Signaling in Plant Resistance

8

Signaling in Plant ResistanceResponses: Divergence andCross-Talk of Defense Pathways

Corn´e M.J. Pieterse, Andreas Schaller, BrigitteMauch-Mani, and Uwe Conrath

8.1 Introduction

Plants possess inducible defense mechanisms to protect themselves against at-tack by microbial pathogens and herbivorous insects. The endogenous sig-naling molecules salicylic acid, ethylene, and jasmonic acid, and the peptidemessenger systemin play important roles in the regulation of these induced de-fense responses. Disease resistance of plants can also be induced by chemi-cal agents, such as 2,6-dichloroisonicotinic acid, benzothiadiazole, and the non-protein amino acid

β

-aminobutyric acid. In most cases, these chemical agentsmimic or ingeniously make use of the same pathways that are activated bythe endogenous defense signals. This review is focussed on the current stateof research on signal transduction pathways involved in induced resistanceagainst pathogens and insects. Recent advances in induced resistance researchrevealed that the signaling pathways involved are interconnected, resulting inoverlap, synergism, and antagonism between the different signal transductionpathways. Divergence and crosstalk of pathways in defense response signalingprovide the plant with flexibility and the opportunity for fine-tuning of resis-tance responses, thereby enabling it to cope with different forms of stress moreefficiently.

8.2 Salicylic Acid Induces Systemic Resistance Responses

Over the past decade it became increasingly clear that the endogenous signal sal-icylic acid (SA) serves multiple roles in plants. For example, SA is involved intheregulation ofcellgrowth (Vanackeretal., 2001), ﬂowering, and thermogenesis(for reviews, see Malamy and Klessig, 1992; Raskin, 1992; Klessig and Malamy,1994;ShahandKlessig,1999).SAalsoplaysacrucialroleinplantdefenseagainst

166

8.2 Salicylic Acid Induces Systemic Resistance Responses 167

pathogens by affecting lesion formation (Weymann et al., 1995) and by activatinginduceddiseaseresistance(Dempseyetal.,1999;ShahandKlessig,1999;Nawrathet al., in this volume). The latter is variously referred to as systemic acquiredresistance (SAR) or induced systemic resistance (ISR). Although these terms aresynonymous(Hammerschmidtetal.,2001),werefertotheSApathway-dependent,induced disease resistance as SAR. SAR is characterized by a long-lasting resis-tance against a broad spectrum of pathogens both at the initial infection site and inthe distal, uninoculated organs. The most compelling evidence for the importantrole of SA in the onset of SAR comes from studies with transgenic tobacco and

Arabidopsis

plants expressing the

NahG

gene from

Pseudomonas putida.

Thisgene encodes a salicylate hydroxylase, which destroys the SA signal by convert-ing it to catechol. Upon pathogen attack,

NahG

transgenic tobacco and

Arabidop-sis

plants do not accumulate enhanced levels of SA nor do they establish SAR(Gaffney et al., 1993; Delaney et al., 1994). The SAR state is activated by manymicrobes that cause tissue necrosis but it can also be induced by exogenous ap-plication of SA or its functional analogs 2,6-dichloroisonicotinic acid (INA) andbenzothiadiazole (BTH) (Ryals et al., 1996; Sticher et al., 1997; Dempsey et al.,1999).The onset of SAR is associated with an early increase in endogenous SA levelsand with the immediate expression of a speciﬁc set of so-called

SAR

genes, someof which encode pathogenesis-related (PR) proteins (Ryals et al., 1996; Sticheretal.,1997;Dempseyetal.,1999).WhileitisknownthatsomePRproteinsdisplayantimicrobial activity (Van Loon and Van Strien, 1999), their actual role in SAR isstill unclear and can depend on the plant-pathogen system. In fact, a strict corre-lation between increased accumulation of PR proteins before challenge pathogenattack and SAR has not always been observed. To gain a better understanding of the mechanisms that contribute to SAR, it is necessary, therefore, to study furtherdefense-associated cellular events that are induced faster or to a greater extentin attacked, SAR-protected plants. Such events include the activation of defense-related genes other than those encoding PR proteins, and the deposition of callose(Kohler et al., 2002).In addition to

SAR

gene expression, SAR is also associated with priming (sen-sitizing) which enhances the plant’s capacity for the rapid and effective acti-vation of cellular defense responses, that are induced only upon contact witha (challenging) pathogen (Kuć, 1987; Katz et al., 1998; Conrath et al., 2002).These responses include hypersensitive cell death (Mittler and Lam, 1996), cellwall fortification (Hammerschmidt and Kuć, 1982; Stumm and Gessler, 1986;Schmele and Kauss, 1990), the production of reactive oxygen species (Doke et al.,1996), and the activation of defense-related genes (Ryals et al., 1996; Sticheret al., 1997).The role of SA in

PR

gene expression as a part of SAR is discussed by Nawrathet al. and will therefore not be discussed here in detail. This section of our reviewwill rather focus on the progress made in elucidating the role of SA in priming forpotentiated activation of cellular defense responses.

168 8. Signaling in Plant Resistance Responses

8.2.1 Salicylic Acid-Induced Priming in a CellCulture Model System

Over the past 13 years, it has been reported that a pretreatment of parsley cell cul-tureswithlowdosesoftheSARinducersSA,INA,andBTHdidnotdirectlyinducevarious assayed, cellular defense responses (Kauss et al., 1992a; 1993; Kauss andJeblick,1995;ThulkeandConrath,1998;Katzetal.,1998;2002).Yet,apreincuba-tionwiththeSARinducersprimedthecellsforpotentiated(augmented)activationof defense responses, that were subsequently induced by otherwise noninducingdoses of an elicitor from

Phytophthora sojae

cell walls (Kauss et al., 1992a; 1993;Kauss and Jeblick, 1995; Thulke and Conrath, 1998; Katz et al., 1998; 2002)

.

The potentiated responses include the early oxidative burst (Kauss and Jeblick,1995), a rapidly induced K

+

/pH response (Katz et al., 2002), the incorporationinto the cell wall of various phenolics and a lignin-like polymer (Kauss et al.,1993), and the secretion of antimicrobial coumarin phytoalexins resulting froman enhanced activity of coumarin biosynthetic enzymes (Kauss et al., 1992a) andaugmented expression of some of the genes encoding these enzymes (Kauss et al.,1992a; 1993; Katz et al., 1998; Thulke and Conrath, 1998). In a similar manner, insoybean suspension cells, physiological concentrations of SA strongly augmenteddefense gene activation, H

2

O

2

accumulation, and the hypersensitive necrosis re-sponse (HR) that was induced by treatment with avirulent

Pseudomonas syringae

pv.

glycinea

(Shirasu et al., 1997). However, since the SA-mediated potentiationof defense responses in soybean cells did not depend on prolonged pre-treatmentwith SA, this mechanism of regulation obviously differs from the time-dependentpriminginculturedparsleycells.Together,theobservationsmadewithparsleyandsoybean suspension cells revealed that plant cell cultures can be suitable modelsystems for studying the SA-, INA-, and BTH-induced priming for potentiatedactivation of cellular plant defense responses.

8.2.2 Salicylic Acid Serves a Dual Role in the Activationof Defense Responses

While elucidating the inﬂuence of SA and BTH on the activation of defense-related genes in the parsley cell culture, it became obvious that the inducer’s effecton gene activation depends on the gene that is being monitored (Katz et al., 1998;Thulke and Conrath, 1998). One set of genes, such as those encoding anionicperoxidase and mannitol dehydrogenase, was found to be directly induced byrelatively low concentrations of the two SAR inducers tested (Katz et al., 1998;Thulke and Conrath, 1998). A second set of parsley defense-related genes, in-cluding those encoding phenylalanine ammonia-lyase (PAL), 4-coumarate:CoAligase, intracellular PR-10 proteins and a hydroxyproline-rich glycoprotein, wasonly faintly responsive to the treatment with relatively low concentrations of SAorBTH.Yet,alreadyatlowinducerconcentrations,thesegenesdisplayedSA-andBTH-dependent potentiation of their expression following treatment with a lowelicitordose(Katzetal.,1998;ThulkeandConrath,1998).Forinstance,morethan

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