Journal of Pure and Applied Microbiology, June 2018. Vol. 12(2), p.

733-749

Plant Growth Promoting Rhizobacteria (PGPR) -

Prospective and Mechanisms: A Review
V. Jeyanthi and S. Kanimozhi

P.G. & Research Department of Microbiology, Asan Memorial

College of Arts and Science, Chennai, India.

http://dx.doi.org/10.22207/JPAM.12.2.34

(Received: 10 April 2018; accepted: 12 May 2018)

Plant growth-promoting rhizobacteria (PGPR) are naturally occurring soil bacteria

that colonize plant roots, which is an important environment for plant microbe interactions.
PGPR have attracted special attention for their ability to enhance productivity, sustainability
and profitability when food security and rural livelihood are a key priority. Chemical fertilizers
used in agriculture and pathogenic microorganisms attacking plants show harmful impact on
the ecosystem. The potentiality of PGPR offers an attractive way to replace the use of chemical
fertilizers, pesticides and other supplements. PGPR affect plant growth and development directly
or indirectly, either by releasing plant growth regulators or other biologically active substances,
and uptake of nutrients through fixation and mobilization, reducing harmful effects of pathogenic
microorganisms on plants and by employing multiple mechanisms of action. Besides they play
an important role in soil fertility. This review intends to elucidate the diverse mechanism of
plant growth promoting rhizobacteria in promoting crop production and developing sustainable
agriculture.

Keywords: PGPR, Siderophore, Phytohormone, Antibiosis, ISR.

Agriculture, the science or the practice ecosystem function (Bishnoi, 20152). Agricultural
of cultivating plants, animals and other life forms, sustainability, food security and energy renewability
is certainly one of the factors that boost human depends on a healthy and fertile soil. Imbalance in
civilization and development. Development of nitrogen cycling, nutritional status, physical and
agriculture is an evolutionary process that ultimately biological properties of soil, incidence of pests and
transformed plants from being independent, wild diseases, fluctuating climatic factors and abiotic
progenitors into fully dependent, domesticated stresses are the interlinked contributing factors for
cultivars with the concomitant evolution of reduced agricultural productivity ((Gopalakrishnan
agricultural economics (Zeder, 2009 1). This et al., 2015 3).). The existing approaches to
relationship between humans, the earth and food agriculture include the use of chemical fertilizers,
sources further confirm soil as the foundation herbicides, fungicides and insecticides. These
of agriculture, and microbes play a vital role fertilizers have become essential components of
in sustaining our natural ecosystems. Soil, the modern agriculture because they provide essential
dynamic and valuable natural resource harbouring plant nutrients such as nitrogen, phosphorus and
a vast collection of microorganisms, is vital for the potassium. However, the overuse of fertilizers
production of food and fibre, in addition involved can cause unanticipated environmental impacts
in the maintenance of global nutrient balance and (Shenoy et al., 20014; Adesemoye et al., 20095)
and encounter problems such as, development of
resistance by pathogen to fungicides and rapid
* To whom all correspondence should be addressed.
Tel.: +91 98401 31519;
degradation of the chemicals.
E-mail:[email protected]
734 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria

Towards a sustainable agricultural compounds, such as sugars, organic acids, amino

vision, crops produced need to be equipped acids, enzymes, growth factors and others. The
with disease resistance, salt tolerance, drought composition of these exudates is dependent upon
tolerance, heavy metal stress tolerance and the physiological status and species of plants and
better nutritional value. To accomplish the above microorganisms (Kang et al., 201016). Moreover,
desired crop properties, one possibility is to use these exudates also promote the plant-beneficial
soil microorganisms. The main functions of these symbiotic interactions and inhibit the growth of
bacteria are (1) to supply nutrients to crops, (2) the competing plant species (Nardi et al., 200017;
to stimulate plant growth, (3) to control or inhibit Haas and Defago, 200518). The sugars, amino acids,
the activity of plant pathogens, (4) to improve soil flavanoids, proteins, and fatty acids secreted by
structure, and (5) bioaccumulation or microbial plant roots help to structure the associated soil
leaching of inorganics (Hayat et al., 2010 6). microbiome (Badri et al., 200919; Dennis et al.,
More recently, bacteria have also been used in 201020; Doornbos et al., 201221). The quantity
soil for the mineralization of organic pollutants, and composition of root exudates vary with
i.e. bioremediation of polluted soils (Burd et al., plant developmental stage and the proximity to
20007; Zhuang et al., 20078; Zaidi et al., 20089). neighbouring species (Chaparro et al., 201222).
Multiple types of biological interactions between From these plant-derived small organic molecules,
microorganisms and plants take place in the soil a fraction is further metabolized by microorganisms
(Gouda et al., 201810). This review provides an in the surrounding area as carbon and nitrogen
environment friendly approach to increase crop sources, and some microbe-oriented molecules are
production and health, development of sustainable subsequently re-taken up by plants for growth and
agriculture as well as fertility of soil exploiting development (Kang et al., 201016).
plant growth promoting rhizobacteria Apart from the rhizosphere, the rhizoplane
Rhizosphere is the root surface including the strongly adhering
Rhizosphere is a well characterized soil particles while the root itself is a component
ecological niche comprising volume of soil of the system, because many micro-organisms
surrounding plant roots with highest bacterial (like endophytes) also colonize the root tissues
population that are influenced by root exudates as (Barea et al., 200523). Plant rhizospheric region
defined by Hiltner (190411). Diverse communities is a dynamic and versatile environment of acute
of beneficial soil microorganisms are associated plant microbe interactions for tackling essential
with the root systems of all higher plants (Khalid macro and micro nutrients from a confined nutrient
et al., 200612). It is quiet common that the bacterial pool. They play a significant role both under
population in the rhizosphere are 100–1,000 times stressed and normal conditions for improving
higher than the surrounding soil, also known as the plant growth and developmental processes (Zahir
bulk soil which are not penetrated by plant roots et al., 200424; Glick et al., 200725). Currently, it
and have lower microbial communities within it. is recognized that the rhizosphere microbiome
In contrast the rhizosphere is heavily influenced by harbours thousands of different bacterial, archaeal,
microbes that possess metabolic versatility to adapt viruses, fungal and other eukaryotic taxa (Lagos
and utilize root exudates efficiently. Also, 15% of et al., 201526). Though numerous microorganisms
the root surface is covered by microbial populations coexist in the rhizospheric region, bacteria are the
belonging to several bacterial species (Jha et al., abundant among them. The bacteria colonizing
201013; Govindasamy et al., 201114). Plant roots the rhizosphere habitat are called rhizobacteria
synthesize, accumulate and secrete a diverse array (Kloepper et al., 199127) which influence the
of compounds. The exudation of a wide range of plant growth in a most significant manner (Uren,
chemical compounds modifies the chemical and 200728). Rhizospheric bacteria participate in the
physical properties of the soil and thus, regulates geochemical cycling of nutrients especially carbon,
the structure of soil microbial community in nitrogen, phosphorus and micronutrients as iron,
the immediate vicinity of root surface (Dakora manganese, zinc and copper, and determine their
and Phillips, 200215). Root exudates include the availability for plants and soil microbial community.
releasing of ions, oxygen, water, and organic Plant carbon photosynthates allocated to the root

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 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria 735

and rhizosphere are key microbial activities (Illangumaran and Smith, 201736). One of the
important for plant nutrition such as organic matter mechanisms by which bacteria are adsorbed onto
decomposition, phosphate solubilisation, nitrogen soil particles is by ion exchange. A soil is said to
fixation, mycorrhizal nutrient transport and bio be naturally fertile when the soil organisms are
control of root pests (Larsen et al., 201529). releasing inorganic nutrients from the organic
Plants only prefer those bacteria reserves at a rate sufficient to sustain rapid plant
contributing close to their relevance by releasing growth (Goswami et al., 201637). Gray and Smith
sugars, amino acids, organic acids, vitamins, (200530) have shown that the PGPR associations
enzymes and organic or inorganic ions through root range in the degree of bacterial proximity to the
exudates (Gray and Smith, 200530; Gopalakrishnan root and intimacy of association. The three distinct
et al.,2015 3) producing a environment where characteristics of PGPR are they must be able to
diversity is low (Das et al., 201331). In spite of the colonize the root, they must survive and multiply
numerous bacteria in soil, three types of interaction in microhabitats associated with the root surface,
takes place between rhizosphere bacteria and in competition with other microbiota, at least for
plants which are the positive, negative and neutral the time needed to express their plant promotion/
interactions. Mostly, commensalism is exhibited protection activities and they must promote plant
where a harmless interaction with the host plants growth (Kloepper, 199438; Lucy et al., 200439).
is exhibited without affecting the plant physiology, Based on their relationship with the
whereas in negative interaction phototoxic plants PGPR are classified into two groups,
substances are produced by rhizosphere bacteria. symbiotic bacteria and freeliving rhizobacteria
Positive interaction exerts a positive growth. (Khan, 200540). On the basis of their residing
Multiple microbial interactions enhance bio control sites: iPGPR (Verma et al., 201041) (i.e., symbiotic
in the rhizosphere region (Whipps, 200132). In bacteria), example Rhizobia sp. and Frankia sp.,
this regard, the use of naturally occurring and which live inside the plant cells, produce nodules,
environmentally safe products such as plant and are localized inside the specialized structures;
growth-promoting rhizobacteria (PGPR) has found and ePGPR (i.e., free-living rhizobacteria),
a potential role in developing sustainable systems which live outside the plant cells and do not
in crop production. produce nodules, but still prompt plant growth
Plant growth promoting rhizobacteria (PGPR) (Gray and Smith, 200530). Depending on their
Plant growth promoting rhizobacteria functional activities PGPR are categorized as
(PGPR), a diverse group of soil bacteria, are key (i) biofertilizers (increasing the availability
components of soil plant systems, where they are of nutrients to plant); (ii) phytostimulators
engaged in an intense network of interactions in (plant growth promotion, generally through
the rhizosphere, thus affecting the plant growth phytohormones); (iii) rhizoremediators (degrading
and yield. It was Kloepper and Schroth (198133), organic pollutants); and (iv) biopesticides
who coined the term plant growth promoting (controlling diseases, mainly by the production of
rhizobacteria for these beneficial microbes. antibiotics and antifungal metabolites) (Antoun
Numerous species of soil bacteria which flourish and Prevost, 200542). Many literature studies also
in the rhizosphere of plants, but which may grow show that a single PGPR will often reveal multiple
in, on, or around plant tissues, and stimulate modes of action including biological control
plant growth by a plethora of mechanisms (Kloepper, 200343; Vessey, 200334; Ahmad et al.,
(Vessey, 200334). PGPR’s are the potential tools 200844). Genera of PGPR include Arthrobacter,
for sustainable agriculture and trend for the Azotobacter, Azospirillum, Pseudomonas,
future; they not only ensure the availability of Acetobacter, Micrococcus, Burkholderia, Bacillus,
essential nutrients to plants but also enhance the Paenibacillus, Agrobacterium, Caulobacter,
nutrient use efficiency (Khalid et al., 200935). Chromobacterium, Erwinia, Azospirillum,
The beneficial effects of PGPR involve boosting Flavobacterium, Serratia, Rhizobium and some
key physiological processes, including water and are members of the Enterobacteriaceae (Niranjan
nutrient uptake, photosynthesis, and source-sink Raj et al., 200545; Bhattacharyya and Jha, 201246).
relationships that promote growth and development

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736 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria

Commercialization method of application also influences the success of

A number of PGPR bacterial strains are field trials. Repeated laboratory works followed by
commercially available in the form of formulated field experiments are needed to establish excellent
products which is used as biofertilizers and biocontrol agents into commercial products
biocontrol agents. For the more extensive particularly against plant fungal pathogens
commercialization of plant growth promoting (Suprapta, 201254). Thus, isolation of an effective
bacterial (PGPB) strains, a number of aspects need strain is a prime criterion for better agricultural
to be determined which include (i) determination of development. The first commercial product of
the traits with appropriate biological activities; (ii) Bacillus subtilis was developed during 1985 in
consistency among regulatory agencies in different United States (U.S.). 60–75% of cotton, peanut,
countries regarding what strains can be released soya bean, corn, vegetables and small grain crops
to the environment, and under what conditions raised in U.S. are now treated with commercial
genetically engineered strains are suitable for product of B. subtilis, which become effective
environmental use; (iii) a better understanding against soil borne pathogens such as Fusarium and
of the advantages and disadvantages of using Rhizoctonia (Nakkeeran et al., 200555).
rhizospheric versus endophytic bacteria; (iv) Other commercialized plant growth
selection of PGPB strains that function optimally promoting bacterial strains include Agrobacterium
under specific environmental conditions (Fravel, radiobacter, Azospirillum brasilense, Azospirillum
200747; Arora et al., 201048; Glick, 201249; Gupta lipoferum, Azotobacter chroococcum, Bacillus
et al., 201550). Moreover, commercial success of fimus, Bacillus licheniformis, Bacillus megaterium,
PGPR strains requires cost-effective and viable Bacillus mucilaginous, Bacillus pumilus, Bacillus
market demand, constant and broad spectrum spp., Bacillus subtilis, Bacillus subtilis var.
action, safety and stability, longer shelf life, amyloliquefaciens, Burkholderia cepacia, Delfitia
low investment and easy availability of career acidovorans, Paenobacillus macerans, Pantoea
materials. Inorder to retain the confidence of agglomerans, Pseudomonas aureofaciens,
farmers on the efficacy of the antagonistic strain Pseudomonas chlororaphis, Pseudomonas
quality control is vital (Bhattacharyya and Jha, fluorescens, Pseudomonas solanacearum,
201246). According to Nandakumar et al. (200151) Pseudomonas spp., Pseudomonas syringae,
different stages in the process of commercialization Serratia entomophilia, Streptomyces griseoviridis,
include isolation of antagonist strains, screening, Streptomyces spp., Streptomyces lydicus and
pot tests and field efficacy, mass production and various Rhizobia spp. (Figueiredo et al., 201056;
formulation development, fermentation methods, Glick, 201249). PGPR-based commercialization is at
formulation viability, toxicology, industrial a boom and several industries are commercializing
linkages and quality control. The selection of best bacterial and fungal strains as PGPR-based
antagonistic strain is carried out by screening biofertilizers, of which some of the important
the biocontrol ability of rhizosphere bacteria for PGPR strains along with their commercial products
antagonism against Sclerotium rolfsii, the causal are portrayed here. The U.S. market based on
organism of root or collar rot in sunflower. The the information of the committee of biological
antagonists were tested for suppression of S. rolfsii products from the American Phytopatology
rot of sunflower in greenhouse as seed and soil Society (APS) in 2005 has registered the following
treatment (Rangeshwaran and Prasad, 200052). products: ten products based on the Bacillus sp.
Potential antagonists Trichoderma harzianum and (BioYield, Companion, EcoGuard, HiStick N/T,
Pseudomonas spp. are tested for their efficacy in Kodiak , Mepplus, Serenade, Sonata, Subtilex,
field trials against Sclerotium rolfsii rot in tomato. Yield- Shield), two products with Burkholderia
Consortium of these bio-agents resulted in plant cepacia (Deny and Intercept), and five products
growth promotion, yield and simultaneously based on Pseudomonas sp. (AtEze, Bio-save,
reduce the disease severity (Singh et al., 201353). BlightBan, Frostban, Spot-Less) (Figueiredo
Due to variations in environmental factors a et al., 2010 56). Bio-formulation of Fusarium
good biocontrol agent under in vitro conditions oxysporum is commercialized by Biofox which
not succeeds in in vivo conditions. Similarly, the is effective against Fusarium moniliforme.

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 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria 737

Bacterial bioformulation of Pseudomonas yield. Biological means of providing the nutrients

aureofaciens commercialized by Ecosoil is such as nitrogen and phosphorus are ideal than
effective against Dollar spot, Anthracnose, Pythium chemical sources which are expensive and cause
aphanidermatum, and Michrochium patch (pink environmental hazards or through compound’s
snow mold). Streptomyces griseoviridis strain K61 that are synthesized by the bacterium, for example
has been commercially formulated by AgBio which phytohormones (Lucy et al., 200440; Khalid et
is known to inhibit Fusarium spp., Alternaria al., 200460; Glick, 201249). Indirectly, the bacteria
brassicola, Phomopsis spp., Botrytis spp., Pythium may exert a positive influence on plant growth by
spp., and Phytophthora spp. that cause seed, root, lessening certain deleterious effects of a pathogenic
stem rot, and wilt disease of ornamental and organism by producing antagonistic substances.
vegetable crops. A biofertilizer containing spores Direct Mechanisms
of Bacillus licheniformis SB3086 produced by The direct mechanisms observed in PGPR
Novozymes can act as phosphate solubilizer include N 2-fixation, mobilization of nutrients
strain and is also effective against Dollar spot via production of phosphatases, siderophores, or
disease of plants. Commercial bioformulation of organic acids, and production of phytohormones
Coniothyrium minitans produced by BIOVED, and enzymes.
Ltd., Hungary, is effective in suppressing Nitrogen Fixation
Sclerotinia sclerotiorum and Sclerotinia minor Nitrogen being a primary limiting factor
which are phytopathogens infecting cucumber, in agriculture found deficient due to various
lettuce, capsicum, tomato, and ornamental flowers. environmental factors. 65% of the nitrogen
Commercial biocontrol “EcoGuard,” marketed as currently utilized in agriculture is obtained through
a concentrated suspension of spores of Bacillus biological nitrogen fixation, also important
licheniformis SB3086 has been found effective as to sustain crop production systems in future
a natural inhibitor of a variety of agronomically (Dakora, 200361). PGPR strains play a major role
important fungal diseases - particularly dollar spot in nitrogen fixation and make it assimilable form
and anthracnose (Goswami et al., 201637). In India, for plants. Nitrogenase (nif) genes required for
more than 40 stakeholders from different provinces nitrogen fixation in nitrogen fixing bacteria are
have registered themselves for the mass production more complex. So for improving this process
of PGPRs with Central Insecticide Board (CSI), genetic strategies have been utilized to modify the
Faridabad, Haryana through collaboration with genes (Glick, 201249; Souza et al., 201562). PGPR
Tamil Nadu Agricultural University, Coimbatore, follow two mechanism of nitrogen fixation. In
India (Bhattacharya and Jha, 2012 46). Since symbiotic nitrogen fixation, legume crops undergo
crops are grown under a diversity of climatic biological nitrogen fixation through symbiotic
and environmental conditions causes disparity association with bacteria and meet their own needs
in the potentiality of PGPR based Biofertilizers without depending external sources (Bhattacharyya
(Kamilova et al., 201557). However, with better and Jha, 201246; Gopalakrishnan et al., 20153).
shelf life and possessing efficient strains it is Symbiotic bacteria which act as PGPR are
possible to develop better biofertilizers exploiting Rhizobium, Bradyrhizobium, Sinorhizobium, and
PGPR in sustainable agriculture, for enhancing Mesorhizobium with leguminous plants, Frankia
productivity (Glick, 201458). with non-leguminous trees and shrubs (Zahran,
Mechanisms of PGPR 200163). Free living nitrogen fixers, which are
The mechanisms by which bacteria can non symbiotic types survive close to root without
influence plant growth differ among species and penetration, fixed nitrogen that are acquired
strains, PGPR affect plant growth in two different through uptake contribute to the nitrogen account
ways, indirectly or directly (Castro et al., 200959). of the plants (Goswami et al., 201637). Non-
There are two mechanisms for promoting plant symbiotic nitrogen fixing rhizospheric bacteria
growth. The direct promotions of plant growth belongs to genera including Azoarcus, Azotobacter,
by PGPR involve either providing the plant with Acetobacter, Azospirillum, Burkholderia,
resources they lack. This facilitates higher plant Diazotrophicus, Enterobacter, Gluconacetobacter,

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738 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria

Pseudomonas and Cyanobacteria, Anabaena, the mobility of organic phosphorus through

Nostoc (Vessey, 200334). microbial turnover and/or increase the root system
Many species of microorganisms are (Richardson and Simpson, 201171). These bacteria
used in the cultivation of plants of economic secrete different types of organic acids which lower
interest, facilitating the host plant growth without the pH in the rhizosphere and thus release the
the use of nitrogenous fertilizers. For instance, phosphorus available to plants (Kaur et al., 201672).
the production of soybean (Glycine max L.) is an Bacteria from genera such as Achromobacter,
excellent example of the efficiency of biological Agrobacterium, Bacillus, Enterobacter, Erwinia,
nitrogen fixation through the use of different strains Escherichia, Flavobacterium, Mycobacterium,
of Bradyrhizobium sp., such as B. japonicum and B. Pseudomonas and Serratia are highly efficient
elkanii (Alves et al., 200464; Torres et al., 201265). in solubilising unavailable complexed phosphate
The importance of endophytic nitrogen fixing into available inorganic phosphate ion (Goldstein,
bacteria has also been the object of studies in non 200173). Rhizobia, including R. leguminosarum,
leguminous plants such as sugarcane (Saccharum R. meliloti, Mesorhizobium mediterraneum,
officinarum L.) (Thaweenut et al., 201166). Other Bradyrhizobium sp. and B. japonicum are the
studies have suggested that Bradyrhizobia colonize potential phosphate solubilizers (Vessey, 200334;
and express nif H not only in the root nodules Egamberdiyeva et al., 200474; Rodrigues et al.,
of leguminous plants but also in the roots of 200675).
sweet potatoes (Ipomoea batatas L.), acting as Siderophore
diazotrophic endophytes (Terakado-Tonooka et The transition metal iron is an essential
al., 200867). The plant growth promoting bacteria micronutrient and bioactive metal crucial for the
related to genus Azospirillum have been largely growth and metabolism of bacteria. Iron plays a
studied because of their efficiency in promoting the key role in electron transport, oxidation–reduction
growth of different plants of agronomical interest. reactions, detoxification of oxygen radicals,
The genus Burkholderia includes species that fix synthesis of DNA precursors and in many other
nitrogen B. vietnamiensis, a human pathogenic biochemical processes (Hider and Kong, 201076).
species, was efficient in colonizing rice roots and Based on their iron-coordinating functional groups,
fixing nitrogen (Govindarajan et al., 200868). In structural features and types of ligands, bacterial
addition to Burkholderia, the potential of biological siderophores have been classified into four main
nitrogen fixation and endophytic colonization of classes such as carboxylates, hydroxamates, phenol
bacteria belonging to the genera Pantoea, Bacillus catecholates and pyoverdines (Mohandas, 200477;
and Klebsiella were also confirmed in different Fernandez et al., 200578). Generally, rhizobacteria
maize genotypes (Ikeda et al., 201369). differs regarding the siderophore cross-utilizing
Phosphate solubilisation ability. Some are capable of using siderophores
Next to nitrogen, phosphorus is the of the same genus (homologous siderophores)
important key element in the nutrition of plants. while others could utilize those produced by other
It exists in both inorganic (bound, fixed, or labile) rhizobacteria of different genera (heterologous
and organic (bound) forms. The availability siderophores) (Khan et al., 200979).
of phosphorus to plants is influenced by pH, In aerobic environments, iron occurs in the
compaction, aeration, moisture, temperature, texture form of insoluble hydroxides and oxyhydroxides
and organic matter of soils, crop residues, extent are not accessible to both plants and microbes
of plant root systems and root exudate secretions (Rajkumar et al., 2010 80). Being a transition
and available soil microbes (Gopalakrishnan et element, iron gets rapidly oxidized from soluble
al., 20153). Phosphorus is involved in metabolic ferrous (Fe 2 ) to insoluble ferric (Fe 3 ) state
processes of plant, as photosynthesis, energy (Murugappan et al., 2012 81 ). Siderophores
transfer, signal transduction, macromolecular enhances the iron bioavailability by influencing
biosynthesis and respiration (Khan et al., 201070). the low solubility of iron (Wittenwiler, 200782).
Soil phosphorus cycle mediate phosphorus Siderophores attach on the mineral surface and
availability to plants. PGPR’s directly solubilise facilitate dissolution by coordinating the iron atom
and mineralise inorganic phosphorus or facilitate in a soluble complex (Kraemer et al., 200683).

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 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria 739

Under iron limiting conditions microorganisms abscisic acid. Soil microrganisms, particularly
and plants rely on chelating agents to solubilise the rhizosphere bacteria, possess the potential to
and transport inorganic iron. The membrane produce these hormones (Zakir et al., 200424).
receptor and the ferric siderophore transporter are Indole-3-acetic acid
the common transporter for high affinity microbial Indole-3-acetic acid (IAA) is the member
acquisition of iron (Neilands, 198184; Crowley of the group of phytohormones and is generally
et al., 199185). Microbes release siderophores considered the most important native auxin which
to scavenge iron from these mineral phases by is low-molecular weight, organic substances. This
formation of soluble Fe3+ complexes that can substance termed auxin was identified as indole-
be taken up by active transport mechanisms 3-acetic acid (Kögl and Kostermans, 193493;
(Saharan and Nehra, 201186). Bacteria secrete the Went and Thimann, 193794). This phytohormone
siderophore to overcome the iron limitation and auxin is a key regulator of many aspects of plant
provide plants with Fe, enhancing their growth growth and development, including cell division
directly by increasing the availability of iron in the and elongation, differentiation, tropisms, apical
soil surrounding the roots (Krewulak and Vogel, dominance, senescence, abscission, and flowering
200887; Vejan et al., 201688). Plants uptake iron (Woodward and Bartel, 200595 ; Teale et al., 200696
when they are able to recognize the bacterial ferric- ; Ahemad and Kibret, 201497). The auxin level
siderophore complex (Masalha et al., 200089). Not is usually higher in the rhizosphere, where high
only iron, siderophores also form stable complexes percentage of rhizosphere bacteria is likely to
with other heavy metals that are of environmental synthesize auxin as secondary metabolites because
concern, such as cadmium, copper, lead and of the rich supplies of root exudates. The production
zinc, as well as with radionuclide’s including of auxin (IAA), has been recognized as an
uranium (Neubauer et al., 200090). Binding of the important factor in direct plant-growth-promoting
siderophore to a metal increases the soluble metal abilities of rhizosphere bacteria (Dilfuza, 201198).
concentration (Rajkumar et al., 201080). Hence, For various PGPR, it has been demonstrated that
bacterial siderophores help to alleviate the stresses enhanced root proliferation is related to bacterial
imposed on plants by high soil levels of heavy IAA biosynthesis. Upon inoculation of plants with
metals. PGPR, a change in root architecture is observed,
Microorganisms have evolved highly mainly as an increase in root hairs and lateral
specific pathways that employ low molecular roots and shortening of the root length. Also,
weight, high affinity iron chelators to solubilise rhizobacterial IAA loosens plant cell walls and as
iron prior to transport. Gram-negative bacteria take a result facilitates an increasing amount of root
up ferri-siderophore complexes via specific outer exudation that provides additional nutrients to
membrane receptors in a process that is driven by support the growth of rhizosphere bacteria (Glick,
the cytosolic membrane potential and mediated by 201249). Moreover, down-regulation of IAA as
the energy-transducing TonB-ExbB-ExbD system. signalling is associated with the plant defense
Bacteria, such as Gram-positive, that lack an outer mechanisms against a number of phyto-pathogenic
membrane, use binding-protein-dependent ABC bacteria as evidenced in enhanced susceptibility
permeases to allow ferri-siderophores to traverse of plants to the bacterial pathogen by exogenous
their cytosolic membrane (Crowely et al., 199185; application of IAA or IAA produced by the
Andrews et al., 200391). pathogen (Spaepen and Vanderleyden, 201199).
Phytohormones IAA biosynthesis is widespread among
Chemicals occurring naturally within plant-associated bacteria (Patten and Glick, 1996100;
plant tissues have a regulatory, rather than a Giickmann et al., 1998101). Bacteria can use this
nutritional role in growth and development. These phytohormone to interact with plants as part of their
compounds, which are generally active at very low colonization strategy, including phytostimulation
concentrations, are known as phytohormones or and basal plant defense mechanisms. IAA can also
plant growth substances (George et al., 200892). be a signaling molecule in bacteria and therefore
Classes of well-known phytohormones include can have a direct effect on bacterial physiology
auxins, gibberellins, cytokinins, ethylene, and (Spaepen et al., 2007102). More than 80% of the

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740 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria

bacteria isolated from the rhizosphere are capable whereas beneficial bacteria tend to use the IPyA
to synthesize IAA (Khalid et al., 200460). IAA pathway (Spaepen et al., 2007 102; Mano and
production under in vitro condition has been Nemoto, 2012119). This helps the bacteria to evade
reported by many researches, in Azospirillum the plant regulatory signals and so the IAA induces
sp. (Lambrecht et al., 2000103; Dobbelaere et al., uncontrolled growth in plant tissues. In contrast
2001104), Azotobacter sp. (Zahir et al., 2000105), the useful bacteria such as PGPR synthesize IAA
Azotobacter chrococcum, Bacillus megaterium via the indole pyruvic acid pathway and the IAA
BHUPSB14, Pseudomonas fluorescens, P.putida secreted is thought to be strictly regulated by the
(Patten and Glick, 2002106; Verma et al., 201041; plant regulatory signals (Patten and Glick, 1996100).
Peyvandi et al., 2010107), Rhizobium sp. (Ghosh Cytokinins
et al., 2008108), Pseudomonas aeruginosa (Khare Cytokinins are a class of phytohormones
and Arora, 2010109), Acetobacter diazotrophicus which are known to promote cell divisions, cell
L1(Patil et al., 2011110 ) and in Rhizobium enlargement and tissue expansion in certain plant
leguminosarum (Dazzo et al., 2000111). Tsavkelova parts (Werner et al., 2003120). Cytokinins play
et al. (2006112) observed IAA production in fungi a major or minor role throughout development,
in genera Aspergillus sp., Fusarium sp. and from seed germination to leaf and plant senescence
Paecilomyces sp. Ruanpanun et al. (2010113) found and modulate physiological processes important
high IAA producing nematophagous actinomycete throughout the life of the plant, including
and fungal isolates such as Streptomyces sp. and in photosynthesis and respiration (Salisbury and
Aspergillus sp. Ross, 1992121; Arshad and Frankenberger, 1993122).
Bacterial production of IAA suggests Plants and plant associated microorganisms have
that the pathways involved in IAA production been found to contain over 30 growth promoting
may play an important role in defining the effect compounds of the cytokinin group. It has been found
of the bacterium on the plant. Though bacterial that as many as 90% of microorganisms found in
biosynthesis of IAA can occur by a variety of the rhizosphere are capable of releasing cytokinins
pathways, tryptophan has been identified as a (Nieto and Frankenberger, 1990123). Several plant
main precursor for IAA biosynthesis pathways growth promoting rhizobacteria Azotobacter
in bacteria (Sarwar and Kremer, 1995114; Patten sp., Rhizobium sp., Pantoea agglomerans,
and Glick, 1996100; Kravchenko et al., 2004115; Rhodospirillum rubrum, Pseudomonas fluorescens,
Kamilova et al., 2006116). According to Ghosh and Bacillus subtilis and Paenibacillus polymyxa can
Basu (2006117) among the three different isomers of produce cytokinins along with other growth-
tryptophan, the bacteria produced higher amount promoting substances (Gutiérrez-Mañero et al.,
of IAA with the supplementation of L-tryptophan 2001124). Cytokinin production has been reported
(138 µg/ml) than in D-tryptophan (15 µg/ml) in various PGPR, like Arthrobacter giacomelloi,
or DL-tryptophan (84 µg/ml). In earlier work Azospirillum brasilense, Bradyrhizobium
Dullaart (1970118) explained this process due to japonicum, Bacillus licheniformis, P.fluorescens
the utilisation of this essential amino acid partly and Paenibacillus polymyxa (Timmusk et al.,
in protein synthesis and partly for the formation 1999125; Per-rig et al., 2007126). Plant responses
of other indole compounds in addition to IAA. to exogenous applications of cytokinin result in
The indole-3-acetamide (IAM) pathway is the best either one of the following effects (a) enhanced
characterized pathway in bacteria. In this two-step cell division; (b) enhanced root development; (c)
pathway tryptophan is first converted to IAM by enhanced root hair formation; (d) inhibition of
the enzyme tryptophan-2-monooxygenase (IaaM), root elongation; (e) shoot initiation and certain
encoded by the iaaM gene. In the second step other physiological responses (Frankenberger and
IAM is converted to IAA by an IAM hydrolase Arshad, 1995127).
(IaaH), encoded by iaaH. In plant-associated Gibberellins
bacteria, both the IAM and the indole-3- pyruvic Gibberellins are a class of phytohormones
acid (IPyA) pathway are distributed among the most commonly associated with modifying plant
sequenced genomes. Phytopathogenic organisms morphology by the extension of plant tissue,
tend to use the IAM pathway to produce IAA, particularly stem tissue (Salisbury, 1994 128).

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 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria 741

These are synthesized by higher plants, fungi, crop performance (Li et al., 2005138; Bhattacharyya
and bacteria. They are involved in several plant and Jha, 201246). Under stress conditions like those
developmental processes, including cell division generated by salinity, drought, water logging,
and elongation, seed germination, stem elongation, heavy metals and pathogenicity, the endogenous
flowering, fruit setting, and delay of senescence level of ethylene is significantly increased which
in many organs of a range of plant species negatively affects the overall plant growth. Plant
(MacMillan, 2002129). They can also regulate root growth promoting rhizobacteria which possess
hair abundance and hence promotes the root growth the enzyme, 1-aminocyclopropane-1-carboxylate
(Bottini et al., 2004130). The ability of bacteria to (ACC) deaminase, which is the precursor for
synthesize gibberellins-like substances was first ethylene (Chen et al., 2013139) is secreted into the
described in Azospirillum brasilense (Tien et al., rhizosphere and is readsorbed by the roots, where
1979131) and Rhizobium (Williams and Mallorca, it is converted into ethylene. This accumulation
1982132). Production of gibberellins had been of ethylene leads to a downward spiral effect, as
detected in different bacterial genera that inhabit poor root growth leads to a diminished ability to
the plant root system including Azotobacter, acquire water and nutrients, which, in turn, leads
Arthrobacter, Azospirillum, Pseudomonas, to further stress (Martinez-Viveros et al., 2010140).
Bacillus., Acinetobacter, Flavobacterium, The destruction of ethylene is done by PGPR via
Micrococcus, Agrobacterium, Clostridium, the enzyme ACC deaminase. This enzyme can
Rhizobium, Burkholderia and Xanthomonas (Joo diminish or prevent some of the harmful effects
et al., 2005133; Tsakelova et al., 2006112; Hayat et of the high ethylene levels (Glick et al., 1998141).
al., 20106). Plant growth promotion by gibberellin- The ACC deaminase acts on ACC, an immediate
producing plant growth promoting bacteria and ethylene precursor in higher plants, degrading this
this positive effect on plant biomass is frequently chemical to alphaketobutyrate and ammonium,
associated with an increased content of gibberellins (Glick et al., 1998 141; Mayak et al., 2004 142).
in plant tissues was reported by several workers Rhizosphere bacteria with ACC deaminase
(Joo et al., 2005133; Kang et al., 201016). activity belonging to the genera, Achromobacter
Abscisic acid (Govindasamy et al., 2008143), Azospirillum (Li
Abscisic acid (ABA) plays a primary role et al., 2005138), Bacillus (Ghosh et al., 2003144),
in water-stressed environment, such as found in arid Enterobacter (Li and Glick, 2001145), Pseudomonas
and semiarid climates where it helps in combating (Govindasamy et al., 2008143) and Rhizobium
the stress through stomatal closure of leaves. (Duan et al., 2009146) have been isolated from
Therefore, its uptake by and transport in plant and different soils.
its presence in the rhizosphere could be extremely Indirect Mechanisms
important for plant growth under water stress There are many indirect ways through
conditions (Frankenberger and Arshad, 1995127). which PGPR act as plant growth promoters with
Rhizobium sp., B. japonicum and Azospirillium sp. their biocontrol properties and induction of systemic
had been reported to produce abscisic acid (Dangar resistance against phytopathogens. Plant growth
and Basu, 1987134; Dobbelaere et al., 2003135; promoting organisms have certain properties
Boiero et al., 2007136). for biocontrol of various phytopathogens. This
Ethylene includes (1) production of antibiotics; (2) secretion
Apart from being a plant growth regulator, of siderophores enabling iron uptake depriving the
ethylene has also been recognized as a stress fungal pathogens in the vicinity; (3) production of
hormone (Saleem et al., 2007 137). Ethylene is lytic enzymes such as chitinase, â-1, 3 glucanase,
essential for the growth and development of protease and lipase which lyse the pathogenic
plants, but it has different effects on plant growth fungal and bacterial cell walls; (4) induces systemic
depending on its concentration in root tissues. resistance in plants by metabolites (Zahir et al.,
At high concentrations, it can be harmful, as it 200424; Hafeez et al., 2006147; Narayanasamy,
induces defoliation and cellular processes that lead 2008148; Reddy, 2013149).
to inhibition of stem and root growth as well as Antibiotics
premature senescence, all of which lead to reduced One of the most effective mechanism

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742 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria

by which PGPR employ to prevent proliferation Induced systemic resistance

of phytopathogens is the synthesis of antibiotics. The uses of plant growth promoting
Antibiotics include a heterogeneous group of strains are reported to trigger the resistance of
organic, low-molecular-weight compounds that plants against pathogens (Ramamoorthy et al.,
are deleterious to the growth or metabolic activities 2001156). Induced resistance (ISR) is a state of
of other microorganisms (Duffy, 2003150). There enhanced defensive capacity developed by a plant
are six classes of antibiotic compounds linked to when appropriately stimulated. Systemic acquired
the biocontrol of root diseases are, phenazines, resistance (SAR) and induced systemic resistance
phloroglucinols, pyoluteorin, pyrrolnitrin, cyclic (ISR) are two forms of induced resistance which
lipopeptides (all of which are diffusible) and can be differentiated on the basis of the nature of
hydrogen cyanide (HCN which is volatile) (Haas the elicitor and the regulatory pathways involved
and Défago, 200518). The mechanism of action (Choudhary et al., 2007157). SAR can be triggered
is to inhibit synthesis of pathogen cell walls, by exposing the plant to virulent, avirulent, and non
influence membrane structures of cells and inhibit pathogenic microbes and involves accumulation
the formation of initiation complexes on the small of pathogenesis-related proteins (chitinase and
subunit of the ribosome (Maksimov et al., 2011151). glucanase), and salicylic acid. ISR does not
An efficient antibiotic, 2, 4-diacetylphloroglucinol involve the accumulation of pathogenesis-related
(DAPG) produced by pseudomonads, causes proteins or salicylic acid, but instead, relies on
membrane damage to Pythium spp. and is pathways regulated by jasmonate and ethylene and
particularly inhibitory to zoospores of this these hormones stimulate the host plant’s defense
oomycete (de Souza et al., 2003152). responses against a variety of plant pathogens
Lytic enzymes (Yan et al., 2002158; Glick, 201249). Bacterial
The growth and activities of pathogens components too induce induced systemic resistance
can be suppressed by the secretion of lytic enzymes. such as lipopolysaccharides, flagella, siderophores,
These are cell wall degrading enzymes such as etc., (Doombos et al., 2012159). PGPR-mediated
glucanases, proteases, chitinases, and lipases etc, induced systemic resistance has been shown to
secreted by biocontrol strains of PGPR involved effectively suppress Phytophthora blight caused
in the lysis of fungal cell wall (Neeraja et al., by Phytophthora capsici on squash (Zhang et al.,
2010153).These enzymes either digest the enzymes 2010160).
or deform components of cell wall of fungal
pathogens. Hydrolytic enzymes directly contribute CONCLUSION
in the parasitisation of phytopathogens and rescue
plant from biotic stresses. The role of three types Plant growth promoting rhizobacteria in
of chitinolytic enzymes are as follows (a) 4-β-ILT- rhizosphere soil is highly dynamic, more versatile
acetylglucosaminidases splits the chitin polymer in transforming, mobilizing and solubilising
into GlcNAc monomers in an exo-type fashion; the nutrients. Therefore, the rhizobacteria are
(b) endochitinases cleave randomly at internal sites the dominant deriving forces in recycling the
over the entire length of the chitin microfibril; and soil nutrients and consequently, they are crucial
(c) exochitinases catalyse the progressive release for soil fertility. They may be extensively used
of diacetylchitobiose in a stepwise fashion such in plant growth promotion as it acts as a plant
that no monosaccharides or oligosaccharides are nourishment and enrichment source which would
formed (Haran et al., 1996154). b -Glucanases replenish the nutrient cycle between the soil
can act via two possible mechanisms, Exo- and plant roots , exhibits detoxifying potential,
b-glucanases hydrolyse the b-glucan chain by controls phytopathogen thereby exerts a positive
sequentially cleaving glucose residues from the influence on crop productivity and ecosystem
non-reducing end. Endo- b -glucanases cleave functioning, hence can be implemented in
b-linkages at random sites along the polysaccharide agriculture. With better research and development,
chain, releasing smaller oligosaccharides (Pitson et these microbial populations use would become a
al., 1993155). reality and instrumental and build stability and

J PURE APPL MICROBIOL, 12(2), June 2018.

 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria 743

productivity of agro-ecosystems, thus leading 12. Khalid, A., Akhtar, M.J., Mahmood, M.H., Arshad,
us towards an ideal agricultural system with M. Effect of substrate-dependent microbial
sustainability, improvement in human health, ethylene production on plant growth.
benefits environment and ecosystem and leads to Microbiology., 2006; 75: 231-236.
13. Jha, C. K., Patel, D., Rajendran, N., Saraf, M.
the production of adequate food for the increasing
Combinatorial assessment on dominance and
world population. informative diversity of PGPR from rhizosphere
of Jatropha curcas L. J. Basic Microbiol., 2010
REFERENCES ; 50: 211–217.
14. G o v i n d a s a m y, V. , S e n t h i l k u m a r, M . ,
1. Zeder, M. A. Evolutionary biology and the Magheshwaran, V., Kumar, U., Bose, P., Sharma,
emergence of agriculture: the value of co-opted V., Annapurna, K. Bacillus and Paenibacillus
models of evolution in the study of culture spp.: Potential PGPR for sustainable agriculture.
change. In: Macroevolution in human prehistory: In: Plant growth and health promoting bacteria
Evolutionary theory and Processual Archaeology. (Maheshwari, DK, ed.). Berlin: Springer-Verlag,
New York: Springer, 2009; pp 157-210. 2011; pp 333–364.
2. Bishnoi, U. PGPR Interaction: An Ecofriendly 15. Dakora, F.D., Philips, D.A. Root exudates as
Approach Promoting the Sustainable Agriculture mediators of mineral acquisition in low-nutrient
System. Adv.Bot.Res., 2015; 75: 81-113. environments. Plant Soil., 2002; 245: 35–47.
3. Gopalakrishnan, S., Sathya, A., Vijayabharathi, 16. Kang, B.G., Kim, W.T., Yun, H.S., Chang, S.C.
R., Varshney, R.K., Laxmipathi Gowda, C.L., Use of plant growth-promoting rhizobacteria
Krishnamurthy, L. Plant growth promoting to control stress responses of plant roots. Plant
rhizobia: challenges and opportunities. Biotech., Biotechnol. Rep., 2010; 4: 179-183.
2015; 5: 355–377. 17. Nardi, S., Concheri, G., Pizzeghello, D., Sturaro,
4. Shenoy, V.V., Kalagudi, G.M., Gurudatta, B.V. A., Rella, R., Parvoli, G. Soil organic matter
Towards nitrogen autotrophic rice. Curr. Sci., mobilization by root exudates. Chemosphere.,
2001; 81:451-457. 2000; 5: 653–65.
5. Adesemoye, A.O., Kloepper, J.W. Plant– 18. Haas, D., Défago, G. Biological control of soil-
microbes interactions in enhanced fertilizer-use borne pathogens by Fluorescent Pseudomonads.
efficiency. Appl.Microbiol.Biotechnol., 2009; 85: Nat. Rev. Microbiol., 2005; 10: 1-13.
1–12. 19. Badri, D.V., Weir, T. L., Van der Lelie, D.,
6. Hayat, R., Ali, S., Amara, U. Soil beneficial Vivanco, J. M. Rhizosphere chemical dialogues:
bacteria and their role in plant growth promotion: plant-microbe interactions. Curr. Opin.
A review. Ann. Microbiol., 2010; 60:579–598. Biotechnol., 2009 ; 20: 642-650.
7. Burd, G.I, Dixon, D.G., Glick, B.R. Plant growth 20. Dennis, P.G., Miller, A.J., Hirsch, P.R. Are root
promoting bacteria that decrease heavy metal exudates more important than other sources of
toxicity in plants. Can. J. Microbiol., 2000; 46 rhizodeposits in structuring rhizosphere bacterial
(3): 237–245. communities? Microbiol. Ecol., 2010; 72 (3):
8. Zhuang, X., Chen, J., Shim, H., Bai, Z. New 313–327.
advances in plant growth promoting rhizobacteria 21. Doornbos, R.F., Van Loon, L.C., Peter, A.H.M.,
for bioremediation. Environ. Int., 2007; 33 (3): Bakker, A. Impact of root exudates and plant
406–413. defense signaling on bacterial communities in
9. Zaidi, S., Usmani, S., Singh, B.R., Musarrat, J. the rhizosphere. Agron. Sustain. Dev., 2012; 32:
Significance of Bacillus subtilis strains SJ-101 227-243.
as a bioinoculant for concurrent plant growth 22. Chaparro, J.M., Sheflin, A.M., Manter, D.K.,
promotion and nickel accumulation in Brassica Vivanco, J.M. Manipulating the soil microbiome
juncea. Chemosphere., 2008; 64:991–997. to increase soil health and plant fertility. Bio.
10. Gouda, S., Kerry, R.G., Das, G., Paramithiotis, Fertil. Soil., 2012; 48 (5):489-499.
S., Shine, H.S., Patra, J.K. Revitalization of plant 23. Barea, J.M., Pozo, M.J., Azcon, R., Aguilar, C.A.
growth promoting rhizobacteria for sustainable Microbial cooperation in the rhizosphere. J. Exp.
development in agriculture. Microbiol. Res., Bot., 2005; 56 (417):1761–1778.
2018; 206:131–140. 24. Zahir, A.Z., Arshad, M., Frankenberger, W.T.
11. Hiltner, L. About recent experiences and Jr. Plant growth promoting rhizobacteria:
problems in the field of soil bacteriology with application and perspectives in Agriculture. Adv
special Consideration of green manure and Agron., 2004; 81:97–168.
fallow. Arb. Dtsch. Land. Gesel., 1904; 98:59–78. 25. Glick, B.R., Cheng, Z., Czarny, J., Duan, J.
J PURE APPL MICROBIOL, 12(2), June 2018.
744 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria

Promotion of plant growth by ACC deaminase- 36. llangumuran, G.,Smith, D.L. Plant Growth
producing soil bacteria. Eur. J. Plant Pathol., Promoting Rhizobacteria in Amelioration of
2007; 119 (3):329–339. Salinity Stress: A Systems Biology Perspective.
26. Lagos, M.L., Maruyama, F., Nannipieri, Front. Plant Sci., 2017; 8:1-14.
P., Mora, M.L., Ogram, A., Jorquera, M.A. 37. Goswami, D., Thakker.J.N, Dhandhukia, P.C.
Current overview on the study of bacteria in the Portraying mechanics of plant growth promoting
rhizosphere by modern molecular techniques: a rhizobacteria (PGPR): A review. Cogent Food
mini review. J. Soil Sci. Plant Nutr., 2015; 15 Agric., 2016; 2:1-19.
(2): 504-523. 38. Kloepper, J.W. Plant growth-promoting
27. Kloepper, J.W., Zablotowick, R.M., Tipping, rhizobacteria (other systems) In: Azospirillum/
E.M., Lifshitz, R. Plant growth promotion Plant Associations (Okon, Y, ed.). Boca Raton,
mediated by bacterial rhizosphere colonizers. FL, USA: CRC Press, 1994; pp 111-118.
In: The Rhizosphere and Plant Growth (Keister, 39. Lucy M., Reed, E., Glick, B.R. Applications of
DL, Cregan, PB, ed.). Dordrecht, Netherlands: free living plant growth promoting rhizobacteria.
Kluwer Academic Publishers, 1991; pp 315-326. Antonie Van Leeuwenhoek., 2004; 86 (1): 1–25.
28. Uren, N.C. Types, amounts, and possible 40. Khan, A.G. Role of soil microbes in the
functions of compounds released into the rhizosphere of plants growing on trace metal
rhizosphere by soil-grown plants. In: The contaminated soils in phytoremediation. J. Trace.
rhizosphere: biochemistry and organic substances Elem. Med. Biol.,, 2005; 18 (4): 355-364.
at the soil–plant interface (Pinton, R, Varanini, 41. Verma, J.P., Yadav, J., Tiwari, K.V., Lavakush,
Z, Nannipieri, P, ed.). Boca Rato´n: CRC Press, Singh, V. Impact of plant growth promoting
2007; pp 1–22. rhizobacteria on crop production. Int. J. Agric.
29. Larsen. J., Jaramillo-López, P., Nájera-Rincon, Res., 2010; 5 (11): 954-983.
M., Gonzaléz-Esquivel, C.E. Journal of Soil 42. Antoun, H., Prévost, D. Ecology of plant
Science and Plant Nutrition, Biotic interactions growth promoting rhizobacteria. In: PGPR:
in the rhizosphere in relation to plant and soil biocontrol and biofertilization (Siddiqui, ZA,
nutrient dynamics. J. Soil Sci. Plant Nutr., 2015; ed.). Dordrecht: Springer, 2005; pp 1–38.
15 (2): 449-463. 43. Kloepper, J.W., 2003. A review of mechanisms
30. Gray, E.J., Smith, D.L. Intracellular and for plant growth promotion by PGPR In: 6th
extracellular PGPR: commonalities and International PGPR Workshop (Reddy, MS,
distinctions in the plant-bacterium signalling Anandaraj, M, Eapen, SJ, Sarma, YR, Kloepper,
processes. Soil Biol. Biochem., 2005; 37: JW, ed.). Calicut, India: Indian Institute of Spices
395–412. Research, 2003; pp 81–92.
31. Das, A.J., Kumar, M., Kumar, R., Plant 44. Ahmad, F., Ahmad, I., Khan, M.S. Screening
Growth Promoting Rhizobacteria (PGPR): of free-living rhizospheric bacteria for their
An Alternative of Chemical Fertilizer for multiple plant growth promoting activities.
Sustainable, Environment Friendly Agriculture. Microbiol. Res., 2008; 163: 173-181.
Res. J. Agriculture & Forestry Sci., 2013; 1(4): 45. Niranjan Raj, S., Shetty, H.S., Reddy, M.S. Plant
21-23. growth-promoting Rhizobacteria: potential green
32. Whipps, J.M., Microbial interactions and alternative for plant productivity. In: PGPR:
biocontrol in the rhizosphere. J. Exp.Bot., 2001; Biocontrol and Biofertilization (Siddiqui, ZA,
52 (1): 487-511. ed.). Dordrecht, Netherlands. Springer, 2005;
33. Kloepper, J.W., Schroth, M.N. Relationship of pp 197-216.
in vitro antibiosis of plant growth promoting 46. Bhattacharyya, P.N., Jha, D. K. Plant growth-
rhizobacteria to plant growth and the displacement promoting rhizobacteria (PGPR): emergence
of root microflora. Phytopathology., 1981; in agriculture. World. J. Microbiol.Biotechnol.,
71:1020–1024. 2012; 28 (4): 1327–1350.
34. Vessey, K.J. Plant growth promoting rhizobacteria 47. Fravel, D. Commercialization of biocontrol
as biofertilizers. Plant Soil., 2003; 255 (2): agents for use against plant pathogens. In: IX
571–586. Reunia˜o Brasileira sobre Controle Biolo´gico
35. Khalid, A., Arshad, M., Shaharoona, B., de Doenc¸as de Plantas, Campinas, (Paulo, S,
Mahmood, T. Plant growth promoting ed.). Brasil: CD-ROM, 2007; pp 1–2.
rhizobacteria and sustainable agriculture. In: 48. Arora, N.K., Khare, E., Maheshwari, D.K. PGPR:
Microbial Strategies for Crop Improvement constraints in bioformulation, commercialization
(Khan, MS, ed.). Verlag Berlin Heidelberg: and future strategies. In: Plant growth and health
Springer, 2009; pp133-160. promoting bacteria (Maheshwari, DK, ed.).
J PURE APPL MICROBIOL, 12(2), June 2018.
 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria 745

Dorderecht: Springer, 2010; pp 97-116. improving growth and yield of wheat. J. Appl.
49. Glick, B.R. Plant Growth-Promoting Bacteria: Microbiol., 2004; 96 (3): 473–480.
Mechanisms and Applications. Scientifica., 2012: 61. Dakora, F.D. Defining new roles for plant and
1-16. rhizobial molecules in sole and mixed plant
50. Gupta, G., Parihar, S.S., Ahirwar, N.K., cultures involving symbiotic legumes. New
Snehi, S.K., Singh, V. Plant Growth Promoting Phytol., 2003; 158: 39 – 49.
Rhizobacteria (PGPR): Current and Future 62. Souza, R.D., Ambrosini, A., Passaglia, L.M.P.
Prospects for Development of Sustainable Plant growth-promoting bacteria as inoculants
Agriculture. J. Microbiol. Biochem. Technol., in agricultural soils. Genet. Mol. Biol., 2015; 38,
2015; 7(2): 096-102. (4): 401-419.
51. Nandakumar, R., Babu, S., Viswanathan, R., 63. Zahran, H.H. Rhizobia from wild legumes:
Sheela, J., Raguchander, T., Samiyappan, R. A diversity, taxonomy, ecology, nitrogen fixation
new bio-formulation containing plant growth and biotechnology. J. Biotechnol., 2001; 91:
promoting rhizobacterial mixture for the 143-153.
management of sheath blight and enhanced grain 64. Alves, B.J.R., Boddey, R.M., Urquiaga, S. The
yield in rice. Biocontrol., 2001; 46 (4):493–510. success of BNF in soybean in Brazil. Plant Soil.,
52. Rangeshwaran, R., Prasad, R.D. Biological 2004; 252:1-9.
control of Sclerotium rot of sunflower. Indian 65. Torres, A.R, Kaschuk, G., Saridakis, G.P., Hungria,
Phytopathol., 2000; 53 (4): 444-449. M. Genetic variability in Bradyrhizobium
53. Singh, S.P., Singh, H.B., Singh, D.K. Trichoderma japonicum strains nodulating soybean Glycine
Harzianum and Pseudomonas sp. mediated max (L.) Merrill. World J. Microbiol. Biotechnol.,
management of Sclerotium rolfsii rot in tomato 2012; 28:1831-1835.
(Lycopersicon esculentum mill.). Bioscan., 2013; 66. Thaweenut, N., Hachisuka, Y., Ando, S.,
8 (3): 801-804. Yanagisawa, S., Yoneyama, T. Two seasons’
54. Suprapta, D.N., Potential of Microbial study on nif H gene expression and nitrogen
Antagonists as biocontrol agents against plant fixation by diazotrophic endophytes in sugarcane
fungal pathogens. J. ISSAAS., 2012; 18 (2):1-8. (Saccharum spp. hybrids): Expression of nifH
55. Nakkeeran, S., Fernando, W.G.D., Siddiqui, genes similar to those of rhizobia. Plant Soil.,
Z.A. Plant growth promoting rhizobacteria 2011; 338:435-449.
formulations and its scope in commercialization 67. Terakado-Tonooka, J., Ohwaki, Y., Yamakawa,
for the management of pests and diseases. In: H., Tanaka, F., Yoneyama, T., Fujihara, S.
PGPR: biocontrol and biofertilization (Siddiqui, Expresses nifH genes of endophytic bacteria
ZA, ed.). Dordrecht, Netherlands: Springer, detected in field-growth sweet potatoes (Ipomoea
2005; pp 257–296. batata L.). Microbes Environl., 2008; 23:89-93.
56. Figueiredo, M.V.B., Seldin, L., de Araujo, 68. Govindarajan, M., Balandreau, J., Kwon, S.W.,
F.F., Ramos Mariano, R.D.L. Plant Growth Weon, H.Y., Lakshminarasimhan, C. Effects of
Promoting Rhizobacteria: Fundamentals and the inoculation of Burkholderia vietnamensis and
Applications. In: Plant Growth and Health related endophytic diazotrophic bacteria on grain
Promoting Bacteria (Maheshwari, DK, ed.). yield of rice. Microb. Ecol., 2008; 55:21-37.
Verlag, Berlin Heidelberg: Springer, 2010; pp 69. Ikeda, A.G, Bassani, L.L, Adamoski, D.,
21-43. Stringari, D., Cordeiro, V.K., Glienke, C., Maria
57. Kamilova, F., Okon, Y., de Weert, S., Hora, K. Steffens, B.R., Hungria, M., GalliTerasawa, L.V.
Commercialization of microbes: Manufacturing, Morphological and genetic characterization
inoculation, best practice for objective field of endophytic bacteria isolated from roots of
testing, and registration. In: Principles of plant- different maize genotypes. Microb. Ecol., 2013;
microbe interactions (Lugtenberg, B, ed.). 65:154-160.
International: Springer 2015; pp 319–327. 70. Khan, M.S., Zaidi, A., Ahemad, M., Oves, M.,
58. Glick, B.R. Bacteria with ACC deaminase can Wani, P.A. Plant growth promotion by phosphate
promote plant growth and help to feed the world. solubilising fungi - Current perspective. Arch.
Microbiol. Res., 2014; 169 (1): 30-39. Agron. Soil Sci., 2010; 56: 73-98.
59. Castro, R.O., Cornejo, H.A.C., Rodriguez, L.M., 71. Richardson, A.E, Simpson, R.J. Soil
Bucio, J.L. The role of microbial signals in plant microorganisms mediating phosphorus
growth and development. Plant Signal Behav., availability. Plant Physiol., 2011; 156:989-996.
2009; 4 (8):701–712. 72. Kaur, H., Kaur, J., Gera, R. Plant Growth
60. Khalid, A., Arshad, M., Zahir, Z.A. Screening Promoting Rhizobacteria: A Boon to Agriculture.
plant growth-promoting rhizobacteria for Int. J. Cell Sci. Biotechnol., 2016; 5: 17-22.
J PURE APPL MICROBIOL, 12(2), June 2018.
746 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria

73. Goldstein, A.H. Bioprocessing of Rock Phosphate 2008; 1778: 1781–1804.

Ore: Essential Technical Considerations for the 88. Vejan. P, Abdullah, R., Khadiran, T., Ismail. S,
Development of a Successful Commercial Boyce, A.N. Role of Plant Growth Promoting
Technology. New Orleans, USA: IFA technical Rhizobacteria in Agricultural Sustainability—A
conference. 2001. Review. Molecules., 2016; 21: 573: 1-17.
74. Egamberdiyeva, D., Qarshieva, D., Davranov, K. 89. Masalha, J., Kosegarten, H., Elmaci, O., Mengel,
Growth and yield of soybean varieties inoculated K. The Central role of Microbial activity for iron
with Bradyrhizobium spp. in N-deûcient acquisition in maize and sunflower. Biol. Fertil.
calcareous soils. Biol. Fert. Soils., 2004; 40:144- Soil., 2000; 30 (5) : 433–439.
146. 90. Neubauer, U., Furrer, G., Kayser, A., Schulin, R.,
75. Rodríguez, H., Fraga, R., Gonzalez, T., Bashan, 2000. Siderophores, NTA, citrate: potential soil
Y. Genetics of phosphate solubilisation and amendments to enhance heavy metal mobility
its potential applications for improving plant in phytoremediation. Int. J. Phytoremediation.
growth-promoting bacteria. Plant Soil., 2006; 2 (4), 353–368.
287:15-21. 91. Andrews, S.C., Robinson, A.K., Rodríguez-
76. Hider, R.C., Kong, X. Chemistry and Biology Quiñones, F. Bacterial iron homeostasis. FEMS
of Siderophores. Nat. Prod. Rep., 2010; 27(5): Microbiol. Rev., 2003; 27(2-3)::215-37.
637-657. 92. George, E. F., Machakova, I., Zazimalova,
77. Mohandass C. Bacterial Siderophores E .Plant Growth Regulators. I: Auxins, their
and their Biotechnological Applications Analogues and Inhibitors In: Plant Propagation
Marine Microbiology: Facts and by Tissue Culture. (George, EF, Hall, MA,
Opportunities. 2004:169 Deklerk, GJ, ed.). Dordrecht, Netherlands:
78. Fernandez V, Ebert G, Winkelmann G. The use of Springer, 2008; 175–204.
microbial siderophores for foliar iron application 93. Kogl. F., Kostermans. D.G.F.R. Heteroauxin
studies. Plant Soil., 2005; 272:245–252. als Stoffwechselprodukt niederer pflanzlicher
79. Khan, M.S., Zaidi, A., Wani, P.A., Oves, M. Role Organismen, Isolierung aus Hefe. Z Phys
of plant growth promoting rhizobacteria in the Chem., 1934; 228:113–121.
remediation of metal contaminated soils. Environ 94. Went, F.W., Thimann, K.V. Phytohormones.,
Chem. Lett., 2009; 7 (1): 1–19. New York: The Macmillan Company. 1937; pp
80. Rajkumar, M., Ae, N., Prasad, M.N.V., Freitas, H. 1-256.
Potential of siderophore-producing bacteria for 95. Woodward, A.W., Bartel, B. Auxin: regulation,
improving heavy metal phytoextraction. Trends action, and interaction. Ann. Bot., 2005; 95:707–
in Biotechnol., 2010; 28 (3):142-148. 735.
81. Murugappan, R.M., Aravinth, A., Rajaroobia, R., 96. Teale, W.D., Paponov, I.A., Palme. K. Auxin
Karthikeyan, M., Alamelu, M.R. Optimization of in action: signalling, transport and the control
MM9 Medium Constituents for Enhancement of plant growth and development. Nat.
of Siderophoregenesis in Marine Pseudomonas Rev. Mol. Cell Biol., 2006; 7: 847–859.
putida Using Response Surface Methodology. 97. Ahemad, M., Kibret, M. Mechanisms and
Indian .J. Microbiol., 2012; 52 (3): 433–441. applications of plant growth promoting
82. Wittenwiler, M. Mechanisms of Iron Mobilization rhizobacteria: Current perspective. J.King Saud
by Siderophores. 2007:1-22. Univ.Sci., 2014; 26 (1):1-20.
83. Kraemer, S.M., Crowley, D., Kretzschmar, 98. Dilfuza, E. Indole-Acetic Acid Production by
R.Siderophores in plant iron acquisition: Root Associated Bacteria and its Role in Plant
Geochemical aspects. Adv. Agron., 2006; 91: Growth and Development. In: Auxins: Structure,
1–46. Biosynthesis and Functions (Andrew, HK,
84. Neilands, J.B. Iron absorption and transport in Michelle, DF, ed.). Nova Science Publishers,
microorganisms. Ann.Rev. Nutr., 1981; 1: 27–46. 2011; pp1-13.
85. Crowley, D.E, Wang, Y.C., Reid, C.P.P., 99. Spaepen, S., Vanderleyden, J. Auxin and
Szaniszlo, P.J. Mechanism of iron acquisition Plant-Microbe Interactions. Cold Spring Harb.
from siderophores by microorganisms and plants. Perspaect Biol., 2011; 3(4):1-13.
Plant Soil., 1991; 130 (1-2): 179-198. 100. Patten, C.L., Glick, B.R. Bacterial biosynthesis
86. Saharan, B.S., Nehra, V. Plant Growth Promoting of indole-3-acetic acid. Can.J.Microbiol., 1996;
Rhizobacteria: A Critical Review. Life Sci. Med. 42 (3):207–220.
Res., 2011; 21:1-30. 101. Glickmann, E., Gardan, L., Jacquet, S.,
87. Krewulak, K.D., Vogel, H.J. Structural biology Hussain, S., Elasri, M., Petit, A., Dessaux, Y.
of bacterial iron uptake. Biochim.Biophys. Acta., Auxin production is a common feature of most
J PURE APPL MICROBIOL, 12(2), June 2018.
 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria 747

pathovars of Pseudomonas syringae. Mol. Plant 112. Tsavkelova, E.A., Klimova, S.Y., Cherdyntseva,
Microbe. Interact., 1998; 11: 156–162. T.A., Netrusov, A.I. Microbial producers of plant
102. Spaepen, S., Vanderleyden, J., Remans.R. Indole- growth stimulators and their practical use: a
3-acetic acid in microbial and microorganism- review. Appl. Biochem. Microbiol., 2006; 42 (2):
plant signaling. FEMS Microbiol. Rev., 2007; 117–126.
31: 425–448. 113. Ruanpanun, P., Tangchitsomkid, N., Hyde, K.D.,
103. Lambrecht, M., Okon, Y., Broek, A.V., Lumyong, S. Actinomycetes and fungi isolated
Vanderleyden, J. Indole-3-acetic acid: a from plant-parasitic nematode infested soils:
reciprocal signalling molecule in bacteria – plant screening of the effective biocontrol potential,
interactions. Trends Microbiol., 2000; 8 (7): 298- indole-3-acetic acid and siderophore production.
300. World J. Microbiol. Biotechnol., 2010; 26 (9):
104. Dobbelaere, S., Croonenborghs, A., Thys, A., 1569–1578.
Ptacek, D., Vanderleyden, J., Dutto, P., Labandera 114. Sarwar, M., Kremer, R.J. Determination of
Gonzalez, C., Caballero-Mellado, J., Anguirre, bacterially derived auxins using a microplate
J.F., Kapulnik, Y., Brener, S., Burdman, S., method. Lett. Appl. Microbiol., 1995; 20 (5):
Kadouri, D., Sarig, S., Okon, Y. Response of 282-285.
agronomically important crops to inoculation 115. Kravchenko, L.V., Azareva, T.S., Makarova,
with Azospirillum. Aust. J. Plant Physiol., 2001; N.M., Tikhonovich, I.A. The effect of tryptophan
28: 871-879. in plant root exudates on the phytostimulating
105. Zahir A., Abbas S. A., Khalid M., Arshad activity of rhizobacteria. Microbiol., 2004; 73:
M. Structure dependent microbially derived 156-158.
plant hormones by improving growth of maize 116. Kamilova F, Kravchenko LV, Shaposhnikov AI,
seedlings. Pak. J. Biol. Sci., 2000; 3:289–291. Azarova T, Makarova N, Lugtenberg B. Organic
106. Patten, C.L., Glick, B., Role of Pseudomonas acids, sugars, and L-tryptophane in exudates
putida indole acetic acid in development of the of vegetables growing on stonewool and their
host plant root system. Appl. Environ. Microbiol., effects on activities of rhizosphere bacteria. Mol.
2002; 68 (8): 3795-3801. Plant Microbe. Interact., 2006; 19 (3):250– 256.
107. Peyvandi, M., Farahani, F., Hussein, M., 117. Ghosh, S., Basu, P.S. Production and metabolism
Noormohamadi, Z., Ataii, S., Asgharzadi, A. of indole acetic acid in roots and root nodules of
Pseudomonas fluorescens and its ability to Phaseolus mungo. Microbiol Res., 2006; 161:
promote root formation of olive microshoots. 362–366.
Int. J. Plant Prod., 2010; 4 (1): 63-66. 118. Dullart, J. The bioproduction of indole-3-acetic
108. Ghosh, S., Sengupta, C., Maiti, T.K., Basu, acid and related compound in root nodules and
P.S. Production of 3- Indolylacetic acid in root roots of Lupinus luteus L. and by its rhizobial
nodules and Culture by a Rhizobium species symbiont. Acta. Bot. Neerl., 1970; 19:573-615.
isolated from root nodules of the Leguminous 119. Mano, Y., Nemoto, K.  The pathway of
pulse Phaseolus mungo. Folia Microbiologica. auxin biosynthesis in plants. J. Exp. Bot.,
2008; 53 (4), 351-355. 2012; 63: 2853–2872.
109. Khare, E., Arora, N.K. Effect of indole-3- 120. Werner, T., Motyka, V., Laucou, V., Smets,
acetic acid (IAA) produced by Pseudomonas R., Onckelen, H.V. Schmülling, T. Cytokinin-
aeruginosa in suppression of charcoal rot disease Deficient Transgenic Arabidopsis Plants Show
of chickpea. Curr. Microbiol., 2010; 61 (1): 64- Multiple Developmental Alterations Indicating
68. Opposite Functions of Cytokinins in the
110. Patil, N.B., Gajbhiye, M., Ahiwale, S.S., Gunjal, Regulation of Shoot and Root Meristem Activity.
A.P., Kapadnis, B.P. Optimization of Indole Plant Cell., 2003; 15: 2532–2550.
3-acetic acid (IAA) production by Acetobacter 121. Salisbury, F.B., Ross, C.W. Hormones and Plant
diazotrophic L1 isolated from Sugarcane. Int.J. Regulators: Auxins and Gibberellins. In: Plant
Environ. Sci., 2011; 2 (1): 295-302. Physiology (Bressan, RA, Handa, AK, ed.).
111. Dazzo, F.B., Yanni, Y.G., Rizk, R., De Bruijn, F.J., Belmont, California: Wadsworth Publishing
Rademaker, J., Squartini, A., Corich, V., Mateos, Company, 1992: pp 357-381.
P., Martinez-Molina, E. Progress in multinational 122. Arshad, M., Frankenberger, W.T. Jr. Microbial
collaborative studies on the beneficial association production of plant growth regulators. In: Soil
between Rhizobium Ieguminosarum by trifolii Microbial Ecology (Frankenberger, Jr. ed). New
and rice. In: The quest for nitrogen fixation in York: Dekker, 1993; pp 307–347.
rice (Ladha, JK, Reddy, PM, ed). Philippines: 123. Nieto, K.F., Frankenberger, W.T. Jr. Microbial
IRR1, Los Banos, 2000; pp 167–189. production of cytokinins .In: Soil Biochemistry
J PURE APPL MICROBIOL, 12(2), June 2018.
748 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria

(Bollag, JM, Stotzky, G. ed.). New York: Dekker, 136. Boiero, L., Perrig, D., Masciarelli, O., Penna, C.,
1990; pp 191–248. Cassan, F., Luna, V. Phytohormone production
124. Gutierrez-Manero F.J., Ramos-Solano, B., by three strains of Bradyrhizobium japonicum
Probanza, A., Mehouachi, J., Tadeo, F.R., Talon, and possible physiological and technological
M. The plant growth-promoting rhizobacteria implications. Appl. Microbiol. Biotechnol., 2007;
Bacillus licheniformis produce high amounts of 74:874–880.
physiologically active gibberillins. Physiologia. 137. Saleem, M., Arshad, M., Hussain, S., Bhatti,
Plantarum., 2001; 111: 206-211. A.S. Perspective of plant growth promoting
125. Timmusk, S., Nicander, B., Granhall, U., Tillberg, rhizobacteria (PGPR) containing ACC
E. Cytokinin production by Paenibacillus deaminase in stress agriculture. J. Ind. Microbiol.
polymyxa. Soil Biol. Biochem., 1999; 31:1847– Biotechnol., 2007; 34 (10):635–648.
1852. 138. Li, Q., Saleh-Lakha, S., Glick, B.R. The effect
126. Perrig D., Boiero M. L., Masciarelli O. A., of native and ACC deaminase-containing
Penna C., Ruiz O. A., Cassán F. D. Plant- Azospirillum brasilense Cd1843 on the rooting
growth-promoting compounds produced by two of carnation cuttings. Can. J. Microbiol., 2005;
agronomically important strains of Azospirillum 51:511-514.
brasilense, and implications for inoculant 139. Chen, L., Dodd, I.C., Theobald,
formulation. Appl. Microbiol. Biotechnol., 2007; J.C., Belimov, A.A., Davies, W.J. The
75: 1143–1150. rhizobacterium Variovorax paradoxus 5C-2,
127. Frankenberger, J.W.T., Arshad, M., Microbial containing ACC deaminase, promotes growth
synthesis of auxins. In: Phytohormones in soils and development of Arabidopsis thaliana via an
(Frankenberger, WT, Arshad, M, ed.). New York: ethylene-dependent pathway. J. Exp.Bot., 2013;
Marcel Dekker, 1995; pp 35–71. 64 (6):1565–1573.
128. Salisbury, F.B. The role of plant hormones. In: 140. Martinez-Viveros, O., Jorquera, M., Crowley,
Plant–Environment Interactions (Wilkinson, RE, D.E., Gajardo, G., Mora, M.L. Mechanisms
ed.). New York: Marcel Dekker. 1994; pp 39–81. and practical considerations involved in
129. MacMillan, J. Occurrence of gibberellins in plant growth promotion by rhizobacteria.
vascular plants, fungi and bacteria. J. Plant J. Soil Sci. Plant Nutr., 2010; 10: 293-319.
Growth Regul., 2002; 20: 387–442. 141. Glick, B.R., Penrose, D.M.,   Li, J. A model for
130. Bottini R., Cassán F., Piccoli P. Gibberellin the lowering of plant ethylene concentrations by
production by bacteria and its involvement in plant growth promoting bacteria. J. Theor. Biol.,
plant growth promotion and yield increase. Appl. 1998; 190: 63-68
Microbiol. Biotechnol., 2004; 65: 497–503. 142. Mayak, S., Tirosh, T., Glick, B.R. Plant growth-
131. Tien, T.M., Gaskins, M.H., Hubbell, D.H. Plant promoting bacteria confer resistance in tomato
Growth Substances Produced by Azospirillum plants to salt stress. Plant Physiol. Biochem.,
brasilense and their Effect on the Growth of 2004; 42 (6): 565-572.
Pearl Millet (Pennisetum americanum L.). Appl. 143. Govindasamy, V., Senthilkumar, M., Upendra-
Environ, Microbiol., 1979; 37(5):1016-1024. Kumar, A. K. PGPR-biotechnology for
132. Williams, P.M., de Mallorca, M.S. Abscisic acid management of abiotic and biotic stresses in
and gibberellin-like substances in roots and root crop plants. In: Potential microorganisms for
nodules of Glycine max. Plant Soil, 1982; 65(1): sustainable agriculture (Maheshwari DK, Dubey
19–26. RC, ed.). New Delhi: IK International, 2008; pp
133. Joo, G.J., Kin, Y.M., Kim, J.T., Rhee, I.K., 26–48.
Kim, J.H., Lee, I.J. Gibberellins-producing 144. Ghosh, S., Penterman, J.N., Little,
rhizobacteria increase endogenous gibberellins R.D., Chavez, R., Glick, B.R. Three newly
content and promote growth of red peppers. J. isolated plant growth-promoting bacilli facilitate
Microbiol., 2005; 43: 510–515. the growth of canola seedlings. Plant Physiol.
134. Dangar, T.K., Basu, P.S. Studies on plant growth Biochem., 2003; 41: 277-281.
substances, IAA metabolism and nitrogenase 145. Li. J., Glick, B.R. Transcriptional regulation
activity in root nodules of Phaseolus aureus o f t h e E n t e ro b a c t e r c l o a c a e U W 4
Roxb. var. mungo. Biologia. Plantarum., 1987; 1-aminocyclopropane-1-carboxylate (ACC)
29:350–354. deaminase gene (acdS). Can. J. Microbiol., 2001;
135. Dobbelaere, S., Vanderleyden, J., Okon, Y. 47:359–367.
Plant growth promoting effects of diazotrophs 146. Duan, J., Müller, K.M., Charles, T.C., Vesely,
in the rhizosphere. Crit. Rev. Plant Sci., 2003; S., Glick, B.R. 1-Aminocyclopropane-1-
22:107–149. carboxylate (ACC) deaminase genes in Rhizobia
J PURE APPL MICROBIOL, 12(2), June 2018.
 Jeyanthi & Kanimozhi: Plant Growth Promoting Rhizobacteria 749

from southern Saskatchewan. Microb. Ecol., 154. Haran, S., Schickler, H., Chet, I. Molecular
2009; 57:423–436. mechanisms of lytic enzymes involved in the
147. Hafeez, F.Y., Yasmin, S., Ariani, D., Rahman, biocontrol activity of Trichoderma harzianum.
M., Zafar, Y., Malik, K.A. Plant growth- Microbiology., 1996; 142: 2321-233.
promoting bacteria as biofertilizer. Agron. 155. Pitson, S. M., Seviour, R. J., McDougall, B.
Sustain. Dev., 2006; 26:143–150. M. Noncelluloytic fungal p-glucanases: their
148. Narayanasamy, P. Molecular Biology in Plant physiology and regulation. Enzyme Microb.
Pathogenesis and Disease Management. In: Techno., 1993; 15: 178-192.
Disease Development. India: Springer, 2008: pp 156. Ramamoorthy, V., Viswanathan, R., Raguchandar,
7-195. J., Prakasham, T. Samiyappan, R. Induction of
149. Reddy, P.P. Plant growth promoting rhizobacteria systemic resistance by plant growth promoting
(PGPR). In: Recent advances in crop protection. rhizobacteria in crop plants against pest and
India: Springer, 2013; pp 131–145. diseases. Crop Protection., 2001; 20: 1-11.
150. Duffy, B. Pathogen self-defense: Mechanisms 157. Choudhary, D.K., Prakash, A., Johr, B. N.
to counteract microbial antagonism. Ann. Rev. Induced systemic resistance (ISR) in plants:
Phytopathol., 2003; 41:501-38. Mechanism of action. Indian J. Microbiol., 2007;
151. Maksimov, Abizgil’dina, R.R., Pusenkova, 47(4): 289-297.
L.I. Plant growth promoting rhizobacteria as 158. Yan Z., Reddy M.S., Ryu C.M., Mc Inroy J.A.,
alternative to chemical crop protectors from Wilson M., Kloepper J.W. Induced systemic
pathogens (Review). Appl. Biochem. Microbiol., protection against tomato late blight elicited by
2011; 47:333-345. PGPR. Phytopathol., 2002; 92: 1329-1333.
152. de Souza, J.T., Weller, D.M., Raaijmakers, 159. Doornbos, R.F., Loon, L.C., Bakker, P.A.H.M.
J.M. Frequency, diversity and activity of 2, Impact of root exudates and plant defense
4-diacetylphloroglucinol producing fluorescent signalling on bacterial communities in the
Pseudomonas spp. in Dutch take-all decline soils. rhizosphere. Agron. Sustain. Dev. 2012; 32:
Phytopathology., 2003; 93: 54-63. 227–243.
153. Neeraja, C., Anil, K., Purushotham, P., Suma, 160. Zhang, S., Thomas L. White, T.L., Martinez,
K., Sarma, P., Moerschbacher, B.M., Podile, M.C., McInroy, J.A., Kloepper, J.W., Klassen,
A.R. Biotechnological approaches to develop W. Evaluation of plant growth-promoting
bacterial chitinases as a bioshield against fungal rhizobacteria for control of Phytophthora blight
diseases of plants. Crit. Rev. Biotechnol., 2010; on squash under greenhouse conditions. Biol
30:231-241. Control., 2010; 53: 129–135.

J PURE APPL MICROBIOL, 12(2), June 2018.