rizosfera 2014

REVIEW PAPER

Rhizosphere: its structure, bacterial diversityand significance

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. Owing to 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 justified move in the direction to

achieve this target. One of the most lucrative options is

to look into the rhizosphere. Rhizosphere may be

defined as the narrow zone of soil that surrounds and

get influenced 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 beneficial 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 � Plant–microbe

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 flux (Barriuso

P. Prashar � N. Kapoor

School of Sciences, IGNOU, New Delhi, India

e-mail: [email protected]

P. Prashar (&) � S. Sachdeva

Department of Biotechnology, FET, MRIU, Sector 43,

Aravalli Hills, Faridabad, India

e-mail: [email protected]; [email protected]

S. Sachdeva

e-mail: [email protected]

123

Rev Environ Sci Biotechnol (2014) 13:63–77

DOI 10.1007/s11157-013-9317-z

et al. 2008). Generally regarded as a thin zone

(1–2 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 defined 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 influence the host plant in a variety of ways.

These may be broadly classified as beneficial 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 microflora 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 field of influence. It was first defined 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 redefined many times to

include the volume of soil influenced 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 defined 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 influenced 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 microflora in the rhizosphere

under the influence 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) 13:63–77

123

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

reflected 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 microflora have revealed significant

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-

field 1960; Cullimore and Woodbine 1963) such

effects have not been found very significant in natural

soil habitats and higher algal populations are generally

recorded in the bulk soils. Soil protozoa form an

important part of the plant–bacteria–protozoa interac-

tions which are critical in nutrient recycling and

selective set-up of beneficial 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 first defined by Whipps

and Lynch (1985) as ‘‘the material lost from plant

roots, including water-soluble exudates, secretions of

insoluble materials, lysates, dead fine roots and gases

like CO2 and ethylene’’. In simple terms it is defined 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 15–60 % of the

total photosynthetic production of the plant and leads

to the accumulation of substantial carbon and energy

reserves in the rhizosphere for the microflora (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 significant process in terms of

studying the carbon fluxes 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 classified

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 significant in terms of total mass of the root

exudates but have comparatively lesser variety than

the first class (Bais et al. 2006).

Exudates may also be classified 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) 13:63–77 65

123

the gradient (Bais et al. 2006). They constitute about

3–5 % of the total carbon fixed during photosynthesis

(Pinton et al. 2001). The active exudates are secreted

through open membrane pores of the plants and have a

specific function such as lubrication and defense

(Jones et al. 2004; Bais et al. 2006).

Another classification 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 benefits 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 CO2 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 beneficial 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

influence 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 influence 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), amplified 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

significantly towards the total plant-derived carbon in soil as well as developing rich microbial diversity in the rhizosphere


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(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 inflated 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 1010 to 1012 per gram of

soil while it is generally less than 108 in the bulk soil

(Foster 1988).

Bacteria are the most abundant microbes in the

rhizosphere and hence they are bound to influence the

plant in a significant 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 efficiency 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 CO2

Toxin production Salinity Root architecture Light intensity

Quorum sensing Water availability Nutrition deficiency 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


123

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 microflora 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 influence 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 influenced 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 significant 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 chiefly 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 influencing the

host plant. Various physical and chemical character-

istics of soil influence 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 efficient 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 Plant–microbe interactions in the rhizosphere

Rhizosphere is the major soil ecological environment

wherein different kinds of plant–microbe 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). Plant–microbe 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 microorganism particularly 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 microflora 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


123

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 microflora

(Kloepper et al. 1999). Those which affect the plant

in negative manner are termed as deleterious

rhizobacteria while those influencing 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 beneficial microorganisms

include nitrogen-fixing 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 2–5 % of the rhizosphere bacteria are PGPR

(Antoun and Prevost 2005). The term PGPR was

coined by Joe Kloepper in late 1970s and was defined

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

classified 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-

fied as PGPR has 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 PGPR community 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 few decades 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 reflects 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 fixation,

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


123

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 microflora

is another chiefly 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 microflora (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 N2 fixation (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, riboflavin and vitamins (Frankenber-

ger and Arshad 1995; Costacurta and Vander-

leyden 1995) are termed as biostimulants.

Another beneficial 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 fipronil 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 fipronil 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-

flora 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 influenced 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


123

the PGPR is to colonize the suitable sites in the

rhizosphere. The effectiveness of PGPR mediated

processes is strongly influenced 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

microflora in the rhizosphere (Nowak 1998). If the

conditions in the root zone are not favorable for PGPR

establishment the synthesis of biologically active

substances, influencing plant health and growth may

either stop or get significantly reduced thus resulting in

Table 2 Plant growth promoting mechanisms of PGPR

Plant growth promoting trait Beneficial effect for plant PGPR involved References

Biological nitrogen fixation:

symbiotic, associative or free

living nitrogen fixers

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 influence 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.


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.


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


Serratia

de Meyer and Hofte (1997),

Bargabus-Larson and

Jacobsen (2007)

Production of organic acids Solubilization of mineral

nutrients for plant uptake.


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 beneficial 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


123

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

bacterium will be defined as an effective root colonizer

if it is able to propagate and survive in the rhizosphere

for several weeks and thus outcompetes the indigenous

microflora (Weller 1988). If the introduced strain is

equipped with certain discriminating feature(s) over

the indigenous microflora 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 flagellar 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); fimbriae

(Vesper and Bauer 1986); exopolysaccharides like

cellulose fibrils (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-specific

recombinases (Granero et al. 2005) and to produce

antibiotics (Mazzola et al. 1992) also influence 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 influence 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 influence 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 efficient 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 significant level.

References

Ahemad M, Khan MS (2010a) Phosphate-solubilizing and

plant-growth-promoting Pseudomonas aeruginosa PS1

improves green gram performance in quizalafop-p-ethyl

and clodinafop amended soil. Arch Environ Contam Tox-

icol 58:361–372

Ahemad M, Khan MS (2010b) Influence of selective herbicides

on plant growth promoting traits of phosphate solubilizing

Enterobacter asburiae strain PS2. Res J Microbiol

5:849–857

Ahemad M, Khan MS (2010c) Insecticide-tolerant and plant-

growth-promoting Rhizobium improves the growth of lentil

(Lens esculentus) in insecticide-stressed soils. Pest Manag

Sci 67:423–429

Ahemad M, Khan MS (2011) Pseudomonas aeruginosa strain

PS1 enhances growth parameters of green gram [Vigna

radiata (L.) Wilczek] in insecticide-stressed soils. J Pest Sci

84:123–131

Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living

rhizospheric bacteria for their multiple plant growth pro-

moting activities. Microbiol Res 168:173–181

Akhtar MS, Siddiqui ZA (2009) Use of plant growth-promoting

rhizobacteria for the biocontrol of root-rot disease complex

of chickpea. Australas Plant Pathol 38:44–50

Aneja KR (2003) Experiments in microbiology, plant pathology

and biotechnology. Age International (P) Limited Pub-

lishers, New Delhi

Antoun H, Prevost D (2005) Ecology of plant growth promoting

rhizobacteria. In: Siddiqui ZA (ed) PGPR: biocontrol and

biofertilization. Springer, Netherlands, pp 1–38

Atlas RM, Bartha R (1993) Microbial ecology: fundamentals

and applications. Benjamin/Cummings, Redwood City


123

Avis TJ, Gravel V, Antoun H, Tweddell RJ (2008) Multifaceted

beneficial effects of rhizosphere microorganisms on plant

health and productivity. Soil Biol Biochem 40:1733–1740

Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004)

How plants communicate using the underground infor-

mation superhighway. Trends Plant Sci 9:26–32

Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The

role of root exudates in rhizosphere interactions with plants

and other organisms. Annu Rev Plant Biol 57:233–266

Barea JM (2000) Rhizosphere and mycorrhiza of field crops. In:

Balazs E, Galante E, Lynch JM, Schepers JS, Toutant JP,

Werner D, Werry PJ (eds) Biological resource manage-

ment: connecting science and policy. Springer, New York,

pp 110–125

Bargabus-Larson RL, Jacobsen BJ (2007) Biocontrol elicited

systemic resistance in sugar beet is salicylic acid inde-

pendent and NPR1 dependent. J Sugar Beet Res 44:17–33

Barriuso J, Solano BR, Lucas JA, Lobo AP, Villaraco AG,

Manero FJG (2008) Ecology, genetic diversity and

screening strategies of plant growth promoting rhizobac-

teria (PGPR). In: Ahmad I, Pichtel J, Hayat S (eds) Plant–

bacteria interactions: strategies and techniques to promote

plant growth. Wiley-VCH Verlag GmbH and Co. KGaA,

Weinheim, pp 1–17

Belimov AA, Kojemiakov AP, Chuvarliyeva CV (1995) Inter-

action between barley and mixed cultures of nitrogen fixing

and phosphate-solubilizing bacteria. Plant Soil 173:29–37

Belimov AA, Safronova VI, Sergeyeva TA, Egorova TN, Mat-

veyeva VA, Tsyganov VE, Borisov AY, Tikhonovich IA,

Kluge C, Preisfeld A, Dietz K, Stepanok VV (2001) Charac-

terization of plant growth promoting rhizobacteria isolated

from polluted soils and containing 1-aminocyclopropane-1-

carboxylate deaminase. Can J Microbiol 47:642–652

Berg G (2000) Diversity of antifungal and plant-associated

Serratia plymuthica strains. J Appl Microbiol 88:952–960

Berg G (2009) Plant–microbe interactions promoting plant

growth and health: perspectives for controlled use of

microorganisms in agriculture. Appl Microbiol Biotechnol

84:11–18

Berg G, Roskot N, Steidle A, Eberl L, Zock A, Smalla K (2002)

Plant-dependent genotypic and phenotypic diversity of

antagonistic rhizobacteria isolated from different Verticil-

lium host plants. Appl Environ Microbiol 68:3328–3338

Berg G, Zachow C, Lottmann J, Gotz M, Costa R, Smalla K

(2005) Impact of plant species and site on rhizosphere-

associated fungi antagonistic to Verticillium dahliae Kleb.

Appl Environ Microbiol 71:4203–4213

Berg G, Opelt K, Zachow C, Lottmann J, Gotz M, Costa R,

Smalla K (2006) The rhizosphere effect on bacteria

antagonistic towards the pathogenic fungus Verticillium

differs depending on plant species and site. FEMS Micro-

biol Ecol 56:250–261

Biswas JC, Ladha JK, Dazzo FB (2000) Rhizobia inoculation

improves nutrient uptake and growth of lowland rice. Soil

Sci Soc Am J 64:1644–1650

Bolton HJ, Fredrickson JK, Elliott LF (1993) Microbial ecology

of the rhizosphere. In: Metting FBJ (ed) Soil microbial

ecology. Marcel Dekker, New York, pp 27–63

Bottini R, Cassan F, Piccoli P (2004) Gibberellin production by

bacteria and its involvement in plant growth promotion and

yield increase. Appl Microbiol Biotechnol 65:497–503

Bowen G, Rovira A (1999) The rhizosphere and its management

to improve plant growth. Adv Agron 66:1–102

Brimecombe MJ, de Leij FA, Lynch JM (2001) The effect of

root exudates on rhizosphere microbial populations. In:

Pinto R, Varanini Z, Nannipierei P (eds) The rhizosphere.

Marcel Dekker, New York, pp 95–141

Brophy LS, Heichel GH (1989) Nitrogen release from roots of

alfalfa and soybean grown in sand culture. Plant Soil

116:77–84

Butler JL, Williams MA, Bottomley PJ, Myrold DD (2003)

Microbial community dynamics associated with rhizo-

sphere carbon flow. Appl Environ Microbiol 69:

6793–6800

Buyer JS, Roberts DP, Russek-Cohen E (2002) Soil and plant

effects on microbial community structure. Can J Microbiol

48:955–964

Cadena MB, Burelle NK, Lawrence KS, van Santen E, Kloepper

JW (2008) Suppressiveness of root-knot nematodes med-

iated by rhizobacteria. Biol Control 47:55–59

Cameron RK, Dixon R, Lamb C (1994) Biologically induced

systemic acquired resistance in Arabidopsis thaliana. Plant

J 5:715–725

Cawoy H, Bettiol W, Fickers P, Ongena M (2011) Bacillus

based biological control of plant diseases. In: Stoytcheva M

(ed) Pesticides in the modern world—pesticides use and

management. InTech, Rijeka, pp 273–302

Chaiharn M, Chunhaleuchanon S, Lumyong S (2009) Screening

siderophore producing bacteria as potential biological

control agent for fungal rice pathogens in Thailand. World

J Microbiol Biotechnol 25:1919–1928

Chanway CP, Holl FB (1992) Influence of soil biota on Douglas

fir (Pseudotsuga menziesii) seedling growth: the role of

rhizosphere bacteria. Can J Bot 70:1025–1031

Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC

(2006) Phosphate solubilizing bacteria from subtropical

soil and their tricalcium phosphate solubilizing abilities.

Appl Soil Ecol 34:33–41

Cheng W, Gershenson A (2007) Carbon fluxes in the rhizo-

sphere. In: Cardon ZG, Whitbeck JL (eds) The rhizo-

sphere—an ecological perspective. Academic Press, San

Diego, CA, pp 31–56

Clark FE (1949) Soil microorganisms and plant roots. Adv

Agron 1:241–288

Costacurta A, Vanderleyden J (1995) Synthesis of phytohor-

mones by plant-associated bacteria. Critical Rev Microbiol21:1–18

Couillerot O, Prigent-Combaret C, Caballero-Mellado J, Mo-

enne-Loccoz Y (2009) Pseudomonas fluorescens and clo-

sely-related fluorescent pseudomonads as biocontrol

agents of soil-borne phytopathogens. Lett Appl Microbiol

48:505–512

Cullimore DR, Woodbine M (1963) Rhizosphere effect of the

pea root on soil algae. Nature 198:304–305

Curl EA, Truelove B (1986) The rhizosphere. Springer, Berlin

de Meyer G, Hofte M (1997) Salicylic acid produced by the

rhizobacterium Pseudomonas aeruginosa 7NSK2 induces

resistance to leaf infection by Botrytis cinerea on bean.

Phytopathology 87:588–593

de Weger LA, van der Vlugt CIM, Wijfjes AHM, Bakker

PAHM, Schippers B, Lugtenberg BJJ (1987) Flagella of a

plant-growth-stimulating Pseudomonas fluorescens strain


123

are required for colonization of potato roots. J Bacteriol

169:2769–2773

de Weger LA, Bakker PAHM, Schippers B, van Loosdrecht

MCM, Lugtenberg BJJ (1989) Pseudomonas spp. with

mutational changes in the O-antigenic side chain of their

lipopolysaccharide are affected in their ability to colonize

potato roots. In: Lugtenberg BJJ (ed) Signal molecules in

plants and plant–microbe interactions. Springer, Berlin,

pp 197–202

Elad Y, Chet I (1987) Possible role of competition for nutrients

in biocontrol of Pythium damping off by bacteria. Phyto-

pathology 77:90–195

Fang M, Kremer RJ, Motavalli PP, Davis G (2005) Bacterial

diversity of rhizospheres of non-transgenic and transgenic

corn. Appl Environ Microbiol 71:4132–4136

Farrar J, Hawes M, Jones D et al (2003) How roots control the

flux of carbon to the rhizosphere. Ecology 84:827–837

Fernandez LA, Zalba P, Gomez MA, Sagardoy MA (2007)

Phosphate-solubilization activity of bacterial strains in soil

and their effect on soybean growth under green house

conditions. Biol Fertil Soils 43:803–805

Fischer SE, Fischer SI, Magris S, Mori GB (2006) Isolation and

characterization of bacteria from the rhizosphere of wheat.

World J Microbiol Biotechnol 23:895–903

Foster RC (1988) Microenvironments of soil microorganisms.

Biol Fertil Soils 6:189–203

Frankenberger WTJ, Arshad M (1995) Phytohormones in soil:

microbial production and function. Dekker, New York

Fridlender M, Inbar J, Chet I (1993) Biological control of soil-

borne plant pathogens by a b-1, 3 glucanase-producing

Pseudomonas cepacia. Soil Biol Biochem 25:1211–1221

Garbeva P, van Veen JA, van Elsas JD (2004) Microbial

diversity in soil: selection of microbial populations by plant

and soil type and implications for disease suppressiveness.

Annu Rev Phytopathol 42:243–270

Garland JL (1996) Patterns of potential C source utilization by

rhizosphere communities. Soil Biol Biochem 36:489–498

Gholami A, Shahsavani S, Nezarat S (2009) The effect of plant

growth promoting rhizobacteria (PGPR) on germination,

seedling growth and yield of maize. Int J Biol Life Sci

1:35–40

Gillis M, Kersters K, Hoste B, Janssens D, Kroppenstedt RM,

Stephan MP, Teixeira KRS, Dobereiner J, de Ley J (1989)

Acetobacter diazotrophicus sp. nov., a nitrogen fixing

acetic acid bacterium associated with sugarcane. Int J Syst

Bacteriol 39:361–364

Glick BR (1995) The enhancement of plant growth promotion

by free living bacterial. Can J Microbiol 41:109–117

Gobat JM, Aragno M, Matthey W (2004) The living soil: fun-

damentals of soil science and soil biology. Science Pub-

lishers, USA

Gomes NCM, Fagbola O, Costa R, Rumjanek NG, Buchner A,

Mendona-Hagler L, Smalla K (2003) Dynamics of fungal

communities in bulk and maize rhizosphere soil in the

tropics. Appl Environ Microbiol 69:3758–3766

Gow NAR, Campbell TA, Morris BM, Osborne MC, Reid B,

Shepherd SJ, van West P (1999) Signals and interaction

between phytopathogenic zoospores and plant roots. In:

England R, Hobbs G, Bainton N, Roberts DMCL (eds)

Microbial signaling and communication. University Press,

Cambridge, pp 285–305

Granero FM, Capdevila S, Contreras MS, Martyn M, Rivilla R

(2005) Two site-specific recombinases are implicated in

phenotypic variation and competitive rhizosphere coloni-

zation in Pseudomonas fluorescens. Microbiol 151:

975–983

Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR:

commonalities and distinctions in the plant–bacterium

signaling processes. Soil Biol Biochem 37:395–412

Grayston SJ, Vaughan D, Jones D (1996) Rhizosphere carbon

flow in trees, in comparison with annual plants: the

importance of root exudation and its impact on microbial

activity and nutrient availability. Appl Soil Ecol 5:29–56

Grayston SJ, Wang SQ, Campbell CD, Edwards AC (1998)

Selective influence of plant species on microbial diversity

in the rhizosphere. Soil Biol Biochem 30:369–378

Greenberg BM, Huang XD, Gerwing P, Yu XM, Chang P, Wu

SS, Gerhardt K, Nykamp J, Lu X, Glick B (2008) Phyto-

remediation of salt impacted soils: greenhouse and the field

trials of plant growth promoting rhizobacteria (PGPR) to

improve plant growth and salt phytoaccumulation. In:

Proceeding of the 33rd AMOP technical seminar on envi-

ronmental contamination and response. Environment

Canada, Ottawa, ON, pp 627–637

Hadfield W (1960) Rhizosphere effect on soil algae. Nature

185:179–180

Haas D, Defago G (2005) Biological control of soil-borne

pathogens by fluorescent pseudomonads. Nat Rev Micro-

biol 3:307–319

Hiltner L (1904) About new experiences and problems in the

field of Bodenbakteriologie. Works Ger Agric Soc 98:

59–78

Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005)

Rhizosphere geometry and heterogeneity arising from root-

mediated physical and chemical processes. New Phytol

168:293–303

Hu X, Li W, Chen Q, Yang Y (2009) Early signal transduction

linking the synthesis of jasmonic acid in plant. Plant Signal

Behav 4:696–697

Huang CJ, Wang TK, Chung SC, Chen CY (2005) Identification

of an antifungal chitinase from a potential biocontrol agent,

Bacillus cereus 28-9. J Biochem Mol Biol 38:82–88

Hwang BK, Ahn SJ, Moon SS (1994) Production, purification

and antifungal activity of the antibiotic nucleoside, tub-

ercidin, produced by Streptomyces violaceoniger. Can J

Bot 72:480–485Ibekwe AM, Poss JA, Grattan SR, Grieve CM, Suarez D (2010)

Bacterial diversity in cucumber (Cucumis sativus) rhizo-

sphere in response to salinity, soil pH, and boron. Soil Biol

Biochem 42:567–575

Igual JM, Valverde A, Cervantes E, Velazquez E (2001) Phos-

phate-solubilizing bacteria as inoculants for agriculture:

use of updated molecular techniques in their study.

Agronomie 21:561–568

Jaeger JH, Lindow SE, Miller S, Clark E, Firestone MK (1999)

Mapping of sugar and amino acid availability in soil around

roots with bacterial sensors of sucrose and tryptophan.


Jangu OP, Sindhu SS (2011) Differential response of inocula-

tion with indole acetic acid producing Pseudomonas sp. in

green gram (Vigna radiata L.) and black gram (Vigna

mungo L.). Microbiol J 1:159–173


123

Jayaprakashvel M, Muthezhilan R, Srinivasan R, Hussain JA,

Gobalakrishnan S, Bhagat J, Kaarthikeyan C, Muth-

ulakshmi R (2010) Hydrogen cyanide mediated biocontrol

potential of Pseudomonas sp. AMET1055 isolated from

the rhizosphere of coastal sand dune vegetation. Adv

Biotech 9:39–42

Jeffery S, Gardi C, Jones A, Montanarella L, Marmo L, Miko L,

Ritz K, Peres G, Roombke J, van der Putten WH (eds)

(2010) The soil environment. In: European atlas of soil

biodiversity, European Commission, Publications office of

the European Union, Luxembourg, pp 17–48

Jeon JS, Lee SS, Kim HY, Ahn TS, Song HG (2003) Plant

growth promotion in soil by some inoculated microor-

ganisms. J Microbiol 41:271–276

Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal

regulation of rhizodeposition. New Phytol 163:459–480

Joshi P, Bhatt AB (2010) Diversity and function of plant growth

promoting rhizobacteria associated with wheat rhizosphere

in north Himalayan region. Int J Environ Sci 1:1135–1144

Joshi P, Tyagi V, Bhatt AB (2011) Characterization of rhizo-

bacteria diversity isolated from Oryza sativa cultivated at

different altitude in north Himalaya. Adv Appl Sci Res

2:208–216

Kamensky M, Ovadis M, Chet I, Chernin L (2003) Soil-borne

strain IC14 of Serratia plymuthica with multiple mecha-

nisms of antifungal activity provides biocontrol of Botrytis

cinerea and Sclerotinia sclerotiorum diseases. Soil Biol

Biochem 35:323–331

Katznelson H, Lochhead AG, Timonin MI (1948) Soil micro-

organisms and the rhizosphere. Botan Rev 14:543–587

Kim PI, Bai H, Bai D, Chae H, Chung S, Kim Y, Park R, Chi YT

(2004) Purification and characterization of a lipopeptide

produced by Bacillus thuringiensis CMB26. J Appl

Microbiol 97:942–949

Kloepper JW (1994) Plant growth-promoting rhizobacteria

(other systems). In: Okon Y (ed) Azospirillum/plant asso-

ciations. CRC Press, Boca Raton, FL, USA, pp 111–118

Kloepper JW, Schroth MN (1978) Plant growth-promoting

rhizobacteria on radishes. In: Gilbert C (ed) Proceedings

4th international conference on plant pathogenic bacteria,

Tours, France, pp 879–882

Kloepper JW, Zablotowick RM, Tipping EM, Lifshitz R (1991)

Plant growth promotion mediated by bacterial rhizosphere

colonizers. In: Keister DL, Cregan PB (eds) The rhizo-

sphere and plant growth. Kluwer Academic Publishers,

Dordrecht, The Netherlands, pp 315–326

Kloepper JW, Ubana RR, Zehnder GW, Murphy JF, Sikora E,

Fernandez C (1999) Plant root-bacterial interactions in

biological control of soilborne diseases and potential

extension to systemic and foliar diseases. Aust Plant Pathol

28:21–26

Kochian L, Pineros M, Hoekenga O (2005) The physiology,

genetics and molecular biology of plant aluminum resis-

tance and toxicity. Plant Soil 274:175–195

Koo SY, Cho KS (2009) Isolation and characterization of a plant

growth-promoting rhizobacterium, Serratia sp. SY5.

J Microbiol Biotechnol 19:1431–1438

Kreuzer K, Adamczyk J, Iijima M, Wagner M, Scheu S, Bon-

kowski M (2006) Grazing of a common species of soil

protozoa (Acanthamoeba castellanii) affects rhizosphere

bacterial community composition and root architecture of

rice (Oryza sativa L.). Soil Biol Biochem 38:1665–1672

Linderman RG (1988) Mycorrhizal interactions with the rhi-

zosphere microflora: the mycorrhizosphere effect. Phyto-

pathology 78:366–371

Lynch JM (1987) The rhizosphere. Wiley Interscience,

Chichester

Lynch JM (1990) Some consequences of microbial rhizosphere

competence for plant and soil. In: Lynch JM (ed) The

rhizosphere. Wiley Interscience, New York, pp 1–10

Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere.

Plant Soil 129:1–10

MacDonald LM, Paterson E, Dawson LA, McDonald AJS

(2004) Short-term effects of defoliation on the soil

microbial community associated with two contrasting Lo-

lium perenne cultivars. Soil Biol Biochem 36:489–498

Maurhofer M, Keel C, Haas D, Defago G (1994) Pyoluteorin

production by Pseudomonas fluorescens strain CHA0 is

involved in the suppression of Pythium damping-off of

cress but not of cucumber. Eur J Plant Pathol 100:221–232

Maurhofer M, Reimann C, Sacherer SP, Heebs S, Haas D,

Defago G (1998) Salicylic acid biosynthetic genes

expressed in Pseudomonas fluorescens strain P3 improve

the induction of systemic resistance in tobacco against

necrosis virus. Phytopathology 88:678–684

Mazzola M, Cook RJ, Thomashow LS, Weller DM, Pierson LS

(1992) Contribution of phenazine antibiotic biosynthesis to

the ecological competence of fluorescent Pseudomonads in

soil habitats. Appl Environ Microbiol 58:2616–2624

Morgan JAW, Whipps JM (2001) Methodological approaches to

the study of rhizosphere carbon flow and microbial popu-

lation dynamics. In: Pinton A, Varanini Z, Nannipieri P

(eds) The rhizosphere: biochemistry and organic sub-

stances at the soil-plant interface. Marcel Dekker, New

York, pp 373–409

Morgan JAW, Bending GD, White PJ (2005) Biological costs

and benefits to plant–microbe interactions in the rhizo-

sphere. J Exp Bot 56:1729–1739

Murphy JF, Zehnder GW (2000) Plant growth-promoting rhi-

zobacterial mediated protection in tomato against tomato

mottle virus. Plant Dis 84:779–784

Naik PR, Raman G, Narayanan KB, Sakthivel N (2008)

Assessment of genetic and functional diversity of phos-

phate solubilizing fluorescent pseudomonads isolated from

rhizospheric soil. BMC Microbiol 8:230–243

Nandakumar R, Babu S, Raguchander T, Samiyappan R (2007)

Chitinolytic activity of native Pseudomonas fluorescens

strains. J Agri Sci Technol 9:61–68

Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara

G, Renella G, Valori F (2007) Microbial diversity and

microbial activity in the rhizosphere. Ciencia del Suelo

(Argentina) 25:89–97

Nguyen C (2003) Rhizodeposition of organic C by plants:

mechanisms and controls. Agronomie 23:375–396

Nie M, Zhang XD, Wang JQ et al (2009) Rhizosphere effects on

soil bacterial abundance and diversity in the Yellow river

deltaic ecosystem as influenced by petroleum contamina-

tion and soil salinization. Soil Biol Biochem 41:2535–2542

Noel TC, Sheng C, Yost CK, Pharis RP, Hynes MF (1996)

Rhizobium leguminosarum as a plant growth promoting


123

rhizobacterium: direct growth promotion of canola and

lettuce. Can J Microbiol 42:279–293

Nowak J (1998) Benefits of in vitro ‘‘biotization’’ of plant tissue

cultures with microbial inoculants. In vitro Cell Dev Biol

Plant 34:122–130

Parmar N, Dufresne J (2011) Beneficial interactions of plant

growth promoting rhizosphere microorganisms. In: Singh

A et al (eds) Bioaugmentation, biostimulation and bio-

control, soil biology, vol 28. Springer, Berlin, pp 27–42

Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhi-

zodeposition shapes rhizosphere microbial community

structure in organic soil. New Phytol 173:600–610

Phillips DA, Fox TC, King MD, Bhuvaneswar TV, Teuber LR

(2004) Microbial products trigger amino acids exudation

from plant roots. Plant Physiol 136:2887–2894

Phillips DA, Fox TC, Six J (2006) Root exudation (net efflux of

amino acids) may increase rhizodeposition under elevated

CO2. Global Change Biol 12:561–567

Pinton R, Varanini Z, Nannipieri P (2001) The rhizosphere as a

site of biochemical interactions among soil components,

plants and microorganisms. In: Pinton R, Varanini Z,

Nannipieri P (eds) The rhizosphere: biochemistry and

organic substances at the soil-plant interface. Marcel

Dekker, New York, pp 1–17

Rajkumar M, Freitas H (2008) Influence of metal resistant-plant

growth-promoting bacteria on the growth of Ricinus com-

munis in soil contaminated with heavy metals. Chemo-

sphere 71:834–842

Rawat S, Izhari A, Khan A (2011) Bacterial diversity in wheat

rhizosphere and their characterization. Adv Appl Sci Res

2:351–356

Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria

and their role in plant growth promotion. Biotechnol Adv

17:319–339

Rokhbakhsh-Zamin F, Sachdev D, Kazemi-Pour N, Engineer A,

Pardesi KR, Zinjarde S, Dhakephalkar PK, Chopade BA

(2011) Characterization of plant-growth-promoting traits

of Acinetobacter species isolated from rhizosphere of

Pennisetum glaucum. J Microbiol Biotechnol 21:556–566

Rouatt JW, Katznelson H, Payne TMB (1960) Statistical eval-

uation of the rhizosphere effect. Soil Sci Soc Amer Proc

24:271–273

Rougier M, Chaboud A (1989) Biological functions of muci-

lages secreted by roots. Symp Soc Exp Biol 43:449–454

Rovira AD (1956) Plant root excretions in relation to the rhi-

zosphere effect I. Plant Soil 7:178–194

Sahu GK, Sindhu SS (2011) Disease control and plant growth

promotion of green gram by siderophore producing Pseu-

domonas sp. Res J Microbiol 6:735–749

Sessitsch A, Coenye T, Sturz AV, Vandamme P, Barka EA,

Salles JF, van Elsas D, Faure JD, Reiter B, Glick BR,

Pruski GW, Nowak J (2005) Burkholderia phytofirmans sp.

nov., a novel plant-associated bacterium with plant-bene-

ficial properties. Int J Sys Evol Microbiol 55:1187–1192

Shetty KG, Hetrick BAD, Figge DAH, Schwab AP (1994)

Effects of mycorrhizae and other soil microbes on reveg-

etation of heavy metal contaminated mine spoil. Environ

Poll 86:181–188

Slusarenko AJ, Epperlein M, Wood RKS (1983) Agglutination

of plant pathogenic and certain other bacteria by pectic

polysaccharides from various plant species. Phytopathol-

ogy 106:337–343

Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S,

Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil

bacterial communities studied by denaturing gradient gel

electrophoresis: plant-dependent enrichment and seasonal

shifts revealed. Appl Environ Microbiol 67:4742–4751

Smit G, Kijne JW, Lugtenberg BJJ (1986) Correlation between

extracellular fibrils and attachment of Rhizobium legu-

minosarum to pea root hair tips. J Bacteriol 168:821–827

Sobral JK, Araujo WL, Mendes R, Geraldi IO, Kleiner AAP,

Azevedo JL (2004) Isolation and characterization of soy-

bean-associated bacteria and their potential for plant

growth promotion. Environ Microbiol 6:1244–1251

Soltani AA, Khavazi K, Rahmani HA, Omidvari M, Dahaji PA,

Mirhoseyni H (2010) Plant growth promoting character-

istics in some Flavobacterium spp. isolated from soils of

Iran. J Agri Sci 2:106–115

Steer J, Harris JA (2000) Shifts in the microbial community in

rhizosphere and non-rhizosphere soils during the growth of

Agrostis stolonifera. Soil Biol Biochem 32:869–878

Teixeira LCRS, Peixoto RS, Cury JC, Sul WJ, Pellizari VH,

Tiedje J, Rosado AS (2010) Bacterial diversity in rhizo-

sphere soil from Antarctic vascular plants of Admiralty

Bay, maritime Antarctica. ISME J 4:989–1001

Thomashow LS, Weller DM (1988) Role of a phenazine anti-

biotic from Pseudomonas fluorescens in biological control

of Gaeumannomyces graminis var. tritici. J Bacteriol

170:3499–3508

Tilak KVBR, Ranganayaki N, Pal KK, De R, Saxena AK,

Nautiyal CS, Mittal S, Tripathi AK, Johri BN (2005)

Diversity of plant growth and soil health supporting bac-

teria. Curr Sci 89:136–150

Trevors JT, van Elas JD (1997) Microbial interaction in soil. In:

van Elas JD, Trevars JT, Wellington EMH (eds) Modern

soil microbiology. Marcel Dekker, New York, pp 215–243

Uren NC (2001) Types, amounts and possible functions of

compounds released into the rhizosphere by soil-grown

plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The

rhizosphere biochemistry and organic substances at the

soil-plant interface. Marcel Dekker, New York, pp 19–40

van Loon LC (2007) Plant responses to plant growth promoting

bacteria. Eur J Plant Pathol 119:243–254

Velineni S, Brahmaprakash GP (2011) Survival and phosphate

solubilizing ability of Bacillus megaterium in liquid inoc-

ulants under high temperature and desiccation stress. J Agr

Sci Tech 13:795–802

Vesper SJ (1987) Production of pili (fimbriae) by Pseudomonas

fluorescens and correlation with attachment to corn roots.


Vesper SJ, Bauer WD (1986) Role of pili (fimbriae) in attach-

ment of Bradyrhizobium japonicum to soybean roots. Appl

Environ Microbiol 52:134–141

Viveros OM, Jorquera MA, Crowley DE, Gajardo G, Mora ML

(2010) Mechanisms and practical considerations involved

in plant growth promotion by rhizobacteria. J Soil Sci Plant

Nutr 10:293–319

Wacquant JP, Ouknider M, Jacquard P (1989) Evidence for a

periodic excretion of nitrogen by roots of grass-legume

associations. Plant Soil 116:57–68


123

Wei G, Kloepper JW, Tuzun S (1996) Induced systemic resis-

tance to cucumber diseases and increased plant growth by

plant growth promoting rhizobacteria under field condi-

tions. Phytopathology 86:221–224

Weishuang Z, Yingheng FEI, Yi H (2009) Soluble protein and

acid phosphatase exuded by ectomycorrhizal fungi and

seedlings in response to excessive Cu and Cd. J Environ Sci

21:1667–1672

Weller DM (1988) Biological control of soilborne plant patho-

gens in the rhizosphere with bacteria. Annu Rev Phytopa-

thol 26:379–407

Whipps JM (1990) Carbon economy. In: Lynch JM (ed) The

rhizosphere. Wiley and Son, Chichester, UK, pp 59–87

Whipps JM, Lynch JM (1985) Energy losses by the plant in rhi-

zodeposition. Ann Proceedings Phytochem J Eur 26:59–71

Zehnder G, Kloepper JW, Yao C, Wei G (1997) Induction of

systemic resistance in cucumber against cucumber beetles

(Coleoptera: Chrysomelidae) by plant growth-promoting

rhizobacteria. J Econ Entomol 90:391–396

Zhu F, Qu L, Hong X, Sun X (2011) Isolation and character-

ization of a phosphate-solubilizing halophilic bacterium

Kushneria sp. YCWA18 from Daqiao Saltern on the coast

of yellow sea of China. J Evid Based Complement Altern

2011:1–6

Zwart KB, Kuikman PJ, van Veen JA (1994) Rhizosphere

protozoa: their significance in nutrient dynamics. In: Dar-

byshire JF (ed) Soil protozoa. CAB International, Wal-

lingford, pp 93–122


123

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