REVI EW PAPER

Rhizosphere: its structure, bacterial diversity

and signicance
Pratibha Prashar

Neera Kapoor

Sarita Sachdeva
Published online: 14 July 2013
Springer Science+Business Media Dordrecht 2013
Abstract Sustainable agricultural practices are the
answer to multifaceted problems that have resulted due
to prolonged and indiscriminate use of chemical based
agronomic tools to improve crop productions for the
last many decades. The hunt for suitable ecofriendly
options to replace the chemical fertilizers and pesti-
cides has thus been aggravated. Owingto their versatile
and unmatchable capacities microbial agents offer an
attractive and feasible option to develop the biological
tools to replace/supplement the chemicals. Exploring
the microorganisms that reside in close proximity to
the plant is thus a justied move in the direction to
achieve this target. One of the most lucrative options is
to look into the rhizosphere. Rhizosphere may be
dened as the narrow zone of soil that surrounds and
get inuenced by the roots of the plants. It is rich in
nutrients compared to the bulk soil and hence exhibit
intense biological and chemical activities. A wide
range of macro and microorganisms including bacte-
ria, fungi, virus, protozoa, algae, nematodes and
microarthropods co-exist in rhizosphere and show a
variety of interactions between themselves as well as
with the plant. Plant friendly bacteria residing in
rhizosphere which exert benecial affect on it are
called as plant growth promoting rhizobacteria
(PGPR). Here we review the structure and bacterial
diversity of the rhizosphere. The major points dis-
cussed here are: (1) structure and composition of the
rhizosphere (2) range of bacteria found in rhizosphere
and their interactions with the plant with a particular
emphasis on PGPR (3) mechanisms of plant growth
promotion by the PGPR (4) rhizosphere competence.
Keywords Sustainable agriculture Rhizosphere
Plant growth promoting rhizobacteria Plantmicrobe
interactions
1 Introduction
Though microbial diversity constitutes most extraor-
dinary and ubiquitous life on earth still they are not
uniformly distributed in various habitats across the
planet. Majority of the microbial populations are
concentrated in nutrient rich niches like the rhizo-
sphere that have a constant supply of easily utilizable
nutrients. Rhizosphere has an enormous pool of soil
microorganisms and is considered as the hot spot for
microbial colonization and activity. It is the largest
ecosystem on earth with huge energy ux (Barriuso
P. Prashar N. Kapoor
School of Sciences, IGNOU, New Delhi, India
e-mail: neerakapoor@ignou.ac.in
P. Prashar (&) S. Sachdeva
Department of Biotechnology, FET, MRIU, Sector 43,
Aravalli Hills, Faridabad, India
e-mail: pprashar@gmail.com; pprashar.fet@mriu.edu.in
S. Sachdeva
e-mail: sarita.fet@mriu.edu.in
1 3
Rev Environ Sci Biotechnol (2014) 13:6377
DOI 10.1007/s11157-013-9317-z
et al. 2008). Generally regarded as a thin zone
(12 mm thick), it holds a large volume of soil in it,
which varies greatly with the plant, soil, root structure
and most importantly the method used to determine it
because it does not have a well dened boundary
(Hinsinger et al. 2005). Due to their close proximity
and/or continuous association with the plant, the
diverse forms of microorganisms found in the rhizo-
sphere inuence the host plant in a variety of ways.
These may be broadly classied as benecial effects
leading to improvement of plant health and growth or
harmful effects, i.e. the pathogenic activities. Thus, it
is very important to understand the composition,
ecology, dynamics and activities of rhizospheric
microbial communities, before we can exploit the
rhizosphere microora as a tool for developing
sustainable agricultural practices.
2 Rhizosphere
The term rhizosphere has been derived from the
Greek word rhiza, meaning root, and sphere,
meaning eld of inuence. It was rst dened by
German scientist Hiltner (1904) as the zone of soil
immediately adjacent to legume roots that supports
high levels of bacterial activity. However, over the
period of time, it has been redened many times to
include the volume of soil inuenced by the root and
parts of root tissues as well as the soil surrounding the
root in which physical, chemical and biological
properties have been changed by root growth and
activity (Pinton et al. 2001). Rhizosphere has been
broadly subdivided into the following three zones
(Clark 1949; Lynch 1987; Pinton et al. 2001) (Fig. 1):
1. Endorhizosphere: that consists of the root tissue
including the endodermis and cortical layers.
2. Rhizoplane: is the root surface where soil particles
and microbes adhere. It consists of epidermis,
cortex and mucilaginous polysaccharide layer.
3. Ectorhizosphere: that consists of soil immediately
adjacent to the root.
Apart from these three basic zones, certain other
layers may be dened in some cases e.g. in plants with
mycorrhizal association, there is a zone termed as the
mycorrhizosphere (Linderman 1988) while in some
other plants another, strongly adhering dense layer
termed as rhizosheath, is found. It consists of root
hairs, mucoid material, microbes and soil particles
(Curl and Truelove 1986). The root itself is a part of
the rhizosphere as endophytic microorganisms colo-
nize the inner root tissues as well (Bowen and Rovira
1999). The volume of the soil which is not a part of the
rhizosphere, i.e. which is not inuenced by the root is
known as bulk soil (Gobat et al. 2004). The dead root
is transformed into soil by rhizospheric activity but it
is different from the bulk soil. Thus, rhizosphere may
be considered as a unique region distinct from the bulk
soil.
2.1 Rhizosphere effect
In the due course of its growth and development, plant
passes through the early stages of seed germination
and seedling growth. During this process a variety of
organic compounds are released from the roots by
exudation, secretion and deposition (Curl and True-
love 1986) making the rhizosphere rich in nutrients as
compared to the bulk soil. This acts as a driving force
for the set up of active and enhanced microbial
populations in root zone, much higher as compared to
the bulk soil (Grayston et al. 1996). This phenomenon
of establishment of rich microora in the rhizosphere
under the inuence of root-secreted nutrients is
referred as the rhizosphere effect or plant effect
(Morgan and Whipps 2001; Antoun and Prevost
Fig. 1 A simplistic diagram of rhizosphere
64 Rev Environ Sci Biotechnol (2014) 13:6377
1 3
2005). It is calculated in terms of rhizosphere ratio, i.e.
R: S by dividing the total number of microorganisms
in the rhizosphere (R) by the corresponding number in
the bulk soil (S) (Aneja 2003). Rhizosphere effect is
reected by the noticeable difference in the structure
of microbial populations of uncultivated and culti-
vated soils (Antoun and Prevost 2005) and the
variations in bacterial and fungal community struc-
tures with rhizosphere related factors such as the crop
variety (Berg et al. 2006), plant growth developmental
stages (Gomes et al. 2003) and soil characteristics (Nie
et al. 2009).
Though greater rhizosphere effect has been
reported for bacteria that show R: S values ranging
between 10 and 100 or even more (Katznelson et al.
1948) than with fungi (Buyer et al. 2002) however
recent studies utilizing cultivation-independent anal-
ysis of soil microora have revealed signicant
rhizosphere effect for soil fungi as well (Gomes
et al. 2003; Berg et al. 2005). For certain classes of soil
bacteria like ammonifying and denitrifying bacteria
(Rouatt et al. 1960) an even more pronounced
rhizosphere effect has been observed whereas it is
almost negligible for algae (Aneja 2003). Though
some reports have been obtained on stimulating
effects of root exudates of plants like tea and pea on
algal populations under controlled conditions (Had-
eld 1960; Cullimore and Woodbine 1963) such
effects have not been found very signicant in natural
soil habitats and higher algal populations are generally
recorded in the bulk soils. Soil protozoa form an
important part of the plantbacteriaprotozoa interac-
tions which are critical in nutrient recycling and
selective set-up of benecial bacterial populations in
the rhizosphere (Kreuzer et al. 2006). Due to the effect
of root derived carbon and large bacterial populations
in the rhizosphere, protozoan population may increase
as much as 35-fold (Zwart et al. 1994) in this zone.
Hence, it may be concluded that owing to the nutrient
richness of rhizosphere and excellent substrate utili-
zation capacities of bacteria, larger bacterial popula-
tions can be encountered in rhizosphere as compared
to other forms of soil microbes.
2.2 Rhizodeposition
The term rhizodeposition was rst dened by Whipps
and Lynch (1985) as the material lost from plant
roots, including water-soluble exudates, secretions of
insoluble materials, lysates, dead ne roots and gases
like CO
2
and ethylene. In simple terms it is dened as
the organic compounds released by living plant roots
into their surrounding environment (Whipps 1990;
Nguyen 2003) and may also include the inorganic ions
(Uren 2001). It is equivalent to almost 1560 % of the
total photosynthetic production of the plant and leads
to the accumulation of substantial carbon and energy
reserves in the rhizosphere for the microora (Curl and
Truelove 1986; Lynch and Whipps 1990). The plant-
derived carbon allocated belowground via roots,
consists of three main components (Cheng and
Gershenson 2007):
1. Roots mass: that may be living or dead.
2. Rhizodeposit: materials of plant origin localized
in the rhizosphere or the surrounding soil which
are utilized and transformed by rhizosphere biota
and mixed with soil organic materials.
3. Carbon dioxide: released as a result of respiration
of roots and root symbionts or microbial
respiration.
Rhizodeposition is a signicant process in terms of
studying the carbon uxes in the rhizosphere. Rhizo-
deposit is subdivided into various parts, i.e. root cap
cells and root tissues (sloughed root hairs and epider-
mal cells) (Rovira 1956), mucilage and root exudates
(Nguyen 2003) (Fig. 2). Root exudates are the most
important part of the rhizodeposit and are classied
into two types depending on their molecular weight.
First class comprises of the low molecular weight
components like water soluble compounds including
simple carbohydrates, amino acids, organic acids,
plant hormones, vitamins, phenolics, sugar phosphate
esters, ions and many other carbon-containing sec-
ondary metabolites (Uren 2001; Farrar et al. 2003;
Bais et al. 2006; Cheng and Gershenson 2007). High
molecular weight exudates form the second class and
these are generally enzymes, proteins and mucilage
(polysaccharides). High molecular weight exudates
are more signicant in terms of total mass of the root
exudates but have comparatively lesser variety than
the rst class (Bais et al. 2006).
Exudates may also be classied as active and
passive exudates on the basis of their role and mode of
secretion from the roots (Rougier and Chaboud 1989;
Bais et al. 2006). Passive exudates have unknown
functions and are diffused from the roots as basal
exudation (output of waste materials) depending on
Rev Environ Sci Biotechnol (2014) 13:6377 65
1 3
the gradient (Bais et al. 2006). They constitute about
35 % of the total carbon xed during photosynthesis
(Pinton et al. 2001). The active exudates are secreted
through open membrane pores of the plants and have a
specic function such as lubrication and defense
(Jones et al. 2004; Bais et al. 2006).
Another classication of the exudates can be made
on the basis of their biological activity and accordingly
they may be the signaling molecules, phytoalexins,
phytohormones, enzymes or allelochemicals (Nanni-
pieri et al. 2007).
Chemical composition of the rhizodeposit is an
important determinant of the functions and ecological
consequences of rhizodeposition (Cheng and Ger-
shenson 2007). The composition, rate and extent of
exudations depend on genetic factors and vary widely
among plant species and environmental conditions
(Kochian et al. 2005). Persistence of root exudates in
the rhizosphere is governed by their chemical prop-
erties, their stability and the soil volume through
which they diffuse. They may loose their properties
and hence get inactivated as a result of processes like
adsorption, biodegradation, volatilization, chemical
degradation, etc. (Nannipieri et al. 2007).
Exudation provides various kinds of physical and
chemical benets to the plant like reduction of friction
between root tips and soil, reduction in root desicca-
tion process and improving the structural stability of
soil (Rougier and Chaboud 1989). Rhizodeposition is
expressed in terms of C release by the roots (CdfR) by
measuring the production of labeled CO
2
in the
rhizosphere of 14C-labelled plants (Nguyen 2003).
However, apart from carbon compounds, various
kinds of nitrogen containing substances are also
released by the plant roots like nitrates (Wacquant
et al. 1989), ammonium ions (Brophy and Heichel
1989) and amino acids (Rovira 1956; Phillips et al.
2004, 2006).
Rhizodeposition is affected qualitatively as well as
quantitatively by a number of biotic and abiotic factors
associated with plant and soil (Rovira 1956; Lynch
and Whipps 1990; Nguyen 2003; Jones et al. 2004) as
summarized in the Table 1.
Exudation and plant health are mutually related.
The quality and quantity of exudates affects the
microbial diversity including the benecial and dele-
terious microorganisms as well as the related ecolog-
ical processes in the rhizosphere (Bolton et al. 1993;
Jaeger et al. 1999; Paterson et al. 2007) which in turn
inuence the plant processes like the rooting patterns,
nutrient availability and pathogen persistence in the
rhizosphere (Bolton et al. 1993; Bowen and Rovira
1999; Barea 2000). At the same time microbial
activities in the rhizosphere modify the root exudation
process and pattern. Thus, it may be said that
rhizodeposition strongly inuence the structural and
functional aspects of microbial communities in the
rhizosphere.
3 Rhizosphere bacterial diversity
Though majority of the soil microorganisms (approx-
imately 99 %) are not culturable, recent advances in
biochemical and molecular genetics techniques for
isolation of unculturable bacterial strains has enabled
the scientists to generate vital information pertaining
to the rhizosphere bacterial communities. Most com-
monly used tools for studying the diversity of uncul-
trable microbes include phospholipid fatty acid
analysis (PLFA), nucleic acid extraction and hybrid-
ization, polymerase chain reaction (PCR) based
methods, rRNA sequencing, G ? C percentages and
DNA re-association between bacteria in the commu-
nity, restriction fragment length polymorphism
(RFLP), amplied ribosomal DNA restriction analysis
Fig. 2 Rhizodeposit. It consists of material of plant origin that is released by the roots and is localized in the rhizosphere. It contributes
signicantly towards the total plant-derived carbon in soil as well as developing rich microbial diversity in the rhizosphere
66 Rev Environ Sci Biotechnol (2014) 13:6377
1 3
(ARDRA), cloning and sequencing techniques and
microarrays (Smalla et al. 2001; Butler et al. 2003;
Teixeira et al. 2010). However, the volume of
literature on the diversity studies of fungal communi-
ties found in rhizosphere is much less than that for
bacterial diversity because similar molecular tools for
isolation and characterization of fungi have been
developed much later.
As described above, rhizosphere has very high
concentrations of easily degradable carbon sources
due to rhizodeposition. This triggers an inated rate of
microbial activity in this soil zone that may be up to 50
times higher than in the bulk soil. Thus, complex food
webs develop in the rhizosphere linking both macro
and microorganisms like bacteria, fungi, nematodes,
protozoa, algae and microarthropods (Jeffery et al.
2010). Rhizophere thus harbors an extremely complex
microbial community qualitatively as well as quanti-
tatively and it includes saprophytes, epiphytes, endo-
phytes, pathogens as well as many advantageous
microorganisms (Avis et al. 2008). Rhizospheric
microbial load ranges from 10
10
to 10
12
per gram of
soil while it is generally less than 10
8
in the bulk soil
(Foster 1988).
Bacteria are the most abundant microbes in the
rhizosphere and hence they are bound to inuence the
plant in a signicant manner. Up to 15 % of the total
root surface may be covered by a variety of bacterial
strains (van Loon 2007). The most common genera of
bacteria that have been reported in the rhizosphere are
Pseudomonas, Bacillus, Arthrobacter, Rhizobia,
Agrobacterium, Alcaligenes, Azotobacter, Mycobac-
terium, Flavobacter, Cellulomonas and Micrococcus.
Predominant bacterial strains in the rhizosphere
includes gram-negative, rod shaped, non-sporulating
bacteria belonging to the groups proteobacteria and
actinobacteria (Atlas and Bartha 1993; Teixeira et al.
2010) of which Pseudomonas are the most abundant.
This may be attributed to the efciency of gram-
negative bacteria to utilize the root exudates and hence
they are stimulated by rhizodeposition while the gram-
positive bacteria are rather inhibited (Steer and Harris
2000). The aerobic bacteria are relatively lesser
because of the reduced oxygen levels in the rhizo-
sphere owing to root respiration (Garbeva et al. 2004).
Gram-positive, rods or cocci and aerobic spore
forming strains like Bacillus and Clostridium are
comparatively lesser but various strains of Bacillus
constitutes the chief gram-positive inhabitants of
rhizosphere (up to 95 % of total gram-positive soil
bacilli) followed by Arthrobacter and Frankia (Bar-
riuso et al. 2008). However, some recent studies have
reported gram-positive bacterial strains, Bacillus in
particular, to be more numerous than the gram-
negative bacteria in crops like strawberry, oilseed
rape, potato (Smalla et al. 2001), wheat (Joshi and
Table 1 Biotic and abiotic factors affecting rhizodeposition
Soil Plant
Biotic Abiotic Biotic Abiotic
Microbial community structure Soil type Plant species Temperature
Microbial community type Soil texture Photosynthesis Moisture
Microbial community activity pH Development stage Humidity
Phytohormone production Impedance Root age Elevated CO
2
Toxin production Salinity Root architecture Light intensity
Quorum sensing Water availability Nutrition deciency Pesticides
Biocontrol agents Organic matter Nodulation Irrigation
Pathogen Redox potential Membrane permeability Ozone
Release of root signal molecules Metal ion content Release of microbial signals Wind speed
Mycorrhiza Compaction Cytosolic concentration Fire
Rooting depth Allelochemical release Available space
Density Latitude, Altitude
Drainage and aeration Erosion
The range and amount of organic and inorganic compounds released by plant roots into the surrounding soil depends on all the listed
soil and plant associated factors
Rev Environ Sci Biotechnol (2014) 13:6377 67
1 3
Bhatt 2010; Rawat et al. 2011) and rice (Joshi et al.
2011), etc. This may be attributed to the ability of
Bacillus to form endospores and produce antimicro-
bial substances that inhibit other competitors. Distri-
bution of microora among the different layers of
rhizosphere has been described in terms of root
colonization which includes microbial growth in the
rhizoplane and/or root tissues and rhizosphere coloni-
zation which includes microbial growth in the adjoin-
ing layers of soil which are under the inuence of the
root (Kloepper et al. 1991; Kloepper 1994). Thus, it
may be summarized that rhizosphere is one of the
richest ecological zones of soil in terms bacterial
diversity.
3.1 Factors affecting rhizosphere bacterial
diversity
The bacterial community structure in the rhizosphere
is inuenced by a variety of biotic and abiotic factors.
Plant itself is the most crucial factor in determining the
predominant bacterial strains in the rhizosphere due to
the signicant role of the root exudates in set-up of
bacterial populations. Plant-related features such as
the cultivars, age of plant and root characteristics have
been found to govern the bacterial diversity and the
predominant species in the rhizosphere (Smalla et al.
2001; MacDonald et al. 2004). Age and developmen-
tal stage of the plant plays a critical role in deciding the
rhizosphere community structure of bacteria. The
rhizosphere of a young plant is chiey inhabited by
r-strategy organisms, i.e. bacterial species which have
fast growth rates and utilize simple substrates pro-
vided by rhizodeposition (Brimecombe et al. 2001).
However, as the aging process continue the dominance
shifts to bacterial communities with relatively slow
growth rates and the capacity to degrade more
complex substrates (k-strategists).
Since soil is the medium for growth and survival of
plant as well as the microbes it is bound to affect the
bacterial populations through direct effects on the
microbial growth and/or indirectly by inuencing the
host plant. Various physical and chemical character-
istics of soil inuence parameters such as nutrient
availability, suitable niches for the bacteria, morpho-
logical and physiological aspects of the bacteria and
many other critical features. Thus, soil pH, salinity,
texture, organic matter content, concentration of
nutrient elements, seasonal effects as well as the
management practices like irrigation, tillage, crop-
ping, fertilizer and pesticide application, residue
incorporation, etc. have been reported as the major
factors affecting the bacterial composition of the
rhizosphere (Grayston et al. 1998; MacDonald et al.
2004; Fang et al. 2005; Ibekwe et al. 2010).
Predominant bacterial strains in the rhizosphere are
those which are the most efcient root colonizers as
satisfactory establishment of the bacteria at suitable
sites inside the rhizosphere is a prerequisite for
maintenance of predominant populations. Further,
the metabolic versatility or the functional diversity
of established bacterial populations in the rhizosphere
is governed by the variety of genetic factors carried by
them and the interactions with other prokaryotic and
eukaryotic organisms including the plant itself (Bar-
riuso et al. 2008). Such interactions in the rhizosphere
are different from those in bulk soil and those that are
not affected by living roots (Garland 1996). Hence, it
may be said that bacterial diversity in the rhizosphere
is derived by many interrelated biotic and abiotic
factors.
3.2 Plantmicrobe interactions in the rhizosphere
Rhizosphere is the major soil ecological environment
wherein different kinds of plantmicrobe interactions
can be observed. As a result of microbial colonization
in and around the growing plant roots various kinds of
relationships such as associative, symbiotic, neutral-
istic or parasitic, may develop, depending upon factors
like nutrient status of the soil, overall soil environ-
ment, plant defense mechanism and certainly the
proliferating microorganism itself (Parmar and Duf-
resne 2011). Plantmicrobe communication is medi-
ated by the root exudates through chemotactic
response of the microorganism towards exudates like
sugars, organic acids and amino acids leading to root
colonization (Bais et al. 2004). Plant roots are also
known to produce some kind of electric signals which
direct the movement of microorganismparticularly for
the zoospores of oomycetes (Gow et al. 1999).
Interactions between plants, pathogenic microorgan-
isms and antagonistic rhizobacteria and fungi are
another key feature observed here (Trevors and van
Elas 1997). Rhizosphere microora provides an
important link between the plant and soil acting as
an intermediate between the two. It tend to affect the
plant in a variety of ways ranging from the affect on
68 Rev Environ Sci Biotechnol (2014) 13:6377
1 3
plant growth and nutrition, its susceptibility to disease
and development of phytopathogens (Glick 1995) to
resistance to heavy metals (Shetty et al. 1994;
Weishuang et al. 2009) and the degradation of
xenobiotics (Greenberg et al. 2008).
Rhizobacteria are a subset of total rhizosphere
bacteria which have the capacity, upon re-introduc-
tion to seeds or vegetative plant parts (such as
potato seed pieces), to colonize the developing root
system in the presence of competing soil microora
(Kloepper et al. 1999). Those which affect the plant
in negative manner are termed as deleterious
rhizobacteria while those inuencing it in a positive
way are called as plant growth promoting rhizobac-
teria (PGPR).
The most important pathogen groups in the soil that
adversely affect plant growth and health are fungi and
nematodes while bacterial and viral pathogens are
lesser known to cause root infections as they cannot
infect the intact root tissue and require an opening to
penetrate into the plant (Lynch 1990). Moreover, non-
spore forming bacteria are unable to survive in the soil
for longer periods. Deleterious rhizosphere bacteria
may produce various kinds of phytotoxins and also
present competition for nutrients and inhibition of
mycorrhizal fungi (Morgan et al. 2005).
Plant friendly or the benecial microorganisms
include nitrogen-xing bacteria, endo and ectomycor-
rhizal fungi and plant growth-promoting rhizobacteria
and fungi. In the subsequent sections plant growth-
promoting rhizobacteria are discussed in detail.
4 Plant growth promoting rhizobacteria (PGPR)
About 25 % of the rhizosphere bacteria are PGPR
(Antoun and Prevost 2005). The term PGPR was
coined by Joe Kloepper in late 1970s and was dened
by Kloepper and Schroth (1978) as the soil bacteria
that colonize the roots of plants by following inocu-
lation on to seed and that enhance plant growth. On
the basis of their location in rhizosphere PGPR can be
classied as extracellular PGPR (ePGPR) found in the
rhizosphere, on the rhizoplane or in the spaces
between the cells of the root cortex and intracellular
PGPR (iPGPR) which exist inside the root cells,
generally in specialized nodular structures (Gray and
Smith 2005). The number of bacterial species identi-
ed as PGPRhas increased substantially in the last few
decades as a result of the numerous studies on a vast
range of plants in hunt of sustainable agriculture tools
as well as the advancements in molecular genetics
techniques leading to up gradation of bacterial taxon-
omy. The range of bacteria being reported to enhance
the plant growth and control plant pathogens includes
various species of Pseudomonas, Bacillus, Azospiril-
lum, Azotobacter, Streptomyces, Klebsiella, Entero-
bacter, Alcaligenes, Arthrobacter, Flavobacterium,
Burkholderia, Bradyrhizobium, Mesorhizobium, Rho-
dococcus and Serratia, etc. (Berg 2000; Berg et al.
2002; Sobral et al. 2004; Sessitsch et al. 2005; Chen
et al. 2006; Fischer et al. 2006; Fernandez et al. 2007;
Naik et al. 2008; Ahmad et al. 2008; Soltani et al.
2010). However, the predominant bacterial species in
the PGPRcommunity which have emerged as the most
widely studied and potent candidates for improvement
of plant growth and health are Pseudomonas and
Bacillus. The range of their favorable activities
include phosphate solubilization (Chen et al. 2006;
Velineni and Brahmaprakash 2011), production and
release of phytohormones like indole acetic acid and
gibberellins (Jeon et al. 2003; Bottini et al. 2004;
Jangu and Sindhu 2011) and biocontrol of soil borne
phytopathogens (Couillerot et al. 2009; Cawoy et al.
2011). In the last fewdecades a large body of literature
reporting the activities of these two bacterial species,
pertaining to plant growth promotion and biocontrol of
phytopathogens has been generated that reects the
potential of these PGPR strains to be developed as
alternative/supplementary agrochemicals.
4.1 Mechanisms of plant growth promotion
by PGPR
PGPR promote plant growth and health by a variety of
direct and indirect mechanisms in a wide range of
plants. Direct plant growth promotion is based on
either stipulation of the plants with favorable bacterial
compounds or improving the nutrient uptake by the
plant from the soil (Glick 1995). It is accomplished
through processes like atmospheric nitrogen xation,
siderophore production and release, phosphate solu-
bilization, synthesis and release of phytohormones,
etc. The indirect promotion of plant growth is
primarily based on the reduction or prevention of the
deleterious affects of phytopathogens, usually the
fungi and the nematodes, thereby controlling the
diseases. Pathogen suppression may be achieved
Rev Environ Sci Biotechnol (2014) 13:6377 69
1 3
through a variety of mechanisms like production and
release of cyanide, antibiotics or extracellular lytic
enzymes including chitinases; proteases; b-1, 3 glu-
canases; cellulases and laminarinases, competition for
nutrients and niches in the rhizosphere, parasitism and
predation.
In addition to this, PGPR enhance the tolerance
capacity of the plant to a variety of environmental
stresses through production of phytohormones and
ACC deaminase. Depending upon the likely mecha-
nisms underlying their favorable effects and contri-
butions towards plant growth promotion, PGPR
generally fall into at least one of the following
categories (Viveros et al. 2010):
I. Bioprotectants: It includes PGPR strains that
suppress the pathogens and hence control plant
diseases. An important mechanism adopted for the
same involves enhancing plant resistance to fungal
(Cameron et al. 1994), bacterial (Wei et al. 1996;
Hu et al. 2009) and viral diseases (Maurhofer et al.
1998; Murphy and Zehnder 2000), insects (Zehn-
der et al. 1997) and nematodes (Cadena et al.
2008). Production and release of metabolites
which reduce the population or activities of
pathogens or deleterious rhizosphere microora
is another chiey found mode of action in many
PGPR strains (Kloepper 1994). For example, the
production of siderophores which bind ferric ions
making them unavailable or scarcely available to
the native pathogenic microora (Haas and Def-
ago 2005), lytic enzymes, diffusible antibiotics,
volatile organic compounds (VOCs), toxins and
biosurfactants (Berg 2009), etc. Competition of
PGPR strains with the pathogens for the limited
nutrients and suitable sites in the rhizosphere is
also a common approach to check the growth of
undesirable organisms in the rhizosphere (Elad
and Chet 1987).
II. Biofertilizers: These are the PGPR strains which
improve the nutrient uptake of the plant thus
resulting in enhanced seed germination and
seedling emergence thereby improving the crop
yield (Glick 1995; Berg 2009). Various mecha-
nisms involved for the same are N
2
xation (Tilak
et al. 2005), improving the phosphorous avail-
ability to plants by solubilization of inorganic
phosphate and mineralization of organic phos-
phate (Rodriguez and Fraga 1999) and release of
organic acids, which help to make the available
forms of nutrients like zinc and others.
III. Biostimulants: PGPR involved in phytohormone
production, i.e. production of secondary metab-
olites such as auxins, indole acetic acid (IAA),
cytokinins, riboavin and vitamins (Frankenber-
ger and Arshad 1995; Costacurta and Vander-
leyden 1995) are termed as biostimulants.
Another benecial trait that has been recognized for
PGPR is their capability to counteract the phytotox-
icity of chemical pesticides. For example, P. aerugin-
osa PS1 reduced the toxic effects of herbicides like
quizalafop-p-ethyl and clodinafop in legumes (Ahe-
mad and Khan 2010a) and produced plant growth
promoting substances even in the presence of the
insecticides pronil and pyriproxyfen in green gram
(Ahemad and Khan 2011). Similarly, another strain E.
asburiae PS2 showed plant growth promoting activ-
ities like phosphate solubilization, production and
release of siderophores, indole acetic acid, exopoly-
saccharides, hydrogen cyanide and ammonia in the
presence of herbicides such as quizalafop-p-ethyl,
clodinafop, metribuzin and glyphosate (Ahemad and
Khan 2010b), a strain of Rhizobium, i.e. MRL3
exhibited plant growth promotion in the soil treated
with insecticides pronil and pyriproxyfen in lentil
plants (Ahemad and Khan 2010c). Thus, it can be said
that PGPR strains may be used to improve plant
growth even in stressed soils that have been treated for
long times with various kinds of chemical agents.
This suggests that plant friendly rhizosphere micro-
ora may be grouped as either plant growth promoting
microorganisms (PGPM) which directly enhance the
plant growth or as biological control agents (BCA)
that effect the plant health by suppressing plant
pathogens thus indirectly affecting its growth (Avis
et al. 2008). Various direct and indirect, plant growth
promoting properties of the PGPR are summarized in
Table 2.
Hence, it may be concluded that plant nutrition and
health is favorably inuenced by PGPR through an
extensive range of direct and indirect mechanisms.
5 Rhizosphere competence
In order to exhibit their plant growth-promotion and
protection capabilities, the foremost requirement for
70 Rev Environ Sci Biotechnol (2014) 13:6377
1 3
the PGPR is to colonize the suitable sites in the
rhizosphere. The effectiveness of PGPR mediated
processes is strongly inuenced by factors such as the
competence and persistence of the particular strain in
the rhizosphere, its root colonizing capacity, synthesis
and release of various metabolites, plant species and
plant genotypes within a species and the competing
microora in the rhizosphere (Nowak 1998). If the
conditions in the root zone are not favorable for PGPR
establishment the synthesis of biologically active
substances, inuencing plant health and growth may
either stop or get signicantly reduced thus resulting in
Table 2 Plant growth promoting mechanisms of PGPR
Plant growth promoting trait Benecial effect for plant PGPR involved References
Biological nitrogen xation:
symbiotic, associative or free
living nitrogen xers
Enhancement in the nitrogen
content of soil and hence
improvement in plant growth
and yield
Enterobacter, Erwinia,
Flavobacterium, Frankia,
Klebsiella, Pseudomonas,
Rhizobium, Azospirillum,
Alcaligenes, Azotobacter,
Acetobacter, Bacillus,
Burkholderia
Gillis et al. (1989), Biswas
et al. (2000), Gholami et al.
(2009), Akhtar and Siddiqui
(2009)
Phytohormone production Favorable inuence on
physiological plant
processes leading to plant
growth promotion
Rhizobium, Pseudomonas,
Azotobacter, Bacillus,
Enterobacter, Alcaligenes
Bradyrhizobium,
Xanthomonas
Frankenberger and Arshad
(1995), Costacurta and
Vanderleyden (1995),
Ahmad et al. (2008)
Siderophore production Enhancement in solubilization
of ferric ions and hence
improvement in iron
availability for plants. Also
contribute towards
phytopathogen inhibition
Pseudomonas, Bacillus,
Serratia, Rhodococcus,
Acinetobacter
Chaiharn et al. (2009), Koo
and Cho (2009),
Rokhbakhsh-Zamin et al.
(2011), Sahu and Sindhu
(2011)
Phosphate solubilization Conversion of insoluble forms
of phosphorus to plant
accessible form, making it
available to the plants.
Bacillus, Pseudomonas,
Rhizobium, Serratia,
Kushneria, Rhodococcus,
Arthrobacter
Igual et al. (2001), Chen et al.
(2006), Zhu et al. (2011)
Antagonistic behavior:
antibiotic production (like
phenazines, 2,4-
diacetylphloroglucinol,
pyoluteorin, pyrrolnitrin,
lipopeptides, etc.)
Inhibition of soil borne
phytopathogens thus leading
to suppression of the
diseases.
Pseudomonas, Bacillus,
Serratia, Streptomyces
Thomashow and Weller
(1988), Hwang et al. (1994),
Maurhofer et al. (1994),
Kamensky et al. (2003),
Kim et al. (2004),
Jayaprakashvel et al. (2010)
Antagonistic behavior:
extracellular lytic enzymes
like chitinases, b-1, 3
glucanases, proteases,
cellulases and laminarinase
Cell lysis of soil borne fungal
pathogens of plants.
Pseudomonas, Bacillus,
Serratia
Fridlender et al. (1993),
Huang et al. (2005),
Nandakumar et al. (2007)
ACC deaminase Hydrolysis of ACC, reduction
in ethylene production and
plant growth promotion.
Pseudomonas, Bacillus Belimov et al. (2001)
Salicylic acid and other elicitors Induced systemic resistance
(ISR) in plants against
pathogens
Pseudomonas, Bacillus,
Serratia
de Meyer and Hofte (1997),
Bargabus-Larson and
Jacobsen (2007)
Production of organic acids Solubilization of mineral
nutrients for plant uptake.
Pseudomonas, Bacillus,
Rhizobium
Belimov et al. (1995), Noel
et al. (1996)
Metal resistance Effective metal sequestering Pseudomonas Rajkumar and Freitas (2008)
A variety of direct and indirect mechanisms are involved in benecial impacts of different strains of PGPR that range from enhanced
nutrient availability for the plant to suppression of pathogens
PGPR Plant growth promoting rhizobacteria, ACC 1-aminocyclopropane-1-carboxylic acid
Rev Environ Sci Biotechnol (2014) 13:6377 71
1 3
the failure of the introduced PGPR strain to promote
plant growth (Chanway and Holl 1992).
Owing to their similar requirements for water,
nutrients and space a stiff competition is generally
observed between the introduced PGPR strain and the
native inhabitants in the rhizosphere. An introduced
bacteriumwill be dened as an effective root colonizer
if it is able to propagate and survive in the rhizosphere
for several weeks and thus outcompetes the indigenous
microora (Weller 1988). If the introduced strain is
equipped with certain discriminating feature(s) over
the indigenous microora that confers it the capacity
to compete for restricted space and nutrients, the strain
succeeds in colonizing the rhizosphere. Characteris-
tics that offer selective advantage to the introduced
strain in the rhizosphere include the agellar motility
(de Weger et al. 1987), ability to utilize root exudates
and adherence to root surfaces mediated by aggluti-
nation (Slusarenko et al. 1983) or with the help of
surface structures like pili (Vesper 1987); mbriae
(Vesper and Bauer 1986); exopolysaccharides like
cellulose brils (Smit et al. 1986) and O-antigens
chains of liposachharides (de Weger et al. 1989), etc.
Possession of these feature(s) thus improves the
probability of successful colonization by manifolds.
Ability of the introduced strain to generate phenotyp-
ically diverse population with the help of site-specic
recombinases (Granero et al. 2005) and to produce
antibiotics (Mazzola et al. 1992) also inuence the
ecological competence. Thus, it may be said that it is
only after the successful establishment of the PGPR
inoculants in the rhizosphere that they may exercise
their effect on the plant.
6 Conclusion
Rhizosphere is a unique ecological zone of soil that is
heavily loaded with nutrients obtained from plant
roots via rhizodeposition. It has a rich pool of potential
bacterial sources equipped with versatile capabilities
to favorably inuence the host plant. Bacteria are the
most abundant organisms that reside in rhizosphere
and a special class of bacteria called as plant growth
promoting rhizobacteria inuence the plant growth by
a variety of direct and indirect mechanisms in a wide
range of crops. They must be therefore; exploited to
develop eco-friendly and safe replacement for chem-
ical based fertilizers and pesticides. However, the
success in developing PGPR mediated tools is greatly
dependent on the development of efcient and sensi-
tive molecular genetics techniques like microarrays
and effective culturing methodologies to provide a
better insight of the structural and functional diversity
of the rhizosphere. Though PGPR have environmental
advantages and are favorably supported by legislative
guidelines as well, their commercial success is highly
dependent on economic factors. Design of economi-
cally feasible large scale production methodologies is
thus another critical requirement. So, deep rooted
research in this area is highly needed. Further Pseu-
domonas and Bacillus have been the most vastly
studied PGPR genera, so far, due to the combined
effects of their functional properties and their pre-
dominance in the rhizosphere. However, a diverse
range of microbial groups must be explored in order to
enhance the working options available so that the use
of chemical based agronomic products can be checked
to a signicant level.
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