Potential of Plant Growth Promoting Rhizobacterias in Agriculture sector: A

Review

Muhammad Asif, Mamoona Naz and Mohsin Bashir

Abstract:
All living organisms directly or indirectly depend upon the agricultural industry and this imparts
too much pressure on food availability and security. To meet this increasing demand of food,
agricultural sector has been shifted from organic products to chemical products resulting in
severe damage to ecosystem, contaminated ground water, eutrophication in water bodies,
unhealthy soils and air pollution. Use of plant growth promoting rhizobacterias (PGPRs) has
been increasing because of its potential in sustainable cultivation and production. These bacterias
colonize in and on the roots of host plant and significantly enhance the plant growth and
development, helps in avoiding biotic and abiotic stresses, suppression of diseases by pests,
production of siderophores, volatile organic compounds and plant growth regulators by
stimulating various mechanisms even at very low concentrations. Many bacterial strains have
been mentioned in this review for their involvement in different crops and their adoption of
mechanisms for significantly affecting various vegetative and floral parameters. Therefore,
inoculation of PGPRs can be considered as eco-friendly practice and can be extensively used as
biofertilizer.

INTRODUCTION of ground water (Klimas and Paukstys,

Agricultural industry: Out of total world’s
land area, 38.47% is covered by agricultural
land with 28.43% arable land while 3.13%
land is permanently used for crop cultivation
and production. Every year 20-25% land is
being degraded and 5-10 million hectares
will be degraded in next coming years
(Abhilash et al., 2016). Agriculture industry
has been improved from the last several
decades to fulfill the food requirement of
continuously increasing population by
relying more on chemical products like
fertilizers, pesticides and insecticides
(Ahemad and Khan, 2012a). This
dependency of plants on fertilizers is
directly related to serious environmental
problems. Nitrates are leached down in the
deep layer of earth leading to contamination
1993) and eutrophication of water bodies
(Ahmad et al., 2005). Addition of
phosphorous in soil, results in precipitation
(Richardson and Simpson, 2011). Heavy
metal concentration of Cd, Pb and Hg also
exceeds the limit and enter the food chain
(Arshad and Frankenberger Jr, 1997;
Baldani et al., 2000) causing diseases in
human beings. Fertilizers also increase the
number of natural pests like flea beetle and
aphids (Eigenbrode and Pimentel, 1988;
Morales et al., 2001). Usage of chemical
products is continuously damaging the
environment and increases the cost of
production (Arshad and Frankenberger,
1992). There are several potential ways for
the sustainable production and restoring the
health status of soil and water by using
sustainable management practices (Ubertino
et al., 2016), bio-fertilizers (Kamkar, 2016;
Suhag, 2016), agricultural intensification
(Shrestha, 2018) and use of genetically
engineered micro-organisms (Pérez et al.,
2016).
What are plant growth promoting
rhizobacterias (PGPRs)?
Beneficial free living, soil bacteria’s
promoting plant growth, usually referred as
plant growth promoting rhizobacteria
(PGPRs) (Kloepper et al., 1989). Soil
surrounded by plant root system called
rhizosphere (Belimov et al., 2001) however
residing bacteria in or on the root system
called rhizobacteria (Beneduzi et al., 2008).
Out of all about 2-5% bacterial species are
referred as plant growth promoting
rhizobacteria (Bent et al., 2001). In PGPRs
bacillus and pseudomonas spp. are dominant
(Podile and Kishore, 2007). In late 1970, Joe
Kloepper coined the term PGPR and is
defined by ‘‘the soil micro-organisms that
make colonize in the rhizosphere of plants
by following inoculation on to seed and that
enhance plant growth’’ (Ahemad and Khan,
2011). By different mechanisms these tiny
micro-organisms have various beneficial
effects on host crop (Raza et al., 2016a;
Raza et al., 2016b). PGPRs have the
prospective for sustainable agriculture and
in sustaining the ecosystem. PGPRs are
known as natural compounds that alter the
plant, prolong flowers and break the
dormancy. The beneficial organisms fall into
two groups; (i) Plant growth promoters by
production of harmones and phosphate
solubilization (ii) Plant disease suppression
by production of anti-biotics (Gore and
Atlin, 2006). Moreover it was also found
when ornamental plants were propagated by
divisional method, these PGPRs utilize ACC
as source of nitrogen (N) and carbon (C)
(Sharp et al., 2011). These organisms’ help
in three different ways (i) prevention of
diseases (Chen et al., 1995; Chen et al.,
2006), (ii) synthesizing compounds (volatile
organic) for the host plants (Cattelan et al.,
1999; Katiyar et al., 2016) and (iii)
facilitating the uptake of nutrients from root
zone (Chandra et al., 2007).
Extracellular and intracellular PGPRs:
PGPRs can also be divided into 2 forms (i)
extracellular plant growth promoting
rhizobacteria (ePGPR) residing in root
cortex and (ii) intracellular plant growth
promoting rhizobacteria (iPGPR) residing in
the specialized structures call nodules
(Martínez-Viveros et al., 2010). The ePGPR
includes Pseudomonas, Azotobacter,
Bacillus, Serratia, Azospirillum,
Arthrobacter, Caulobacter, Erwinia,
Burkholderia, Chromobacterium,
Agrobacterium, Micrococcous,
Flavobacterium and Arthrobacter while
iPGPR includes Rhizobium, Allorhizobium,
Mesorhizobium, Bradyrhizobium and
Frankia species (Bhattacharyya and Jha,
2012).
Role of plant growth promoting
rhizobacteria: Plant Growth Promoting
Rhizobacterias has showed the potential in
enhancing the plant growth and
development by specific traits as shown in
Table 1 (Gupta et al., 2014). PGPRs
stimulate various mechanisms (direct and
indirect) to enhance plant growth by
improving resistance through diseases,
efficiently uptake of nutrients and enhancing
plant physiology (Zakry et al., 2012). The
mechanisms of bacterial strains include (i)
production of volatile organic compounds in
host plant (VOCs) (ii) prevention of diseases
by producing glucanase , chitinase, and
ACC-deaminase (iii) nutrient fixation for
efficient uptake by roots (iv) plant growth
regulators (v) stress tolerance in plants and
(vi) production of siderophores (Choudhary
et al., 2011; García-Fraile et al., 2015).
Although, different plant growth promoting
rhizobacterias has different mode of action
depending on the host plants and also their
number and colonization varies in
rhizosphere (García-Fraile et al., 2015).
PGPRs colonize also vary by many biotic
and abiotic factors: Biotic includes plant
genotypes and defensive mechanisms, its
developmental stages and other residing
microbial community in rhizosphere of plant
while abiotic includes soil management,
compositioon and climatic conditions
(Vacheron et al., 2013).
Nutrients locking: PGPR has the capacity
to lock or fix the nutrient in soil for the
growth and development of crops (Kumar,
2016). Some bacterial strains have potential
to solubilize the phosphate and make the
phosphate ions available for plant roots
(Herrera Paredes and Lebeis, 2016). Many
bacterial species (kocuria) has the capacity
for siderophore production, solubilizing
phosphate and an IAA production for host
plant (Goswami et al., 2014). Azospirillum
are aerobic heterotrophs (Khan et al., 2009)
involved in fixing atmospheric nitrogen
(Khalid et al., 2001) to enhance uptake by
roots and make extensive colonies in
gramineous crop rhizosphere (Kloepper et
al., 1980).
Production of siderophores: These micro-
organisms have the potential to extract the
metal ions like iron (Saha et al., 2016). Iron
is essential element for all living organisms
and accumulates as ‘iron oxides’,
‘hydroxides’ however is not readily utilized
by plant population (Kunc and Macura,
1988). PGPR secretes siderophore (low
molecular weight iron, having side chains
and functional groups that further provide a
high-affinity set of ligands to synchronize
with ferric ions) and provide iron to the
plants to enhance growth when iron is not
available. Phyllobacter strain produced
siderophores and utilized by plants to
sequester iron (Flores_Félix et al., 2015).
Production of volatile organic
compounds: Bacillus, Serratia,
Arthrobacter, Pseudomonas and
Stenotrophomonas have the potential to
produce volatile organic compounds
(VOCs). These VOCs have the capacity to
impart systemic resistance towards plant
pathogens and improving the plant growth.
Bacillus synthesized Acetoin and 2,3-
butanediol and these compounds are
responsible for significant increase in plant
vegetative parameters (Ryu et al., 2003).
Some bacterial species has the capacity to
secrete VOCs that by different mechanisms
enhance resistance against diseases, abiotic
stress tolerance and increases the crop
biomass (Effmert et al., 2012; Kanchiswamy
et al., 2015)
Plant growth regulators: Plant Growth
Regulators (pgr) are the substances which
even at very low concentrations < 1 mM
increase, decrease or modify the
development of crops (Damam et al., 2016),
stomatal movement, differentiation and
development (Vejan et al., 2016). These
PGPRs produced gibberellins, cytokinins,
abscisic acid, ethylene, brassino steroids
however major harmone produced was
indole acetic acid (IAA) (Malik et al., 1997).
IAA showed significantly affect the root hair
development, root proliferation and
respiration rate which in return increased the
uptake of minerals from the plants (Mayak
et al., 1999). It has already been reported
that about 75% of bacterial strains, isolated
from the root zone of plant species have the
ability to synthesize and release harmones
like auxin as secondary metabolites
(Masalha et al., 2000).
Prevention of diseases by producing
glucanase, chitinase, and ACC-
deaminase: Bacterial species like
(Pseudomonas and Bacillus) produced
lipopeptide biosurfactants. These have
potential to be used in bio-control because
of their competitive effect with other
pathogens (De Bruijn et al., 2007;
Raaijmakers et al., 2010). Pseudomonads
produced phenazine possesses the redox
activity and can significantly suppress the
pathogens like F.oxysporum and
Gaeumannomyces graminis (Chin A Woeng
et al., 2003). Antibiotics like (circulin,
colistin) produced by Bacillus ssp. are active
against many pathogenic fungi, gram-
positive and gram-negative bacteria
(Maksimov et al., 2011). P. fluorescens
produced the antibiotic pyrrolnitrin, have the
potential to prevent the gossypium plants
from damping-off disease (Hill et al., 1994).
Stress tolerance in plants: Out of total
about 70% of food crops are extensively
damaged because of abiotic stresses
(flooding, drought, salinity and temperature
fluctuations) and biotic stresses (bacteria,
fuji, nematodes and insects) (Haggag et al.,
2015; Vejan et al., 2016). These micro-
organisms has already showed significant
effect against abiotic stresses as in soybean,
chickpea, and wheat relationship formed
between drought resistance and PGPR
(Ngumbi and Kloepper, 2016). Water-use
efficiency and tolerance to salts was found
in okra plants inoculated with bacterial
strains (Habib et al., 2016). Roots or seeds
inoculation with PGPRs overnight in
cultures of showed significant tolerance
from many biotic stresses (Ngumbi and
Kloepper, 2016).
Application methods: Bacterial strains
show significant result at appropriate
concentration and by using suitable method
of application. Seed inoculation with
rhizobium at turbidity of 5 in McFarland
standards shows production of siderophore
in tomatoes, lettuce and pepper
(García_Fraile et al., 2012; Flores_Félix et
al., 2013). Bacterial specie (pseudomonas)
produced significant amount of Chitinase
and glucanases in Cajanus cajan (Kumar et
al., 2010). Phyllobacterium was inoculated
on strawberries seddling and significantly
solubilize adequate amount of phosphate
(Flores_Félix et al., 2015). During planting
of seedling of wheat incoluation of 2 mL
Azorhizobium help the plant roots in
nitrogen fixation and absorption (Sabry et
al., 1997).
PGPR as biofertilizer: As the trend of
organic farming is gaining popularity in
agricultural production. Biofertilizers are the
products containing micro-organisms when
applied to the parts of host plant like roots,
seed inoculation, seedlings inoculation and
spraying on plant surfaces. These bacterial
species make colonize on root zone or in the
interior parts of roots and enhance
significant growth and development of
crops. Mishra concluded that these
biofertilizers are latent or living cells
involve in boosting phosphate solubilization,
nitrogen fixation and cellulolytic micro-
organisms (Mishra et al., 2013). Bio-
fertilizers contain one or more micro-
organisms increasing plant growth by (i)
increasing plant access to nutrients, (ii)
making more nutrients available to plants
and (iii) replacing nutrients (Malusá and
Vassilev, 2014). Growth promoting effects
in crops and bio-control has significantly
increased by using biofertilizer (combination
of PGPR and compost) (Chen et al., 2011).
Bacillus spp. and Pseodomonas spp. are
known to be effective bio-control agents (De
La Fuente et al., 2006; Gong et al., 2006).
PGPR are classified as the ecofriendly
biofertilizers, restoring the nutrient cycle in
plants, soils and can be used to obtain
organic products.
Table: Role of plant growth promoting rhizobacteria in different crops.

PGPR PGPR Crops Observations References

mechanism

Azospirillium brasilence Nitrogen Festuca arundinacea Increase plant tolerance to polycyclic (Orlandini et al., 2014)
fixation aromatic hydrocarbons

Azospirillium lipoferum Nitrogen Triticum aestivum Promote development of root system (Belimov et al., 2004)
fixation

Azospirillum brasilence Nitrogen Saccharum officinarum Increses the formation of lateral and (Orlandini et al., 2014)
fixation adventitious roots and root hairs

Azospirillum brasilence Nitrogen Zea mays, Glycine max Synthesize indole acetic acid in (Orlandini et al., 2014)
and Bradyrhizobium fixation concentrations that are adequate to induce
japonicum morphological changes and promote growth

Azotobacter Cytokinin Brassica juncia Stimulated plant growth (Orlandini et al., 2014;
chroococcum synthesis Narożna et al., 2015)

Bacillus Auxin Potato Auxin contents of inoculated plants were (Ahmed and Hasnain, 2010)
synthesis enhanced

Bacillus Auxin Solanum lycopersicum Prevent tomato molt virus (Otieno et al., 2015)
amyloliquefaciens synthesis

Bacillus Cytokinin Cucumber Cucumber seedlings subjected to (Sokolova et al., 2011)

synthesis bacterization had well developed lateral
roots.

Bacillus circulans, Cytokinin Vigna radiata Phosphate solubilizing (Otieno et al., 2015)
Cladosporium herbarum synthesis

Bacillus Potassium pepper, cucumber The results showed that there was a (Han and Lee, 2005; Han and
solubilization relatively higher availability of P and K in Lee, 2006)
soils planted with pepper than with
cucumber
Bacillus licheniformis Phosphate Piper nigrum Protection from Myzus persicae (Ajithkumar et al., 2015)
solubilization

Bacillus Antibiotic Alfalfa Filtrates of cultures suppressed alfalfa (Dobereiner, 1961)

production disease caused by P. medicaginis and
inhibited the growth of the pathogen in an
agar plate assay.

Chryseobacterium Siderophore Tomato Siderophore production increased as (Radzki et al., 2013)

production bacterial biomass increased after 16 h of
culture

Gluconacetobacter Nitrogen Sugar cane The endophytic establishment of G. (Muñoz-Rojas and Caballero-
fixation diazotrophicus within stems of sugarcane Mellado, 2003)
was confirmed by the scanning electron
microscopy.

Herbaspirillum Nitrogen Rice GFP-tagged cells of Herbaspirillum sp. (Elbeltagy et al., 2001)
fixation strain B501gfp1 were apparently localized
in intercellular spaces of shoot tissues of 7-
day-old seedlings of O. officinalis W0012.

Pseudomonas Chitinase and Cotton Help cease damping off of cotton (Ramadan et al., 2016;
fluorescens glucanases Santoro et al., 2016)
production

Pseudomonas sp. Anti-biotic and Dianthus caryophyllus Prevent fusarium wilt (Ahemad and Khan, 2012b;
Siderophore Rathore, 2014)
production

Pseudomonas putida, Anti-biotic and Cucumis sativus Prevent cucumber anthracnose Rathore, 2014)
Serratia marcescens Siderophore
production

Pseudomonas putida Anti-biotic Arabidopsis thaliana Improve utilization of plant secondary (Ahemad and Khan, 2012a)
production metabolites

Anti-biotic and Gossypium hirsutum Inferred resistance against Helicoverpa (Ross et al., 1995)
 Siderophore armigera virus
production

Pseudomonas Anti-biotic Phaseolus vulgaris Prevent halo blight (Ramadan et al., 2016)
fluorescens production

Pseudomonas Anti-biotic and Triticum aestivum Help prevent fusarium culmorum (Santoro et al., 2016)
fluorescens Siderophore
production Hordeum vulgare

Pseudomonas Induction of Medicago sativa Increase metabolism, sequester cadmium (Ramadan et al., 2016)
fluorescens plant stress from solution and degrade trichloroethylene
resistance

Pseudomonas cepacia Induction of Gossypium hirsutum Help fight the rhizoctonia solani virus (Pérez-Montaño et al., 2014)
plant stress
resistance

Pseudomonas cepacia ACC Phaseolus vulgaris Prevent Sclerotium rolfsii (Pérez-Montaño et al., 2014)
deaminase
synthesis

Pseudomonas cepacia Induction of Cucumis sativus Prevent pathogens in Pythium ultimum (Pérez-Montaño et al., 2014)
plant stress
resistance

Pseudomonas ACC Vigna radiate Prevent root knot formation (Ngumbi and Kloepper,
aeruginosa, Bacillus deaminase 2016)
subtilis synthesis

Paenibacillus polymyxa Anti-biotic and Phaseolus vulgaris Alleviate adverse effects of drought stress (Ngumbi and Kloepper,
Siderophore and maintain plant 2016)
production
Growth

Paenibacillus polymyxa Siderophore Sesamum indicum Prevent fungal disease (Ngumbi and Kloepper,
production 2016)
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