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AN OVERVIEW OF PGPR/PGPF MEDIATED INDUCED SYSTEMIC RESISTANCE (ISR) IN PLANT DEFENSE

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Plants are exposed to various pathogens such as fungi, bacteria, virus, insect, etc which may cause some short of physiological and morphological disorder in plant, so called diseases. To overcome this disease incidence, plants have some defense mechanisms such as induced systemic resistance (ISR) and systemic acquired resistance (SAR). ISR is mediated by root colonizing plant growth promoting rhizobacteria (PGPR) or plant growth promoting fungi (PGPF) in response of Jasmonic acid (JA) and Ethylene (ET) which is subjected to the expression of defense related enzymes and defense chemicals in order to structural and chemical barrier against pathogen, while SAR is responsible for expression of pathogenesis-related proteins (PR-proteins) in response to a different endogenous signaling molecule, salicylic acid (SA) against necrotizing pathogen. PGPR and PGPF play dual roles in plant growth such as induction of resistance and promoting of growth. In this present work JA-ET dependent ISR is focused for protection of crops against pathogenic agents.
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Review Of ReseaRch
impact factOR : 5.7631(Uif) UGc appROved JOURnal nO. 48514 issn: 2249-894X
vOlUme - 8 | issUe - 6 | maRch - 2019
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AN OVERVIEW OF PGPR/PGPF MEDIATED INDUCED SYSTEMIC
RESISTANCE (ISR) IN PLANT DEFENSE
Parimal Mandal
Department of Botany, Mycology and Plant Pathology Laboratory,
Raiganj University, Uttar Dinajpur, West Bengal, India.
ABSTRACT
Plants are exposed to various pathogens such as
fungi, bacteria, virus, insect, etc which may cause some
short of physiological and morphological disorder in plant,
so called diseases. To overcome this disease incidence,
plants have some defense mechanisms such as induced
systemic resistance (ISR) and systemic acquired resistance
(SAR). ISR is mediated by root colonizing plant growth
promoting rhizobacteria (PGPR) or plant growth promoting
fungi (PGPF) in response of Jasmonic acid (JA) and Ethylene
(ET) which is subjected to the expression of defense related enzymes and defense chemicals in order to
structural and chemical barrier against pathogen, while SAR is responsible for expression of pathogenesis-
related proteins (PR-proteins) in response to a different endogenous signaling molecule, salicylic acid (SA)
against necrotizing pathogen. PGPR and PGPF play dual roles in plant growth such as induction of resistance
and promoting of growth. In this present work JA- ET dependent ISR is focused for protection of crops against
pathogenic agents.
KEYWORDS: Induced Systemic Resistance (ISR), Jasmonic acid (JA) and Ethylene (ET), Defense mechanism
INTRODUCTION
All higher plants have the ability to express various defense mechanisms when they are exposed to
various pathogens such as fungi, bacteria, virus, insect, etc. These mechanisms do not allow pathogen to
cause disease in plant, if the reaction occurs in a timely manner. However, if the defense reactions start at
too late or suppressed, infection of pathogen occurs successfully which may causes disease in plant
(Somssich and Hahlbrock, 1998). There are two different signal transduction pathways in plant such as
systemic acquired resistance (SAR) and induced systemic resistance (ISR). ISR is called as Jasmonic acid-
Ethylene (JA-ET) dependant- plant growth promoting rhizobacteria (PGPR) or plant growth promoting fungi
(PGPF) mediated induced systemic resistance (ISR) which is subjected to the expression of defense related
enzymes and defense chemicals for structural and chemical barrier in host plant against pathogen. While,
SAR is called as salicylic acid (SA) dependant- necrotizing pathogen mediated systemic acquired resistance
which is responsible for expression of pathogenesis related proteins (PR-proteins) playing direct defensive
role against pathogen attract.
A variety of biotic and abiotic inducers/elicitors are reported by several workers for induction of
induced systemic resistance (ISR) and systemic acquired resistance (SAR) in different crops. Among the
abiotic inducers, Meena et al. (2001) used salicylic acid in groundnut, Higa et al. (2001) used active oxygen
radicals in rice, O’Donnell et al. (1996) used ethylene in tomato, Smith-Beaker et al. (1998) used SA and 4–
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hydroxybenzoic acid in cucumber, Cohen et al. (1993) used jasmonic acid and methyl jasmonate in potato
and tomato, Siegrist et al. (2000) used β - aminobutyric acid in tobacco, Kaur and Kolte (2001) used
benzothiadiazole in mustard and wheat plant, Brederode et al. (1991) used UV-light in tobacco, Ernst et al.
(1992) used ozone in tobacco, Klessig et al. (2000) used nitric oxide and Kaku et al. (1997) used N-
acetylchitooligosaccharide in barley. Similarly, some biotic inducers have also been used to enhance in plant
defense reactions such as leaf extract of Azadirachta indica in barley (Paul and Sharma, 2002), Acalypha
indica in ginger (Ghosh and Purkayastha, 2003), Reynoutria sachaliensis in cucumber (Daayf et al., 1995).
Thus it is important for plants for early detection of pathogen and early delivering signal information for ISR
(intracellularly/ intercellularly) to plant for activation of defense machinary such as phytoalexines,
antimicrobial proteins, defense enzymes, reactive oxygen species etc. against pathogen (Shibuya and
Minami, 2001) for management of diseases.
INDUCED SYSTEMIC RESISTANCE (ISR)
The plant root colonizing microorganisms such as plant growth promoting fungi (PGPF) or plant
growth-promoting rhizobacteria (PGPR) may suppress plant disease incidence by triggering defense
mechanism in plant has been reported by several workers (Meera et al., 1995; Munoz et al., 2008). PGPF-
mediated induced systemic resistance (ISR) been studied in great detail on downy mildew disease incidence
in pearl mille using root colonizing fungi, Penicillium sp., Trichoderma sp., Rhizoctonia sp., and Pythium sp.
(Murali et al., 2012). Plant growth promoting fungi (PGPF) or Plant growth promoting rhizobacteria (PGPR)
can suppress the disease in plant by triggering induced systemic resistance (ISR). Induction of ISR by PGPR or
non-pathogenic fungi PGPF differ from SAR for their signal transduction pathways, it is designated by a
separate term ISR proposed by Kloepper et al. (1992) and latter supported by Pieterse et al. (1996). ISR
requires essential endogenous signal molecules, Jasmonic acid (JA) and Ethylene (ET) for its expression in
order to accumulation of defense related enzymes and defense related substances for structural and
chemical barrier against pathogen (such as Peroxidase, Polyphenol oxidase, Chalcone synthase, Phytoalexin,
Phenolic compounds, etc), rather than PR-proteins (Van Loon, 1999). Interestingly, simultaneous activation
of both the JA/ethylene-dependent ISR pathway and the SA-dependent SAR pathway results in an enhanced
level of disease protection. Thus combining both types of induced resistance provides an attractive tool for
the improvement of disease management.
PLANT GROWTH PROMOTING RHIZOBACTERIA (PGPR)
Root colonizing non pathogenic bacteria are generally called as plant growth promoting
rhizobacteria (PGPR) which can be classified into extracellular plant growth promoting rhizobacteria (ePGPR)
and intracellular plant growth promoting rhizobacteria (iPGPR) [Viveros et al., 2010]. The ePGPRs may exist
in the rhizosphere, on the rhizoplane and in the spaces between the cells of root cortex, while, (iPGPRs) are
living within a specialized nodular structure in plant. The bacterial genera (such as Agrobacterium,
Arthrobacter, Azotobacter, Azospirillum, Bacillus, Burkholderia, Caulobacter, Chromobacterium, Erwinia,
Flavobacterium, Micrococcous, Pseudomonas and Serratia) are belongs to ePGPR (Ahemad and Kibret,
2014). The bacterial species such as Allorhizobium, Bradyrhizobium, Mesorhizobium and Rhizobium, and
Frankia are belongs to iPGPR, which can symbiotically fix atmospheric nitrogen with the higher plants
(Bhattacharyya and Jha, 2012). Some common reported PGPR genera exhibit plant growth promoting
activities are Pseudomonas, Azospirillum, Azotobacter, Bacillus, Burkholdaria, Enterobacter, Rhizobium,
Erwinia, Mycobacterium, Mesorhizobium, Flavobacterium, Pseudomonas fluorescens, Pseudomonas syringae
(Maurhofer et al., 1994, Chen et al., 2000; Liu et al., 1995; Wei et al., 1991, Rasmussen et al., 1991, Singh,
2013).
PLANT GROWTH PROMOTING FUNGI (PGPF)
Root colonizing non pathogenic fungi are generally called as plant growth promoting fungi (PGPF)
which are reported to be suppressed disease incidence by triggering induced systemic resistance in
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cucumber and effectively control soil-borne diseases like damping-off caused by Fusarium, Rhizoctonia and
Sclerotium and take-all caused by Gaeumannomyces graminis of a number of crop plants (Narita and Suzuki,
1991; Meera et al., 1994; Hyakumachi et al., 1993). Hence PGPF has dual roles in plant protection which may
trigger induced systemic resistance (ISR) as well as promoting growth of plants (Murali et al., 2012). Some
common plant growth-promoting fungi (PGPF) are reported as Fusarium, Penicillium, Phoma, Trichoderma
(Meera et al., 1994).
SIGNAL TRANSDUCTION PATHWAY OF ISR
PGPR-mediated defense resistance mechanism, so called induced systemic resistance (ISR) is
associated with signal molecules, Jasmonic acid (JA) and Ethylene (ET) response. ISR is responsible for
induction of defense related enzymes and defense related substances rather than PR-Proteins (Figure-1).
Jasmonic acid (JA) plays an important role in plant defense response (Creelman et al., 1992) and its level is
increased under wounding and treatment with pathogen-elicitors that induce genes encoding enzyme for
structural and chemical barrier in plant cell against pathogenic agent. A mutant, mpk4 shows elevated
accumulation of salicylic acid (SA) in the absence of spontaneous necrotizing lesions in Arabidopsis (Petersen
et al., 2000). This mutation in the Mitogen Activated Protein Kinase 4 (MAPK4) gene results in the
constitutive expression of SAR and PR-proteins. While, the wild-type MAPK4 is characteristic to be a negative
regulator of SAR gene expression and a positive regulator of ISR. Constitutive expression of active MAPK
kinase (NtMEK2) in tobacco plant results in the activation of two MAPKs: salicylic-acid-induced protein
kinase (SIPK) and wound-induced protein kinase (WIPK) that lead to the expression of phenylalanine
ammonia lyase (PAL), the first enzyme in the phenylpropanoid pathway that ultimately cause cell death
(Bent et al., 2001).
DEFENSE ENZYMES AND COMPOUNDS
Many defense-related enzymes are involved in ISR gene expression. These includes oxidative
enzymes such as peroxidase (PO) and polyphenol oxidase (PPO) which catalyse the formation of lignin and
other oxidative phenols that contribute to the formation of defense barriers in plant cell structure against
pathogen (Avdiushko et al., 1993). Other enzyme such as tyrosine ammonia lyase (TAL) and phenylalanin
ammonia lyase (Gundlach et al.,1992), chalcone synthase (Creelman et al., 1992) are involved in phytoalexin
or phenolic compound biosynthesis. It is reported that Phenylalanine ammonia lyase (PAL) is a key enzyme
of phenylpropanoid pathway which leads to the deposition of lignin, phytoalexins and phenolic compounds
and form structural and chemical barriers of the plants to the pathogens (Ramamoorthy et al., 2002). The
defense related enzyme, Phenylalanine ammonia lyase (PAL) frequently increases in plants in respond to
pathogen invasion. Maher et al. (1994) reported the increased disease susceptibility of tobacco plants to
Cercospora nicotiana in which PAL activity was suppressed, but over expressed PAL, exhibited reduction of
lesion areas caused by two compatible, necrotrophic pathogens in transgenic tobacco plants. Elicitor
treatment and wounding in parsley and sweet potato increased the activity of PAL. About a 3-fold increase in
phenolic content was observed 4 days after challenge inoculation with C. personatum following
pretreatment with SA in groundnut (Meena et al., 2001). Polyphenol oxidase (PPO) catalyses the synthesis of
defense substances like tannin which is toxic to pathogenic microorganisms (Mahadevan and Sridhar, 1996;
Chen et al., 2000) and formation of oxidative phenols that contribute to the inhibition of pathogen to the
plant cell (Avdiushko et al., 1993). Peroxidase activity is changed under various environmental stresses such
as heavy metals, salts, temperature (Kiwan and Lee, 2003), air pollution (Lee et al., 2000). It is related with
the defense reaction in plants that lead to the detoxification of the reactive oxygen species (Higa et al.,
2001).
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Figure-1: Molecular level plant defense related signal transduction pathway: A- Plant Growth promoting
rhizobacteria (PGPR)/ Plant Growth promoting fungi (PGPF) mediated signalling pathway, Induced Systemic
Resistance (ISR) which require Jasmonic acid (JA) and Ethylene as elicitor signalling molecules and produce a
diverse array of defense related enzymes (such as peroxidase, polyphenol oxidase, chalcone synthase etc.)
and defense related substances (such as phytoalexin, anti-microbial phenolic compounds, etc); B-
Narcotizing pathogen mediated signalling pathway, Systemic Acquired Resistance (SAR) which require
endogenous salicylic acid (SA) signalling and produce Pathogenesis-related proteins (PR-proteins).
Table 2. Differentiation between the mechanisms of SAR and ISR
SAR
Differences 1. SAR is mediated by necrotizing
pathogen
2. It is switch on in response of a
endogenous signalling molecule- Salicylic
acid (SA)
3. It is subjected to the expression of
Pathogenesis related proteins (PR-
proteins)
4. It has direct inhibitory role against
pathogenic agents.
1. ISR is mediated by non pathogenic
microorganism such as Plant growth
promoting rhizobacteria (PGPR) or Plant
growth promoting fungi (PGPF)
2. It is switch on in response of two
different signalling molecules Jasmonic
acid (JA) and Ethylene (ET).
3. It is subjected to the expression of
diverse range of defense enzymes and
defense chemicals such as Phenylalanin
ammonia lyase (PAL), Peroxidase (PO),
Polyphenol oxidase (PPO), Chalcone
synthase phytoalexin, phenolic compound
etc.)
4. It has indirect inhibitory activity such as
involve in structural and chemical barrier
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5. SAR is regulated by NahG and NPR1
6. It is used the term Systemic acquired
resistance (SAR)
7. MAPK4 is characteristic to be a
negative regulator of SAR gene
expression
against pathogenic agents
5. SAR is not regulated by NahG and NPR1
6. It is used the term Induced Systemic
resistance (ISR)
7. MAPK4 is characteristic to be a positive
regulator of ISR
CONCLUSION:
ISR is effective against a broad range of pathogenic microorganism. It requires JA and ET as essential
signalling molecules, rather than SA. The wild-type MAPK4 is a negative regulator of SAR gene expression
and a positive regulator of ISR.
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Acknowledgment
Author is thankful to CSIR and UGC for their financial support.
Parimal Mandal
Department of Botany, Mycology and Plant Pathology Laboratory, Raiganj University,
Uttar Dinajpur, West Bengal, India.
... The diverse genera of non-pathogenic fungi, known as plant growth-promoting fungi (PGPF), colonize roots, enhancing plant growth and aiding in disease suppression and induced systemic resistance (Figure 4). PGPF play a crucial role in sustainable agriculture, promoting crop production in an environmentally friendly manner (Mandal, 2019) [87] . They directly enhance various aspects of plant growth and development and indirectly regulate it by suppressing pathogens and mitigating stress (Hossain and Sultana, 2020) [62] . ...
... The diverse genera of non-pathogenic fungi, known as plant growth-promoting fungi (PGPF), colonize roots, enhancing plant growth and aiding in disease suppression and induced systemic resistance (Figure 4). PGPF play a crucial role in sustainable agriculture, promoting crop production in an environmentally friendly manner (Mandal, 2019) [87] . They directly enhance various aspects of plant growth and development and indirectly regulate it by suppressing pathogens and mitigating stress (Hossain and Sultana, 2020) [62] . ...
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Rhizosphere is the main sink of plant growth-promoting microbes (PGPMs), where they colonize profusely; promote plant growth, biomass production, and yield; and activate the defense system of host by direct and indirect mechanisms. They are capable to multiply at different ecological niches of roots and modify root functioning by improving the mineral and water acquisition. The rhizospheric mircobiome may have neutral, detrimental, or positive effect on plant health. Currently, plant growth-promoting rhizobacteria (PGPR) and plant growth-promoting fungi (PGPF) are commonly used as biopesticides against many pathogenic diseases of agricultural crops including medicinal and spice crops. The influence of PGPM interaction with medicinal and spices herbs enhances the antioxidant defense associated with non-enzymatic and enzymatic reactions that protect the plant against herbivory and pathogen attack. Therefore, impact of pathogenic stress on medicinal and spice crops can minimize by utilizing the antagonistic potential of PGPMs instead of chemical fertilizers, owing to their features such as environmentally safe, rapid multiplication rate, broad spectrum of mechanism, and high compatibility over other rhizobacteria. This chapter discusses the novelty of PGPMs in rhizosphere and their antagonistic potential in the reduction of pathogens stress of many medicinal and spice crops by various modes of action particularly antioxidant defense mechanisms. The chapter also highlights the progress of morphological as well as physiological characteristics of plants on PGPM inoculation.
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