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181
Plant Growth-Promoting Rhizobacteria:
An Eco-friendly Approach for Sustainable
Agroecosystem
Sohel S. Shaikh , Riyaz Z. Sayyed , and M.S. Reddy
Contents
1 Introduction 182
2 PGPR as Plant Growth Promoters 183
2.1 Biological Nitrogen Fixation 183
2.2 Phosphate Solubilization 185
2.3 Phytohormone Production 185
2.4 Production of ACC Deaminase 186
3 PGPR as Biocontrol Agents (BCAs) 187
3.1 Competition 187
3.2 Induced Resistance 189
3.3 Lysis of Cell Components 190
3.4 Antibiosis 191
4 Merits of PGPR as Bioinoculants 192
5 Commercial Aspects of PGPR 192
6 Conclusions and Future Prospects 193
References 194
Abstract Soil-borne diseases caused by fungal and bacterial pathogens are a major
threat to crop and its yield. These diseases signifi cantly reduce the crop yield and lead to
the production of micronutrient defi cient staple crops. Consumption of these staple
crops or food has been the main cause of many micronutrient defi ciency disorders in
human beings, for instance, iron defi ciency anemia (IDA) caused due to iron defi ciency.
Frequent use of chemical fungicides to control these diseases and use of chemical fertil-
izers to promote plant growth and crop yield have widely affected the agroecosystem
and have various detrimental effects and numerous side effects. Sustainable control of
such plant diseases has been an important challenge to agricultural fi eld. Continuous
search for eco-friendly management of plant disease and promotion of plant growth and
S. S. Shaikh • R. Z. Sayyed (*)
Department of Microbiology , Shri S. I. Patil Arts, G. B. Patel Science and
S.T.S.K.V.S. Commerce College , Shahada. Dist-Nandurbar , Maharashtra 425 409 , India
e-mail: riyaz829@yahoo.co.in; sayyedrz@gmail.com
M. S. Reddy
Department of Entomology and Plant Pathology , 209 Life Sciences Building ,
Auburn University , Auburn , AL 36849 , USA
© Springer International Publishing Switzerland 2016
K.R. Hakeem et al. (eds.), Plant, Soil and Microbes,
DOI 10.1007/978-3-319-27455-3_10
182
crop yield has headed toward the use of plant growth-promoting rhizobacteria (PGPR)
as an effective and eco-friendly means of controlling soil-borne phytopathogens and
simultaneously promoting the plant growth. This chapter focuses on various aspects and
mechanisms of biocontrol of plant pathogens; plant growth promotion, commercializa-
tion of their wide applications, and future prospects of PGPR are also discussed.
Keywords Plant diseases • Biocontrol • Plant growth promotion • Plant growth-
promoting rhizobacteria
1 Introduction
The rhizosphere represents a highly dynamic site for interactions between roots,
pathogenic and benefi cial soil microbes, invertebrates, and other competitors of root
(Yadav et al. 2015 ). Associations among the rhizospheric have been categorized as
positive, neutral, or negative associations. Positive associations, which contribute to
plant growth promotion and biological control of plant diseases, include symbiotic
associations with epiphytic microbes, mycorrhizal fungi, and root colonization by
biocontrol agents (BCAs). Negative associations include competition or antago-
nism (Pliego et al. 2011 ). All those organisms present in rhizosphere play very
important role in plant health promotion or demotion. The rhizobacteria that exert a
benefi cial effect on plant growth are called as plant growth-promoting rhizobacteria
(PGPR), while those which caused detrimental effect are referred to as plant delete-
rious rhizobacteria (PDB) (Kloepper et al. 1980 ). PGPR are also termed plant
health-promoting rhizobacteria (PHPR), yield-increasing bacteria (YIB), or nodule-
promoting rhizobacteria (NPR) (Kloepper et al. 1989 ; Hayat et al. 2010 ).
Since the last few decades, the world had paid attention to the PGPR due to their
promising nature to the environment. The most essential factor for obtaining highest
yield in all agriculture systems has been the use of chemical fertilizers; however,
chemical fertilizers have adversely affected the soil health. Thus, the use of PGPR
as an alternative to chemical fertilizers and pesticides has good potential in increas-
ing the productivity of crops; its supplication will reduce the use of agrochemical
and therefore will help in eco-friendly agricultural practices. Increase in crop yield
through the use of PGPR can be achieved directly or indirectly (Glick 1995 ; Akhtar
and Siddiqui 2010 ). Some PGPR promote the plant growth by direct mechanisms
(Vessey 2003 ; Ahemad and Kibret 2014 ) and act as biofertilizers when pathogen’s
pressure is absent (Lugtenberg and Kamilova 2009 ). Indirect mechanism includes
the inhibition of phytopathogens by several biocontrol mechanisms (Labuschagne
et al. 2010 ). The various ways of functioning of PGPR include synthesis of phyto-
hormones, acceleration of uptake of certain soil nutrients, and prevention of plant
diseases (Hayat et al. 2010 ).
S.S. Shaikh et al.
183
PGPR also improve root development, mineral nutrition, seed germination, and water
uptake (Akhtar and Siddiqui 2010 ; Akhtar et al. 2010 ; Akhtar and Azam 2014 ). Large
number of reviews and chapters have been published recently focusing the various aspects
of PGPR (Akhtar and Siddiqui 2010 ; Heydari and Pessarakli. 2010; Khan et al. 2010 ;
Labuschagne et al. 2010 ; Hayat et al. 2010 , 2012 ; Saharan and Nehra 2011 ; Saraf et al.
2011 ; Simova et al. 2011 ; Beneduzi et al. 2012 ; Glick 2012 ; Sayyed et al. 2012 , 2013 ;
Ashraf et al. 2013 ; Junaid et al. 2013 ; Sharma et al. 2013a , b ; Ahemad and Kibret 2014 ;
Behera et al. 2014 ; Mabood et al. 2014 ; Shaikh and Sayyed 2015 ). However, in-depth
studies on different aspects of plant growth promotion and various mechanisms of biocon-
trol of plant pathogens are needed to be focused. Commercial aspects of their wide appli-
cations and future prospects of PGPR are also discussed in this chapter.
2 PGPR as Plant Growth Promoters
Plant growth promotion is the most important eco-friendly and sustainable aspect of
PGPR. A large number of bacterial species including Alcaligenes , Azospirillum ,
Arthrobacter , Acinetobacter , Bradyrhizobium , Bacillus , Burkholderia , Enterobacter ,
Erwinia , Flavobacterium , Pseudomonas , and Rhizobium associated with the rhizo-
sphere of plant and are able to exert many benefi cial effects on plant growth (Saharan
and Nehra 2011 ; Ahemad and Kibret 2014 ). There are several mechanism by which
PGPR can increase the plant growth; they are also known as direct mechanisms of plant
growth promotion, and these include nitrogen fi xation, production of phytohormones,
lowering of ethylene concentration by producing ACC deaminase, and solubilization of
phosphorous and various other minerals. These mechanisms are mentioned in Fig. 1 .
2.1 Biological Nitrogen Fixation
Nitrogen is a vital macronutrient for growth and yield of crop. Although nitrogen is
abundantly (78 %) available in the atmosphere, it is not available for growing crops
(Gupta et al. 2012 ; Ahemad and Kibret 2014 ). The process of conversion of atmo-
spheric or insoluble N
2 into soluble form by plants is known as biological N
2 fi xa-
tion. It is eco-friendly in nature and best substitute for sustainable agriculture
(Cheng 2008 ). Nitrogen fi xation changes nitrogen to ammonia by nitrogen-fi xing
microorganisms by a set of complex metaloenzyme system called nitrogenase (Kim
and Rees 1994 ; Rees and Howard 2000 ). Enzyme nitrogenase has two components,
i.e., Fe protein and iron, molybdenum cofactor (Dixon and Kahn 2004 ). This
enzyme system is under the control of nif genes (Dixon and Kahn 2004 ; Glick
2012 ). Nitrogen-fi xing organisms are generally categorized as symbiotic and non-
symbiotic nitrogen fi xing. Symbiotic N
2 fi xers belonging to the family that forms
association with leguminous plants include Azorhizobium , Bradyrhizobium ,
Rhizobium , Allorhizobium , Sinorhizobium , Frankia , and Mesorhizobium (Hayat
Plant Growth-Promoting Rhizobacteria: An Eco-friendly Approach for Sustainable…
184
et al. 2012 ; Rashid et al. 2015 ). Nonsymbiotic free-living nitrogen-fi xing bacteria
include Achromobacter , Azotobacter , Azospirillum , Alcaligenes , Acetobacter ,
Arthrobacter , Azomonas , Beijerinckia , Bacillus , Corynebacterium , Clostridium ,
Derxia , Enterobacter , Pseudomonas , Klebsiella , Rhodospirillum , and Xanthobacter
(Vessey 2003 ; Barriuso et al. 2008 ). Symbiotic rhizobia form relationships with
legumes in response to fl avonoid molecules released from the legume host (Hayat
et al. 2012 ; Rashid et al. 2015 ). These plant compounds induce the expression of
nodulation genes (nod genes) in rhizobia, which produce lipo-chitooligosaccharide
signals that trigger mitotic cell division in roots, leading to the formation of nodules
(Matiru and Dakora 2004 ). This nodule is the site for symbiotic nitrogen fi xation
and is formed as a result of a series of interactions between leguminous plants and
rhizobia (Hayat et al. 2012 ; Rashid et al. 2015 ). N 2 fi xation is an ATP-consuming
process that requires a large amount of ATP; it would be advantageous if rhizobial
carbon sources were directed toward oxidative phosphorylation, resulting in the
synthesis of ATP (Gamalero and Glick 2011 ; Glick 2012 ). Oxygen is both inhibi-
tory to enzyme nitrogenase and is a suppressor of nif gene expression, but it is
required for rhizobial respiration. Toxicity of oxygen is taken care by leghemoglo-
bin, which binds free oxygen tightly, resulting in an increase in nitrogenase activity
(Gamalero and Glick 2011 ). The plant produces the globin portion of leghemoglo-
bin; more effi cient strains of Rhizobium spp. may be genetically cloned with bacte-
rial hemoglobin genes (Ramirez et al. 1999 ).
Plant growth
Promotion
Phosphate
Solubilization
PGPR
Nitrogen
Fixation
Phytoharmone
Production
ACC deaminase
Production
Induced
Resistance Antibiosis
Cell wall
Lysis
Competition
Siderophore
Production
Biocontrol
Fig. 1 Showing the schematic view of various mechanisms of plant growth promotion and bio-
control by PGPR
S.S. Shaikh et al.
185
2.2 Phosphate Solubilization
Phosphorus is the second important key element after nitrogen as a mineral nutrient
in terms of quantitative plant requirement (Yadav et al. 2012 ; Sharma et al. 2013a ).
It plays a vital role in most of the major metabolic reactions, viz., photosynthesis,
signal transduction, energy transfer, biosynthesis of macromolecules, and respira-
tion (Khan et al. 2010 ; Yadav et al. 2012 ). Despite this fact, the most of this phos-
phorus is insoluble which present in organic and inorganic form and therefore not
available for plant growth (Glick 2012 ). This problem can be solved by phosphate-
solubilizing bacteria (PSB) which solubilize the insoluble phosphate into a soluble
form and make available to the plant for its growth and development, and hence
PSB are widely used in biofertilizer preparation. PSB plays an important role in the
phosphate nutrition of plants in a more eco-friendly manner. The naturally abundant
PSB solubilize insoluble phosphate and convert it into soluble forms for the crop
plants (Hayat et al. 2012 ). Conversion of inorganic unavailable phosphate into avail-
able forms, viz., H
2 PO 4 − and HPO
4 2− for uptake of plant, is a phenomenon known as
mineral phosphate solubilization (Yadav et al. 2012 ; Behera et al. 2014 ).
The mechanisms of inorganic P solubilization are excretion of H
+ ; production of
organic acid like acetate, lactic acid, oxalic acid, tartaric acid, succinic acid, citric
acid, gluconic acid, ketogluconate, and glycolic; and biosynthesis of acid phospha-
tase (Kim et al. 1997 ; Rodríguez and Fraga 1999 ; Lal 2002 ; Arcand and Schneider
2006 ). This helps in lowering the pH,or in enhancing chelation of the cations bound
to phosphate, by competing with P for adsorption sites on the soil and by forming
soluble complexes with metal ions associated with insoluble P (Ca, Al, Fe), and thus
P is released (Sharma et al. 2013a ). The organic phosphorus is released from the
organic compound by phosphatases (phosphohydrolase) that dephosphorylates the
phospho-ester bonds, phytases, which releases phytic acid and phosphonatases and
C–P lyases, enzymes that perform C–P cleavage of phosphonates (Behera et al.
2014 ). Many researchers have reported phosphate solubilization and plant growth
promotion activity by PGPR (Rodríguez and Fraga 1999 ; Sayyed et al. 2007 ;
Chuang et al. 2007 ; Afzal and Bano 2008 ; Richardson et al. 2009 ; Zaidi et al. 2009 ;
Collavino et al. 2010 ; Bashan et al. 2013 ).
2.3 Phytohormone Production
Phytohormones are also called as plant growth regulators (PGRs) and are important
for plant growth and development. Various PGPR are known to produce phytohor-
mone, namely, auxins, cytokinin, and gibberellins (Pliego et al. 2011 ; Saharan and
Nehra 2011 ; Hayat et al. 2012 ). When plants encounter growth-limiting conditions,
they often attempt to adjust the levels of their endogenous phytohormones in order
to decrease the negative effects (Salamone et al. 2005 ). Phytohormones are organic
in nature which promote the growth of plants, even at very low concentrations, and
Plant Growth-Promoting Rhizobacteria: An Eco-friendly Approach for Sustainable…
186
help in tissue development. Plant growth promotion by phytohormone-producing
PGPR has been reported by many workers (Joo et al. 2005 ; Sayyed et al. 2007 ;
Spaepen et al. 2007 ; Akhtar and Siddiqui 2009 ; Kang et al. 2009 ; Ahemad and
Khan 2012 ; Megala and Elango 2013 ).
Indol acetic acid (IAA) is a most studied phytohormone produced by 80 % rhi-
zospheric bacteria (Patten and Glick 1996 ; Akhtar and Siddiqui 2009 ). It affects cell
division and germination of tuber germination; increases the rate of xylem and root
development; controls processes of vegetative growth; initiates lateral and adventi-
tious root formation; mediates responses to light, gravity, and fl orescence; and
affects photosynthesis, pigment formation, biosynthesis of various metabolites, and
resistance to stressful conditions (Tsavkelova et al. 2006 ; Spaepen et al. 2009 ;
Spaepen and Vanderleyden 2011 ; Ahemad and Kibret 2014 ).
Production of other phytohormones by PGPR has been identifi ed, but not to the
same extent as IAA (Vessey 2003 ). Another group of phytohormones produced by
PGPR includes cytokinin which induces division of plant cells in the presence of
auxin; the root or shoot differentiation depends on the balance between the auxin
and cytokinin (Pliego et al. 2011 ). Gibberellins (gibberellic acid) are mainly
involved in cell division and elongation of cells within the subapical meristems and
hence plays a key role in elongation of internode, seed germination, fl owering in
plants, and pollen tube growth. Like auxins and cytokinins, gibberellic acids also act
in combination with other hormones (Pliego et al. 2011 ).
2.4 Production of ACC Deaminase
Ethylene, a gaseous phytohormone, causes root growth inhibition (Ma et al. 2014 ).
Synthesis of ethylene is known to occur under stress conditions. Biotic stress condi-
tions include infection by pathogens, and abiotic stress conditions include drought.
For this reasons, ethylene is also known as the stress hormone. In the plant, produc-
tion of ethylene involves the conversion of S-adenosyl methionine (SAM) to 1- ami
nocyclopropane- 1-carboxylate (ACC) and 50-deoxy-50 methyl thioadenosine
(MTA) by ACC synthase (Pliego et al. 2011 ). Some PGPR have the capability to
produce ACC deaminase, an enzyme which cleaves ACC, the immediate precursor
in the biosynthetic pathway for ethylene in plants (Glick et al. 1998 ). So such bac-
teria which produce ACC deaminase indirectly inhibit the ethylene biosynthesis,
thereby promoting the plant root growth and also protecting plant from stress, viz.,
salination, fl ooding and organic toxicants, drought, heavy metals, toxic organic
compounds, and pathogens (Belimov et al. 2005 ; Glick 2005 ; Glick et al. 2007a , b ;
Hao et al. 2007 ; Farwell et al. 2007 ; Rodriguez et al. 2008 ; Gamalero et al. 2009 ;
Gamalero and Glick 2011 ). Several bacterial strains have been found to produce
ACC deaminase such as Acinetobacter , Achromobacter , Agrobacterium ,
Alcaligenes , Azospirillum , Bacillus , Burkholderia , Enterobacter , Pseudomonas ,
Ralstonia , Serratia , Rhizobium , etc. (Shaharoona et al.
2007 ; Nadeem et al. 2007 ;
Zahir et al. 2008 , 2009 ; Kang et al. 2010 ). Nodulation of legumes and mycorrhizal
S.S. Shaikh et al.
187
establishment in the host plant induce increases in ethylene content. In this regard,
ACC deaminase-producing bacteria, which lower the ethylene content in the plants,
can increase both nodulation and mycorrhizal colonization in pea and cucumber,
respectively (Ma et al. 2003 ; Gamalero et al. 2008 ). Duan et al. ( 2009 ) reported that
12 % of isolated Rhizobium sp., possessed this enzyme.
3 PGPR as Biocontrol Agents (BCAs)
The term biocontrol refers to the use of microbial antagonist to suppress the disease
or pathogen. Biocontrol of pathogen involves application of benefi cial rhizobia or
their metabolites that neutralizes the negative effects caused by pathogens and thus
promote positive responses by the plant (Junaid et al. 2013 ). Biological control of
plant diseases using antagonist PGPR has emerged in recent years in agriculture as
greater step toward sustainability, and public concern about the use of hazardous
chemical fungicides and plant disease suppression by PGPR is the best possible
alternative of reducing the doses of agrochemicals and its severity in agroecosys-
tem. There are various mechanisms involved in biocontrol of plant diseases caused
by PGPR. These mechanisms are generally classifi ed as competition, lysis of cell
components, antibiosis, and induction of host resistance. These biocontrol mecha-
nisms indirectly promote the plant growth by reducing severity of diseases, hence,
also known as indirect mechanisms of plant growth promotion. Table 1 shows sev-
eral examples of biological control by PGPR.
3.1 Competition
The PGPR-based BCAs compete for nutrients, space, and essential elements with
pathogen, thereby displacing and suppressing the growth of pathogen (Duffy 2001 ;
Sharma et al. 2013b ). Both the BCAs and the pathogens compete with one another
for the nutrients and space to get established and survive in the environment. In this
competition, the one which possesses greater metabolic diversity and competitive
potential will survive.
So far as the competition for nutrients is concerned, BCAs compete for the rare
but essential micronutrients, such as iron and manganese (Junaid et al. 2013 ). The
best example of this mechanism is iron competition. Iron is abundantly present in
the earth, but is not available to the living organisms, due to the aerobic atmosphere
of this planet which has converted the surface iron into insoluble form like oxyhy-
droxide. Maximum of 10
−18 M of free ferric ion is present in solution at biological
pH; however, iron is one of the essential nutrients required by the microorganism for
synthesis of ATP, reduction of ribotide precursors of DNA, formation of heme, and
a variety of functions (Saraf et al.
2011 ). This presents a big challenge for microor-
ganisms which require iron at micromolar concentrations for growth. This very less
Plant Growth-Promoting Rhizobacteria: An Eco-friendly Approach for Sustainable…
188
Table 1 Few examples of biocontrol of plant disease by PGPR
PGPR Pathogen Disease Reference
Fluorescent
pseudomonads Colletotrichum
falcatum Red rot of
sugarcane Viswanathan and
Samiyappan (
2002 )
Serratia sp., fl uorescent
pseudomonad Ralstonia
solanacearum Wilt of tomato Guo et al. (
2004 )
P. fl uorescens ,
Pseudomonas sp. Fusarium culmorum Seedling blight,
foot rot, and head
blight diseases of
cereals
Khan et al.
2006
Bacillus sp.,
Chromobacterium
violaceum
F. oxysporum Crown rot in
sorghum Idris et al. (
2007 )
Pseudomonas sp. Microdochium nivale Seedling blight of
wheat Amein et al. (
2008 )
Pseudomonas
chlororaphis , Fluorescent
pseudomonads
Macrophomina
phaseolina Charcoal rot of
sorghum Das et al. (
2008 )
Brevibacterium
laterosporus ,
Pseudomonas
fl uorescens , Serratia
marcescens
Pythium ultimum Root rot in
sorghum Idris et al. (
2008 )
Burkholderia cepacia Fusarium sp. Dry rot of potato Recep et al. (
2009 )
Bacillus licheniformis ,
Bacillus sp., P.
aeruginosa ,
Streptomyces fradiae
Sunfl ower necrosis
virus Sunfl ower
necrosis Srinivasan and
Mathivanan (
2009 )
Fluorescent
pseudomonad Sarocladium oryzae Sheath rot Saravanakumar et al.
(
2009 )
Acinetobacter sp.,
Enterobacter sp. Ralstonia
solanacearum Wilt of tomato Xue et al. (
2009 )
Pseudomonas
fl uorescens , Enterobacter
cloacae
Fusarium sp. Dry rot of potato Al-Mughrabi
2010
Bacillus. subtilis Monilinia laxa Brown rot of
nectarine Casals et al.
2010
Bacillus subtilis ,
Burkholderia cepacia F. oxysporum Vascular wilt of
tomato Shanmugam and
Kanoujia ( 2011 )
Chryseobacterium
wanjuense Phytophthora capsici Phytophthora
blight of pepper Kim et al. (
2012 )
Bacillus sp. F. oxysporum f. sp .
cucumerinum Wilt of cucumber Li et al. (
2012 )
Bacillus megaterium , B.
subtilis , Pseudomonas
sp.,
Aspergillus niger Root rot of peanut Yuttavanichakul et al.
(
2012 )
Pseudomonas putida ,
Bacillus cereus Ralstonia
solanacearum Wilt of tomato Kurabachew and
Wydra (
2013 )
(continued)
S.S. Shaikh et al.
189
concentration of ion cannot support the growth of organism (Heydari and Pessarakli
2010 ). To survive in such environment, certain organism produces ion-binding
ligands called siderophore to scavenge iron from the environment (Hider and Kong
2010 ). Some microorganisms produce siderophore that chelates the available iron
and competitively prevents the iron nutrition of phytopathogen (Siddiqui et al. 2007 ;
Akhtar and Siddiqui 2009 ; Chaiharn et al. 2009 ; Sayyed and Chincholkar 2009 ).
Siderophore is produced by Alcaligenes , Pseudomonas , Bradyrhizobium , Bacillus ,
Enterobacter , and Rhizobium (Shaikh et al. 2014 ; Shaikh and Sayyed 2015 ; Sayyed
and Patel 2011 ; Sayyed et al. 2013 ). Many different environmental factors affect the
synthesis of siderophores, notably the chemical nature of the organic carbon and
energy source (Sayyed et al. 2010 ), metals (Sayyed and Chincholkar 2010 ), amino
acids (Sayyed et al. 2010 , 2011 ), and organic nitrogen sources (Sayyed et al. 2005 ,
2010 ). Any factor infl uencing siderophore production infl uences the performance of
PGPR in plant growth promotion and phytopathogens suppression (Sharma and
Kaur 2010 ).
BCAs also compete with the pathogen for physical occupation of the site and
thereby delay the root colonization by the pathogen and exhaust the limited avail-
able substrate (Heydari and Pessarakli 2010 ). PGPR must be able to compete with
the pathogen and effi ciently colonize the rhizosphere of the plants to be protected
(Akhtar and Siddiqui 2010 ). Root colonization is widely believed to be an essential
aspect for biocontrol (Weller 1983 ; Parke 1991 ). Rhizosphere colonization is the
fi rst step in the pathogenesis of soil-borne microorganisms and also is crucial in the
application of microorganisms for benefi cial purposes (Lugtenberg et al.
2001 ).
3.2 Induced Resistance
Some biocontrol agents induce a sustained change in the plant, increasing its toler-
ance to infection by a pathogen, a phenomenon known as induced resistance. In
some cases, it is clear that induced resistance by BCAs involves the same suite of
genes and gene products involved in the well-documented plant response known as
Table 1 (continued)
PGPR Pathogen Disease Reference
Bacillus subtilis Curtobacterium
fl accumfaciens Wilt of common
bean Martins et al. ( 2013 )
Pseudomonas
chlororaphis subsp.
Aurantiaca
F. graminearum Head blight on
wheat Hu et al. (
2014 )
Bacillus. subtilis Sporisorium
reilianum Head smut in corn Mercado-Flores et al.
(
2014 )
Brevibacterium iodinum Stemphylium
lycopersici Gray leaf spot
disease in pepper Son et al. (
2014 )
Bacillus thuringiensis , B.
cereus Ralstonia
solanacearum Wilt of eucalyptus Santiago et al. (
2015 )
Plant Growth-Promoting Rhizobacteria: An Eco-friendly Approach for Sustainable…
190
systemic acquired resistance (SAR) (Handelsman and Stabb 1996). SAR is a state
of defense that is activated throughout the plant following the primary infection by
pathogens (Ryals et al. 1996 ). SAR and induced systemic resistance (ISR) are two
forms of induced resistance wherein plant defenses are preconditioned by prior
infection or treatment that results in resistance against subsequent challenge by a
pathogen or parasite (Choudhary et al. 2007 ). ISR involves salicylic acid, jasmonic
acid, and ethylene in the signaling (Niranjan et al. 2005 ; Pieterse et al. 2014 ) within
the plant, and these hormones stimulate the host plant’s defense responses against a
variety of plant pathogens, including fungal, bacterial, and viral pathogens, as well
as nematodes and insects (Glick 2012 ; Beneduzi et al. 2012 ). SAR is characterized
by the activation of SAR genes, including genes that encode pathogenesis-related
proteins, which are used as markers for the state of induced resistance (Mandal and
Ray 2011 ). PGPR elicit ISR in plants by increasing the physical and mechanical
strength of the cell wall as well as changing the physiological and biochemical reac-
tions of the host (Labuschagne et al. 2010 ). This results in the synthesis of defense
chemicals such as peroxidase and pathogenesis-related proteins (Nandakumar et al.
2001 ; Silva et al. 2004 ; Labuschagne et al. 2010 ). Several rhizobacteria trigger the
systemic acquired resistance (SAR) pathway by secreting salicylic acid at the root
surface, while other rhizobacteria trigger salicylic acid-independent SAR pathway.
This salicylic acid-independent pathway which is dependent on jasmonic acid and
ethylene signaling has been studied in Arabidopsis thaliana (Choudhary et al.
2007 ). The accumulation of salicylic acid for the expression of SAR was demon-
strated by using transgenic NahG plants which express the bacterial salicylate
hydroxylase nahG gene, making them incapable of accumulating salicylic acid
(Lawton et al. 1996 ). The following bacterial-derived compounds are also involved
in ISR including cell wall components such as fl agella, lipopolysaccharides, metab-
olites like siderophores, cyclic lipopeptides, volatile compounds like acetoin and
2,3-butanediol, antibiotics, phenolic compounds, and quorum-sensing molecules
(Vleesschauwer and Hofte 2009 ; Lugtenberg and Kamilova 2009 ). Biosurfactants
most specifi cally cyclic lipopeptide act as ISR signaling molecule in plants; cyclic
lipopeptides like fengycin, iturin, and surfactin families from Bacillus sp. are known
to have induced resistance mechanisms in plants (Ongena and Jacques 2008 ). Also
the receptor for bacterial fl agellin has been identifi ed as involved in ISR (Gomez-
Gomez and Boller 2000 ). In fi eld treatment, many PGPR strains applied as seed
coating or in drenching have shown induction of ISR either protected cucumber
plants from anthracnose caused by Colletotrichum lagenarium , angular leaf spot
caused by Pseudomonas syringae pv. lachrymans , or bacterial wilt caused by
Erwinia tracheiphila (Zehnder et al. 2001 ).
3.3 Lysis of Cell Components
Many rhizobacteria release hydrolytic enzymes that hydrolyze a wide variety of
polymeric compounds like chitin, proteins, cellulose, hemicellulose, and
DNA. Expression and secretion of such enzymes by these rhizobacteria help in
S.S. Shaikh et al.
191
inhibiting plant pathogen (Pal and Gardener 2006 ). Production of cell wall-
degrading enzymes such as chitinases, glucanases, cellulases, and proteases is
known to cause lysis and degradation of the fungal cell walls and thus help in bio-
control of fungal plant pathogens (Mabood et al. 2014 ).
Among these enzymes, chitinases are of prime importance; chitinases are pro-
duced by rhizobacteria to utilize chitin as a source of carbon and energy. B. subtilis
BSK17 is known to produce chitinase and β-1,3-glucanase to help in their compe-
tence and antagonistic activity (Dubey et al. 2014 ). Chitinase and β-1,3-glucanase
have been reported as major class of lytic enzyme that dissolve the major constitu-
ent of fungal cell wall like chitin and laminarin (Kumar et al. 2012 ). Chitinase-
producing Paenibacillus illinoisensis provides control of blight in pepper ( Capsicum
annuum ) caused by Phytophthora capsici (Jung et al. 2005 ). Jung et al. ( 2003 ) also
demonstrated the biocontrol potential of chitinase-producing Paenibacillus illi-
noisensis KJA-424 against damping off caused by Rhizoctonia solani . Dunne et al.
( 1997 ) demonstrated the biocontrol of Pythium ultimum in sugar beet by protease-
producing Stenotrophomonas maltophilia . Chitinase- and protease-producing
Pseudomonas sp. Pantoea dispersa and Enterobacter ammrenus strains inhibited
the growth of Fusarium sp. and M. phaseolina (Gohel et al. 2004 ). β-1, 3-glucanase
plays signifi cance role in biocontrol of Lysobacter enzymogenes (Palumbo et al.
2005 ). Chitinase-producing Bacillus suly reduced the severity of Fusarium infec-
tion produced under greenhouse conditions (Hariprasad et al. 2011 ).
3.4 Antibiosis
Production of antibiotics by PGPR is one of the major mechanisms studied for bio-
control of plant diseases. These antibiotics cause fungistasis, inhibition of germina-
tion of fungal spores, lysis of fungal mycelia, or fungicidal effects (Sindhu et al.
2009 ). A large number of antibiotics, including diacetylphloroglucinol (DAPG),
oomycin A, phenazines, pyocyanin, pyrroles, pyoluteorin, pantocin, hydrogen cya-
nide (HCN), mupirocin, pyrrolnitrin, iturins, bacillomycin, surfactin, zwittermicin
A, etc., are produced by PGPR (Nielsen et al. 2002 ; de Souza et al. 2003 ; Fernando
et al 2005 ; Sindhu et al 2009 ; Akhtar and Siddiqui 2010 ; Ahanger et al. 2014 ;
Mabood et al. 2014 ; Shaikh and Sayyed 2015 ). Several BCAs produce multiple
antibiotics that inhibit one or more pathogen (Islam et al. 2005 ; Junaid et al. 2013 ).
Phenazines are the largest family of heterocyclic nitrogen-containing pigment
known to have broad-spectrum antibiotic activity (Thomas et al. 2003 ). The major-
ity of antibiotics is produced by Bacillus sp., which are active with both gram-pos-
itive and gram-negative bacteria and pathogenic fungi Alternaria solani , Aspergillus
fl avus , Botryosphaeria ribis , Colletotrichum gloeosporioides , Fusarium oxyspo-
rum , Helminthosporium maydis , Phomopsis gossypii , etc. (Maksimov et al. 2011 ).
Synthesis of antibiotics is affected by many factors like carbon source, pH, tempera-
ture, and trace elements (Milner et al. 1996 ; Duffy and Defago 1997 , 1999 ).
Plant Growth-Promoting Rhizobacteria: An Eco-friendly Approach for Sustainable…
192
DAPG-producing Pseudomonas sp. shows potent in vitro and in vivo antifungal
activity against Fusarium oxysporum causing wilt of tomato (Kang 2012 ).
Bacillomycin D-producing Bacillus subtilis shows antifungal potential against
Aspergillus fl avus (MakMoyne et al. 2001 ). Koumoutsi et al. ( 2004 ) studied bacil-
lomycin D-producing Bacillus amyloliquefaciens that inhibited the Fusarium oxys-
porum causing wilt disease. Mycosubtilin-producing Bacillus sp. decrease the
incidence of damping off disease causing Pythium aphanidermatum (Leclere et al.
2005 ). Bacillus sp., producing iturin, inhibits germination of Penicillium roqueforti
(Chitarra et al. 2003 ) and Colletotrichum trifolii (Duville and Boland 1992 ). Iturin
produced by Bacillus sp. also exhibited antifungal activity against Aspergillus fl avus
(Moyne et al. 2001 ).
4 Merits of PGPR as Bioinoculants
(a) Biocontrol agents give protection to the crop throughout the crop period.
(b) They do not cause toxicity to the plants.
(c) Application of biocontrol agents is safer to the environment and to the person
who applies them.
(d) They multiply easily in the soil and leave no residual problem.
(e) Biocontrol agents not only control the disease but also enhance plant growth by
exerting benefi cial effects on root and other benefi cial soil microfl ora and also
increase the crop yield.
(f) Biocontrol agents are very easy to handle and apply to the target.
(g) Biocontrol agent can be combined with biofertilizers.
(h) They are easy to manufacture and amenability for growth on an inexpensive
medium in fermenter.
(i) It is harmless to human beings and animals and non-production of secondary
metabolites that might be toxic to humans.
(j) High genetic stability.
5 Commercial Aspects of PGPR
Over the last few years, several investigations have been initiated to fi nd BCAs for
the suppression and control of plant diseases caused by various fungi, bacteria, and
viruses. Despite the numerous reports of successful experiments, there has been
limited commercial success because of inconsistent fi eld performance (Sayyed
et al. 2005 ). The demand of fertilizers in India is increased signifi cantly in the last
few years. Figure 2 shows the fertilizer consumption (N, P, and K) in India from
1974–1975 to 2010–2011. Intensity of per hectare consumption of fertilizer is more
in Northern (91.5 kg/ha avg.) and Southern (85.3 kg/ha avg.) Region vis-à-vis
Eastern (44.7 kg/ha avg.) and Western (40.7 kg/ha avg.) region. By 2020, fertilizer’s
S.S. Shaikh et al.
193
demand in India is projected to increase shoot up to 41.6 million tonnes. If chemical
fertilizers are replaced by biofertilizers, the environmental risk of using chemical
fertilizers and their negative effects can be substantially reduced. The Government
of India has been promoting the use of biofertilizers in agriculture through the
National Project on Development and Use of Biofertilizers (NPDB).
Stability of the end products of biofertilizers during storage is high. Biocontrol
strains are also resistant to standard fungicides, compatible with other chemical and
physical treatments, and safer to the useful soil rhizobia. Under NPDB scheme, the
Government provides nonrecurring grants-in-aid up to INR 20,000,00 for setting up
of biofertilizer production units of 150 MT capacity. This grant-in-aid is offered to
State Departments of Agriculture/cooperatives/public sector undertakings of fertil-
izers, NGOs, and private agencies provided their proposals are received from
respective State Governments.
6 Conclusions and Future Prospects
PGPR improved the nutrient status of plants through various direct or indirect
mechanisms and also protect plants against the phytopathogens. Thus, awareness
must be brought among the farmers or end users about the positive aspects of PGPR
as biofertilizer and BCAs, because it is not only cost effective but also have other
positive aspects. This PGPR technology is acceptably applied to the maintained
conditions like a laboratory or greenhouse, but fi eld application and root coloniza-
tion need to be improved. Future challenge is not only to prove the biocontrol of
plant diseases but also to improve their effi cacy and durability under soil
Fig. 2 Shows the fertilizer consumption (N, P, and K) in India from 1974–1975 to 2010–2011
Plant Growth-Promoting Rhizobacteria: An Eco-friendly Approach for Sustainable…
194
environment. This can be achieved through a better understanding of the biological
control mechanisms and interactions between plant and microbes as well as micro-
bial ecology in the soil. The aim should be to enhance the crop yield on a sustain-
able basis while maintaining the quality and health of soil. To achieve this, the
knowledge of PGPR for different crop rhizospheric needs to be improved. Genetic
engineering could result in construction of new biocontrol strains with enhanced
production of antifungal metabolites, multiple plant growth potential in single stain,
improved competence for space or nutrient, wider host range, or enhanced tolerance
to biotic and abiotic stress. More effi ciency of biocontrol agents can be improved by
developing the improved cultural practices and suitable delivery systems, favorable
for their establishment in the rhizosphere and effi cient root colonization potential.
Acknowledgment Author RZS is thankful to UGC New Delhi for providing fi nancial support in
the form of a major research project.
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