Role of plant hormones in plant defence responses

Rajendra Bari Æ Jonathan D. G. Jones

Received: 5 August 2008 / Accepted: 12 November 2008 / Published online: 16 December 2008

� Springer Science+Business Media B.V. 2008

Abstract Plant hormones play important roles in regu-

lating developmental processes and signaling networks

involved in plant responses to a wide range of biotic and

abiotic stresses. Significant progress has been made in

identifying the key components and understanding the role

of salicylic acid (SA), jasmonates (JA) and ethylene (ET)

in plant responses to biotic stresses. Recent studies indicate

that other hormones such as abscisic acid (ABA), auxin,

gibberellic acid (GA), cytokinin (CK), brassinosteroids

(BR) and peptide hormones are also implicated in plant

defence signaling pathways but their role in plant defence

is less well studied. Here, we review recent advances made

in understanding the role of these hormones in modulating

plant defence responses against various diseases and pests.

Keywords Hormones � Plant defence � Pathogen �Virulence � Signaling � Peptide � Biotrophs � Necrotrophs

Introduction

In their natural environment, plants encounter a vast array

of pathogenic microorganisms such as fungi, oomycetes,

bacteria, viruses and nematodes. These diverse pathogens

deliver effector molecules (also called virulence factors)

into the plant cell to promote virulence and cause disease.

Despite the presence of a large number of microorganisms

in the surroundings of plants, few microorganisms are able

to attack any particular plant species. Plants are able to

protect themselves against microbes and disease is the

exception rather than the rule. Plant defence mechanisms

are usually complex and composed of multiple layers of

defence that are effective against diverse array of patho-

gens. Plants utilize preformed physical and chemical

barriers that hinder pathogen entry and infection. In addi-

tion, plants have evolved a wide variety of inducible

defence mechanisms that are triggered upon pathogen

recognition. These inducible defences include multifaceted

molecular, biochemical, and morphological changes, such

as oxidative burst, expression of defence-related genes,

production of antimicrobial compounds, and/or pro-

grammed cell death (van Loon et al. 2006).

Plants defend themselves against most potential micro-

bial pathogens through a basal defence mechanism (also

called innate immune system). The current view of the

plant immune system has been represented as a ‘zigzag’

model in which the perception of microbial- or pathogen-

associated molecular patterns (MAMPs or PAMPs) by host

encoded pattern recognition receptors (PRRs) results in

PAMP triggered immunity (PTI). Successful pathogens

secrete effectors that suppress PTI and thus induce disease

resulting in effector triggered susceptibility (ETS). As a

counter defence strategy, plants recognise a given effector

either directly or indirectly and activate effector-triggered

immunity (ETI) resulting in disease resistance (Chisholm

et al. 2006; Jones and Dangl 2006). The activation of PTI

or ETI enhances plant disease resistance and restricts

pathogen growth. Hence, the timely recognition of an

invading microorganism coupled with the rapid and

effective induction of defence responses appears to make a

key difference between resistance and susceptibility.

Plants produce a wide variety of hormones, which

include auxins, gibberellins (GA), abscisic acid (ABA),

R. Bari � J. D. G. Jones (&)

The Sainsbury Laboratory, John Innes Centre, Colney Lane,

Norwich NR4 7UH, UK

e-mail: jonathan.jones@tsl.ac.uk

R. Bari

e-mail: rajendra.bari@tsl.ac.uk

123

Plant Mol Biol (2009) 69:473–488

DOI 10.1007/s11103-008-9435-0

cytokinins (CK), salicylic acid (SA), ethylene (ET), jasmo-

nates (JA), brassinosteroids (BR) and peptide hormones.

Recently, strigolactones are identified as a new class of

plant hormones (Gomez-Roldan et al. 2008; Umehara et al.

2008). Plant hormones play important roles in diverse

growth and developmental processes as well as various

biotic and abiotic stress responses in plants. Infection of

plants with diverse pathogens results in changes in the level

of various phytohormones (Adie et al. 2007; Robert-

Seilaniantz et al. 2007). The identification and characteriza-

tion of several mutants affected in the biosynthesis,

perception and signal transduction of these hormones has

been instrumental in understanding the role of individual

components of each hormone signaling pathway in plant

defence. Substantial progress has been made in under-

standing individual aspects of phytohormone perception,

signal transduction, homeostasis or influence on gene

expression. However, the underlying molecular mecha-

nisms by which plants integrate stress induced changes in

hormone levels and initiate adaptive responses are poorly

understood. Microbial pathogens have also developed the

ability to manipulate the defence-related regulatory network

of plants by producing phytohormones or their functional

mimics. This results in hormonal imbalance and activation

of inappropriate defence responses (Robert-Seilaniantz

et al. 2007). For example, production of coronatine—a

JA-Ile mimic by Pseudomonas syringae pv. tomato (Pst)

bacteria, triggers the activation of JA-dependent defence

responses leading to the suppression of SA-dependent

defence responses and promotion of disease symptoms

(Cui et al. 2005; Laurie-Berry et al. 2006). In addition,

coronatine has been shown to prevent PAMP-induced

stomatal closure which facilitates bacterial entry into the

leaf (Melotto et al. 2006). However, we still have limited

knowledge on complex regulatory networks where multiple

hormonal pathways interact and influence plant defence

responses. This review focuses on major recent advances

made in the identification of different hormonal compo-

nents involved in defence responses of plants against

various pests and diseases.

Salicylic acid, jasmonates and ethylene

Three phytohormones—SA, JA and ET, are known to play

major roles in regulating plant defence responses against

various pathogens, pests and abiotic stresses such as

wounding and exposure to ozone (Glazebrook 2005;

Lorenzo and Solano 2005; Broekaert et al. 2006; Loake

and Grant 2007; Balbi and Devoto 2008). SA plays a

crucial role in plant defence and is generally involved in

the activation of defence responses against biotrophic and

hemi-biotrophic pathogens as well as the establishment of

systemic acquired resistance (SAR, Grant and Lamb 2006).

Mutants that are affected in the accumulation of SA or are

insensitive to SA show enhanced susceptibility to bio-

trophic and hemi-biotrophic pathogens. Recently, it has

been shown that, methyl salicylate, which is induced upon

pathogen infection, acts as a mobile inducer of SAR in

tobacco (Park et al. 2007). SA levels increase in pathogen-

challenged tissues of plants and exogenous applications

result in the induction of pathogenesis related (PR) genes

and enhanced resistance to a broad range of pathogens.

By contrast, JA and ET are usually associated with

defence against necrotrophic pathogens and herbivorous

insects. Although, SA and JA/ET defence pathways are

mutually antagonistic, evidences of synergistic interactions

have also been reported (Schenk et al. 2000; Kunkel and

Brooks 2002; Beckers and Spoel 2006; Mur et al. 2006).

This suggests that the defence signaling network activated

and utilized by the plant is dependent on the nature of the

pathogen and its mode of pathogenicity. In addition, the

lifestyles of different pathogens are not often readily

classifiable as purely biotrophic or necrotrophic. Therefore,

the positive or negative cross talk between SA and JA/ET

pathways may be regulated depending on the specific

pathogen (Adie et al. 2007). However, in natural environ-

ments, plants often cope with multiple attackers and

therefore plants employ complex regulatory mechanisms to

trigger effective defence responses against various patho-

gens and pests. How plants prioritize one response over the

other is not known, however.

Although JAs are involved in diverse processes such as

seed germination, root growth, tuber formation, tendril

coiling, fruit ripening, leaf senescence and stomatal opening,

they play crucial roles in plant defence responses against

insects and microbial pathogens. Several studies have

demonstrated that concentrations of JA increase locally in

response to pathogen infection or tissue damage and exog-

enous application of JA induced the expression of defence-

related genes (Lorenzo and Solano 2005; Wasternack

2007). Over the past decade, several mutants affected in JA

signal perception and transduction have been isolated and

characterised. Three main JA-signaling components

include—coronatine insensitive 1 (COI1), jasmonate

resistant 1 (JAR1) and Jasmonate insensitive 1/MYC2

(JIN1/MYC2) (Fig. 1). COI1 encodes an F-box protein

involved in the SCF-mediated protein degradation by the

26S proteasome and is required for most JA-mediated

responses (Xie et al. 1998). JAR1 encodes a JA amino acid

synthetase involved in the conjugation of isoleucine to JA

(JA-Ile) which is considered to be the bioactive JA mole-

cule perceived by plants (Staswick and Tiryaki 2004;

Thines et al. 2007). JIN1/MYC2 encodes a transcription

factor involved in the transcriptional regulation of some JA

responsive gene expression (Lorenzo et al. 2004).

474 Plant Mol Biol (2009) 69:473–488

123

The recent discovery of jasmonate ZIM-domain (JAZ)

proteins has advanced our understanding of the molecular

mechanisms of JA signaling in plants. It has been reported

that COI1 or COI1-JAZ complex acts as a receptor for JA-

Ile in Arabidopsis (Katsir et al. 2008). JAZ proteins are

repressors of JA signaling which have been shown (JAZ1

and JAZ3) to interact with JIN1/MYC2 and inhibit the

expression of JA-responsive genes. JA (more specifically

JA-Ile) promotes interaction between JAZ proteins and the

SCFCOI1 ubiquitin ligase, leading to the ubiquitination and

subsequent degradation of JAZ proteins by the 26S pro-

teasome. The degradation of JAZ proteins allows

transcription factors (such as MYC2) to activate the

expression of JA-responsive genes (Chini et al. 2007;

Thines et al. 2007). It is interesting to note that JAZ genes

are induced by JA. In addition, myc2 mutants are defective

in some but not all JA responses. Recently, JA signaling

has been implicated in the long-distance information

transmission leading to systemic immunity in Arabidopsis

(Truman et al. 2007). Rapid accumulation of JA in phloem

exudates of leaves challenged with an avirulent strain of

Pst and increased accumulation of JA biosynthetic gene

transcripts as well as JA levels in systemic leaves suggests

that JA could act as a mobile signal in Arabidopsis

pathogen immunity (Truman et al. 2007). However, Cha-

turvedi et al. (2008) demonstrate that the mobile signal in

SAR is likely to be jasmonates and not JA itself.

JA signaling plays a prominent role in promoting plant

defence responses to many herbivores including caterpil-

lars, beetles, thrips, leafhoppers, spider mites, fungal gnats

and mired bugs (Browse and Howe 2008). For example, JA

signaling is activated in response to attack by Manduca

sexta caterpillars in tobacco (Kahl et al. 2000), spider mite

Tetranychus urticae in tomato (Li et al. 2002a) and Pieris

rapae caterpillars or Frankliniella occidentalis thrips in

Arabidopsis (Reymond et al. 2004; De Vos et al. 2005).

However, not all herbivores activate JA signaling in plants.

The silverleaf whitefly Bemisia tabaci activates SA sig-

naling and suppresses JA signaling in Arabidopsis

(Kempema et al. 2007) indicating that SA and other hor-

mones are also important for the resistance of plants against

some herbivores. However, compared to JAs, the contri-

bution of other phytohormones to host resistance against

herbivores appears to be relatively minor (Bodenhausen

and Reymond 2007; Koornneef and Pieterse 2008; Zheng

and Dicke 2008). Treatment of plants with JA results

in enhanced resistance to herbivore challenge (Howe and

Jander 2008). Moreover, mutants defective in the

biosynthesis or perception of JA show compromised

resistance to herbivore attackers (Paschold et al. 2007;

Zarate et al. 2007). These results indicate that JA plays a

dominant and conserved role in plant resistance to herbi-

vore attack.

Interaction between defence signaling pathways is an

important mechanism for regulating defence responses

against various types of pathogens. In the recent years,

several components regulating the cross-talk between SA,

JA and ET pathways have been identified. However, the

underlying molecular mechanisms are not well understood.

Some of the important components mediating the cross-

talk between defence signaling pathways are described

below.

Interactions between SA, JA and ET signaling

pathways

SA and JA/ET

One of the important regulatory components of SA sig-

naling is non-expressor of PR genes 1 (NPR1), which

interacts with TGA transcription factors that are involved

in the activation of SA-responsive PR genes (Fig. 1, Dong

2004). Arabidopsis npr1 plants are compromised in the

SA-mediated suppression of JA responsive gene expression

indicating that NPR1 plays an important role in SA-JA

interaction (Spoel et al. 2007). Downstream of NPR1,

Fig. 1 An overview of major components involved in different plant

hormone signaling after biotic stress in plants. Biotic stress results in

changes in different phytohormone levels. Alterations in plant

hormone levels results in the changes in the expression of defence

related genes and activation of defence responses. Major components

involved in different hormone perception and signaling are shown. A

plus (?) sign indicates positive interaction whereas a minus (-) sign

indicates negative interaction. See text for further details and

abbreviations. (Abbreviations: ABA, abscisic acid; ARFs, Auxin

response factors; Aux/IAA, Auxin/Indole-3 acetic acid; BR, brassi-

nosteroid; BRI1, BR insensitive 1; BAK1, BRI1-associated kinase1;

BIN2, BR insensitive 2; BRZ1, brassinazole resistant 1; BES1, BRI1

ems suppressor 1; CK, cytokinin; ERF, ethylene response factor; ET,

ethylene; GA, gibberellin; GID1, gibberellin insensitive dwarf1; JA,

jasmonates; SA, salicylic acid; TFs, transcription factors; TIR1,

transport inhibitor response 1)

Plant Mol Biol (2009) 69:473–488 475

123

several WRKY transcription factors play important roles in

the regulation of SA-dependent defence responses in plants

(Wang et al. 2006; Eulgem and Somssich 2007). The

Arabidopsis WRKY70 has been found to regulate the

antagonistic interaction between SA- and JA-mediated

defences. Overexpression of WRKY70 resulted in the con-

stitutive expression of SA-responsive PR genes and

enhanced resistance to the biotrophic pathogen Erysiphe

cichoracearum but repressed the expression of JA-

responsive marker gene PDF1.2 and compromised resis-

tance to the necrotrophic pathogen Alternaria brassicicola

(A. brassicicola) (Li et al. 2004, 2006). In contrast, sup-

pression of WRKY70 expression caused an increase in

PDF1.2 transcript levels and enhanced resistance to

A. brassicicola (Li et al. 2006). These results suggest that

WRKY70 acts as a positive regulator of SA-dependent

defences and a negative regulator of JA-dependent defen-

ces and plays a pivotal role in determining the balance

between these two pathways. Recently, WRKY62 has been

reported to be induced by MeJA and SA synergistically. In

addition, the analysis of loss and gain of function mutants

in Arabidopsis plants revealed that WRKY62 downregu-

lates JA-responsive LOX2 and VSP2 genes. These results

suggest potential involvement of WRKY62 in the SA-

mediated suppression of JA-responsive defence in

Arabidopsis (Mao et al. 2007).

Mitogen activated protein kinase 4 (MPK4) has been

identified as another key component involved in mediating

the antagonism between SA- and JA-mediated signaling in

Arabidopsis. The Arabidopsis mpk4 mutants show elevated

SA levels, constitutive expression of SA responsive PR

genes and increased resistance to Pst. In contrast, the

expression of JA responsive genes and the resistance to

A. brassicicola were found to be impaired in mpk4 mutants

(Petersen et al. 2000; Brodersen et al. 2006). These results

indicate that MPK4 acts as a negative regulator of SA

signaling and positive regulator of JA signaling in

Arabidopsis. Another important regulator identified to

affect antagonism between SA and JA mediated signaling

is a glutaredoxin, GRX480. Glutaredoxins are disulfide

reductases which catalyze thiol disulfide reductions and are

involved in the redox regulation of protein activities

involved in a variety of cellular processes (Meyer et al.

2008). Recently, GRX480 has been shown to interact with

TGA transcription factors involved in the regulation of SA

responsive PR genes (Ndamukong et al. 2007). The

expression of GRX480 is induced by SA and requires TGA

transcription factors and NPR1. Furthermore, the expres-

sion of JA responsive PDF1.2 gene was inhibited by

GRX480 (Ndamukong et al. 2007). These findings suggest

that SA-induced NPR1 activates GRX480, which forms a

complex with TGA factors and suppresses the expression

of JA-responsive genes.

A recent identification of a senescence specific tran-

scription factor WRKY53 represents an additional

component involved in mediating the cross-talk between

SA and JA signaling (Miao and Zentgraf 2007). WRKY53

has been shown to interact with the JA-inducible protein

epithiospecifying senescence regulator (ESR). More

importantly, the expression of these genes is antagonisti-

cally regulated in response to JA and SA suggesting that

WRKY53 and ESR mediate negative cross-talk between

pathogen resistance and senescence in Arabidopsis (Miao

and Zentgraf 2007). The JA-responsive transcription factor

JIN1/MYC2 acts as a negative regulator of SA signaling

during Pst DC3000 infection in Arabidopsis. The jin1

mutant plants showed increased accumulation of SA,

enhanced expression of PR genes and increased resistance

to Pst DC3000 compared to the wild type plants (Laurie-

Berry et al. 2006).

JA and ET

Several studies indicate that JA- and ET-signaling often

operate synergistically to activate the expression of some

defence related genes after pathogen inoculation (Penninckx

et al. 1998; Thomma et al. 2001; Glazebrook 2005).

Microarray analysis of defence related genes revealed

significant overlap in the number of genes induced by both

JA and ET (Schenk et al. 2000). Furthermore, the induction

of PDF1.2 gene by A. brassicicola was found to be

inhibited in both jasmonate insensitive mutant coi1 and

ethylene insensitive mutant ein2 (Penninckx et al. 1998;

Thomma et al. 2001). The Arabidopsis cev1 mutant, that is

defective in the cellulose synthase gene CesA3, displays

constitutively active JA and ET responses indicating that

CEV1 acts as a negative regulator of JA and ET signaling

in Arabidopsis (Ellis et al. 2002). It has been shown that an

Arabidopsis transcription factor, ethylene response factor 1

(ERF1) acts as a positive regulator of JA and ET signaling

(Lorenzo et al. 2003). Recently, several members of ERF

family have been shown to play important role in mediat-

ing defence responses in Arabidopsis (McGrath et al.

2005). The Arabidopsis transcription factor MYC2 has also

been shown to regulate the interaction between JA and ET

mediated defence signaling. However, MYC2 induces JA

mediated expression of wound response genes but repres-

ses the expression of pathogen responsive genes. This

indicates that MYC2 differentially regulates JA-responsive

pathogen defence and wound response genes in Arabid-

opsis (Lorenzo and Solano 2005; Dombrecht et al. 2007).

It is becoming evident that plants modulate the relative

abundance of SA, JA and ET levels, modify the expression

of defence-related genes and coordinate complex interac-

tions between defence signaling pathways to activate an

effective defence response against attack by various types

476 Plant Mol Biol (2009) 69:473–488

123

of pathogens and pests. However, how plants coordinate

these complex interactions and what are the molecular

mechanisms involved is not clear. Identification of

molecular players involved in the complex interactions and

fine-tuning the balance between different signaling path-

ways will broaden our understanding of hormone-mediated

defence signaling network in plants.

Auxin

Auxin promotes the degradation of a family of transcrip-

tional repressors called Auxin/Indole-3-acetic acid (Aux/

IAA). Aux/IAA proteins bind to auxin response factors

(ARFs) and inhibit the transcription of specific auxin

response genes (Fig. 1, Leyser 2006). It has been shown

that transport inhibitor response 1 (TIR1) is an auxin

receptor that interacts with Aux/IAA proteins (Kepinski

and Leyser 2005; Dharmasiri et al. 2005). TIR1 encodes an

F-box protein that forms an Aux/IAA-SCFTIR1 (SKP1,

Cullin and F-box proteins) complex and leads to the deg-

radation of Aux/IAA proteins via ubiquitin/26S proteasome

pathway (Parry and Estelle 2006). To regulate plant growth

and development, auxin can induce the expression of three

groups of genes: Aux/IAA family, GH3 family and small

auxin-up RNA (SAUR) family (Woodward and Bartel

2005). GH3 genes encode IAA-amido synthetases that are

involved in the regulation of auxin homeostasis by conju-

gating excess IAA to amino acids (Staswick et al. 2005).

Most of the total auxin in plants is found in the conjugated

form and the formation of auxin conjugates is one of the

important regulatory mechanisms for the activation or

inactivation of IAA.

Auxin responsive GH3 genes have been shown to play

roles in plant defence responses in Arabidopsis and Rice.

Recently, it has been shown that GH3.5 acts as a bifunc-

tional modulator in both SA and auxin signaling during

pathogen infection (Zhang et al. 2007). Similarly, Ding

et al. (2008) reported that over expression of GH3-8

resulted in enhanced resistance to the rice pathogen

Xanthomonas oryzae pv. oryzae (Xoo), which causes bac-

terial blight disease in rice, and this resistance was shown

to be independent of SA and JA signaling. In addition,

GH3-8 over expressing rice plants accumulated higher

levels of conjugated IAA (IAA-Asp) and reduced levels of

free IAA compared to wild type plants. Interestingly,

infection of rice plants with Xoo induced the expression of

several IAA biosynthetic genes and resulted in increased

accumulation of free IAA. Moreover, GH3-8 over

expressing plants showed reduced expression of SA and JA

responsive genes as well as reduction in the levels of SA

and JA compared to wild type plants (Ding et al. 2008).

These findings suggest that GH3-8 mediated resistance to

Xoo in rice is independent of SA and JA pathways. Xoo-

induced auxin production activates the expression of ex-

pansins that result in the loosening of the cell wall and thus

could potentiate pathogen growth. This is supported by the

observation that the expression of expansin genes was

suppressed in the Xoo resistant GH3-8 over expressors

(Ding et al. 2008). These results suggest that inhibition of

expansin expression by suppressing auxin signaling might

act as a physical barrier to restrict Xoo infection in rice.

Treatment of Arabidopsis plants with an SA analog,

benzothiadiazole S-methyl ester (BTH) resulted in the

repression of a number of auxin responsive genes. These

genes included an auxin importer AUX1, an auxin exporter

PIN7, auxin receptors TIR1 and AFB1, and genes belong-

ing to auxin inducible SAUR and Aux/IAA family (Wang

et al. 2007). Similarly, it was found that majority of the

above auxin inducible genes were also repressed in sys-

temic tissues after induction of SAR. This indicates that

SAR response involves down regulation of auxin respon-

sive genes. However, the level of free auxin did not change

after SA treatment. In addition, SA has been shown to

inhibit the expression of an auxin inducible reporter

DR5::GUS. Wang et al. (2007) argue that SA stabilizes

Aux/IAA auxin repressors by limiting auxin receptors that

are needed for the down regulation of Aux/IAA proteins.

Exogenous application of auxin has been shown to

promote disease caused by Agrobacterium tumefaciens

(Yamada 1993), Pseudomonas savastanoi (Yamada 1993)

and Pst DC3000 (Navarro et al. 2006; Chen et al. 2007).

Similarly, co-inoculation of P. syringae pv. maculicola

(Psm) 4326 and auxin has been found to promote both

disease symptom and pathogen growth in Arabidopsis

(Wang et al. 2007). These results indicate that auxin is

involved in the attenuation of defence responses in plants.

In contrast, blocking auxin responses has been shown to

increase resistance in plants. Auxin resistant axr2-1

mutants of Arabidopsis showed reduction in Psm 4326

growth compared to wild type plants (Wang et al. 2007).

Several studies have shown that pathogen infection

results in imbalances in auxin levels as well as changes in

the expression of genes involved in auxin signaling. For

example, infection with Pst DC3000 resulted in increased

IAA levels in Arabidopsis (O’Donnell et al. 2003). Inter-

estingly, the bacterial type III effector avrRpt2, which

encodes a cysteine protease, has been shown to modulate

host auxin physiology to promote pathogen virulence and

disease development in Arabidopsis (Chen et al. 2007).

Global gene expression analysis using microarrays

revealed that Pst DC3000 induces auxin biosynthetic genes

and represses genes belonging to Aux/IAA family and

auxin transporters. Thus, Pst DC3000 activates auxin

production, alters auxin movement and derepresses auxin

signaling thereby modulating auxin physiology in

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Arabidopsis (Thilmony et al. 2006). This suggests that

auxin promotes disease susceptibility and repression of

auxin signaling could potentially result in enhanced resis-

tance in plants. Indeed, down regulation of auxin signaling

has been shown to contribute to plant induced immune

responses in Arabidopsis. Navarro et al. (2006) showed

that down regulation of auxin receptor genes by over

expression of a micro RNA (miR393), which targets auxin

receptors, increased resistance against Pst DC3000 in

Arabidopsis. In contrast, activation of auxin signaling

through over expression of an auxin receptor that is par-

tially refractory to miR393-mediated transcript cleavage,

enhanced susceptibility to Pst DC3000 (Navarro et al.

2006). These results suggest that auxin promotes suscep-

tibility to bacterial disease, and that down-regulation of

auxin signaling is part of the plant induced immune

response.

Recently, Llorente et al. (2008) reported that repression of

auxin signaling either through mutations in the auxin sig-

naling components or interference with auxin transport

compromises resistance of Arabidopsis plants to the necro-

trophic fungi Plectosphaerella cucumerina (P. cucumerina)

and Botrytis cinerea (B. cinerea). Moreover, infection of

virulent necrotrophs such as P. cucumerina results in the

down regulation of auxin response genes in Arabidopsis

(Llorente et al. 2008). This suggests that auxin signaling is

an important component involved in modulating plant

responses to necrotrophic fungi. However, the expression of

marker genes of SA- and JA-signaling pathways was not

impaired in auxin signaling mutants upon P. cucumerina

infection. This indicates that the susceptibility of auxin

signaling mutants to necrotrophic fungi is not dependent on

SA- or JA-mediated defence pathways.

Viral pathogens also manipulate auxin signaling com-

ponents to promote virulence and cause disease. For

example, the interactions of tobacco mosaic virus (TMV)

replicase with Aux/IAA proteins affect the transcriptional

activation of auxin-responsive genes and promote the

development of disease symptoms in Arabidopsis and

tomato (Padmanabhan et al. 2005, 2006, 2008). Further-

more, the TMV replicase was shown to interact with and

disrupt the nuclear localization of several related Arabid-

opsis Aux/IAA proteins (Padmanabhan et al. 2006). This

indicates that TMV could disrupt Aux/IAA functions as a

means to reprogram the cellular environment for virus

replication and spread (Padmanabhan et al. 2008).

Taken together, emerging evidence suggests that auxin

acts as an important component of hormone signaling

network involved in the regulation of defence responses

against various biotrophic and necrotrophic pathogens.

Auxin regulates the expression of genes associated with the

biosynthesis, catabolism and signaling pathways of other

hormones (Paponov et al. 2008) and modulates defence

and development responses. However, how auxin levels

affect the balance of other hormones and fine tune defence

responses specific to different pathogens remains to be

discovered.

Abscisic acid

ABA is involved in the regulation of many aspects of plant

growth and development including seed germination,

embryo maturation, leaf senescence, stomatal aperture and

adaptation to environmental stresses (Wasilewskaa et al.

2008). Several recent papers have reported that ABA plays

important roles in plant defence responses (Mauch-Mani

and Mauch 2005; Mohr and Cahill 2007; de Torres-Zabala

et al. 2007; Adie et al. 2007). However, the role of ABA in

plant defence appears to be more complex, and vary among

different types of plant-pathogen interactions.

In general, ABA is shown to be involved in the negative

regulation of plant defence against various biotrophic and

necrotrophic pathogens. For example, the ABA-deficient

sitiens mutant of tomato showed more resistance to

B. cinerea (Audenaert et al. 2002), Pst (Thaler and

Bostock 2004), Oidium neolycopersici (Achuo et al. 2006)

and Erwinia chrysanthemi (Asselbergh et al. 2008) than

wild type plants. Similarly, the ABA-deficient aba2-1

mutant of Arabidopsis showed more resistance to Fusarium

oxysporum (Anderson et al. 2004) and the aba1-1 mutant

showed less susceptibility to Hyaloperonospora arabidopsidis

(Mohr and Cahill 2003) compared to wild type plants. The

Arabidopsis mutants impaired in ABA biosynthesis or

sensitivity show more resistance to Pst DC3000 (de Torres-

Zabala et al. 2007) and B. cinerea (Adie et al. 2007).

Likewise, exogenous application of ABA enhances sus-

ceptibility of various plant species to bacterial and fungal

pathogens. For example, application of ABA enhanced the

susceptibility of Arabidopsis plants to Pst (de Torres-

Zabala et al. 2007), soybean plants to Phytophthora sojae

(Mohr and Cahill 2001) and rice plants to Magnaporthe

grisea (Koga et al. 2004). Recently, Yasuda et al. (2008)

reported that ABA treatment suppressed SAR induction

indicating that there is an antagonistic interaction between

SAR and ABA signaling in Arabidopsis. Taken together,

these results suggest that ABA acts as a negative regulator

of defence responses in various plant pathosystems.

However, the role of ABA as a positive regulator of

defence has also been reported (Mauch-Mani and Mauch

2005). ABA activates stomatal closure that acts as a barrier

against bacterial infection (Melotto et al. 2006). As a

result, ABA deficient mutants show more susceptibility to

Pst. In addition, treatment with ABA protects plants

against A. brassicicola and P. cucumerina indicating that

ABA acts as a positive signal for defence against some

478 Plant Mol Biol (2009) 69:473–488

123

necrotrophs (Ton and Mauch-Mani 2004). In contrast,

mutants deficient in ABA are more sensitive to infection by

the fungal pathogens A. brassicicola, Pythium irregulare

(P. irregulare) (Adie et al. 2007) and Leptosphaeria

maculans (Kaliff et al. 2007). These results demonstrate

that ABA is not a positive regulator of plant defence

against all necrotrophs and its role depends on individual

plant pathogen interactions.

Pathogen challenge results in the alteration of ABA

levels in plants. For example, tobacco plants infected with

TMV showed increased ABA levels and treatment with

ABA enhanced TMV resistance in tobacco (Whenham

et al. 1986). Similarly, Arabidopsis plants challenged with

Pst DC3000 accumulated higher levels of ABA and JA

compared to unchallenged plants (de Torres-Zabala et al.

2007). These data suggest that some pathogens might have

evolved abilities to produce ABA or ABA-mimic to

interfere with the host defence. Interestingly, in planta

expression of the bacterial type III effector, AvrPtoB,

increases foliar ABA and JA levels in Arabidopsis (de

Torres-Zabala et al. 2007). However, changes in ABA

levels are relatively moderate compared to the changes in

the levels of SA, JA or ET after pathogen challenge

(Mauch-Mani and Mauch 2005). Moreover, there is a

strong similarity between the transcripts induced by ABA

and bacterial type III effectors in Arabidopsis. Genome

wide expression analyses have revealed the existence of a

significant (42%) overlap in the expression of genes reg-

ulated by ABA and bacterial type III effectors in

Arabidopsis (de Torres-Zabala et al. 2007). Similarly, meta

analysis of pathogen inducible genes in Arabidopsis

showed that approximately one-third of the ABA-regulated

genes are induced by P. irregulare infection (Adie et al.

2007). This indicates that ABA plays an important role in

the activation of plant defence through transcriptional

reprogramming of plant cell metabolism. Moreover, Adie

et al. (2007) also demonstrated that ABA is required for JA

biosynthesis and the expression of JA responsive genes

after P. irregulare infection.

How ABA modulates plant defence responses? ABA has

been shown to induce resistance partly through priming the

deposition of callose (Flors et al. 2008). Hernandez-Blanco

et al. (2007) provide evidence for a direct involvement of

ABA signaling in the control of Arabidopsis resistance to

R. solanacearum. Arabidopsis mutants affected in cellu-

lose synthase genes required for secondary cell-wall

formation show increased induction of ABA-responsive

defence-related genes. This suggests that ABA could exert

its effect on plant defence by modulating cell wall

metabolism in Arabidopsis. Recently, it has been shown

that ABA induced the expression of a catalase (CAT1), a

scavenger of H2O2, and at the same time activated H2O2

production. ABA-induced CAT1 expression and H2O2

production is mediated by AtMKK1- and AtMPK6-cou-

pled MAPK signaling cascades (Xing et al. 2008).

Moreover, H2O2 treatment induced the expression of CAT1

in a concentration-dependent manner (Xing et al. 2008).

This suggests that H2O2 might be involved in ABA-

induced CAT1 expression and CAT1 is probably involved

in its feedback regulation of the H2O2 signaling apart from

its ROS scavenging function. Accumulating evidence

suggests that ABA regulates defence responses through its

effects on callose deposition, production of reactive oxygen

intermediates and regulation of defence gene expression.

However, the exact molecular mechanism of ABA action

on plant defence responses against diverse pathogens

remains unclear. Since ABA is involved in both biotic and

abiotic stress signaling, the cross-talk between these sig-

naling pathways and the molecular mechanisms involved

remain obscure. Dissecting key factors involved in ABA

mediated cross-talk between biotic and abiotic stress sig-

naling merits extensive future study.

Gibberellin

Gibberellin (GA) was originally identified as a substance

secreted from the fungus Gibberella fujikuroi, which cau-

ses ‘bakanae’ (or foolish seedling) disease in rice

(Kurosawa 1926). GA promotes plant growth by stimu-

lating degradation of negative regulators of growth called

DELLA proteins. The rice GA receptor gibberellin insen-

sitive dwarf1 (GID1) interacts with the rice DELLA

protein slender rice1 (SLR1) in a GA-dependent manner

(Fig. 1). The binding of GID1 to DELLA results in ubiq-

uitination and degradation of DELLA via a ubiquitin E3

ligase SCF complex and the 26S proteasome (Ueguchi-

Tanaka et al. 2005; Griffiths et al. 2006). GAs are pro-

duced not only by higher plants, but also by fungi and

bacteria (MacMillan 2001). It is supposed that GAs in

fungi and bacteria are secondary metabolites that act as

signaling factors to establish the interaction with host

plants. GA has received little attention in the elucidation of

signaling components involved in defence responses.

However, emerging evidence suggests that GA signaling

components play major roles in plant disease resistance and

susceptibility.

Recently, it has been found that Arabidopsis DELLA

proteins, which act as negative regulators of GA signaling,

control plant immune responses by modulating SA and JA

dependent defence responses (Navarro et al. 2008). The

Arabidopsis quadruple-della mutant that lacks four DELLA

genes (gai-t6, rga-t2, rgl1-1, rgl2-1) is very susceptible to

the fungal necrotrophic pathogens A. brassicicola and

B. cinerea, but more resistant to biotrophic pathogens Pst

DC3000 and Hyaloperonospora arabidopsidis (Navarro

Plant Mol Biol (2009) 69:473–488 479

123

et al. 2008). Furthermore, Pst DC3000-challenged qua-

druple-della mutants showed earlier and stronger induction

of SA marker genes PR-1 and PR-2 whereas the expression

of JA/ET marker gene PDF1.2 (Plant defensin 1.2) was

significantly delayed in the quadruple-della mutants com-

pared to Pst DC3000 challenged wild type plants. In

contrast, DELLA over accumulating mutants, such as ga1-3,

gai and sly1-10, were more resistant to A. brassicicola and

more susceptible to Pst DC3000. These results suggest that

DELLA proteins promote resistance to necrotrophs by

activating JA/ET-dependent defence responses but suscep-

tibility to biotrophs by repressing SA-dependent defence

responses in Arabidopsis. Thus, DELLA proteins appear to

integrate plant defence response pathways involving SA and

JA/ET. DELLA proteins have also been shown to integrate

responses to independent hormonal and environmental sig-

nals of adverse conditions (Achard et al. 2006). Since GA

stimulates degradation of DELLA proteins, it is likely that

GA promotes resistance to biotrophs and susceptibility to

nectrotrophs. In support of this hypothesis, exogenous

application of GA resulted in enhanced resistance to Pst

DC3000 and susceptibility to A. brassicicola in Arabidopsis

indicating that GA acts as a virulence factor for necrotrophic

pathogens. These results suggest that Gibberella might

secrete GA as a virulence factor to promote the degradation

of DELLA proteins and attenuate JA-dependent defence

responses resulting in the loss of DELLA-mediated growth

restraint.

How DELLA proteins regulate defence responses

against various biotrophic and necrotrophic pathogens?

Recently, it has been shown that DELLA proteins promote

the expression of genes encoding ROS detoxification

enzymes thereby regulating the levels of ROS after biotic

or abiotic stress (Achard et al. 2008). In consistence with

this, della penta mutants (that lack all five DELLA genes)

accumulate higher levels of ROS after biotic stress and

show down regulation of ROS detoxification enzymes

compared to wild type plants (Bari and Jones, unpublished

results). Thus, it seems that DELLA proteins regulate plant

defence responses against various biotrophic and necro-

trophic pathogens at least in part through the modulation of

ROS levels in plants. How DELLA proteins regulate the

expression of ROS detoxification enzymes and how

DELLA-mediated modulation of ROS levels act as bio-

logical signals to regulate plant growth and stress responses

remains unclear.

Mutants affected in GA perception have been shown to

affect defence responses in plant. It has been demonstrated

that gid1 mutant of rice, defective in GA receptor, accu-

mulates higher GA levels and shows enhanced resistance to

the blast fungus Magnaporthe grisea compared to wild

type plants (Tanaka et al. 2006). In addition, the expression

of a GA inducible protein PBZ1 (probenazole inducible 1)

was found to be elevated in gid1 mutants. Probenazole is a

fungicide which is effective against blast disease in rice

(Midoh and Iwata 1996). Furthermore, the expression of

PBZ1 is induced by rice blast infection. Since, gid1

mutants accumulate high amounts of GA, PBZ1, and show

increased resistance to the blast fungus, the accumulation

of PBZ1 appears to play important role in resistance

against blast in rice. This indicates that GA signaling

components play roles in defence signaling in rice (Tanaka

et al. 2006).

Modulation of bioactive GA levels through GA deacti-

vating enzymes has been shown to affect disease resistance

in plants. Recently, Yang et al. (2008) reported that a GA

deactivating enzyme called Elongated Uppermost Inter-

node (EUI) regulates bioactive GA levels and is involved

in disease resistance against bacterial and fungal pathogens

in rice. The loss of function eui mutants accumulate high

levels of GAs and show compromised resistance whereas

EUI overexpressors accumulate low levels of GAs and

show increased resistance to Xoo and M. oryzae in rice

(Yang et al. 2008). Consistent with this, eui plants treated

with a GA biosynthesis inhibitor, uniconazole, restored

resistance whereas exogenous application of GA to EUI

overexpressors compromised resistance to Xoo. These

results indicate that GA plays a negative role in basal

disease resistance in rice.

Viral proteins have also been shown to affect GA sig-

naling components in plants. For example, expression of a

GA biosynthetic enzyme, ent-kaurene oxidase, was

repressed in rice plants infected with rice dwarf virus

(RDV) resulting in a dwarf phenotype (Zhu et al. 2005). It

has been shown that P2 protein of RDV interacts with rice

ent-kaurene oxidases and affects the production of GA.

RDV infected rice plants showed significant reduction in

GA level and treatment of infected plants with GA restored

normal growth phenotype (Zhu et al. 2005). Infection of

rice plants with RDV results in stunting and dark leaves,

symptoms that are characteristic of GA-deficient rice

mutants. These observations indicate that RDV modulates

GA metabolism to promote disease symptoms in rice.

Accumulating evidence indicates that GA and its sig-

naling components play important roles in regulating

defence responses against various biotrophic and necro-

trophic pathogens. However, the mechanism of GA action

on defence responses is largely unknown and several

interesting questions remain to be answered. For example,

what other GA biosynthesis and signaling components are

potential targets of pathogen effectors? How does GA

regulate the expression of defence genes and modulate

changes in metabolism in response to pathogen attack? Do

pathogens modulate GA levels in planta? What is the

dynamics of DELLA protein complexes in response to

pathogens attack? What are the DELLA downstream

480 Plant Mol Biol (2009) 69:473–488

123

targets involved in plant immunity? It would be interesting

to know how GA modulates the balance of other hormone

levels and regulates appropriate defence and developmen-

tal responses in plants.

Cytokinin

Cytokinins (CK) are plant hormones involved in diverse

processes including stem-cell control, vascular differenti-

ation, chloroplast biogenesis, seed development, growth

and branching of root, shoot and inflorescence, leaf

senescence, nutrient balance and stress tolerance (Muller

and Sheen 2007). Although, the role of CK in plant defence

is poorly understood, there are indications that CK is

involved in the regulation of plant defence responses

against some pathogens. CK plays an important role in the

development of club root disease caused by Plasmodio-

phora brassicae in Arabidopsis (Siemens et al. 2006).

Global gene expression analysis of P. brassicae infected

Arabidopsis resulted in differential expression of more than

1,000 genes compared to control plants. Interestingly,

genes involved in cytokinin homeostasis (cytokinin syn-

thases and cytokinin oxidases/dehydrogenases) were

strongly downregulated. Transgenic plants overexpressing

cytokinin oxidase/dehydrogenase genes showed resistance

against P. brassicae infection suggesting that cytokinin

acts as a key factor in the development of clubroot disease

in Arabidopsis (Siemens et al. 2006). However, the

molecular mechanism how CK influences plant defence is

not known. Recently, infection with Rhodococcus fascians

has been shown to modulate cytokinin metabolism in

Arabidopsis (Depuydt et al. 2008). It has been shown that

A. tumefaciens modifies CK biosynthesis by sending a key

enzyme into plastids of the host plant to promote tumori-

genesis (Sakakibara et al. 2005). Constitutive activation of

a resistance (R) protein in Arabidopsis has been shown to

display morphological defects through the accumulation of

CK indicating the involvement of CK pathway in some R

protein-mediated responses (Igari et al. 2008).

Brassinosteroids

Brassinosteroids (BRs) are a unique class of plant hor-

mones that are structurally related to the animal steroid

hormones and involved in the regulation of growth,

development and various physiological responses in plants

(Bajguz 2007). Although, BRs are known to influence

various developmental processes including seed germi-

nation, cell division, cell elongation, flowering,

reproductive development, senescence, and abiotic stress

responses in plants, very little is known about their role in

plant responses to biotic stresses.

Emerging evidence indicates that BRs are involved in

the regulation of plant defence responses. It has been

reported that BR enhances resistance to TMV, Pst and

Oidium sp. in tobacco. Similarly, BR was shown to

increase the resistance of rice plants against M. grisea and

Xanthomonas oryzae infection (Nakashita et al. 2003).

However, BR induced resistance does not require SA

biosynthesis and activation of PR gene expression indi-

cating that BR mediated resistance is independent of SA

mediated defence signaling in plants. Exogenous applica-

tion of 24-epibrassinolide, a BR, was shown to prevent the

development of disease symptoms on tomato plants inocu-

lated with Verticillium dahliae, whereas untreated plants

showed moderate to severe disease symptoms (Krishna

2003). Similarly BR sprayed potato plants showed resis-

tance to infection by Phytophthora infestans and this

resistance was found to be associated with increases in the

levels of ABA and ET (Krishna 2003). This suggests that

there is a cross-talk between BR and other hormone sig-

naling in mediating defence responses in plants.

Several important components of BR signaling are also

involved in the modulation of plant defence responses.

Recently, three independent research groups have dem-

onstrated the involvement of a critical component of

brassinosteroid signaling, BRI1-associated kinase 1

(BAK1) in the regulation of basal defence and pro-

grammed cell death in plants (Chinchilla et al. 2007;

Kemmerling et al. 2007; Heese et al. 2007). BAK1 is

known to interact with the BR receptor, BRI1, and

mediate BR signal transduction in plants (Li et al. 2002b;

Nam and Li 2002). BAK1 (also known as SERK3,

somatic embryogenesis-related kinase 3) is up regulated

in response to PAMPs (such as flg22 and elf18) and

mutant bak1 plants in Arabidopsis are compromised in

PAMP responses as evidenced by loss of ROS burst and

growth inhibition in response to flg22 (Chinchilla et al.

2007; Heese et al. 2007). Interestingly, bak1 mutants

developed spreading necrosis upon pathogen infection.

Furthermore, bak1 mutants showed enhanced susceptibil-

ity to necrotrophic pathogens such as A. brassicicola and

B. cinerea, whereas resistance to biotrophic pathogen

H. parasitica was enhanced in the mutant compared to

wild type plants (Kemmerling et al. 2007). Moreover,

exogenous BR application failed to restore resistance to

fungal pathogens and mutants affected in other BR sig-

naling components did not show enhanced susceptibility

to the above fungal pathogens (Kemmerling et al. 2007).

Heese et al. identified the Nicotiana benthamiana homo-

log of BAK1 and found that knockdown of the protein in

this plant allowed enhanced growth of bacteria on the

Plant Mol Biol (2009) 69:473–488 481

123

plants. These findings suggest that BAK1 plays a BR-

independent role in regulating cell death in Arabidopsis.

Another related protein BAK1-like 1 (BKK1) has been

shown to function redundantly with BAK1 and is

involved in the positive regulation of BR dependent plant

growth pathway and negative regulation of BR-indepen-

dent cell-death pathway in Arabidopsis (He et al. 2007).

Interestingly, BAK1 has been found to interact with the

flagellin receptor, FLS2, in a ligand-dependent manner

(Chinchilla et al. 2007; Heese et al. 2007). These data

suggest a model where binding of flagellin to FLS2 pro-

motes the formation of an active complex with BAK1

which results in the activation of downstream signaling

components. However, the function of BAK1 in plant

defence is BR-independent suggesting that BAK1 has

dual role in the regulation of plant defence and devel-

opment. Recently, Shan et al. (2008) demonstrated that

bacterial effectors, AvrPto and AvrPtoB, target BAK1 and

prevent the flagellin induced FLS2-BAK1 interaction,

thereby impeding the initiation of PAMP-signaling. This

indicates that BAK1 is an important regulator of PAMP-

signaling and it is possible that BAK1 interacts with other

unknown PRRs which might be targets for bacterial

effectors.

It has been shown that beet curly top virus (BCTV) C4

functionally interacts with brassinosteroid insensitive 2

(BIN2), a glycogen synthase kinase 3-like (GSK3-like)

protein kinase involved in brassinosteroid signaling in

Arabidopsis (Piroux et al. 2007). BIN2 is one of the 10

GSK3-like kinases in Arabidopsis (Jonak and Hirt 2002)

and is considered to be a negative regulator of the brassi-

nosteroid signal transduction pathway (Li and Nam 2002).

It has been demonstrated that BIN2 phosphorylates tran-

scription factors BRI1-ems-suppressor 1 (BES1) and

brassinazole-resistant 1 (BZR1) and targets them for deg-

radation by the proteasome (Li and Nam 2002). It appears

that binding of BCTV viral protein C4 to BIN2 subverts

brassinosteroid signaling by downregulating BIN2 activity

and activating the transcription of BES1 and BZR1

responsive genes (Piroux et al. 2007).

BR has also been reported to affect the expression of

genes involved in defence as well as biosynthesis of

other hormones. For example genes involved in biosyn-

thesis of ET (ACC synthase) and JA (OPR3) in

Arabidopsis, were induced by BR (Yi et al. 1999;

Muessig et al. 2006). Whether JA or ET is required for

BR induced resistance is not known. Collectively, these

results indicate that BRs and its signaling components are

involved in the modulation of plant defence responses

against various pathogens. However, our knowledge on

the role of BR on plant defence has started to emerge

and the molecular mechanisms involved remains to be

understood.

Peptide hormones

Peptide hormones comprise a new class of hormones and

are involved in the regulation of various aspects of plant

growth and development including defence responses

against attacking pathogens and pests (Matsubayashi and

Sakagami 2006; Farrokhi et al. 2008). The peptide hor-

mones are usually processed from larger polypeptide

precursors. Examples of plant peptide hormones include

systemin, hydroxyproline-rich glycopeptides, AtPep1,

CLAVATA3, PHYTOSULFOKINE, POLARIS, ROTUN-

DIFOLIA4/DEVIL1, inflorescence deficient in abscission

gene (IDA), early nodulin 40 (ENOD40), nodule specific

cysteine-rich (NCR), and S-locus cysteine-rich protein

(SCR).

Defence-related peptide hormones include systemin

(Pearce et al. 1991), hydroxyproline-rich glycopeptide

systemins (Pearce et al. 2001, 2007; Pearce and Ryan

2003) from solanaceous plants and AtPep1 peptide from

Arabidopsis (Huffaker et al. 2006). These peptides are

from 18 to 23 amino acids in length, are processed from

wound- and JA-inducible precursor proteins, and play roles

in the activation of local and systemic responses against

wounding and pest attack. Systemin is synthesized from

prosystemin and stored in the cytoplasm (Narvaez-Vasquez

and Ryan 2004). In contrast, hydroxyproline-rich glyco-

peptide systemins are processed from precursors that are

synthesized through the secretory pathway and localized in

the cell walls (Narvaez-Vasquez et al. 2005). Initially,

systemin was considered to be the systemic signal

responsible for the activation of systemic defence respon-

ses against wounding and herbivore attack (Pearce et al.

1991; McGurl et al. 1992). However, recent grafting

experiments with JA biosynthetic and perception mutants

indicate that the systemic signal is likely to be derived from

the octadecanoid pathway but not necessarily JA itself (Li

et al. 2002c; Lee and Howe 2003) because neither JA nor

systemin is needed in the systemic, undamaged leaves of

tomato plants. This suggests that systemin acts at or near

the site of wounding by inducing and amplifying the

JA-derived mobile signal and activates the systemic

response (Schilmiller and Howe 2005).

Systemin regulates the expression of several genes

involved in the octadecanoid pathway and herbivore

defence in tomato (Ryan 2000). Tomato plants over-

expressing prosystemin show enhanced resistance whereas

plants with reduced systemin levels show more suscepti-

bility to insect herbivory (Orozco-Cardenas et al. 1993).

Likewise, overexpression of the tobacco hydroxyproline-

rich glycopeptide precursor gene resulted in the activation

of proteinase inhibitor genes and increased resistance to

feeding by Helicoverpa armigera larvae in tobacco (Ren

and Lu 2006). Both systemin and hydroxyproline-rich

482 Plant Mol Biol (2009) 69:473–488

123

glycopeptides can activate the expression of anti-herbivore

proteinase inhibitors and polyphenol oxidase in response to

wounding and methyl jasmonate. AtPep1, a 23 amino acid

peptide derived from precursor PROPEP1 in Arabidopsis,

acts as an elicitor and activates the expression of defence

related genes (Huffaker et al. 2006). The gene encoding the

precursor can be induced by wounding, methyl jasmonate,

ethylene and SA. Constitutive expression of PROPEP1

gene in Arabidopsis results in the constitutive transcription

of PDF1.2 and enhanced resistance to P. irregulare

(Huffaker and Ryan 2007). These results suggest that

defense-signaling peptides play important roles in the

activation of defence against invaders probably by ampli-

fying the signal initiated by wounding and elicitors.

However, the underlying molecular mechanism involved in

the activation of these peptide hormones in regulating plant

defence remains elusive.

Conclusions and perspectives

Plant hormones regulate complex signaling networks

involving developmental processes and plant responses to

environmental stresses including biotic and abiotic stresses.

Significant progress has been made in identifying the key

components and understanding plant hormone signaling

(especially SA, JA and ET) and plant defence responses

(Fig. 1). Several recent studies provide evidence for the

involvement of other hormones such as ABA, auxin, GA,

CK and BR in plant defence signaling pathways. Treatment

of plants with some hormones results in the reprogramming

of the host metabolism, gene expression and modulation of

plant defence responses against microbial challenge.

Depending on the type of plant–pathogen interactions,

different hormones play positive or negative roles against

various biotrophic and necrotrophic pathogens (Fig. 2).

However, the underlying molecular mechanisms are not

well understood and several questions remain to be

answered. For example, how is the intracellular level of

phytohormones regulated in response to various

pathogens?

Plant hormone signaling pathways are not isolated but

rather interconnected with a complex regulatory network

involving various defence signaling pathways and devel-

opmental processes. To understand how plants coordinate

multiple hormonal components in response to various

developmental and environmental cues is a major chal-

lenge for the future. It is important to note that the type of

interactions and plant responses to stresses vary depending

on the pathosystem as well as the time, quantity and the

tissue where hormones are produced. Another important

question to answer is how different hormone-mediated

developmental and defence-related responses are regulated

in specific tissues and cell types? Most of the studies in

understanding phytohormone signaling have been done

using seedlings and there is limited study on mature leaves.

More studies using mature leaves are necessary to under-

stand the role of hormone signaling components involved

in plant defence against various pathogens.

In addition to the production of hormones by plants,

several plant pathogens also produce phytohormones or

their functional mimics to manipulate defence-related

regulatory network of plants. Emerging evidence suggests

that plant pathogens manipulate components of hormone

biosynthesis and signaling machinery leading to hormone

imbalances and alterations in plant defence responses. This

is one of the strategies used by some pathogens to confer

virulence and cause disease. However, we have very lim-

ited knowledge on how pathogen effectors confer virulence

by modulating hormone signaling components. Recent

global expression profiling studies in response to pathogen

challenges are providing useful information about different

components involved in the complex interactions between

hormone-regulated defence signaling pathways. However,

additional studies involving mature leaves and detailed

time course experiment will be necessary to extend our

understanding of the complex regulatory mechanisms

operating between plant hormone signaling and plant

defence responses. A better understanding of phytohor-

mone-mediated plant defence responses is important in

designing effective strategies for engineering crops for

disease and pest resistance.

Acknowledgements We apologize to our colleagues whose work

could not be cited in this review because of space limitations. We

thank, Lionel Navarro, Alexandre Robert-Seilaniantz and Georgina

Fabro for critical comments. The Sainsbury Lab is funded by the

Gatsby Charitable Foundation. R. Bari is funded by a grant from the

BBSRC.

Fig. 2 A simplified model showing the involvement of different

hormones in the positive or negative regulation of plant resistance to

various biotrophic and necrotrophic pathogens. The arrows indicate

activation or positive interaction and blocked lines indicate repression

or negative interaction. See text for further details and abbreviations

Plant Mol Biol (2009) 69:473–488 483

123

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