial IAA is
identified as an effector molecule in plantmicrobe interactions, both in pathogenesis and phytostimulation (Spaepen and Vanderleyden 2011). An important molecule that
alters the level of IAA synthesis is the amino acid tryptophan, identified as the main precursor for IAA, and thus
plays a role in modulating the level of IAA biosynthesis
(Zaidi and others 2009). Strangely, tryptophan stimulates
IAA production, whereas anthranilate, a precursor for
tryptophan, reduces IAA synthesis. By this mechanism,
IAA biosynthesis is fine-tuned because tryptophan inhibits
anthranilate formation by a negative feedback regulation
on anthranilate synthase, resulting in an indirect induction
of IAA production (Spaepen and others 2007). However,
supplementation of culture media with tryptophan increases IAA production by most of the rhizobacteria (Spaepen
and Vanderleyden 2011). Biosynthesis of tryptophan starts
from the metabolic node chorismate in a five-step reaction
encoded by the trp genes. The branch point compound
chorismate is synthesized starting from phosphoenolpyruvate and erythrose 4-phosphate in the Shikimate pathway, a
common pathway for mechanisms and applications of plant
growth-promoting rhizobacteria: current perspective of the
biosynthesis of aromatic amino acids and many secondary
metabolites (Spaepen and Vanderleyden 2011; Merino and
others 2008; Dosselaere and Vanderleyden 2001). Starting
with tryptophan, at least five different pathways have been
described for the synthesis of IAA, and most pathways
show similarity to those described in plants, although some
intermediates can differ (Spaepen and Vanderleyden 2011;
Patten and Glick 1996): (1) IAA formation via indole-3pyruvic acid and indole-3-acetic aldehyde is found in a
majority of bacteria like Erwinia herbicola; saprophytic
species of the genera Agrobacterium and Pseudomonas;
certain representatives of Bradyrhizobium, Rhizobium,
Azospirillum, Klebsiella, and Enterobacter. (2) The conversion of tryptophan into indole-3-acetic aldehyde may
involve an alternative pathway in which tryptamine is
formed as in Pseudomonads and Azospirilla. (3) IAA
123
biosynthesis via indole-3-acetamide formation is reported

for phytopathogenic bacteria Agrobacterium tumefaciens,
Pseudomonas syringae, and E. herbicola; saprophytic
Pseudomonads (for example, Pseudomonas putida and P.
fluorescens). (4) IAA biosynthesis that involves tryptophan
conversion into indole-3-acetonitrile is found in the
cyanobacterium (Synechocystis sp.). (5) The tryptophanindependent pathway, more common in plants, is also
found in Azospirilla and cyanobacteria. Most rhizobium
species have been shown to produce IAA (Ahemad and
Khan 2011, 2012b). Because IAA is involved in multiple
processes including cell division, differentiation, and vascular bundle formation, these three processes are also
essential for nodule formation. Hence, it seems likely that
auxin levels in the host legume plants are necessary for
nodule formation (Glick 2012; Spaepen and others 2007).
It is also reported that the inoculation with Rhizobium
leguminosarum bv. viciae, wherein the IAA biosynthetic
pathway had been introduced, produced potential nitrogen
fixing root nodules containing up to 60-fold more IAA than
nodules formed by the wild-type counterpart in Vicia hirsute (Camerini and others 2008). Environmental stress
factors which modulate the IAA biosynthesis in different
bacteria include acidic pH, osmotic and matrix stress, and
carbon limitation (Spaepen and others 2007). Among
genetic factors, both the location of auxin biosynthesis
genes in the bacterial genome (either plasmid or chromosomal) and the mode of expression (constitutive versus
induced) have been shown to affect the level of IAA production. The location of auxin biosynthesis genes can
affect the IAA level, as plasmids are mostly present in
multiple copies. This can be illustrated by the difference in
the IAA level between the rhizobacterial strains, Pseudomonas savastanoi pv. savastanoi and P. syringae pv.
syringae. In the former strain, the genes for auxin biosynthesis are present on a plasmid, whereas in the latter one,
the corresponding genes are located on the chromosomal
DNA, resulting in a lower IAA production. The IAA production in P. syringae pv. Syringae could be increased
many fold by introducing a low-copy plasmid, carrying the
IAA biosynthetic operon (Spaepen and Vanderleyden
2011; Spaepen and others 2007; Patten and Glick 1996).
Involvement of PGPR-formulated cytokinins was also
observed in root initiation, cell division, cell enlargement,
and increase in root surface area of crop plants through
enhanced formation of lateral and adventitious roots
(Werner 2005). It has been established that the working
pathways of these phytostimulators leading to overall
development in crop plants are differently regulated by
catabolite repression (Zaidi and others 2009) as a physiological regulator of biofilm formation. Generally, ethylene
is an essential metabolite for the normal growth and
development of plants (Khalid and others 2006). This plant

growth hormone is produced endogenously by approximately all plants and is also produced by different biotic
and abiotic processes in soils and is important in inducing
multifarious physiological changes in plants. Apart from
being a plant growth regulator, ethylene has also been
established as a stress hormone (Saleem and others 2007).
Under stress conditions like those generated by salinity,
drought, water logging, heavy metals, and pathogenicity,
the endogenous level of ethylene is significantly increased
which negatively affects overall plant growth. For instance,
a high concentration of ethylene induces defoliation and
other cellular processes that may lead to reduced crop
performance (Saleem and others 2007; Bhattacharyya and
Jha 2012).
ACC Deaminase Activity
Plant growth-promoting rhizobacteria that possess the
enzyme,
1-aminocyclopropane-1-carboxylate
(ACC)
deaminase facilitate plant growth and development by
decreasing ethylene levels, inducing salt tolerance and
reducing drought stress in plants (Nadeem and others 2007;
Zahir and others 2008). Currently, bacterial strains
exhibiting ACC deaminase activity have been identified in
a wide range of genera such as Acinetobacter, Achromobacter, Agrobacterium, Alcaligenes, Azospirillum,
Bacillus, Burkholderia, Enterobacter, Pseudomonas, Ralstonia, Serratia, and Rhizobium (Shaharoona and others
2007a, b; Nadeem and others 2007; Zahir and others 2008,
2009; Kang and others 2010). Such rhizobacteria take up
the ethylene precursor ACC and convert it into 2-oxobutanoate and NH3 (Arshad and others 2007). Several forms
of stress are relieved by ACC deaminase producers, such as
the effects of phytopathogenic microorganisms (viruses,
bacteria, and fungi), and resistance to stress from polyaromatic hydrocarbons, heavy metals, radiation, wounding, insect predation, high salt concentration, draft,
extremes of temperature, high light intensity, and flooding
(Glick 2012; Lugtenberg and Kamilova 2009). As a result,
the major noticeable effects of seed/root inoculation with
ACC deaminase-producing rhizobacteria are plant root
elongation, promotion of shoot growth, and enhancement
in rhizobial nodulation and N, P, and K uptake as well as
mycorrhizal colonization in various crops (Nadeem and
others 2007; Shaharoona and others 2008; Nadeem and
others 2009; Glick 2012).
Indirect Mechanisms
The application of microorganisms to control diseases,
which is a form of biological control, is an environmentally
friendly approach (Lugtenberg and Kamilova 2009). The
major indirect mechanism of plant growth promotion in

rhizobacteria is through acting as biocontrol agents (Glick
2012). In general, competition for nutrients, niche exclusion, induced systemic resistance and antifungal metabolite
production are the chief modes of biocontrol activity in
PGPR (Lugtenberg and Kamilova 2009). Many rhizobacteria have been reported to produce antifungal metabolites
like HCN, phenazines, pyrrolnitrin, 2,4-diacetylphloroglucinol, pyoluteorin, viscosinamide, and tensin (Bhattacharyya and Jha 2012).
Competition for Nutrient and Niches
Offensive PGPB colonization and defensive retention of
rhizosphere niches are enabled by production of bacterial
allelochemicals, including iron-chelating siderophores,
antibiotics, biocidal volatiles, lytic enzymes, and detoxification enzymes (Compant and others 2005). Iron is an
essential growth element for all living organisms. The
scarcity of bioavailable iron in soil habitats and on plant
surfaces creates a furious competition (Loper and others
2007). Under iron-limiting conditions, PGPB produce low
molecular weight compounds called siderophores to competitively acquire ferric ion (Whipps 2001). Although
various bacterial siderophores differ in their abilities to
sequester iron, in general, they deprive pathogenic fungi of
this essential element because the fungal siderophores have
lower affinity. Some PGPB strains go one step further and
draw iron from heterologous siderophores produced by
cohabiting microorganisms (Loper and Henkels 1999;
Wang and others 1993; Whipps 2001). Siderophore
biosynthesis is generally tightly regulated by iron-sensitive
Fur proteins, the global regulators GacS and GacA, the
sigma factors RpoS, PvdS, and FpvI, quorum-sensing
autoinducers such as N-acyl homoserine lactone, and sitespecific recombinases (Ravel and Cornelis 2003). However, some data demonstrate that none of these global
regulators is involved in siderophore production. Neither
GacS nor RpoS significantly affected the level of siderophores synthesized by Enterobacter cloacae CAL2 and
UW4 (Saleh and Glick 2001). RpoS is not involved in the
regulation of siderophore production by Pseudomonas
putida strain WCS358 (Kojic and others 1999.). In addition, GrrA/GrrS, but not GacS/GacA, are involved in
siderophore synthesis regulation in Serratia plymuthica
strain IC1270, suggesting that gene evolution occurred in
the siderophore-producing bacteria (Ovadis and others
2004). A myriad of environmental factors can also modulate siderophore synthesis, including pH, the level of iron
and the form of iron ions, the presence of other trace elements, and an adequate supply of carbon, nitrogen, and
phosphorus (Compant and others 2005).
123

Antibiosis
The basis of antibiosis as a biocontrol mechanism of PGPR
has become increasingly better understood over the past
two decades (Whipps 2001). A variety of antibiotics have
been identified, including compounds such as amphisin,
2,4-diacetylphloroglucinol (DAPG), hydrogen cyanide,
oomycin A, phenazine, pyoluteorin, pyrrolnitrin, tensin,
tropolone, and cyclic lipopeptides produced by pseudomonads (Raaijmakers and others 2002; de Souza and
Raaijmakers 2003; Nielsen and Sorensen 2003). A further
list of such compounds includes oligomycin A, kanosamine, zwittermicin A, and xanthobaccin produced by
Bacillus, Streptomyces, and Stenotrophomonas spp. (Kim
and others 1999). Interestingly, some antibiotics produced
by PGPR are finding new uses as experimental pharmaceuticals, and this group of bacteria may offer an untapped
resource for compounds to deal with the alarming ascent of
multidrug resistant human pathogenic bacteria. Regulatory
cascades of these antibiotics involve GacA/GacS or GrrA/
GrrS, RpoD, and RpoS, N-acyl homoserine lactone
derivatives, and positive autoregulation (Bloemberg and
Lugtenberg 2001; Haas and Keel 2003). Antibiotic synthesis is tightly linked to the overall metabolic status of the
cell, which in turn is dictated by nutrient availability and
other environmental stimuli, such as major and minor
minerals, type of C source and supply, pH, temperature,
and other parameters (Duffy and Defago 2000). Trace
elements particularly zinc (Zn), and C source levels influence the genetic stability/instability of bacteria, affecting
their ability to produce secondary metabolites (Duffy and
Defago 2000). It is important to note that many strains
produce secondary antimicrobial metabolites and that
conditions favoring one compound may not favor another
(Duffy and Defago 1999). Thus, the varied arsenal of
biocontrol strains may enable antagonists to perform their
ultimate objective of pathogen suppression under the
widest range of environmental conditions. For example, in
P. fluorescens, CHA0 biosynthesis of DAPG is stimulated
and pyoluteorin is repressed in the presence of glucose as a
C source. As glucose is depleted, however, pyoluteorin
becomes the more abundantly antimicrobial compound
produced by this strain (Duffy and Defago 1999). This
ensures a degree of flexibility for the antagonists when
confronted with a different or a changeable environment.
Biotic conditions play an important role in biosynthesis of
antibiotics (Duffy and Defago 1997; Haas and Keel 2003;
Duffy and Defago 2004. Furthermore, plant growth and
development also influence antibiotic production, because
biological activity of DAPG producers is not induced by
the exudates of young plant roots but is induced by the
exudates of older plants, which results in selective pressure
against other rhizosphere microorganisms (Picard and
123
others 2000). Plant host genotype also plays a significant

role in the disease suppressive interaction of plants with a
microbial biocontrol agent, as demonstrated by Smith and
others (1999).
Lytic Enzyme Production
A variety of microorganisms also exhibit hyperparasitic
activity, attacking pathogens by excreting cell wall
hydrolases (Chernin and Chet 2002). Chitinase produced
by S. plymuthica C48 was found to inhibit spore germination and germ tube elongation in B. cinerea (Frankowski
and others 2001). The ability to produce extracellular
chitinases is considered crucial for S. marcescens to act as
an antagonist against Sclerotium rolfsii, and for Paenibacillus sp. strain 300 and Streptomyces sp. strain 385 to
suppress F. oxysporum f. sp. cucumerinum. It has been also
demonstrated that extracellular chitinase and laminarinase
synthesized by P. stutzeri digest and lyse mycelia of F.
solani (Lim and others 1991). Although chitinolytic
activity appears less essential for PGPR such as S. plymutica IC14 when used to suppress S. sclerotiorum and B.
cinerea, synthesis of proteases, and other biocontrol traits
are involved. The b-1,3-glucanase synthesized by Paenibacillus sp. strain 300 and Streptomyces sp. strain 385 lyse
fungal cell walls of F. oxysporum f. sp. Cucumerinum
(Singh and others 1999). B. cepacia synthesizes b-1,3glucanase that destroys the integrity of R. solani, S. rolfsii,
and P. ultimum cell walls. Similar to siderophores and
antibiotics, regulation of lytic enzyme production (proteases and chitinases in particular) involves the GacA/GacS
or GrrA/GrrS regulatory systems and colony phase variation (Lugtenberg and others 2001; Ovadis and others
2004).
Detoxification and Degradation of Virulence Factors
Another mechanism of biological control is the detoxification of virulence factors of the pathogens. For example,
certain biocontrol agents are able to detoxify albicidin
toxin produced by X. albilineans (Zhang and Birch 1996).
The detoxification mechanisms include production of a
protein that reversibly binds the toxin in both Klebsiella
oxytoca and A. denitrificans, as well as esterase-mediated
irreversible detoxification of albicidin found in Pantoea
dispersa. Several different microorganisms, including
strains of B. cepacia and Ralstonia solanacearum, can also
hydrolyze fusaric acid, a phytotoxin produced by various
Fusarium sp. (Toyoda and Utsumi 1991). More often
though, pathogen toxins display broad spectrum activities
and suppress the growth of microbial competitors, or
detoxify antibiotics produced by some biocontrol
microorganisms, as a self-defense mechanism against

biocontrol agents. Recently, it has been discovered that

certain PGPR quench the pathogen quorum-sensing
capacity by degrading autoinducer signals, thereby blocking expression of numerous virulence genes (Molina and
others 2003; Newton and Fray 2004). Because most, if not
all, bacterial plant pathogens rely upon autoinducer mediated quorum sensing to turn on gene cascades for their key
virulence factors (for example, cell degrading enzymes and
phytotoxins), this approach holds tremendous potential for
alleviating disease, even after the onset of infection, in a
curative manner. Biocontrol activities also apply to endophytic bacteria due to synthesis of metabolites with
antagonistic activities towards plant pathogens. For
example, Castillo and others demonstrated that munumbicins, antibiotics produced by the endophytic bacterium
Streptomyces sp. strain NRRL 30562 isolated from Kennedia nigriscans, inhibit in vitro growth of phytopathogenic fungi, P. ultimum, and F. oxysporum.
Subsequently, it has been reported that certain endophytic
bacteria isolated from field grown potato plants reduced the
in vitro growth of Streptomyces scabies and X. campestris
through production of siderophore and antibiotic compounds (Sessitsch and others 2005). Interestingly, the
ability to inhibit pathogen growth by endophytic bacteria,
isolated from potato tubers, decreases as the bacteria colonize the host plants interior, suggesting that bacterial
adaptation to this habitat occurs within their host and may
be tissue type and tissue site specific (Sturz and others
1999). Aino and others (1997) have also reported that the
endophytic P. fluorescens strain FPT 9601 synthesizes
DAPG and deposits DAPG crystals around and in the roots
of tomato, thus demonstrating in planta production of
antibiotics by endophytes.
Induced Systemic Resistance
The use of induced systemic resistance and systemic
acquired resistance as a strategy for pest management is
suitable and marketable to the producers. The co-evolution
flanked by plants and potential microbial pathogens has
been depicted as a zigzag model (Jones and Dang 2006).
According to the zigzag model, the primary inducible
responses are a result of the perception of chemical elicitors, microbe-associated molecular patterns (MAMPs),
pathogen-associated molecular patterns (PAMPs), and/or
damage-associated molecular patterns (DAMPs). MAMPs
explain broad microbe-derived molecules in conjunction
with those instigating from PGPR, whereas PAMPs
exclusively illustrate molecules from pathogenic microbes,
for example, fungi, oomycetes, and bacteria (Henry and
others 2012; Newman and others 2013). As a consequence,
PAMPs are a subgroup of MAMPs (Maffei and others
2012; Wiesel and others 2014). These molecules could
collectively be described as patterns that elicit immunity

(PEIs) and are frequently prominent by transmembrane
pattern recognition receptors (PRRs) in plant cells (Maffei
and others 2012; Newman and others 2013). Upon identification of MAMP- or DAMP-derived patterns, PTI
(PAMP- or pattern-triggered immunity) is activated in the
plant and the alleged molecules could be illustrated as
immune elicitors (Fig. 2). This defense reaction intends to
confine the growth of the intruder and can advance towards
systemic induced resistance that renders the plant relatively
tolerant to subsequent pathogen attack (Henry and others
2012).
Induced resistance is further divided into systemic
acquired resistance (SAR) or induced systemic resistance
(ISR). Systemic acquired resistance is generally differentiated by localized necrosis, expression of pathogenesis
related (PR) protein genes, and entails the salicylic acid
(SA) pathway, whereas ISR is normally activated by plant
growth-promoting rhizobacteria (PGPR) (Walters and
others 2013), is not connected with necrosis, and encompasses the jasmonic acid (JA) and ethylene (ET) pathways
(Henry and others 2012). Typical responses of PTI comprise cell wall modifications and the assembly of reactive
oxygen species (ROS) which can be persistently cytotoxic
and are imperative in signaling. Further, responses comprise the generation of phytoalexins, expression of PR
proteins, activation of mitogen activated protein kinase
(MAPK) pathways, and defense signaling linking calcium
(Ca2?) influx from extracellular spaces and variations in
free-cytosolic Ca2? concentrations (Garcion and others
2007). To counteract the preliminary plant defense reaction, thriving microbes have developed specific effectors
that stimulate identification of defense elicitors or subsequent plant defense mechanisms to promote effector-triggered susceptibility (ETS). Conversely, if these pathogen
effectors are in turn identified by cognate plant resistance
(R) proteins, the subsequent line of inducible response,
effector-triggered immunity (ETI), is instigated that frequently capitulates a hypersensitive resistance response
(HR) (Deslandes and Rivas 2012). The product of plant/
microbe associations can result in symbiosis and disease
resistance, and is directed by extra levels of complicated
co-evolution. Certainly, it must be identified that pathogen
colonization of plants can produce dynamic pathogenic,
mutualistic, or parasitic interactions of anecdotal intensity
and specificity. It is thus indispensable for the plant to
assess the range of risk and to escalate suitable and
impartial responses. These may vary from priming, being
prepared to counteract sooner to a definite attack, or
expression of PTI-based defense mechanisms to yield
incompatibility if the microbe/pathogen is incapable of
repressing these responses. Numerous research reports
have confirmed that a few of the inconsistency adept with
123

Fig. 2 Schematic representation of induced systemic resistance
ISR defense via inoculation with plant growth-promoting

rhizobacteria (PGPR) can be overcome by using multiple
strains (Ghignone and others 2012; Pii and others 2015).
Consequently, it is suggested that multiple strains be
assorted in concert if at all feasible when endeavoring to
stimulate ISR via PGPR inoculation.
mechanisms involved in the plant associated lifestyle and

whole biocontrol process achieved by PGPR. The revolutionary technological developments in high-throughput
DNA sequencing have resulted in the publication of many
whole genome sequences. The complete genome
sequencing of various PGPRs with different strains along
with respective resource links for whole genome sequences
is described in Table 1.
Genomic Sequencing in PGPR Strains

Bacillus
The recent progress in next-generation sequencing (NGS)
technologies such as Illumina (Bennett, 2004), 454
pyrosequencing (Margulies and others 2005; IonTorrent
(Rusk 2011), and PacBio (Eid and others 2009) has overcome the shortcomings of traditional Sanger sequencing by
increasing throughput, scalability, speed, and resolution.
Genome sequences of many PGPR isolates from the genera
Bacillus, Pseudomonas, and Enterobacter are now available (Chen and others 2007; Taghavi and others 2009;
Loper and others 2012). This information can contribute to
increase the knowledge on factors and mechanisms
involved in biocontrol and plant growth promotion. A great
challenge is now to uncover and elucidate the genetic
123
Manzoor and others (2013) illustrated the whole genome

assembly of the B. amyloliquefaciens UCMB5036 with a
comparative genome assembly method. The strain has
shown great potential for the promotion of plant growth
and the prevention of diseases in oilseed rape (Brassica
napus) and Arabidopsis thaliana (Magno-Perez and others
2015).
The B. amyloliquefaciens UCMB5036 genome contains
3842 predicted open reading frames (ORFs), of which
95.39 % of the genetic proportion had counterparts in the
FZB42 genome, this suggests a high degree of gene synteny to the reference genome. The genomic sequence
http://www.ncbi.nlm.nih.gov/nuccore/CP011534
http://www.ebi.ac.uk/ena/data/view/CVPA00000000
Koberl and others (2015)

Kang and others (2015)
Hou and others (2015)
Kim and others (2011)
Hu and others (2012)
Rong and others (2012)
Brown and others (2012)
Bacillus amyloliquefaciens strain Co1-6
Bacillus pumilus strain WP8
Delftia tsuruhatensis MTQ3

Chromobacterium sp. strain C-61
Streptomyces sp. strain TOR3209
Mitsuaria sp. strain H24L5A
Rhizobium sp. strain CF142
http://www.ncbi.nlm.nih.gov/nuccore/CAEI01000169
Pantoea sp. strain GM01
Pantoea sp. strain YR343
http://www.ncbi.nlm.nih.gov/nuccore/CAEI01000001
Pantoea ananatis B1-9
http://www.ncbi.nlm.nih.gov/nuccore/AKKE00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKIT00000000
Weilharter and others (2011)
Burkholderia phytofirmans PsJNT
Burkholderia
http://www.ncbi.nlm.nih.gov/nuccore/AJVM00000000
http://genome.jgi-psf.org/ent_6/ent_6.home
Taghavi and others (2010)
Enterobacter sp. 638
Rhizobium sp. strain AP16
Enterobacter
http://www.ncbi.nlm.nih.gov/nuccore/AKKA00000000
Rhizobium sp. strain CF122
http://www.ncbi.nlm.nih.gov/nuccore/AJWE00000000
http://www.ncbi.nlm.nih.gov/nuccore/CAFG01000607
http://www.ncbi.nlm.nih.gov/nuccore/CAFG01000001
http://www.ncbi.nlm.nih.gov/nuccore/AGNH00000000
http://www.ncbi.nlm.nih.gov/nuccore/CAEE01001118
http://www.ncbi.nlm.nih.gov/nuccore/LCZH00000000
http://www.ncbi.nlm.nih.gov/nuccore/CAEE01000001
http://www.ncbi.nlm.nih.gov/nuccore/HF563562
http://www.ncbi.nlm.nih.gov/nuccore/AKKB00000000
Manzoor and others (2013)
http://www.ncbi.nlm.nih.gov/nuccore/AJST00000000
Brevibacillus sp. strain CF112

Bishnoi and others (2015)
http://www.ncbi.nlm.nih.gov/nuccore/HE617159
Bacillus sp. strain 5B6
B. subtilis strain UD1022
http://www.ncbi.nlm.nih.gov/nuccore/AWQY00000000
Blom and others (2012)
Bacillus amyloliquefaciens subsp. plantarumCAU B946
B. amyloliquefaciens UCMB5036
Zhao and others (2015)

Lefort and others (2014)
Bacillus amyloliquefaciens Strain UASWS BA1
http://www.ncbi.nlm.nih.gov/nuccore/HE774679.1
Bacillus amyloliquefaciens subsp. plantarum YAU B9601-Y2
Bacillus amyloliquefaciens strain BH072
http://www.ncbi.nlm.nih.gov/nuccore/AMPK00000000
Lee and others (2012)

Hao and others (2012a, b)
Bacillus amyloliquefaciens strain M27
http://www.nature.com/nbt/journal/v25/n9/extref/nbt1325-S1.pdf
Song and others (2012)

Chen and others (2007)
Bacillus amyloliquefaciens FZB42
Bacillus
Resource link
Reference
Bacillus sp. strain JS
Strain
PGPR class
Table 1 The genomic sequence of the diverse PGPR strains with resource links
123
123
Pseudomonas
http://www.ncbi.nlm.nih.gov/nuccore/AIPP00000000
http://www.ncbi.nlm.nih.gov/nuccore/AFOX00000000
Jeong and others (2011)

Shin and others (2012)
Tong and others (2013)
P. polymyxa ATCC 842T
Paenibacillus terrae HPL-003
P. polymyxa strain ATCC 12321
Pseudomonas sp. R81
Pseudomonas sp. strain GM49
Pseudomonas sp. strain GM 30


Pseudomonas abietaniphila KF717
Pseudomonas fluorescens Wayne1R

Pseudomonas fluorescens Wood1R
Pseudomonas fluorescens F113

Pseudomonas putida B001
Pseudomonas putidaBIRD-1
http://www.ncbi.nlm.nih.gov/nuccore/ARYD00000000
Huang and Yousef (2012)
Paenibacillus polymyxa OSY-DF
Pseudomonas sp. R62
http://www.ncbi.nlm.nih.gov/nuccore/HE577054
Eastman and others (2014)
Paenibacillus polymyxa CR1

Li and others (2014)
http://www.ncbi.nlm.nih.gov/nuccore/JYCW00000000
Niu and others (2011)
Paenibacillus polymyxa M-1
Paenibacillus polymyxa SQR-21
http://www.ebi.ac.uk/ena/data/view/CVPD00000000
Liang and others (2015)
Paenibacillus polymyxa strain EBL06
Paenibacillus polymyxa E681
Ma and others (2011)

Koberl and others (2015)
Paenibacillus polymyxa SC2

Paenibacillus polymyxa strain Mc5Re-14
Paenibacillus
Resource link
Reference
Strain
PGPR class
Table 1 continued

PGPR class
Table 1 continued
Kimura and others (2015)
Rong and others (2012)
Park and others (2011)
Redondo-Nieto and others

(2012)
http://www.ncbi.nlm.nih.gov/nuccore/AKJM00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJT00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJS00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJJ00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJI00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJL00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJQ00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJK00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJN00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJP00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJH00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJG00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJE00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJU00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJD00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJF00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJO00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJB00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJR00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJC00000000
http://www.ncbi.nlm.nih.gov/nuccore/AKJV00000000
http://www.ncbi.nlm.nih.gov/nuccore/BBQR01000097
http://www.ncbi.nlm.nih.gov/nuccore/BBQR01000001
http://www.ncbi.nlm.nih.gov/nuccore/CAFF01000001
http://www.ncbi.nlm.nih.gov/nuccore/CAFF01001437
http://www.ncbi.nlm.nih.gov/nuccore/CADX01000001
http://www.ncbi.nlm.nih.gov/nuccore/CAED01000001
http://www.ncbi.nlm.nih.gov/nuccore/CADX01000090
http://www.ncbi.nlm.nih.gov/nuccore/AHZN00000000
http://www.ncbi.nlm.nih.gov/nuccore/AHZM00000000
Mathimaran and others

(2012)
Matilla and others (2011)
Resource link
Reference
Strain
123

of B. amyloliquefaciens UCMB5036 confirmed the presence of non-ribosomal peptide synthetase (NRPS) and
polyketide synthase (PKS) gene clusters: surfactin (srf),
fengycin (fen), difficidin (dfn), bacilysin (bac), macrolactin
(mln), bacillaene (bae), bacillomycin D (bmy), and bacillibactin (dhb) (Montor-Antonio and others 2015). These
are responsible for the synthesis of secondary metabolites,
including antifungal and antibacterial compounds. The
genome also contains genes involved in the catabolism of
plant-derived compounds, resistance to heavy metals and
drugs, motility and chemotaxis, root colonization, and
other functions that presumably give the bacterium an
advantage in developing a symbiotic relationship with
plants. The identification of genes involved in the ability of
rhizobacterial strains to improve plant growth creates the
potential to improve the performance of biocontrol strains
or to construct novel biocontrol strains by genetic modification. Complete operons, as well as single genes under the
control of their own regulatory genes or regulated by the
constitutive expression of the tac or lac promoters, have
been transferred to rhizobacterial strains (Glick 2015).
Using a combination of immune-fluorescence and an
rRNA-targeting probe that monitors the presence and
metabolic activity of P. fluorecens DR54 inoculant cells in
the sugar beet rhizosphere, Lubeck and others (2000)
showed that bacteria at the root tips are metabolically most
active and that indigenous bacteria enter the rhizosphere
two days after inoculation. Niazi and others (2014) illustrated genome analysis of B. amyloliquefaciens
UCMB5033 comprised of about 4,071,167 bp long circular
chromosome that consists of 3912 protein-coding genes, 86
tRNA genes, and 10 rRNA operons. Comparative genome
analysis of B. amyloliquefaciens UCMB5033 might reveal
mechanisms by which UCMB5033 mediates plant protection and growth promotion, will further enable the investigations of the biochemical and regulatory mechanisms
behind the symbiotic relationship, and will shed light on
the activity of PGPR in different environments. Bacillus
amyloliquefaciens subsp. plantarum UCMB5033 is of
special interest for its ability to promote host plant growth
through production of stimulating compounds and suppression of soil borne pathogens by synthesizing antibacterial and antifungal metabolites or priming plant defense
as induced systemic resistance. Manzoor and others (2013)
showed the genome sequence of Bacillus amyloliquefaciens strain UCMB5036, a plant growth-promoting bacterium isolated from a cotton plant. Its genome contains
gene clusters involved in non-ribosomal synthesis of secondary metabolites known for their antimicrobial activities.
The availability of this genome will provide novel insights
into plant bacterium associated activities. Niazi (2014)
reported the Bacillus amyloliquefaciens subsp. plantarum
strain UCMB5113 is a Gram-positive rhizobacterium that
123
can colonize plant roots and stimulate plant growth and

defense based on unknown mechanisms. This reinforcement of plants may provide protection to various forms of
biotic and abiotic stresses. To determine the genetic traits
involved in the mechanism of plant bacteria association,
the genome sequence of UCMB5113 was obtained by
assembling paired-end Illumina reads (Niazi and others
2014). The assembled chromosome of 3,889,532 bp was
predicted to encode 3656 proteins. Genes that potentially
contribute to plant growth promotion such as indole-3acetic acid (IAA) biosynthesis, acetoin synthesis, and
siderophore production were identified (Niazi and others
2014). Moreover, annotation identified putative genes
responsible for non-ribosomal synthesis of secondary
metabolites and genes supporting environment fitness of
UCMB5113 including drug and metal resistance. Hossain
and others (2015) demonstrated the growth-promoting and
disease-inhibiting activities of plant growth-promoting
rhizobacteria (PGPR) strains and the genomes of
12 Bacillus subtilis group strains with PGPR activity were
sequenced and analyzed. These B. subtilis strains revealed
far above the ground genomic diversity, whereas the genomes of B. amyloliquefaciens strains (a member of the B.
subtilis group) are vastly conserved. A pairwise BLASTp
matrix showed that gene family similarity among Bacillus genomes ranges from 32 to 90 %, with 2839 genes
within
the
core
genome
of B.
amyloliquefaciens subsp. plantarum. Comparative genomic analyses
of B. amyloliquefaciens strains identified genes that are
linked with biological control and colonization of roots
and/or leaves, including 73 genes exclusively correlated
with subsp. plantarum strains that have envisaged functions associated with signaling, transportation, secondary
metabolite production, and carbon source utilization. Shao
and others (2015) isolated the plant growth-promoting
rhizobacteria (PGPR) strain Bacillus amyloliquefaciens SQR9 from the cucumber rhizosphere which was
known to act as bio control against pathogen invasion and
promote plant growth via extensive root colonization. The
authors analyzed gene products using transcriptional analysis like dhaS, patB, yclB, yclC, yhcX, and ysnE involved
in IAA biosynthesis. The genes spatB, yclC,
and dhaS represent an impending entire IPyA corridor of
IAA biosynthesis in SQR. Bishnoi and others (2015)
revealed the whole genome sequence of the recently
illustrated B. subtilis strain UD1022. The UD1022 genome
consists of a 4.025-Mbp chromosome, compared to the
genome sequence of B. subtilis strain 168. 3583 Coding
sequences (CDSs) had a strong bidirectional homolog
([ 85 % identity), 164 had weaker or unidirectional
homologs ([50 % identity), 439 were unique to UD1022,
and 421 were unique to B. subtilis strain 168. UD1022 is
more specific comprising genes for several amino acid

biosynthesis, transport, and metabolism, cell wall proteins,

carbohydrate metabolisms, and metal (copper, cobalt-zinccadmium), and antibiotic (b-lactam, tetracycline, and
vancomycin) resistance.
Pseudomonas
Several bacterial strains of the Pseudomonas genus provide
plant growth stimulation, plant protection against pests, or
bioremediation. Among these bacteria, P. fluorescens
Pf29Arp reduces the severity of take-all, a disease caused
by the pathogenic fungus Gaeumannomyces graminis var.
tritici (Ggt) on wheat roots (Daval and others 2011). Proteome analysis of the pathogenic bacteria Xanthomonas
campestris pv. campestris in association with Brassica
oleracea and Pseudomonas savastanoi pv. savastanoi
resulted in comprehensive expression analysis including
stress and metabolic proteins (Andrade and others 2008). In
addition, an initiative to build a genomic encyclopedia of
the rhizobacterial strain P. fluorescens SBW25 (PfSBW25)
on the basis of short-run non-contiguous sequence data is
underway at Oxford University (Trippe and others 2013).
Shen and others (2013) demonstrated comparative genomic
analysis of four representative PGPR, P. chlororaphis, and
P. fluorescens which were non-pathogenic biocontrol
agents, and some P. aeruginosa and P. stutzeri strains
exhibited plant growth-promoting activities. Jacobs and
others (2012) illustrated the transcriptomics profile of Ralstonia solanacearum in vitro and revealed the significance
of T3SS in vir cascade of Ralstonia (45 % regulated by HR
and Hrp gene). Marchi and others (2013) obtained a draft
genome of Pf29Arp and subsequent comparative genomic
analyses have revealed that this bacterial strain is closely
related to strains of the P. brassicacearum-like subgroup
including P. brassicacearum ssp. brassicacearum NFM421
and P. fluorescens F113. Despite an overall chromosomal
organization similar to these strains, a number of features
including antibiotic synthesis gene clusters from secondary
metabolism are not found in the Pf29Arp genome. But
Pf29Arp possesses different protein secretion systems
including type III (T3SS) and type VI (T6SS) secretion
systems. Pf29Arp is the first Pseudomonas sp. strain
described with four T6SS clusters (cluster I, II, III, and IV).
Calderon and others (2015) analyzed the whole genome of
Pseudomonas chlororaphis PCL1606 rhizobacterium that
has biocontrol activity against many soilborne phytopathogenic fungi. The resulting genome is 6.66-Mb, and
comparative genomic analysis of P. chlororaphis PCL1606
showed a diverse spectrum of traits implicated in multitrophic interactions with plants and microbes as well as
biological control. The genome sequence of P. chlororaphis PCL1606 demonstrated sequences homologous to
biosynthetic genes for the antifungal compounds 2-hexyl,
5-propyl resorcinol (HPR), hydrogen cyanide, and pyrrolnitrin; this is the first report of pyrrolnitrin encoding genes
in this P. chlororaphis strain. Chen and others (2015) also
reported plant growth-promoting rhizobacterium, Pseudomonas chlororaphis HT66, that releases phenazine-1carboxamide with high yield, as compared to genomic
sequenced P. chlororaphis strains, GP72, 3084 and O6.
However, all these four strains could synthesize antimicrobial metabolites including diverse phenazines and
insecticidal protein FitD. Udaondo and others (2015)
demonstrated comprehensive comparative analysis of nine
strains and the first characterization of the Pseudomonas
putida pangenome which produces solvent tolerant strains
important for the biosynthesis of added-value chemicals.
Pan and Hu (2015) reported Pseudomonas sp. 10B238
putative novel species of Pseudomonas, isolated from a
deep-sea sediment of the South China Sea, which had the
genetic potential to produce secondary metabolites related
to non-ribosomal peptides (NRPs), as well as showed
moderate antimicrobial activities.
Acebo-Guerrero and others (2015) isolated 127 rhizobacterial strains from cacao rhizosphere, three isolates
(CP07, CP24, and CP30) among which were identified
as Pseudomonas chlororaphis, revealed in vitro antagonistic activity against P. palmivora. Recently, novel species of
the genus Pseudomonas having insoluble phosphorus solubilizing activity were sequenced, namely Pseudomonas
rhizosphaerae IH5T (=DSM 16299T) isolated from the
rhizospheric soil of grass growing in Spain. Roquigny and
others (2015) demonstrated biocontrol activity against
various plant pathogens in PGPR Pseudomonas fluorescens LBUM223. This strain produces the antimicrobial
metabolite, phenazine-1-carboxylic acid, involved in the
biocontrol of Streptomyces scabies, the causal agent of
common scab of potato. The complete genome sequence
of P. fluorescens LBUM223 revealed a total of 176,424
raw subreads and an average length of 5556 bp.
Enterobacter
The genome sequence of Enterobacter cloacae subsp.
Dissolvens SDM strain was determined by 454 genome
sequencer (454GS FLX) (Xu and others 2012). The genome sequence contains 286,872 reads with an average
length of 356 bp at more than 20-fold coverage with the
G ? C content of 55.1 %. The reads were assembled using
the Newbler Assembler (454 Life Science) into 168 large
contigs ([500 bp) with a length of 4,923,170 bp (Xu and
others 2012). Liu and others (2013) illustrated the genomic
analysis of Enterobacter cloacae species including an
extremely diverse group of bacteria that are associated with
plants, soil, and humans. Publication of the complete
genome sequence of the plant growth-promoting
123

endophytic E. Cloacae subsp. cloacae ENHKU01 provided

an opportunity to perform the first comparative genome
analysis between strains of this dynamic species. Examination of the pangenome of E. cloacae showed that the
conserved core genome retains the general physiological
and survival genes of the species, whereas genomic factors
in plasmids and variable regions determine the virulence of
the human pathogenic E. cloacae strain; additionally, the
diversity of fimbriae contributes to variation in colonization and host determination of different E. cloacae strains
(De Maayer and others 2014). Comparative genome analysis further illustrated that E. cloacae strains possess
multiple mechanisms for antagonistic action against other
microorganisms, which involve the production of siderophores and various antimicrobial compounds, such as
bacteriocins, chitinases, and antibiotic resistance proteins
(Donaldson and others 2014). The presence of Type VI
secretion systems is expected to provide further fitness
advantages for E. cloacae in microbial competition, thus
allowing it to survive in different environments (Decoin
and others 2014). Competition assays were performed to
support our observations in genomic analysis, where E.
cloacae subsp. cloacae ENHKU01 demonstrated antagonistic activities against a wide range of plant pathogenic
fungal and bacterial species. Comparative genome analysis
reveals the antagonistic potential of E. cloacae (Liu and
others 2013. The multiple antagonistic mechanisms of E.
cloacae are expected to contribute to its success in competition against other microbes in various environmental
niches, thus allowing different strains of E. cloacae to
survive in diverse environments.
Proteomic Approach to Improve PGPR

Application
Proteomics is one of the best strategies used to reveal the
expressions of whole proteins in cells and their interactions
(Paul and others 2006). The term proteome is used here to
describe the complex state of an organism under defined
conditions rather than its complete protein repertoire
(James 1997). In a wider context, effective protein separation and identification in the different groups of PGPR
can provide researchers with targets for different bioactivities, enhanced growth promotion and induced resistance
for plant disease management (Walters and others 2005).
The mechanisms of osmotolerance of PGPR by up-regulation of stress proteins contributing to the plant health are
of immense importance; likewise, Pseudomonas fluorescens MSP-393 is a proven biocontrol agent for many of
the crops grown in saline soils of coastal ecosystem (Paul
and Nair 2008). It was observed that the root colonization
potential of the strain was not hampered with higher
123
salinity in soil. As a means of salt tolerance, the strain de

novo synthesized the osmolytes, Ala, Gly, Glu, Ser, Thr,
and Asp in their cytosol. The proteome analysis of the
bacteria employing 2D gel electrophoresis and MALDITOF techniques are prerequisite for understanding the
mechanism of salt tolerance (Kohler and others 2015;
Chakraborty and others 2015). 2D-PAGE strategy has been
widely used in understanding stress responses as well as in
understanding constitutive differences between developmental stages or genotypes (Vanderschuren and others
2013). Kandasamy and others (2009) explained plant
growth promotional activity of Pseudomonas fluorescens strain KH-1 in rice leaf sheaths through the differential expression of 23 proteins namely putative p23 cochaperone, thioredoxin h-rice, ribulose-bisphosphate carboxylase large-chain precursor, nucleotide diphosphate
kinase, proteasome sub-unit protein, and putative glutathione S-transferase protein. Besides, the above mentioned molecular biological techniques available, highthroughput whole genome gene expression tools, that is,
microarrays and proteomics, will provide improved
knowledge on the gene(s) and pathways induced during
host-PGPR interaction (Afroz and others 2013). In one
study, Shoresh and Harman (2010) characterized Trichoderma harzianum and maize interactive proteins and
reported the metabolic pathways induced by T. harzianum.
The Bacillus amyloliquefaciens strain KPS46 was investigated for its ability to activate extracellular protein elicitors
in enhanced plant growth and induced systemic resistance
of soybean plants (Buensanteai and others 2008). 2-DGE
was used to separate extracellular proteins secreted by
KPS46 wild type and by N19G1, a UV-derived mutant of
KPS46 with reduced production of extracellular proteins
and lacking growth promotion and induced resistance
activity. The 20 extracellular protein spots that were known
to be secreted by various mechanisms were identified. The
analysis revealed a number of proteins that might be
involved in plant growth promotion and induced resistance
by acting as plant growth regulators, accumulating biofertilizer/nutrients, producing antibiotic compounds, stimulating metabolism, or functioning in defense against stress
factors (Buensanteai and others 2008). Besides, some
amino acid metabolism proteins were present in the KPS46
extracellular medium like glutamine and glutamate, the
main nitrogen donors in the cell. Similarly, in concurrence
with the analysis of the extracellular proteome of a Bacillus
species in relation to plant growth enhancement and
induced resistance, the genome of a B. amyloliquefaciens
strain, FZB42, has been sequenced (Chen and others 2007).
Most of the cytosolic proteins expressed at higher levels
were found in P. polymyxa E681 cells grown in the presence of barley rather than in the absence of barley (Seul
and others 2007). Proteins detected at a lower level in the

supernatant of P. polymyxa E681 cells grown in the presence of barley were lipoprotein, glucose-6-phosphate
1-dehydrogenase, heat-shock protein HtpG, spermidine
synthase, OrfZ, ribonuclease PH, and coenzyme PQQ
synthesis protein, and flagellar hook associated protein,
whereas proteins detected at a higher level in the supernatant of P. polymyxa E681 cells grown in the presence of
barley included D-alanyl-D-alanine ligase A, isopentenyldiphosphate delta-isomerase, ABC transporter ATP-binding protein Uup, and lipase (Seul and others 2007). However, apart from sample preparation issues, the biggest
limitation for using the proteomic approach to identify
proteins from PGPR is the limited information available in
protein databases (Schenk and others 2012). Most of the
characterized proteins in the Swiss-Prot and EMBL protein
databases are from B. subtilis. Ultimately, the approaches
used in proteomic study could increase understanding of
the modes of action by which PGPR enhanced plant growth
at molecular and biochemical levels.
Conclusion and Perspectives

In communion with the current repugnance towards
chemical fertilizers and pesticides, and consumption, there
is an explicit prominence on utilization of organic inputs
and microbial inoculants which play a significant role in
sustainable agriculture. Although large-scale commercialization of some PGPRs like Azospirillum, Azotobacter,
Bacillus, Burkholderia, Pseudomonas, Rhizobium, and
Serratia has been actualized; however, there are numerous
new PGPR like Azoarcus, Exiguobacterium, Methylobacterium, Paenibacillus, and Pantoea with substantial beneficial activities which have not achieved commercial scales
of production unlike their more recognized antecedents.
These PGPR can offer inspiring opportunity for enhanced
yield and production of staple food crops. Moreover, the
progress in techniques for detection and quantification of
elements spanning the fields of transcriptomics, proteomics, and metabolomics, together with adequate bioinformatics tools, might provide more articulate and holistic
approaches to comprehend plantmicrobe interactions.
There is also the inevitability of intensifying the research
field of functional genomics towards metabolomic profiling, even though technically it is cumbersome in some
cases. The study of genomics can provide us comprehensible association between changes in gene expression or
protein synthesis and observed alteration in phenotype.
To comprehend the impediment of the fundamental
mechanisms, it is essential to relate techniques that allow
an inclusive evaluation of the plants response at diverse
hierarchical ranks. Nevertheless, exclusive of proteomics
and metabolomics, only an inequitable perception of the
systems response can be acquired, because not all genes

that are transcribed are also translated into functional gene
products. The blend of proteomics and metabolomics with
transcriptomics to elucidate plantmicrobe interactions is
still inadequate. In the coming era, these techniques are
expected to prompt evolution in conception of microbederived and plant-derived proteins and metabolite substitutes that activate vulnerability or resistance. Thus, the
detection of new regulatory standards or defense pathways
that release the viewpoint for recuperating plant protection
can be visualized.
References
Acebo-Guerrero Y, Hernandez-Rodrguez A, Vandeputte O, Miguelez-Sierra Y, Heydrich-Perez M, Ye L, El Jaziri M (2015)
Characterization of Pseudomonas chlororaphis from Theobroma
cacao L. rhizosphere with antagonistic activity against Phytophthora palmivora (Butler). J Appl Microbiol 119:11121126.
doi:10.1111/jam.12910
Afroz A, Zahur M, Zeeshan N, Komatsu S (2013) Plant-bacterium
interactions analyzed by proteomics. Front Plant Sci 4:21
Ahemad M, Khan MS (2011) Toxicological assessment of selective
pesticides towards plant growth promoting activities of phosphate solubilizing Pseudomonas aeruginosa. Acta Microbiol
Immunol Hung 58:169187
Ahemad M, Khan MS (2012a) Effect of fungicides on plant growth
promoting activities of phosphate solubilizing Pseudomonas
putida isolated from mustard (Brassica compestris) rhizosphere.
Chemosphere 86:945950
Ahemad M, Khan MS (2012b) Effects of pesticides on plant growth
promoting traits of Mesorhizobium strain MRC4. J Saudi Soc
Agric Sci 11:6371
Ahemad M, Kibret M (2014) Mechanisms and applications of plant
growth promoting 386 rhizobacteria: current perspective. J King
Saud Univ Sci 26:120
Ahmed E, Holmstrom SJ (2014) Siderophores in environmental
research: roles and applications. Microbial Biotechnol
7(3):196208
Aino M, Maekawa Y, Mayama S, Kato H (1997) Biocontrol of
bacterial wilt of tomato by producing seedlings colonized with
endophytic antagonistic pseudomonads. In: Ogoshi A, Kobayashi K, Homma Y, Kodama F, Kondo N, Akino S (eds) Plant
growth-promoting Rhizobacteriapresent status and future
prospects. Faculty of agriculture. Hokkaido University, Sapporo,
pp 120123
Andrade AE, Silva LP, Pereira JL, Noronha EF, Reis FB Jr, Bloch C
Jr, Mehta A (2008) In vivo proteome analysis of Xanthomonas
campestris pv. campestris in the interaction with the host plant
Brassica oleracea. FEMS Microbiol Lett 281(2):167174
Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998)
Potential of Rhizobium and Bradyrhizobium species as plant
growth promoting rhizobacteria on non-legumes: effects on
radishes (Raphanus sativus L.). Plant Soil 204:5767
Arora NK, Kang SC, Maheshwari DK (2001) Isolation of siderophore
producing strains of Rhizobium meliloti and their biocontrol
potential against Macrophomina phaseolina that causes charcoal
rot of groundnut. Curr Sci 81:673677
Arshad M, Saleem M, Hussain S (2007) Perspectives of bacterial
ACC deaminase in phytoremediation. Trends Biotechnol
25:356362
123

Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51(2):163190
Ashraf MA, Asif M, Zaheer A, Malik A, Ali Q, Rasool M (2013)
Plant growth promoting rhizobacteria and sustainable agriculture: a review. Afr J Microbiol Res 7(9):704709
Baha N, Bekki A (2015) An approach of improving plant salt
tolerance of Lucerne (Medicago sativa) grown under salt stress:
use of Bio-inoculants. J Plant Growth Regul 34(1):169182
Bakker P, Berendsen R, Doornbos R, Wintermans P, Pieterse C
(2013) Rhizosphere revisited: root microbiomics. Front Plant Sci
165:17
Barea JM, Richardson AE (2015) Phosphate mobilisation by soil
microorganisms. In: Lugtenberg B (ed) Principles of plantmicrobe interactions. Springer, Heidelberg, pp 225234
Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2013a) Microbial
interactions in the rhizosphere. In: de Bruijn FJ (ed) Molecular
microbial ecology of the rhizosphere, vol 1. Wiley, Hoboken,
pp 2944
Barea JM, Pozo MJ, Lopez-Raez JA, Aroca R, Ruz-Lozano JM,
Ferrol N, Azcon R, Azcon-Aguilar C (2013b) Arbuscular
mycorrhizas and their significance in promoting soil-plant
systems sustainability against environmental stresses. In: Rodelas B, Gonzalez-Lopez J (eds) Benefiial plant-microbial interactions: Ecology and applications. CRC Press, Boca Raton,
pp 353387
Bashan Y, de-Bashan LE, Prabhu SR, Hernandez JP (2014) Advances
in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (19982013). Plant Soil
378:133
Bennett S (2004) Solexa Ltd. Pharmacogenomics 5:433438
Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol
Biotechnol 28:13271350
Bishnoi U, Polson SW, Sherrier DJ, Bais HP (2015) Draft genome
sequence of a natural root isolate, Bacillus subtilis UD1022, a
potential plant growth-promoting biocontrol agent. Genome
Announc 3(4):e00696-15
Bishop PE, Jorerger RD (1990) Genetics and molecular biology of an
alternative nitrogen fixation system. Plant Mol Biol 41:109125
Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant
growth promotion and biocontrol by rhizobacteria. Curr Opin
Plant Biol 4:343350
Blom J, Rueckert C, Niu B, Wang Q, Borriss R (2012) The complete
genome of Bacillus amyloliquefaciens subsp. plantarum CAU
B946 contains a gene cluster for nonribosomal synthesis of iturin
A. J Bacteriol 194(7):18451846
Boiero L, Perrig D, Masciarelli O, Penna C, Cassan F, Luna V (2007)
Phytohormone production by three strains of Bradyrhizobium
japonicum and possible physiological and technological implications. Appl Microbiol Biotech 74(4):874880
Bolan N, Kunhikrishnan A, Thangarajan R, Kumpiene J, Park J,
Makino T, Kirkham MB, Scheckel K (2014) Remediation of
heavy metal (loid)s contaminated soilsto mobilize or to
immobilize. J Hazard Mater 266:141166
Brown SD, Utturkar SM, Klingeman DM, Johnson CM, Martin SL,
Land ML, Pelletier DA (2012) Twenty-one genome sequences
from Pseudomonas species and 19 genome sequences from
diverse bacteria isolated from the rhizosphere and endosphere of
Populus deltoides. J Bacteriol 194(21):59915993
Browne P, Barret M, Morrissey JP, OGara F (2013) Molecular-based
strategies to exploit the inorganic phosphate-solubilization
ability of Pseudomonas in sustainable agriculture. In: de Bruijn
FJ (ed) Molecular microbial ecology of the rhizosphere, vol 2.
Wiley, Hoboken, pp 615628
Bruto M, Prigent-Combaret C, Muller D, Moenne-Loccoz Y (2014)
Analysis of genes contributing to plant-beneficial functions in
123
plant growth-promoting rhizobacteria and related Proteobacteria.

Sci Rep 4:6261
Buensanteai N, Athinuwat D, Chatnaparat T, Yuen GY, Prathuangwong S (2008) Extracellular proteome of Bacillus amyloliquefaciens KPS46 and Its effect on enhanced growth promotion and
induced resistance against bacterial pustule on soybean plant.
Kasetsart J Nat Sci 42:1326
Calderon CE, Ramos C, de Vicente A, Cazorla FM (2015) Comparative genomic analysis of Pseudomonas chlororaphis PCL1606
reveals new insight into antifungal compounds involved in
biocontrol. Mol Plant 28(3):249260
Camerini S, Senatore B, Lonardo E, Imperlini E, Bianco C, Moschetti
G, Rotino GL, Campion B, Defez R (2008) Introduction of a
novel pathway for IAA biosynthesis to rhizobia alters vetch root
nodule development. Arch Microbiol 190:6777
Carvalhais LC, Dennis PG, Tyson GW, Schenk PM (2013) Rhizosphere metatranscriptomics: challenges and opportunities. In: de
Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere,
vol 2. Wiley, Hoboken, pp 11371144
Cattelan AJ, Hartel PG, Fuhrmann JJ (1999) Screening for plant
growthpromoting rhizobacteria to promote early soybean
growth. Soil Sci Soc Am J 63(6):16701680
Chabot R, Beauchamp CJ, Kloepper JW, Antoun H (1998) Effect of
phosphorus on root colonization and growth promotion of maize
by bioluminescent mutants of phosphate-solubilizing Rhizobium
leguminosarum biovar phaseoli. Soil Biol Biochem
30(12):16151618
Chakraborty S, Salekdeh GH, Yang P, Woo SH, Chin CF, Gehring C,
Komatsu S (2015) Proteomics of important food crops in the
Asia Oceania Region: current status and future perspectives.
J Prot Res 14(7):27232744
Chen XH, Koumoutsi A, Scholz R et al (2007) Comparative analysis
of the complete genome sequence of the plant growth-promoting
bacterium Bacillus amyloliquefaciens FZB42. Nat Biotech
25(9):10071014
Chen Y, Shen X, Peng H, Hu H, Wang W, Zhang X (2015)
Comparative genomic analysis and phenazine production of
Pseudomonas chlororaphis, a plant growth-promoting rhizobacterium. Geno Data 4:3342
Chernin L, Chet I (2002) Microbial enzymes in biocontrol of plant
pathogens and pests. In: Burns RG, Dick RP (eds) Enzymes in
the environment: activity, ecology, and applications. Marcel
Dekker, New York, pp 171225
Chin-A-Woeng TF, Bloemberg GV, Van der Bij AJ, Van der Drift
KM, Schripsema J, Kroon B, de Bruijn FJ (1998) Biocontrol by
phenazine-1-carboxamide-producing Pseudomonas chlororaphis
PCL1391 of tomato root rot caused by Fusarium oxysporum f.
sp. radicis-lycopersici. Mol Plant 11(11):10691077
Cohen AC, Bottini R, Pontin M, Berli FJ, Moreno D, Boccanlandro
H, Piccoli PN (2015) Azospirillum brasilense ameliorates the
response of Arabidopsis thaliana to drought mainly via
enhancement of ABA levels. Physiol Plant 153(1):7990
Compant S, Duffy B, Nowak J, Clement C, Barka EA (2005) Use of
plant growth-promoting bacteria for biocontrol of plant diseases:
principles, mechanisms of action, and future prospects. Appl
Environ Microbiol 71(9):49514959
Crowley DE, Kraemer SM (2007) Function of siderophores in the
plant rhizosphere. In: Pinton R, Varanini Z, Nannipieri P (eds)
The rhizosphere, biochemistry and organic substances at the soilplant interface. CRC Press, Boca Raton, pp 73109
Daniels R, Vanderleyden J, Michiels J (2004) Quorum sensing and
swarming migration in 448 bacteria. FEMS Microbiol Rev
28:261289
Daval S, Lebreton L, Gazengel K, Boutin M, Guillerm-Erckelboudt
AY, Sarniguet A (2011) The biocontrol bacterium Pseudomonas
fluorescens Pf29Arp strain affects the pathogenesis-related gene

expression of the take-all fungus Gaeumannomyces graminis var. tritici on wheat roots. Mol Plant Path 12(9):839854
De Maayer P, Chan WY, Rubagotti E, Venter SN, Toth IK, Birch PR,
Coutinho TA (2014) Analysis of the Pantoea ananatis pangenome reveals factors underlying its ability to colonize and
interact with plant, insect and vertebrate hosts. BMC Genom
15(1):404
de Souza JT, Raaijmakers JM (2003) Polymorphisms within the PrnD and
PltC genes from pyrrolnitrin and pyoluteorin-producing Pseudomonas and Burkholderia spp. FEMS Microbiol Ecol 43:2134
Decoin V, Barbey C, Bergeau D, Latour X, Feuilloley MG, Orange N,
Merieau A (2014) A type VI secretion system is involved in
Pseudomonas fluorescens bacterial competition. PLoS One
9(2):89411
Deslandes L, Rivas S (2012) Catch me if you can: bacterial effectors
and plant targets. Trend Plant Sci 17:644655
Donaldson JR, Shields-Menard S, Barnard JM, Revellame E, Hall JI,
Lawrence A, French WT (2014) Characterization of the novel
Enterobacter cloacae strain JD6301 and a genetically modified
variant capable of producing extracellular lipids. Agricul Food
Analyt Bacteriol 4:212223
Dosselaere F, Vanderleyden J (2001) A metabolic node in action:
chorismate-utilizing enzymes in microorganisms. Crit Rev
Microbiol 27:75131
Duffy BK, Defago G (1997) Zinc improves biocontrol of Fusarium
crown and root rot of tomato by Pseudomonas fluorescens and
represses the production of pathogen metabolites inhibitory to
bacterial antibiotic biosynthesis. Phytopath 87(12):12501257
Duffy BK, Defago G (1999) Environmental factors modulating
antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl Environ Microbio
65(6):24292438
Duffy BK, Defago G (2000) Controlling instability in gacS-gacA
regulatory genes during inoculant production of Pseudomonas
fluorescens biocontrol strains. Appl Environ Microbiol
66(8):31423150
Duffy BK, Defago G (2004) Potential role of pathogen signaling in
multitrophic plant-microbe interactions involved in disease
protection. Appl Environ Microbiol 70(3):18361842
Eastman AW, Weselowski B, Nathoo N, Yuan ZC (2014) Complete
genome sequence of Paenibacillus polymyxa CR1, a plant
growth-promoting bacterium isolated from the corn rhizosphere
exhibiting potential for biocontrol, biomass degradation, and
biofuel production. Genome Announc 2(1):e01218-13
Egamberdiyeva D (2007) The effect of plant growth promoting
bacteria on growth and nutrient uptake of maize in two different
soils. Appl Soil Ecol 36:184189
Eid J, Fehr A, Gray J et al (2009) Real-time DNA sequencing from
single polymerase molecules. Science 323:133138
Farag MA, Zhang H, Ryu CM (2013) Dynamic chemical communication between plants and bacteria through airborne signals:
induced resistance by bacterial volatiles. J Chem Ecol
39(7):10071018
Figueiredo MVB, Burity HA, Martinez CR, Chanway CP (2008)
Alleviation of water stress effects in common bean (Phaseolus
vulgaris L.) by co-inoculation Paenibacillus x Rhizobium tropici.
Applied Soil Ecol 40:182188
Figueiredo MDVB, Seldin L, de Araujo FF, Mariano RDLR (2011)
Plant growth promoting rhizobacteria: fundamentals and applications. In: Maheshwari DK (ed) Plant growth and health
promoting bacteria. Springer, Berlin, pp 2143
Frankowski J, Lorito M, Scala F, Schmidt R, Berg G, Bahl H (2001)
Purification and properties of two chitinolytic enzymes of
Serratia plymuthica HRO-C48. Arch Microbiol 176:421426
Fu Q, Liu C, Ding N, Lin Y, Guo B (2010) Ameliorative effects of
inoculation with the plant growth-promoting rhizobacterium
Pseudomonas sp. DW1 on growth of eggplant (Solanum

melongena L.) seedlings under salt stress. Agric Water Manag
97(12):19942000
Gadd GM (2010) Metals, minerals and microbes: geomicrobiology
and 473 bioremediation. Microbiology 156:609643
Garcion C, Lamotte O, Metraux JP (2007) Mechanisms of defense to
pathogens: biochemistry and physiology. In: Walters DR,
Newton AC, Lyon GD (eds) Induced resistance for plant
defence. Blackwell Publishing, Oxford, pp 109132
Ghignone S, Salvioli A, Anca I, Lumini E, Ortu G, Petiti L, Bonfante
P (2012) The genome of the obligate endobacterium of an AM
fungus reveals an interphylum network of nutritional interactions. ISME J 6(1):136145
Ghosh UD, Saha C, Maiti M, Lahiri S, Ghosh S, Seal A, Mitra Ghosh
M (2014) Root associated iron oxidizing bacteria increase
phosphate nutrition and influence root to shoot partitioning of
iron in tolerant plant Typha angustifolia. Plant Soil
381(12):279295
Glaeser SP, Imani J, Alabid I, Guo H, Kumar N, Kampfer P,
Hartmann A (2015) Non-pathogenic Rhizobium radiobacter F4
deploys plant beneficial activity independent of its host Piriformospora indica. ISME J. doi:10.1038/ismej.2015.163
Glick BR (2010) Using soil bacteria to facilitate phytoremediation.
Biotechnol Adv 28:367374
Glick BR (2012) Plant growth-promoting bacteria: Mechanisms and
applications. Scientifica (Cairo) 115
Glick BR (2015) Biocontrol mechanisms. In: Glick BR (ed)
Beneficial plant-bacterial interactions. Springer, Heidelberg,
pp 123157
Glick BR, Patten CL, Holguin G, Penrose GM (1999) Biochemical
and genetic mechanisms used by plant growth promoting
bacteria. Imperial College Press, London
Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant
growth by ACC deaminase-producing soil bacteria. Eur J Plant
Pathol 119:329339
Guo JK, Ding YZ, Feng RW, Wang RG et al (2015) Burkholderia
metalliresistens sp. nov., a multiple metal-resistant and phosphate-solubilising species isolated from heavy metal-polluted
soil in Southeast China. Antonie van Leeuwenhoek
107(6):15911598
Haas D, Keel C (2003) Regulation of antibiotic production in rootcolonizing Pseudomonas spp. and relevance for biological
control of plant disease. Annu Rev Phytopathol 41:117153
Han J, Sun L, Dong X, Cai Z, Sun X, Yang H, Song W (2005)
Characterization of a novel plant growth-promoting bacteria
strain Delftia tsuruhatensis HR4 both as a diazotroph and a
potential biocontrol agent against various plant pathogens. Syst
Appl MicrobioL 28(1):6676
Hao K, He P, Blom J, Rueckert C, Mao Z, Wu Y, Borriss R (2012a)
The genome of plant growth-promoting Bacillus amyloliquefaciens subsp. plantarum strain YAU B9601-Y2 contains a gene
cluster for mersacidin synthesis. J Bacteriol 194(12):32643265
Hao X, Xie P, Johnstone L, Miller SJ, Rensing C, Wei G (2012b)
Genome sequence and mutational analysis of plant-growthpromoting
bacterium
Agrobacterium
tumefaciens
CCNWGS0286 isolated from a zinc-lead mine tailing. Appl
Environ Microbiol 78:53845394
Heidari M, Golpayegani A (2012) Effects of water stress and
inoculation with plant growth promoting rhizobacteria (PGPR)
on antioxidant status and photosynthetic pigments in basil
(Ocimum basilicum L.). J Sau Soc of Agric Sci 11(1):5761
Henry G, Thonart P, Ongena M (2012) PAMPs, MAMPs, DAMPs
and others: an update on the diversity of plant immunity
elicitors. Biotechnol Agron Soc Environ 16:257268
ber neue Erfahrung und Problems auf dem Gebiet
Hiltner L (1904) U
der Bodenbakteriologie und unter besonderer Berucksichtigung
123

der Grundungung und Brache. Ara Dtsch Landwirt Gellschaft
98:5978
Hossain MJ, Ran C, Liu K, Ryu CM, Rasmussen-Ivey CR, Williams
MA, Liles MR (2015) Deciphering the conserved genetic loci
implicated in plant disease control through comparative
genomics of Bacillus amyloliquefaciens subsp. plantarum. Front
Plant Sci 6:631
Hou Q, Wang C, Guo H, Xia Z, Ye J, Liu K, Ding Y (2015) Draft
genome sequence of Delftia tsuruhatensis MTQ3, a strain of
plant growth-promoting rhizobacterium with antimicrobial
activity. Genome Announc 3(4):e00822-15
Hu D, Li X, Chang Y, He H, Zhang C, Jia N, Wang Z (2012) Genome
sequence of Streptomyces sp. strain TOR3209, a rhizosphere
microecology regulator isolated from tomato rhizosphere. J Bacteriol 194(6):1627
Huang E, Yousef AE (2012) Draft genome sequence of Paenibacillus
polymyxa OSY-DF, which coproduces a lantibiotic, paenibacillin, and polymyxin E1. J Bacteriol 194(17):47394740
Indiragandhi P, Anandham R, Madhaiyan M, Sa TM (2008)
Characterization of plant growth-promoting traits of bacteria
isolated from larval guts of diamondback moth Plutella
xylostella (Lepidoptera: Plutellidae). Curr Microbiol 56:327
333
Jacobs JM, Babujee L, Meng F, Milling A, Allen C (2012) The in
planta transcriptome of Ralstonia solanacearum: conserved
physiological and virulence strategies during bacterial wilt of
tomato. MBio 3:e00114-12
James P (1997) Protein identification in the post-genome era: the
rapid rise of proteomics. Qua Rev Biophysic 30(4):279331
Jeong H, Park SY, Chung WH, Kim SH, Kim N, Park SH, Kim JF
(2011) Draft genome sequence of the Paenibacillus polymyxa
type strain (ATCC 842T), a plant growth-promoting bacterium.
J Bacteriol 193(18):50265027
Jha Y, Subramanian RB (2014) PGPR regulate caspase-like activity,
programmed cell death, and antioxidant enzyme activity in
paddy under salinity. Physiol Mol Biol Plant 20(2):201207
Jing YX, Yan JL, He HD, Yang DJ, Xiao L, Zhong T, Yuan M, Cai
XD, Li SB (2014) Characterization of bacteria in the rhizosphere
soils of polygonum pubescens and their potential in promoting
growth and Cd, Pb, Zn uptake by Brassica napus. Int J
Phytoremed 16:321333
Jones JD, Dang JL (2006) The plant immune system. Nature
444:323329
Kamilova F, Validov S, Azarova T, Mulders I, Lugtenberg B (2005)
Enrichment for enhanced competitive plant root tip colonizers
selects for a new class of biocontrol bacteria. Environ Microbiol
7(11):18091817
Kandasamy S, Loganathan K, Muthuraj R, Duraisamy S, Seetharaman S, Thiruvengadam R, Ramasamy S (2009) Understanding
the molecular basis of plant growth promotional effect of
Pseudomonas fluorescens on rice through protein profiling. Prot
Sci 7(1):47
Kang BG, Kim WT, Yun HS, Chang SC (2010) Use of plant growthpromoting rhizobacteria to control stress responses of plant
roots. Plant Biotechnol Rep 4(3):179183
Kang Y, Shen M, Wang H, Zhao Q (2015) Complete genome
sequence of Bacillus pumilus strain WP8, an efficient plant
growth-promoting
rhizobacterium.
Genome
Announc
3(1):e01452-14
Kaur G, Reddy MS (2014) Influence of P-solubilizing bacteria on
crop yield and soil fertility at multilocational sites. Eur J Soil
Biol 61:3540
Khalid A, Akhtar MJ, Mahmood MH, Arshad M (2006) Effect of
substrate-dependent microbial ethylene production on plant
growth. Microbiology 75:231236
123
Khan MS, Zaidi A, Wani PA (2006) Role of phosphate-solubilizing

microorganisms in sustainable agriculturea review. Agron
Sustain Dev 27:2943
Khan MS, Zaidi A, Wani PA, Oves M (2009) Role of plant growth
promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:119
Khodair TA, Galal GF, El-Tayeb TS (2008) Effect of inoculating
wheat seedlings with exopolysaccharide-producing bacteria in
saline soil. J Appl Sci Res 4:20652070
Kim J, Rees D (1994) Nitrogenase and biological nitrogen fixation.
Biochemistry 33:389397
Kim KY, Jordan D, McDonald GA (1998) Enterobacter agglomerans, phosphate solubilizing bacteria, and microbial activity in
soil: effect of carbon sources. Soil Biol Biochem 30(8):995
1003
Kim BS, Moon SS, Hwang BK (1999) Isolation, identification and
antifungal activity of a macrolide antibiotic, oligomycin A,
produced by Streptomyces libani. Can J Bot 77:850858
Kim JF, Jeong H, Park SY, Kim SB, Park YK, Choi SK, Park SH
(2010) Genome sequence of the polymyxin-producing plantprobiotic rhizobacterium Paenibacillus polymyxa E681. J Bacteriol 192(22):61036104
Kim HJ, Park JY, Han SH, Lee JH, Rong X, Gardener BBM, Kim YC
(2011) Draft genome sequence of the biocontrol bacterium
Chromobacterium
sp.
strain
C-61.
J
Bacteriol
193(23):68036804
Kim BK, Chung JH, Kim SY, Jeong H, Kang SG, Kwon SK, Kim JF
(2012) Genome sequence of the leaf-colonizing bacterium
Bacillus sp. strain 5B6, isolated from a cherry tree. J Bacteriol
194(14):37583759
Kimura N, Yamazoe A, Hosoyama A, Hirose J, Watanabe T, Suenaga
H, Fujihara H, Futagami T, Goto M, Furukawa K (2015) Draft
genome sequence of Pseudomonas abietaniphila KF717 (NBRC
110669), isolated from biphenyl-contaminated soil in Japan.
Genome Announc 3(2):e00059-15
Kloepper JW, Beauchamp CJ (1992) A review of issues related to
measuring colonization of plant roots by bacteria. Can J
Microbiol 38(12):12191232
Kloepper JW, Schroth MN (1981) Plant growth-promoting rhizobacteria and plant growth under gnotobiotic conditions. Phytopathol
71:642644
Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance
and promotion of plant growth by Bacillus spp. Phytopathol
94:12591266
Kloepper JW, Gutierrez-Estrada A, McInroy JA (2007) Photoperiod
regulates elicitation of growth promotion but not induced
resistance by plant growth-promoting rhizobacteria. Can J
Microbio 53(2):159167
Koberl M, White RA, Erschen S, El-Arabi TF, Jansson JK, Berg G
(2015) Draft genome sequence of Paenibacillus polymyxa strain
Mc5Re-14, an antagonistic root endophyte of Matricaria
chamomilla. Genome Announc 3(4):e00861-15
Kohler J, Hernandez JA, Caravaca F, Roldan A (2009) Induction of
antioxidant enzymes is involved in the greater effectiveness of a
PGPR versus AM fungi with respect to increasing the tolerance
of lettuce to severe salt stress. Environ Exp Bot 65(2):245252
Kohler C, Lourenco RF, Bernhardt J, Albrecht D, Schuler J, Hecker
M, Gomes SL (2015) A comprehensive genomic, transcriptomic
and proteomic analysis of a hyperosmotic stress sensitive aproteobacterium. BMC Microbiol 15(1):71
Kojic M, Degrassi G, Venturi V (1999) Cloning and characterization
of the rpoS gene from the plant growth-promoting Pseudomonas
putida WCS358: RpoS is not involved in siderophore and
homoserine lactone production. Biochem Biophys Acta
1489:413420

Kumar V, Behl RK, Narula N (2001) Establishment of phosphate
solubilizing strains of Azotobacter chroococcum in the rhizosphere and their effect on wheat cultivars under greenhouse
conditions. Microbiol Res 156:8793
Lee SY, Kim BY, Ahn JH, Song J, Seol YJ, Kim WG, Weon HY
(2012) Draft genome sequence of the biocontrol bacterium
Bacillus amyloliquefaciens strain M27. J Bacteriol
194(24):69346935
Lefort F, Calmin G, Pelleteret P, Farinelli L, Osteras M, Crovadore J
(2014) Whole-genome shotgun sequence of Bacillus amyloliquefaciens strain UASWS BA1, a bacterium antagonistic to plant
pathogenic fungi. Genome Announc 2(1):e00016-14
Lekberg Y, Koide RT (2014) Integrating physiological, community,
and evolutionary perspectives on the arbuscular mycorrhizal
symbiosis. Botanty 92:241251
Li S, Yang D, Qiu M, Shao J, Guo R, Shen B, Shen Q (2014)
Complete genome sequence of Paenibacillus polymyxa SQR-21,
a plant growth-promoting rhizobacterium with antifungal activity and rhizosphere colonization ability. Genome Announc
2(2):e00281-14
Liang S, Jin D, Wang X, Fan H, Bai Z (2015) Draft genome sequence
of Paenibacillus polymyxa EBL06, a plant growth-promoting
bacterium isolated from wheat phyllosphere. Genome Announc
3(3):0041400415
Lim JH, Kim SD (2013) Induction of drought stress resistance by
multi-functional PGPR Bacillus licheniformis K11 in Pepper.
Plant Pathol J 29(2):201
Lim HS, Kim YS, Kim SD (1991) Pseudomonas stutzeri YPL-1
genetic transformation and antifungal mechanism against Fusarium solani, an agent of plant root rot. Appl Environ Microbiol
57:510516
Liu WY, Wong CF, Chung KMK, Jiang JW, Leung FCC (2013)
Comparative genome analysis of Enterobacter cloacae. PLoS
One 8:115
Loper JE, Henkels MD (1999) Utilization of Heterologous siderophores enhances levels of iron available to Pseudomonas
putida in the rhizosphere. Appl Environ Microbiol
65(12):53575363
Loper JE, Kobayashi DY, Paulsen IT (2007) The genomic sequence
of Pseudomonas fluorescens Pf-5: insights into biological
control. Phytopathology 97(2):233238
Loper JE, Hassan KA, Mavrodi DV, Davis EW et al (2012)
Comparative genomics of plant-associated Pseudomonas spp.:
insights into diversity and inheritance of traits involved in
multitrophic interactions. PLoS Gen 8:1002784
Lubeck PS, Hansen M, Sorensen J (2000) Simultaneous detection of
the establishment of seed-inoculated Pseudomonas fluorescens
strain Dr54 and native soil bacteria on sugar beet root surfaces
using fluorescence antibody and in situ hybridization techniques.
FEMS Microbiol Ecol 33:1119
Lugtenberg B (2015) Life of microbes in the rhizosphere. In:
Lugtenberg B (ed) Principles of plant-microbe interactions.
Springer, Heidelberg, pp 715
Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541556
Lugtenberg BJJ, Dekkers L, Bloemberg GV (2001) Molecular
determinants of rhizosphere colonization by Pseudomonas.
Annu Rev Phytopathol 39:461490
Ma M, Wang C, Ding Y, Li L, Shen D, Jiang X et al (2011) Complete
genome sequence of Paenibacillus polymyxa SC2, a strain of
plant growth-promoting rhizobacterium with broad-spectrum
antimicrobial activity. J Bacteriol 193(1):311312
Maffei ME, Arimura GI, Mithofer A (2012) Natural elicitors,
effectors and modulators of plant responses. Nat Prod Rep
29(11):12881303
Magno-Perez C, Martinez-Garcia PM, Hierrezuelo J, RodriquezPalenzuela P, Arrebola E, Ramos C, Romero DF (2015)

Comparative genomics within the Bacillus genus reveal the
singularities of two robust Bacillus amyloliquefaciens biocontrol
strains. Mol Plant 28(10):11021116
Manzoor S, Niazi A, Bejai S, Meijer J, Bongcam-Rudloff E (2013)
Genome sequence of a plant-associated bacterium, Bacillus
amyloliquefaciens
strain
UCMB5036.
Gen
Announc
1(2):e00111e00113
Marchi M, Boutin M, Gazengel K, Rispe C, Gauthier JP, GuillermErckelboudt AY, Lebreton L, Barret M, Daval S, Sarniguet A
(2013) Genomic analysis of the biocontrol strain Pseudomonas
fluorescens Pf29Arp with evidence of T3SS and T6SS gene
expression on plant roots. Environ Microbiol Rep 5:393403
Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben
LA, Volkmer GA (2005) Genome sequencing in microfabricated
high-density picolitre reactors. Nature 437(7057):376380
Mathimaran N, Srivastava R, Wiemken A, Sharma AK, Boller T
(2012) Genome sequences of two plant growth-promoting
fluorescent Pseudomonas strains, R62 and R81. J Bacteriol
194(12):32723273
Matilla MA, Pizarro-Tobias P, Roca A, Fernandez M, Duque E,
Molina L, Ramos JL (2011) Complete genome of the plant
growth-promoting rhizobacterium Pseudomonas putida BIRD-1.
J Bacteriol 193(5):1290
Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria
that confer resistance to water stress in tomatoes and peppers.
Plant Sci 166:525
McKenzie RH, Roberts TL (1990) Soil and fertilizers phosphorus
update. In: Proceedings of Alberta soil science workshop
proceedings, Edmonton, Alberta. p 84104 Feb 2022
Merino E, Jensen RA, Yanofsky C (2008) Evolution of bacterial trp
operons and their regulation. Curr Opin Microbiol 11:7886
Molina L, Constantinescu F, Reimmann C, Duffy C, Defago G (2003)
Degradation of pathogen quorum-sensing molecules by soil
bacteria: a preventive and curative biological control mechanism. FEMS Microbiol Ecol 45:7181
Montor-Antonio JJ, Sachman-Ruiz B, Lozano L, Del Moral S (2015)
Draft genome sequence of Bacillus amyloliquefaciens JJC33M,
isolated from sugarcane soils in the Papaloapan region, Mexico.
Genome Announce 3(1):e01519-14
Nadeem SM, Zahir ZA, Naveed M, Arshad M (2007) Preliminary
investigations on inducing salt tolerance in maize through
inoculation with rhizobacteria containing ACC deaminase
activity. Can J Microbiol 53:11411149
Nadeem SM, Zahir ZA, Naveed M, Arshad M (2009) Rhizobacteria
containing ACC-deaminase confer salt tolerance in maize grown
on salt-affected fields. Can J Microbiol 55:13021309
Neilands JB (1995) Siderophores: structure and function of microbial
iron transport compounds. J Biol Chem 270:2672326726
Neubauer U, Nowack B, Furrer G, Schulin R (2000) Heavy metal
sorption on clay minerals affected by the siderophore desferrioxamine B. Environ Sci Technol 34(13):27492755
Newman MA, Sundelin T, Nielsen JT, Erbs G (2013) MAMP
(microbe associated molecular pattern) triggered immunity in
plants. Front Plant Sci 4:139
Newton JA, Fray RG (2004) Integration of environmental and hostderived signals with quorum sensing during plantmicrobe
interactions. Cell Microbiol 6(3):213224
Nia SH, Zarea MJ, Rejali F, Varma A (2012) Yield and yield
components of wheat as affected by salinity and inoculation with
Azospirillum strains from saline or non-saline soil. J Saudi Soc
Agric Sci 11:113121
Niazi A (2014) Genome-wide analyses of Bacillus amyloliquefaciens
strains provide insights into their beneficial role on plants. Thesis
123

submitted to Swedish University of Agricultural Sciences,
Uppsala
Niazi A, Manzoor S, Asari S, Bejai S, Meijer J, Bongcam-Rudloff E
(2014) Genome analysis of Bacillus amyloliquefaciens subsp.
plantarum UCMB5113: a rhizobacterium that improves plant
growth and stress management. PLoS One 9(8):e104651
Nielsen TH, Sorensen J (2003) Production of cyclic lipopeptides by
Pseudomonas fluorescens strains in bulk soil and in the sugar
beet rhizosphere. Appl Environ Microbiol 69:861868
Niu B, Rueckert C, Blom J, Wang Q, Borriss R (2011) The genome of
the plant growth-promoting rhizobacterium Paenibacillus polymyxa M-1 contains nine sites dedicated to nonribosoml synthesis
of lipopeptides and polyketides. J Bacteriol 193(20):58625863
Olivares J, Bedmar EJ, Sanjuan J (2013) Biological nitrogen fiation in
the context of global change. Mol Plant 26:486494
Ovadis M, Liu X, Gavriel S, Ismailov Z, Chet I, Chernin L (2004) The
global regulator genes from biocontrol strain Serratia plymuthica
IC1270: cloning, sequencing, and functional studies. J Bacteriol
186:49864993
Pan HQ, Hu JC (2015) Draft genome sequence of the novel strain
Pseudomonas sp. 10B238 with potential ability to produce
antibiotics from deep-sea sediment. Marine Genom 23:5557
Park JY, Han SH, Lee JH, Han YS, Lee YS, Rong X, Kim YC (2011)
Draft genome sequence of the biocontrol bacterium Pseudomonas putida B001, an oligotrophic bacterium that induces
systemic resistance to plant diseases. J Bacteriol
193(23):67956796
Parray JA, Kamili AN, Reshi ZA, Hamid R, Qadri RA (2013)
Screening of beneficial properties of rhizobacteria isolated from
Saffron (Crocus sativus L.) rhizosphere. Afr J Microbiol Res
7(23):29052910
Parray JA, Kamili AN, Reshi ZA, Qadri RA, Jan S (2015)
Interaction of rhizobacterial strains for growth improvement
of Crocus sativus L. under tissue culture conditions. Plant Cell
Tiss Organ Cul 121(2):325334
Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3- acetic
acid. Can J Microbiol 42:207220
Paul D, Nair S (2008) Stress adaptations in a plant growth promoting
rhizobacterium (PGPR) with increasing salinity in the coastal
agricultural soils. J Basic Microbiol 48(5):378
Paul D, Dineshkumar N, Nair S (2006) Proteomics of a plant growthpromoting rhizobacterium, Pseudomonas fluorescens MSP-393,
subjected to salt shock. World J Microbiol Biotechnol 22(Suppl
4):369374
Pavel VL, Sobariu DL, Fertu IDT, Statescu F, Gavrilescu M (2013)
Symbiosis in the environment biomanagement of soils contaminated with heavy metals. Europ J Sci Theol 9:211224
Picard C, Di Cello F, Ventura M, Fani R, Guckert A (2000)
Frequency and biodiversity of 2,4-diacetylphloroglucinol-producing bacteria isolated from the maize rhizosphere at
different stages of plant growth. Appl Environ Microbiol
66:948955
Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C (2015)
Microbial interactions in the rhizosphere: beneficial influences of
plant growth-promoting rhizobacteria on nutrient acquisition
process- a review. Biol Fertil Soil 51:403415
Qurashi AW, Sabri AN (2012) Bacterial exopolysaccharide and
biofilm formation stimulate chickpea growth and soil aggregation under salt stress. Braz J Microbiol 11:8391
Raaijmakers JM, Vlami M, de Souza JT (2002) Antibiotic production
by bacterial biocontrol agents. Antonie Leeuwenhoek
81:537547
Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of
siderophore-producing bacteria for improving heavy metal
phytoextraction. Trends Biotechnol 28:142149
123
Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives

of plant-associated microbes in heavy metal phytoremediation.
Biotechnol Adv 30:15621574
Ramadoss D, Lakkineni VK, Bose P, Ali S, Annapurna K (2013)
Mitigation of salt stress in wheat seedlings by halotolerant
bacteria isolated from saline habitats. Springer Plus 2(6):17
Ravel J, Cornelis P (2003) Genomics of pyoverdine-mediated iron
uptake in pseudomonads. Trends Microbiol 11:195200
Redondo-Nieto M, Barret M, Morrisey JP, Germaine K, MartnezGranero F, Barahona E, Rivilla R (2012) Genome sequence of
the biocontrol strain Pseudomonas fluorescens F113. J Bacteriol
194(5):12731274
Rojas A, Holguin G, Glick BR, Bashan Y (2001) Synergism between
Phyllobacterium sp. (N2-fixer) and Bacillus licheniformis (Psolubilizer), both from a semiarid mangrove rhizosphere. FEMS
Microbiol Ecol 35(2):181187
Rong X, Gurel FB, Meulia T, Gardener BBM (2012) Draft genome
sequences of the Pseudomonas fluorescens biocontrol strains
Wayne1R and Wood1R. J Bacteriol 194(3):724725
Roquigny R, Arseneault T, Gadkar VJ, Novinscak A, Joly DL, Filion
M (2015) Complete genome sequence of biocontrol strain
Pseudomonas fluorescens LBUM223. Genom Announc
3(3):e00443-15
Rusk N (2011) Torrents of sequence. Nat Meth 8:44
Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspective of
plant growth promoting rhizobacteria (PGPR) containing ACC
deaminase in stress agriculture. J Indian Microbiol Biotechnol
34:635648
Saleh SS, Glick BR (2001) Involvement of gacS and rpoS in
enhancement of the plant growth-promoting capabilities of
Enterobacter cloacae CAL2 and Pseudomonas putida UW4. Can
J Microbiol 47:698705
Salvioli A, Ghignone S, Novero M, Navazio L, Bagnaresi P, Bonfante
P (2015) Symbiosis with an endobacterium increases the fitness
of a mycorrhizal fungus, raising its bioenergetic potential. ISME
J 10(1):130144
Sandhya V, Grover M, Reddy G, Venkateswarlu B (2009) Alleviation
of drought stress effects in sunflower seedlings by the
exopolysaccharides producing Pseudomonas putida strain
GAP-P45. Biol Fertil Soil 46(1):1726
Santner A, Calderon-Villalobos LIA, Estelle M (2009) Plant
hormones are versatile chemical regulators of plant growth.
Nat Chem Biol 5:301307
Schenk PM, Carvalhais LC, Kazan K (2012) Unraveling plantmicrobe interactions: can multi-species transcriptomics help?
Trend Biotechnol 30(3):177184
Schmidt W (1999) Mechanisms and regulation of reduction-based
iron uptake in plants. New Phytol 141:126
Sessitsch A, Coenye T, Sturz AV, Vandamme P, Ait Barka E, Salles
JF, van Elsas JF, Faure D, Reiter B, Glick BR, Wang-Pruski G,
Nowak J (2005) Burkholderia phytofirmans sp. nov., a novel
plantassociated bacterium with plant beneficial properties. Int J
Syst Evol Microbiol 55:11871192
Seul K, Park S, Ryu C, Lee Y, Ghim S (2007) Proteome analysis of
Paenibacillus polymyxa E681 affected by barley. J Microbiol
Biotechnol 17(6):934
Shaharoona B, Arshad M, Khalid A (2007a) Differential response of
etiolated pea seedlings to inoculation with rhizobacteria capable
of utilizing 1-aminocyclopropane-1-carboxylate or L-methionine. J Microbiol 45:1520
Shaharoona B, Jamro GM, Zahir ZA, Arshad M, Memon KS (2007b)
Effectiveness of various Pseudomonas spp. and Burkholderia
caryophylli containing ACC-deaminase for improving growth
and yield of wheat (Triticum aestivum L.). J Microbiol Biotechnol 17:13001307

Shaharoona B, Naveed M, Arshad M, Zahir ZA (2008) Fertilizerdependent efficiency of Pseudomonads for improving growth,
yield, and nutrient use efficiency of wheat (Triticum aestivum
L.). Appl Microbiol Biotechnol 79:147155
Shanker AK, Maheswari M, Yadav SK, Desai S, Bhanu D, Attal NB,
Venkateswarlu B (2014) Drought stress responses in crops.
Funct Integ Genom 14(1):1122
Shao J, Li S, Zhang N, Cui X, Zhou X, Zhang G, Zhang R (2015)
Analysis and cloning of the synthetic pathway of the
phytohormone indole-3-acetic acid in the plant-beneficial
Bacillus amyloliquefaciens SQR9. Microb Cell factor
14(1):130
Sharma A, Johri BN, Sharma AK, Glick BR (2003) Plant growthpromoting bacterium Pseudomonas sp. strain GRP3 influences
iron acquisition in mung bean (Vigna radiata L. Wilzeck). Soil
Biol Biochem 35:887894
Shen X, Hu H, Peng H, Wang W, Zhang X (2013) Comparative
genomic analysis of four representative plant growth-promoting
rhizobacteria in Pseudomonas. BMC Genom 14(1):1
Shin SH, Kim S, Kim JY, Song HY, Cho SJ, Lee KI, Yang KS (2012)
Genome sequence of Paenibacillus terrae HPL-003, a xylanaseproducing bacterium isolated from soil found in forest residue.
J Bacteriol 194(5):1266
Shoresh M, Harman GE (2010) Differential expression of maize
chitinases in the presence or absence of Trichoderma harzianum
strain T22 and indications of a novel exo-endo-heterodimeric
chitinase activity. BMC Plant Biol 10(1):136
Singh S, Kapoor KK (1999) Inoculation with phosphate-solubilizing
microorganisms and a vesicular-arbuscular mycorrhizal fungus
improves dry matter yield and nutrient uptake by wheat grown in
a sandy soil. Bio Fert Soil 28(2):139144
Singh PP, Shin YC, Park CS, Chung YR (1999) Biological control of
Fusarium wilt of cucumber by chitinolytic bacteria. Phytopath
89:9299
Smith KP, Handelsman J, Goodman RM (1999) Genetic basis in
plants for interactions with disease-suppressive bacteria. Proc
Natl Acad Sci USA 96:47864790
Song JY, Kim HA, Kim JS, Kim SY, Jeong H, Kang SG et al (2012)
Genome sequence of the plant growth-promoting rhizobacterium
Bacillus sp. strain JS. J Bacteriol 194(14):37603761
Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol 3(4):a001438
Spaepen S, Vanderleyden J, Remans R (2007) Indole- 3-acetic acid in
microbial and microorganism-plant signaling. FEMS Microbiol
Rev 31:425448
Sturz AV, Christie BR, Matheson BG, Arsenault WJ, Buchanan NA
(1999) Endophytic communities in the periderm of potato tubers
and their potential to improve resistance to soil-borne plant
pathogens. Plant Pathol 48:360369
Suarez C, Cardinale M, Ratering S, Steffens D, Jung S, Montoya
AMZ, Schnell S (2015) Plant growth-promoting effects of
Hartmannibacter diazotrophicus on summer barley (Hordeum
vulgare L.) under salt stress. Appl Soil Ecol 95:2330
Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens
N, Barac T, Vangronsveld J, van der Lelie D (2009) Genome
survey and characterization of endophytic bacteria exhibiting a
beneficial effect on growth and development of poplar trees. App
Taghavi S, van der Lelie D, Hoffman A, Zhang Y-B, Walla MD et al
(2010) Genome sequence of the plant growth promoting
endophytic bacterium Enterobacter sp. 638. PLoS Genet
6(5):e1000943
Tangahu BV, Sheikh Abdullah SR, Basri H, Idris M, Anuar N,
Mukhlisin M (2011) A review on heavy metals (As, Pb, and Hg)
uptake by plants through phytoremediation. Int J Chem Eng.
Article ID 939161
Ting ASY (2015) Microbial cells dead or alive: prospect, potential

and innovations for heavy metal removal. In: Chandra R (ed)
Advances in biodegradation and bioremediation of industrial
waste. CRC Press, Boca Raton, pp 3166
Tong YJ, Ji XJ, Liu LG, Shen MQ, Huang H (2013) Genome
sequence of Paenibacillus polymyxa ATCC 12321, a promising
strain for optically active (R, R)-2, 3-butanediol production.
Genome Announc 1(4):e00572-13
Toyoda H, Utsumi R (1991) Method for the prevention of Fusarium
diseases and microorganisms used for the same. U.S. Patent No.
4,988,586
Trippe K, McPhail K, Armstrong D, Azevedo M, Banowetz G (2013)
Pseudomonas fluorescens SBW25 produces furanomycin, a nonproteinogenic amino acid with selective antimicrobial properties.
BMC Microbiol 13:111
Udaondo Z, Molina L, Segura A, Duque E, Ramos JL (2015) Analysis
of the core genome and pangenome of Pseudomonas putida.
Ullah A, Heng S, Munis MFH, Fahad S, Yang X (2015a) Phytoremediation of heavy metals assisted by plant growth promoting
(PGP) bacteria: a review. Environ Exp Bot 117:2840
Ullah A, Mushtaq H, Ali H, Munis MFH, Javed MT, Chaudhary HJ
(2015b) Diazotrophs- assisted phytoremediation of heavy metals: a novel approach. Environ Sci Pollut Res 22:25052514
Upadhyay SK, Singh JS, Saxena AK, Singh DP (2011) Impact of
PGPR inoculation on growth and antioxidant status of wheat
under saline conditions. Plant Biol 14:605611
Validov SZ, Kamilova F, Lugtenberg BJ (2009) Pseudomonas putida
strain PCL1760 controls tomato foot and root rot in stonewool
under industrial conditions in a certified greenhouse. Biol
Control 48(1):611
Vanderschuren H, Lentz E, Zainuddin I, Gruissem W (2013)
Proteomics of model and crop plant species: status, current
limitations and strategic advances for crop improvement.
J Proteom 93:519
Vansuyt G, Robin A, Briat JF, Curie C, Lemanceau P (2007) Iron
acquisition from Fe-pyoverdine by Arabidopsis thaliana. Mol
Plant Microb Interact 20:441447
Verma SC, Ladha JK, Tripathi AK (2001) Evaluation of plant growth
promoting and colonization ability of endophytic diazotrophs
from deep water rice. J Biotech 91(2):127141
Vessey JK (2003) Plant growth-promoting rhizobacteria as biofertilizers. Plant Soil 255:571586
Walker V, Couillerot O, Von Felten A, Bellvert F, Jansa J, Maurhofer
M et al (2011) Variation of secondary metabolite levels in maize
seedling roots induced by inoculation with Azospirillum, Pseudomonas and Glomus consortium under field conditions. Plant
Soil 356:151163
Walters D, Walsh D, Newton A, Lyon G (2005) Induced resistance
for plant disease control: maximizing the efficacy of resistance
elicitors. Phytopathology 95(12):13681373
Walters DR, Ratsep J, Havis ND (2013) Controlling crop diseases
using induced resistance: challenges for the future. J Exp Bot
64:12631280
Wang Y, Brown HN, Crowley DE, Szaniszlo PJ (1993) Evidence for
direct utilization of a siderophore, ferrioxamine B in axenically
grown cucumber. Plant Cell Environ 16:579585
Weilharter A, Mitter B, Shin MV, Chain PS, Nowak J, Sessitsch A
(2011) Complete genome sequence of the plant growth-promoting endophyte Burkholderia phytofirmans strain PsJN. J Bacteriol
193(13):33833384
Werner D (2005) Production and biological nitrogen fixation of
tropical legumes. In: Nitrogen fixation in agriculture, forestry,
ecology, and the environment. Springer, pp 113
Whipps JM (2001) Microbial interactions and biocontrol in the
rhizosphere. J Exp Bot 52(1):487511
123

Wiesel L, Newton AC, Elliott I (2014) Molecular effects of resistance
elicitors from biological origin and their potential for crop
protection. Front Plant Sci 5:655
Wisniewski-Dye F, Vial L, Burdman S, Okon Y, Hartmann A (2015)
Phenotypic variation in Azospirillum spp and other root-associated bacteria. In: De Bruijn FJ (ed) Biological nitrogen fixation.
Wiley, Hoboken, pp 10471054
Xu Y, Wang A, Tao F, Su F, Tang H, Ma C, Xu P (2012) Genome
sequence of Enterobacter cloacae subsp. dissolvens SDM, an
efficient biomass-utilizing producer of platform chemical 2,3butanediol. J Bacteriol 194(4):897898
Yadav J, Verma JP, Jaiswal DK, Kumar A (2014) Evaluation of
PGPR and different concentration of phosphorus level on plant
growth, yield and nutrient content of rice (Oryza sativa). Ecol
Eng 62:123128
Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help
plants tolerate abiotic stress. Trend Plant Sci 14(1):14
Yao L, Wu Z, Zheng Y, Kaleem I, Li C (2010) Growth promotion and
protection against salt stress by Pseudomonas putida Rs-198 on
cotton. Eur J Soil Biol 46:4954
Yong X, Chen Y, Liu W, Xu L, Zhou J, Wang S, Chen P, Ouyang P,
Zheng T (2014) Enhanced cadmium resistance and accumulation
in Pseudomonas putida KT2440 expressing the phytochelatin
synthase gene of Schizosaccharomyces po mbe. Lett Appl
Microbiol 58:255261
Younesi O, Moradi A (2014) Effects of plant growth-promoting
rhizobacterium (PGPR) and arbuscular mycorrhizal fungus
(AMF) on antioxidant enzyme activities in salt-stressed bean
(Phaseolus vulgaris L.). Agric 60(1):1021
123
Yue HT, Mo WP, Li C, Zheng YY, Li H (2007) The salt stress relief
and growth promotion effect of Rs-5 on cotton. Plant Soil
297(12):139145
Zahir ZA, Munir A, Asghar HN, Shaharoona B, Arshad M (2008)
Effectiveness of rhizobacteria containing ACC-deaminase for
growth promotion of pea (Pisum sativum) under drought
conditions. J Microbiol Biotechnol 18:958963
Zahir ZA, Ghani U, Naveed M, Nadeem SM, Asghar HN (2009)
Comparative effectiveness of Pseudomonas and Serratia sp.
containing ACC-deaminase for improving growth and yield of
wheat (Triticum aestivum L.) under salt-stressed conditions.
Arch Microbiol 191:415424
Zahran HH (2001) Rhizobia from wild legumes: diversity, taxonomy,
ecology, nitrogen fixation and biotechnology. J Biotechnol
91:143153
Zaidi A, Khan MS, Ahemad M, Oves M (2009) Plant growth
promotion by phosphate solubilizing bacteria. Acta Microbiol
Immunol Hung 56:263284
Zhang L, Birch RG (1996) Biocontrol of sugar cane leaf scald disease
by an isolate of Pantoea dispersa which detoxifies albicidin
phytotoxins. Lett Appl Microbiol 22:132136
Zhang H, Murzello C, Sun Y, Kim MS, Xie X, Jeter RM, Pare PW
(2010) Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Mol Plant
23(8):10971104
Zhao X, de Jong A, Zhou Z, Kuipers OP (2015) Complete genome
sequence of Bacillus amyloliquefaciens strain BH072, isolated
from honey. Genome Announc 3(2):e00098-15

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Current Perspectives on Plant GrowthPromoting Rhizobacteria

Javid A.Parray, Sumira Jan, Azra

Your article is protected by copyright and all

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Current Perspectives on Plant Growth-Promoting Rhizobacteria

Received: 22 October 2015 / Accepted: 23 December 2015

& Parvaiz Ahmad

Center for Research and Development (CORD), University of

ICAR- Central Institute of Temperate Horticulture, Rangreth,

Department of Biotechnology, University of Kashmir,

Department of Microbiology and Biotechnology, Faculty of

Department of Botany, S.P. College, Srinagar,

microbe-derived and plant-derived protein and metabolite

Author's personal copy

still under debate (Glick 2012). Nevertheless, few studies

PGPR and Their Potential in Improving Plant

efficiently due to their inability to survive and compete in the

Author's personal copy

5-fold increase in Cd accumulation, which led to an increase

depending on the plant tissue. Exposure of an athkt1

Author's personal copy

conditions (Fu and others 2010). According to this study,

Author's personal copy

(VOCs) and proteins like heat-shock proteins (HSPs) and

Mechanism of Action of PGPR

Author's personal copy

applied phosphatic fertilizers, and the rest are rapidly

(Singh and Kapoor 1999), Bradyrhizobium japonicum

Author's personal copy

1995). In the aerobic environment, iron occurs principally

chlorotic symptoms and iron chlorophyll a and chlorophyll

Author's personal copy

stimulates seed and tuber germination; increases the rate of

biosynthesis via indole-3-acetamide formation is reported

Author's personal copy

major indirect mechanism of plant growth promotion in

Author's personal copy

others 2000). Plant host genotype also plays a significant

Author's personal copy

biocontrol agents. Recently, it has been discovered that

collectively be described as patterns that elicit immunity

Author's personal copy

Fig. 2 Schematic representation of induced systemic resistance

ISR defense via inoculation with plant growth-promoting

mechanisms involved in the plant associated lifestyle and

Genomic Sequencing in PGPR Strains

Manzoor and others (2013) illustrated the whole genome

Koberl and others (2015)

Bacillus amyloliquefaciens strain Co1-6

Bacillus pumilus strain WP8

Delftia tsuruhatensis MTQ3

Streptomyces sp. strain TOR3209

Mitsuaria sp. strain H24L5A

Rhizobium sp. strain CF142

Brown and others (2012)

Pantoea sp. strain GM01

Pantoea sp. strain YR343

Kim and others (2012)

Pantoea ananatis B1-9

Weilharter and others (2011)

Burkholderia phytofirmans PsJNT

Taghavi and others (2010)