8

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

Cor.(N F M.J. PrL I ERse. Aronees Sr n qr r en, Bnicr r rcMAUCH,MANL ÀND UwE CoNRATE

8.1 Introduction

Pbnts possess inducible defense mechanisms to protect rhemselves against at-. tack by microbial parhog€n$ and herbivorous insects. The endogerous sig-

nding molecules salicylic Àcid, èthylene, and jasmooic acid, and the pepddeme$senger systemin play irnpoÍant loles ir the regulation of rhcse induced de_fense Íesponses. Disease rcsistance of plants cên also be induc€d by chemi-cal €enls. such a" 2.6-dichloroisonicodnic acid, benzoLhrrdiazol,r. anjrhe non-prctcin JJnino ocid l3-rmi@burync acid. In rnosr case,. rhe6e chcnriJÀt agenlsmimic oc ingenrouqly make/usc of the sarne pathwals rhar arc acrivbted by$e endogenous deÍ€nse signals. This revicw is focussed on the cunent stateof reseaÍch oD signal transduction pathwàys involved in induced resistanceagÍiiDst pathogens aDd insecls, Receut advànces in induced resistalce researchÍevealed that the signaling patbways involvcd are interconnecled. rcsultina inovcrlflp. syoeÍgisrn. d anragonisrn berwcc rhe dilïcrent signal uanduciionpathways. Djvergence and oosstalk of pathways in defense ràsponse signalingprovide tbe planr with Ílexibiiiry ànd the opportunity for line-tuning of resis,tance responses, thereby enabling it to cope wirh differenr fbnÍs of siress nroreefÍiciently.

,i

ó.2 Sallcyltc Actd Induces Syslernic Resistance Responses

Ovei thê pasl decade ir bec,nne increasingty clear rhat the endogenous signal saiicylic acid (SA) seÍves multiple roles jn ptants. For example. SA is nrvolvcd inthc regulation of cell growlh (Vanacker er al.. 2001), ilowering, and thcnnogenesis(1or reviews. see Maiamy ànd Klessig, 1992: Raskin, 1992; Klessig and MalamÍ1994: Shah andKtessig, 1999). SA alsoptays affucialroie in plant rlefense againsr

166

- 8.2 Salicylic Aci.l IndNes Syíedi. l{esislancè IteípnsÈs )61

pathoge s by affecling lesior formation (Weymann et lr1., 1995) and by activarinsinduced diseaseresistance (Denpsey etal.,1999:Sháh and Klessig, 1999;Nàwrah

: et al.. in lhis volume). The lalter is variousiy refered to as systcmic acquiredresistarce (SAR) o. induced systemic resistance (ISR). Althoush these terns arcsynonymons (Hanmerschmidt et al., 2001), we Ícier to the SA pathway'dependÈnt,induced discase resistànce as SAR- SAR is cha.acterized try à long lasting resistance against a broad specirum of pathogens troth ai thc inirial infecrion site and inthe distal, xninoculared organs. The most compelling evidence fbr the impoÍantrole ofSA in the onset of SAR comes Íiom studics with trunsgenic tobácco àndArabidotsis plAtlts e\prcssjng the NolG gene lion Pseu.lomonas put,Ja. Thlsgene encodes a salicylate hydrcxylase, which destroys the SA signal by conveÍing jt to catechol. Upon pathogen attack. NdrC transgenic tobacco and Á,'.rridop-rís plÀnts do not accumulale enhanced ievels oí SA nor do they cstablish SAR(GaffÍey et al., 1993;Dolaney er à1.. 1994). The SAR srate is activated by nanymicrobes that cause tis$ue neorcsis but it can also bc irduced by exogenous ap-plication of SA o. it$ tunctional analog$ 2.6-dichioroisonicorinic acjd (lNA) arrdbenzothiaóazole (BTH) (Ryals et al., 1996; Sticher et al., 1997; Dempsey et al.,r999).

The onset ofSAR is associated with an early increase in endogenous SA levelsand with fie immediale expression ofa specific ser of so-called SAR genes, someof which eocode pathogenesis-related (PR) proteins (RyÀis et .r1., 1996; Slicheret rl., 1997;Denpsey et a1., 1999). fr'hile it is known that some PR proieins displayanrimicrobial acdvity (Van Loon and Van Strien, 1999), Xheir aclual rolein SARisstill unclear and can depend on the plant-pathogen system, [n tàct, a stÍict co|re-lation beMeen incleased acoumulAtion of Pll proteins befofe challenge pathogenaíack and SAR has not alwrys beer observed. To gnin a belter undeGtanding ofthe mechanisms that conlribute to SAR, it is necess$y, theÍefore, 1o study furthsrdelense-associated c€llular events th are induced fast€r or lo a greater extenti attacked, SAR-protccted plênts. Such events include thc Activêtion ofdcfense-related genes other thàn lhose encodirg PR proteins. and the deposition ofcallose(Kobler et à1., 2002).

ln àddition to SAR gêne expÍession, SAR is also associated with pdming (sen-sirizing) whicb enhances làe planfs capacity fbr the ràpid and etective acti-vation of cellular detênse responses. that are induced only upon contàcl witha (ch.dlenging) pàthogen (Kuó, 1987t Katz et al., 1998; Conràlh et a1.,2002).Thesc Ésponses include hypersensirive cell dcath (Mittler and Lam, 1996), cellwall lbdificaiion (Hnmmerschmidt ànd Kuó, 1982; Stunrm and Ccssler. 1986;Scbmele and Kauss, 1990), Èc poduction ofÍeactive oxygen spècies (Doke et ê1..1996), and lhc àcrivàrion of defènse-related genes (Ryals et al., 1996; Sticherer al.. 199?).

The rolc ofSA in PR gene expression as apaft of SAR is discussed by Nawrathet al. ànd wil theÍefore not be discussed here in detail. This seclion of our rcviewwill raLher lbcus on the progress made in elucidating the role ofSA in prnning foroolentiated activation of cellular defense rcsDonses.

168 8. Signalins ni Plaht Resisl.nce Rcslonses

8.2.1 Salicylic Acid-Induced Primíng ín a CellCulture Model System

Over the past I 3 ye{s. it hàs been reported that a prctreatnenr of parsiey cell cut_t .es wjlh low doses ofthe SAR inducers SA, INA, and BTH did nor diÍectly jnducevadous assayed, cellular defense respoNes (Kauss et at., 1992a; 1993: Kauss andJeblick, 1995;ThulkeandCo Íh, 1998;Katzctal.. 1998i2002).yet.apreincubaftn with the SAR inducers pdned the cc s for potentiared (augncnted) acrivalionof defènse Íesponses, rhat were subse4uentty induced by olhen ise noniDducingdoses of an elicild írom P hytophíhoÍa sai@ .e[ \ràlls (Kauss et at.. 1 992ai 1993;Kauss and Jebljck, 1995; Thotke and Conrath. i998; Karz ct a1., 1998; 2002).The potentiated rcsponses iÍclude the earty oxidarivc burst (Kauss and Jcbtick,1995), a rupidly nrduced Kr/pH response (Kàtz et a1., 2002), rhe incorporàtioninto 01e cell lvall of v.uiors phenolics and a lignin-tikc ptymcr (Kauss c1 àt..1993). and the secrelion of anlinricfobial coumarin phyroatexins rcsutrirg fionran cnhanced ac(ivity oí co marin biosynrhctic enzymres (Kauss er al., 1992;) andaugrnented expÍession of some oi ttrc genes cÍcoding rhese enzymes (Kauss et al.,1992a; 1993;Ka(zetal . . l998;Thulko.ndConrat l r . lggS).Inasinnlarnranner, insoybcan suspension cells, pbysiologicat conccnrEiions ofSA srrungly augmenreddeiènse gere acrivnrion, HrO2 accunr lation, and the hypemensitive recrosi$ re_sponse (HR) thar wlls induccd by trcahe0twith avi rlcnr pstudotllanas Aingacpv. gryd,n?r/ (Shirasu et al.. 1997). HoweveÍ, sirce rtre SA_neclialcd porenriAii rof defense responses in soybean cetls did not depend on prolonged p;c-íeallncDtwilh SA, this mechanism ofrcgulAlion obviousty difièÍs iionr th; li;c_dependcnrp nring ir culrrfêd parsley cells. Togerher, rhe obscrvations made wirh par;ley andsoybean suspcnsion cells revealcd thai plflnl cell cullures can be suir4ble modelsystenN lbf srudying rhe SA,INA-, and BTH-irducêd prining for porenliàledrctivoiion oí cellulal llaDl deibnse responscs.

8.2.2 Salícylic Acid. Serves a Dual Role ín íhe Activationof Deknse Responses

Whilc elucidaling tfie inftucnce ot' SA and BTH on (he adivation of dcl.cnse_relàled genês nt ihe parslcy cell crlrurc, irbecane obvious rhal lhe iDducer,s etïecron gene acLivation depcnds on rhc gene rhàlis being monirofcd (Katz cr it., 1998iThulke aDd Coffath, 1998). ODc ser oí geDes, such as those encoding anionicperoxidasc and mannitol delrydrcgenase. was tbrmd io bc direcLiy jnduced byÍelatively low conccntrarions of the rrvo SAR inducers tcsted (Krrz et a1., 19S8;Thulke and ConftÍh, 1998). A second sei of pa$tey defense related geDcs, iD_cluding ftose encoding phenylrtaDine amnronialyÀse (pAL), 4_coumarareiCoAligase, intracellular PR-10 proteins an.l à hydroxyproline rich glycoprorein, wasonly l.tirÍly responsive to tbe trearneni wirh relarively low coiceDtr;dons ot SAot BTH. Yct. alrcady à1low induceÍconcenrarions, rhese genes displayed SA, andBTH Jer denr porel IJ|or o,heÍ e{prc*ion n, l tow.ng.rerrnf l , r w h J to\^r lcr{ordo\cÍK. /er . r ' . . tuqx:Thutke,rnJConrjr t . tq,rS,t_, , r inr t r r , .c,nrorerfan

I2 Salicylic Acid Induces Systcmjc Iresislance ResNnses 169

0.5 n1molaf SA was required to activaLe PÁl. using oniy SA, whereas as tirile as0.01 mnolíu SA greally potentiàtcd the activation oirhe p,,{/. gene by an olheÍwi$eÍaintly inducing elicitor concentration (Thulkc .tnd ConrÀrh, 1998). These resulrsrevealed a dual role tor SAR indrceÍs thc acrivation ofptan! deièrse rcsponses:a dncct one in the immediare induction of cedain delense genes al higher inducerconcentrations. .tnd an indirec! one which requires only k,w doscs of rhc induc_ers to pdme for poientialcd activaLion 01 ànother class of detènse genes. As thepolcntiation by SA and BIH of both elicired PAa gcDe expressioD and coumarinsccretion strongly dcpcnded on an exrended preincubation period,ihe SAR irduc_ers are assumed to mediate à tine-depenrlenr n:sponse dla1 lihifts the ce $ on rhcaled (Kalz ct al.. 1998;ThLrlke and Conràrh, 1998). Wherherthis shiínrcludes thcproposcd syrthesis of ceilular tàctols with cmcial rolcs in the cooÍdnration andcxpression ofceil llr deferse rcsporses remained n certain.

Siuilar obse rlions ro those made in parsley hnve been rcpoÍed fbr cowpêaseedlings (Latunde-Dada and Lrcas,200l). The B rH medialed SARresponse ofcowpea is associàlcd with rapid and transient increases in (hc activity of pAL rndchaicone isomcrase followed by accelenled accumulaiion ofkievitone and phttse-ollidin phytoàlexjns in infcclcd hypocotyts. Theseresponses werenotobserysd inindlrcecl, uninooulated tiss[cs, suggesring thrt the protecrion ofcowper seedlingsby BTH is medialed viA potentiation oico.ly defènse mcchanisms (Larunde,Dadaand Luc s,200l). In cuounrber hypocoryls winh lNA-induced SAR (Fr 1h et at.,1996), .rnd in wolrded soybear tissue (CríÈam ond Craham, 1994), potentia-tion was also detecred lbr thc development of eliciiítion competency. Whelhefthe enhanccd induction of elicirlrtion compcrency is based on a similar prinringlrechaoislll 1o thc one described nbove lblpàrslcy cells is unclear

8.2.3 Actívators of SAR Induce Priming in Arabidopsisln Arubitkrysis, BTH direclly activates PR-J and pdmes fic pt.mrs fbÍ potcnli-ated PÁl genc cxpression induccd by phytopathogcnic ptcu.tomonas srringdapv.rardro (Prr) (KohlcÍ cl al., 2002). BTH-jnduced priming atso augmenls borh pÁtgene activation and cnllose deposition induced by cilhcr Drechanicalty woundingthe lcêves with forceps or irnt!|aring Ècm with warer (K)hteret aI..2002). Theseobscrvations with Árdri.loPrlr not only confi|m rhe abovc described dual delbr SAR irducers in the àcLivalion ofcelh ar planr delènse responses, they alsosuggest thal priming rnight be connnon ro sevêml signaling pàthways, mediatingcrosstalk bètween pathogen delènsc od wound or osDoric stress rcsponses (see

lntriguingly. when SAR was bjologically induced by pr€vjous iníèction of,,tzi-,id?r,r with an avirulenl suain ol Prr, there was porenlided rcrivaiion of boththe P.,lr and the PR- 1 genc rpon chêllenge tufection with virutent pr, (Camerone1al., 1999i Van Wees er al., 1999: Kohter c1!1.,2002). pdnring is thus 1iLclyto plày àn itnpoÍant fole not only in chemically induced bur also jn pathogen-activêted SAR ofplnnts. The sànlc conclusion was drawn from srudics with SA-primed transgenic lobacco plants displaying porentiatcd expression of chjmeric

170 8 S,sna!fs in PhnrResi{ance Re\Pnhes

Asp.trdgtL, olfci alis PR-I::GUS and PAL-3::GUS delense genes alter woundingor pathogcn attack (Mur eÍ al., 1996). The Atubiíloprts adfl mulanl constitutivclydjsplays enhanced rcsistance ro P,rÍ (strain DC3000) and to the fungal parhogenEistphe cicho/dcearuul (Frye and Innes,1998). Tnterestingly, edfl difers fÍomother enhanced disease resistance mutants because it shows no constitutive ex-pressid ot' PÀ- / and PR 2. alttough t anscripts of b(Íh of these genes accumulateafler patbogen à1tack. Tlris finding, and the fact that edl/ shows stronger expres,sion of delense responses. such as the HR and calose deposittun, after infectionslrongly suggest ar involvement ofEDR1 in prining. È] Ri codcs for à pulalivcmitogen-activated protein kinase kinase kinase (MAPKKK) and mediates diseascresistance via SA jnducible delènse responses (Frye et al., 2001). FuluÍe muta-tjonal approaches in Á.aáidoprtr are expected to yicld nrore genes that play a rolein plilnins.

'lhc A/abi.lopsis nprl nlttant (also known as rtnl orraii) accunrulêtes wild,type levels of SA when lÍealed with avirulent pathogens but is unablc to morntbjologically or chen caily induced SAR (Cao ct al., 1994i Delaney er al., 1995;Shah et al., 1997). lnterestinglÍ the polentiation by DTH-pdming ol bolh PrÊinduced PAa gene activation and wound- or watcr infiLaadon-induced PÁa geneexpression ard callose depositior are absenr in u/r/ (Koïler et al.. 2002). TheArabidops is ctt I

^t1d ctts mutanis, on the other hànd, which expÍess conslilurive

SAR in the rbsence of a preueahrent with SAR iDducoÍs (BowliDg et n1., 1994;1997), arc pcnnanently primed for polentialed PAt genc aclivÍrti(nr by Pí infectionand lbr augmenled PÁt gcne exprcssion and callose deposition ufon woundingoÍ water inÍiltftioD (Kohlcr ct al., 2002). Consiitutive pdmirg in .2rl rnd.lrjcould bc due lo thc expresshn of a n ltiplicity ot' defense-relatcd genes in theseplanls, or thc Acliv.rtion ofolher strcss response mechanisms bcsidcs SAR (Bochc!,tj., I998; ClÀrkc e1al.,2001), Àlthough these possibililies Ícm.ir renrote. MoreIikely, however, thc enhanced levels of S A in ópd and .Z/-5 (Bowling el rl ., L 994;1997) c,tusc apcmarently pfined (4larm) staie. Because 01' constilurive prin ing,éZrl iiDd.zr5might be abletorapidly and effectively inducc thcirvarious cellulafdeícrse mechanislns, thus leading to eDhancedresistance to pilhogens, woundirg,or watef inliltration (Kohler et al., 2002). In this context ir is notewoÍhy tharthe constitutively enhanced pathog€n rêsistnncc ol: another Á/db ópsLÍ rnrtant.cpd'2, has becn nscibed li) thc potenliítted induction of the PR -1 gcnc rponintèciion with virulcnt Ps? udomonas syrnryae s$dns (Boch er al., 1998). Thcrc isevidencc thal a rull ?drl Jlutation suppresses the disease fesistÀnoe of bolb ?//ênd.?/ó but only patially that of.?/5, indicating a difièrenl rcquir enrent of CP,Rgenes for IIDS I (ClaÍke et d., 2001). EDSI nlso likcly plays a role in primins inconnexion witlr PAD4 (Jiragc er al., 2001). Akhough boih proreins áct rpslrean1ot prthogen irduced SA accumulation, theÍ exFession car be potentiatcd bySA-prc treahnent of the plants- It has been proposcd thai EDSI is involved in"rheanplification of delàrsc rcsponses. porsilrly by associating with PAD4 (Feys et al.,2001).

The strong corehtion berween fte presence of SAR,tnd priming suppoísthe conclusion that prilning is an impoÍarr mcchanisnr for SAR in planis. This

8.3 Jaynodc Acid and l]ihylctre: Important Signals in P]art Defensc Responses t7l

rssumpnon is iurther substaDtiated by thc close corelation bcrwecn the abililyof various chemicals 1o nrduce SAR againsr bbàcco nosaic virus (IMV) in |o,bacco (Co ath cl al.. 1995) and their capabitjry to prnnc for potentiared pALcxpressior induced by eirheÍ elicilor lreatn1ent in parsley cells (KaLz cr rt., 1998jTfiulke and Conràth. 1998) or Psl inlcction, wounding, or w.t1cr infitrrario inÁr,rtloPsir phDts (Kohler er al.,2002).In addirion, in N.,tc-aansgenic lobaccoplanrs lhat are unable io establish SA-rnedialed prining. horh thc onscr ofthe HRard fte acrivation of !n rclive oxygen responsive chiíneic Aspdragus oltcitul$PR- lrrGUS rcpoÍter gere were significardy delayed whenintècred with avirulenrPr?utlonionads.The aïteruaLion of priming and the loss ofpolentirrcd producrionolactive oxygen specics were accompanied by a lack ofresisrance to the bacteria(Mur et al.. 2000). FuÍhe nore, overexpfessing the disease resisrance gene pZ5in tomato potentiates pathogen-induced detènse genccxpression lndenhanccs ltrcresistance 1() Pr/(He et a1.,20íJl). Finatly, aconrplete or parrial inrcrivarion oftheMLO prolein was shown lo pdme young barlcy scedlings fbrpolcntiatedindrclionoldcfcnsc Ícsponse! associated wilh enhànccd rcsistance againslpowdery nildcw(Buschgcs cl r l . , 1997).

8.3 Jasmo c Acid and Ethylene: Important Signalsin Plant Defense Responses

ApnÍ from SA,lhc dcfcnsc signnling molecules j0sMnric acid (JA) ond ethytcnc(ET) have àlso been implictltcd in the fegulation ofresisranoe rcsponses. Ill manyoa$os, irlèclion by microbinl pnthogcns and atXack by hcrbivofous insects wasshown |o be associated wilh cnhÀnced prod crion of rhese phyrohornoues ndconoom it^n1 activÀtion ol distinct sets o I defense-relalcd genes (De Laal (nd VanLooD, I98l ;Gundlncheral . , l992; Pei ia-Cortés er at. , 1993; Mauch er al . , 1994iRoymond el Al., 2000i Schenk elal., 2000). Conrpe ing èridence for a role of JAànd ET in discrsc resistAnce came ftom gcnctic .rualyses ofmrLants.tnd tmnsgenicplants thal Írc lrcctcd in the biosynthesis or pcrccplion oí rhesc conpounds. Inmany plnnl-pàthogcn inlcractions, JA and ET appcarcd to be involvcd in localànd/or sys€Íric induction ol defense responses.

8.3.1 Genetic EvkJence for a Role of Jasmonic Ac/tl andEthllene in Pathogen Resistance

Gerctic cv cDce of a role for JA in plant delensc cáme particularly from rnalyses ()1 A/drrlopsts mtrtanls affected jn n\e biosynlhesis of perceprion of JA.The JA-response Í1utanl .,t/ displays enhanced susceplibility to the necrotrophictungi Altemutia bntsi.icola rnd BotJtí, cincrca(Thommà ct al.. 1998), andrhebacterial soft-rot pathogen Etuinia camtovorc (Norman-Sêllcrblad et a|..2000).ADothef JA-insensiiive Ár?r;drprir mutànt../d//, allows enhànccd growth of Prrin the lcaves (Pieterseerê1.. 1998). Thcse nndings dernonsrrare thàlJA dependenrdefense rcsponses contribute to Èe basal resistancc of Ár.róiloprir àgàtusr

1 72 8. Sismling in Plant Resistdce Responses

ditrdent Íncrobial pathoge,s. FuÍhemorc, bolhjd/ I at\óthc fad3 JidT Íaà8 Áple

murant of,4 /dáidoprir, which is deficient in the biosvnthesis oí the JA precursor

linolenic acid. exhibit susceptibility to nommlly nonpathogenic soilbome P]í,t&,i

sDD. (Staswick et al., 1998; Vijayan el al., 1998), indicàling that JA al$o plavs a

ràie nr nonhosr re ' i ' rance. A role ror lA In delen'e rgr insr herbr\orr 'U' insecr ' i '

indicated by the obscrvati onthaÍ rhe Arobi.lopsis Íad3.fd./7/dd8 nutanl exhibited

exbemely high moÍality after altack by lawae of the conmon saprophagous fun-

gal Enàr, Btudysia impatie,s (Mcconn et al., 1997) Furthermorc, a JA-delicient

tomato rnutànt, deÊl, was íound to be compromised in the wound-inducible ex-

pression of defense genes and rcsistancc lo MÍrndrca rdta làrvae (t{owe et al '

r996).The role of ET plant resistancc se€ms nore anbiguous ln sone cases. ET is

involved hdiseàscresisfance, wheLeas in other cases itis associated wilh svmptomdevelopment. For inslaDce, several ET insensitive mutants of Átzrridoptlt havebeen repoÍted lo exhib;t cnhanced susceplibility to B. cizred (Thonmà et ai.'1999). Psr (PieteÍse et al., 1998), and lt .ïIldlovord (Norman-Sette$lad et al.'2000), indicating thàt ÉT-dependenl defense respo|ses contribute to basal resjs-tance rgainst these pathogens. A sinilar phenomenon was obseNcd in tornaba d soybean mulants with rednccd sensitivity to llT. which developed morc se-

vere symptoms when inibcted by the flrngal padrogcÍts B. cinerea (Díaz et ^1.'

2OO2), Septoria gbcinea, or l?hi.ocíonia solani (HoflmaD ei al '

1999) ln addi-lion. ET-insensitive tobacoo plants tÍaosfo ncd wilh the nrutmt ET Íecepior gene

etrl frol:, Arabidopsis óisplàyed susceptibilily to the normÀlly nonprlhogenicootrlycere Pytlxíun sllvattclr?t (Knoester ct al, 1998). Thus, ET obfiously alsoplays a role in nonhost rcsistànce, In othcr citses, teduccd ET sensitivity was as-sociated with disease tolerance. For €xÀrnple, ET-inscnsidve hmato genolypes

.rllowed growlh of virule Psl ^íd

Xanthamonus cam\estrtt p\' \)ettcatorla Ír1

levels similar lo those in wild4ype lomllto plants, but dcveloped less sevcre dis-ease sylnplonN (Lundetà1.,1998;Ciardi elal.,2000) A similaf phenolncnon wasibund in theET-insensitive ein2 m$Nt ol Arabidoprir, which displaved iDcreasedtolcrance to virulent Pst an X. canpert p\. !:íh1prrrltr (BenÍ et al , 1992) ln

addition, soyirean mutants with Íeduced sensilivity to ET developed disease symp-lolns sídlar or lcss-severe than those in tbe wild type when inÍecled with thelracreriat pathogen P ry/i, gae p\. Íllycinea oÍ iJ|'e .ronyceÏe Pb'tophthota v.itte

íHolTnr.m et à1., 1999). In these interactions, ET is clearly involved in svmptdndevelonrncr)r . ÍJr | |er rhal in . l i 'eJ.e rc. icraÍce

l he dual Íole of Ë1 nr plant defensc might reflecl ils involvement in varrousphysiologic,tl processes in the plant ET plàys an inportanl tole ín scnescence(Abeles ei al.. 1992) and lesn development oÍ h)persensitively reaciing plant

iissues (Knoester ei al., 2001). Since necrohophic pathogens feed on ded cells,both tunctions of ET migbt be favonble 1br the development of diseÀse causcdby such lypcs ofpàthogens. Biolrophic pathogens, in contras!. neêd living cells tocomplete then lift cycle. Thus. the sàme functions óf clhylene mighl help to rcstrictthese types ofpàthogens. Suppor! for this hypothesis comes tiom expcdments withhypersensinvely rcàcling^rabtlrprl!plànls. On the one hand, the hypelsensitively

'8.3 Jasnonic Acid and EthyleDc: ItnloÍaÍ Sign.ls in Plant Defense Respo.ses 113

respondirg tissue wxs nore susceplible trr iDfecrion by the necrotrophic fungi B.c inerca and Scle roti,tíI1 ,'cle'Driorud, bnt, on the other hand, inl bited the grow rof biotophic parhogens (Govrin ard Levire,2000).

8.3.2 lasmonic Acid- and Ethylene-Medíated I duce(lD ek n s e s a gaí n st Pcttho g e ns

Bcsidcs lheir role in basal resistance, JA and ËT also frnclion as kDy Íeg latorsnr iÍduced dclènse responses lhat aci syslcmically to enhancc Íesisll|nce àgainstsubsequentpaibogcn rltàck. For inslancc, iffeclion ofÁ,.dridopr,r wjth the fungalpathogen Á. ,/drrictcold results ir local and sy(cmic activation of the PrF1.2gcne, encoding a plant defensin with anti-i\nrgal prcperties. Mulant analysis Íe-\realcdlhaL PDF1.2 gene expressior is regulÀted through àJA- ànd ET-dcpcndentsignaling palhway that functions independently of SA (PcnÍinckx ct à1., 1996;1998). Another cxàmple comes hom studies on the interàction betwecn the bao-terjAl pathogen É. carutot,on ànC, its host plànts tobacco and Á/dlr;dolrir. In-fection of leaves of thesc planls wi$ Zl. carorrrofd, or trealmert of the lea\]eswith eiicitors of this pathogen, activrted an SA'independert sysremic resistanceand a set of defense-rclded genes that differs fÍom thal induced upo[ exogenousapplicarion of SA (Vidal et al., 1997; Norman-Setlerblad et al., 2000). Interesr-ingly, most of fte E. catotorcru-]]I.d'rced Eenes appeared to be rcgulaled by JAand ET'

Another lypc oí JA,ET-dependcnt iDduced pàthogcn resistance js triggercd byselected $irÀiDs ofnonpathogenic ÍhizospheÍe bacleria. Slrains that were isoldedtiom nalu|?lly disease-suppÍessive soils, mainly liuotesce Pseuàomonas spp.,wefe found to promote planl growth by suppÍessing soilbo e pathogens. Thisbiologicd control activiry is etlective under field conditions (Z€hndeÍ et aI.,2001)and in commeÍcial greenhouses (t€eman et ai., 1995), and can be the result ofcompctilion lbr nutrients, sidefophorc-medialed comp€tition for iron, antibiosis.or secÍetioD oflytic erzynes (Bakker et al., 1991). Some of the biobgicrl contro Islrains reduc€ disease through r planlncdiÀled mcchanism thaiis phcnolypicrllysimilar to pathogen-induced SAR. rs l}|c induced resislàncc is systomicÀlly ic-tivated and is effective .tgainsr vdious types of paÍhogcns. This typc of induccddisedse resistance is rêfèrred to heÍe as rhizobacleria-m€dialed inducêd systiemicresisrance (ISR) (Van Loon et a1., 1998; Pieterse et al., 2002).1í Arobitlopsis,rhizobncte.ia-mediated ISR activated by Prd domon as lluorcscens WCS4ll Í

^\dPseuàomanus putidaWCS35Sr has been shown to function indepcndcDtiy ofSÀand PÀ Sene aciivnrion (Piclerse el al., 1996; Ván Wees er al., 1997). Instead,rhizobacieria-mediatcd ISR signaling requires JA ànd El becàuse Ar.rà;drpsirmutants imprircd in theii ability to respond to either of these two phytohormonesare unable to cxpÍess ISR (Pieterse et a1.. 1998i Ton et al., 2001; 2002a). The stateof rhizob.tctcrià-mediated ISR is not ody ifldependent of PR gene expression.but is àlso Íot associated with the activêtion of othef known deferse-related genes(Vàn WeÈs etal.. 1999). Upon chauenge wilh apàlhogcn, however,lSR exprcssing

174 8. Signalingin PldtResistance R€sporses

plants show enhanced expressjon of ceÍah JA- and ET-responsive genes such asA|VSP, PDF1.2, axÍl HEL (Van Wees et al., I999; Hase and pieterse. uDpublishedobscÍvàtions), suggesting that ISR expressnlg tissue is primed 1() activate specificJA- and ET-inducible genes fasteÍ and/or ro a higher level upon pathogen altack.As mentioned above, the priming phenonenon fias alÍcady been obseNed in orherprocesses in planls Íesponding ro stress signàls and is Íegarded to enhance rheplant's ability to delènd itself against differenr types of bjoric or abiotic srress(Conrath et a1.,2002).

8.3.j Prímíng of Defense Re,sponses DuringRh i zttbact e ri q - M e d i ared I SR

Although expressnrn of rhizobacteria-mediÍed ISR in Á/dá?dorrtr reouil-es aninlact response to both JA and ET (Pierenc et at.. 1998), the andvsis of locatand s)"r f ln ic le\el \ ofrhe\e pldnr honnunec rcvc!teJ rh:,r t5R j , n;r rAsocraredwith changcs in fte produclion of these signals (pieterse et a1.,2000). Tbis findinq\uggesl. rhnt l )R i . ba\eJ,rn 0n enhanrcJ senrt i \ i r ) ro rhc,e ptanr norm.neirather than on an incÍease in rheir produclidr. tf fiis is true, IsR,expressing ptrntsare pimed 1o re&t fasrer or more strongly (o JA and ET produced after p{tlhogcn

The hypothesis rhltt ISR mày be based on an enhanced sensirivirv to JA is suD_portcd hy rhe r inr l in8 rhir óc cxprer\ ion or rhe JA. induciHe genc .1ry5p $Lspotcntiai€d in lsR-expressing leavcs rfrer chêllcnge with pr/ (Van Wees et al..1999). In the same study, the exprcssioo of scvcral orber JA-Íesponsive geneswas tcstod as well. but these ihiled to show an enhar[ed cxpr€ssior lcvet in ISR-exprcssing leaves, suggesting tbat ISR in ár,a/rjdoprÀ iÍi associaled with Doxenti_i l ion , ' Í r specir ic sct of Iqrespon"r!È tenes. l rotenrial i . , I . ) t í leten"c rc, fonsesby JA has b€en rcporred inother sysrems as well. FoÍ instánce, Dre{catlrrenl wirhmclhyljrsmollale potentiates thc clicitation oi various phenylpfop&noid defenserespoDses in parslcy s r$pen sion cell cu lrures (Kauss er at., I 992b) and Drinles thêmÍor(nluncedin,hcrr , ,nofrhees' lyo\ iJ.ru\ebuf. | |Krus\crat . t roa; M^reoveÍ,JA potentiates thc expression ofthe PR-1 gcnc in Íicc and the tcvcl oíresislanceÀE|irsÍ Maqnuparthc gtis"a induoed by tow doses ot INA (Schwcizer et al.. 1997).

'lhe mlc of ethylene nr priming is lnorc complcx. After lrc hnenr wirh a sa!.umting dose of I millinolar of the elhylene pi:,cursor t -anrinocyclopÍopane, I _c,uàoxylate (ACC), IsR-expressing planrs emir signiticanrly more elhylcne thanAcc-treated conuolplants (Pielêl.se ctr1..2000). Evidenrly, rhe capàciry Lo conveÍACC t{) erhylcnc is increased in IsR-expÍessing ptants. Berarse ft infected tis,sues. ACC tevels rapidly increase as a resrllt of pathogen-induced ACC synrháscêctivily, thc enhanccd Acc-converLing capaciry of IsR,expressing plànts likelypdn1cs the plant for a fasrer or grcater prodxcrion of elhytene upon parhogen êt-tack. h Pr. iniècted Árari./.?.r,r ptanrs induced for ISR, rhe plo.lucrior of ET wasirdecd enlranced dudng the first 24 horlls after inl'cction compared ro uninduccdplanls (Hrse andPiele e, unpubtislrcd observalhu). tnrerestingly, exogcnous ap-plication of ACC has treen sholvn ro jnduce resistance agiinst Is, tu,4/aói./orrir

8.1 Sr steDim: Peptide Signdls in fte SIsretuic WoundRcsponsc 175

(Pieterse et al.. 1998). Thcrefore. .L faster or ererter producrior of ET in rhc nritial phase of infèction migirt contribure b the cDhanccd resistance againsr thispathogen

8.4 Systemins: Peptide Signals in The SystemicWound Response

In the errly 1970s, Green rndRyàn (1972) obseNed an accumulàtionotproteinasehhibirors (Pls) in 1onàto and potato plants after herbivore hduced or ncchanicalwounding in bolb the irjured leaves and undxmaged paÉs ol the plants. lr rhislàndnrr* study, Green and Ryan (1972) suggested rhis systemic reaction ro bean inducjble defense response dircclcd against herbivorous insects.Itis now cieaÍtbat the syslemic wound response js not limited io prolcinrse inhibirors bul ratherircludes a large nunbeÍ oiprlÍeins which may contib lo, direcily or indirectly,to efiarced insect resislanco in nany plant species (ConsrÀbel. 1999; Reymondet al.. 2000i Ryan, 2000i Wírlling, 2000). The wornd Íesponse in the Srftrdcer"atimcted consideÍablc rXtentior over the past 30 years aDd has developcd inro .rmoclel system ol bng'distance signaling in plrnts. Much efibrr has bccn dcvotodto the ideÍrlilication ofa hypothelical wonnd signal thal is gcnerêtcd at the site ofiniury, transmiltcd thfooghout the acrirl parts of the planr, and oApablc of ind cirrgthe exprcssiur of defense genes in undàmAgcd tissues. PhysicAl slin li such ashydraulic waves thnt result frcn the rclease of xylcm tension upor wounding oractionaodva alior potcntids have been inplica|ed iD the wo nd signal transduc-xion process, as well as cbcmical rignaling moleculcs including JA, ET, abscisicacid, oligogalaciuronides (OCAs), andsystemins. Tlre rctivity of these signals andfteir contfibution 10 long-dislancc s ignrl trímsduction has bccn coveredin severalreviews (Schaller and Ryan, 1995;Bowlcs, 1998; Ryan, 2000i de Bruxelles ondRobefts, 2001; León el al., 2001) and js .rlso discussed by Korth and ]'honrp-son (this volu|ne). This section will il1slead locus on systemins, d]eir discovery,nclivily. and signàling properties.

8.4. I Syuemins in Diflcrenr Plant STecir sThe sysbnnc wound rcspoDsc of tonrato phrts is charactcrizcd by ihe àccumu-lation of a large number of dofcnsc proteins (systemic wound rcsponse pKÍeins,SWRP9 (Ryan, 2000). A search lor thê hypotheticêl signàling molcctrle(s) thrrxllows Lomàto plàlls to respond systemically to à lócrl stimulus (i.e., wounding),led to the iílenlilicátion of$e n|stplantpeptide with a signaling function in 1991(Pearce et al., 1991;Ryàn, 1992). A l8-amino-acid pêptide wís isolared from rheleaves oí romato plants oD the básis ofits abilityto indxce thc cxpression ofSWRPSusing a sensitive bioassay. Thc peptide was Damed "systenin" to emphasize itscentral role as ar inducing compound and the systemic naturÈ of thc rcsponse(Pearce et al., l99l). Based on the syslemin rmnlo acid sequence, the CDNA andgenc of prosystcnrin were cloned. and found to encode a sysrenin precursor of

] /6 8. Signaling in Pla.tRosjstarce Resporses

200 amino acids (Mccurl and Ryan, I992i Mccurl et À1., 1992). The slslenrinsequence is 1èrmd close to the C-telminus of rhe precwor Therc is a single genclbr prosystenin m lhc haploid romato genone from which two difièrenr polypeptides are dcrived by diffcrential splicing of the pre-mRNA. The polynorphism islocated in the nonsyslenir poÍion of the polypeprides a|d does nor seem to allècitheir wound signaling propeties (I-i and Howe, 2001). Highly sinilar prosys-iemins have been identiÍied in closely related plànt species (potrto. belt pepper,ànd black nighlshade) exhibiring 73 88 % identiry wiih the tomalo scqucnc€, btrtnot outside the family of Soldn.rcea? (Constabel er al., 1998). Honology,bascdapproaches failed to identify prosystemin in the more dislantly retated tobacco.A search for tobacco signding molecules funclionally retà(cd to tomaro sysieminidentiGed two l8-an1ino-acid peptide induceÍs of PI synthesis in tobacco leaves(Pcàrce et ai.,2001). The 1wo pepiides are derived from a singtc F€cuNorprcteinoI 165 anrino rcids. The prccursor. of the tobacco systenrins is not homobsousto the Eeviously identified prosys(cnrins fro'n other Sblafta.?íe bu1 conhnrs sc,quence motifi presenr àlso in hydroxyprohrerich cell waltgtycoproteins (pearceet al., 2001). Likewisc, bbacco systemins themselves bcar no structurat similar-jty 1() tonlato syÍemin- Therefore, systemins.re now considered to represerr aslíoctu|àlly diverce gro p olpolypeprides that àro produced in injr.ed plauts andfuncli('l as signaling nrolccules in the activation of delènse genes (penrce et al.,2001). Syste icresponsesto herbivore attack have been documentcd in moíethal00 plaot species (Kartan ard BAldwin, 1997).I1willbe intercstug ro scc whichpÍoteirs cxcd syÍcmir f-unction iD thescplants ond whcthefor not lirÍhcr disrinctprcleins hnvc cvolved 1() perlbrm systcnrin\ signaling trnclion. In the lbllowilgdiscussion oi syslcnrin aclivity aDd sigraling we will fbcus on the propcrlics 01,the lomato peptidc. fresenlly dre only onc tlml has beeD tboroughly invesligdtcd.

8.4.2 The Attiviry ol Tomato SysreninÀwcdth ofphysiological data poirÍ towaÍd arólelofsyslemin as a signal nr(, teculenr thc wound sigll.Ll lransduction pathway iÍ lonrato plants. ln addiln 1o,tw?pgcne expression, the synihetic tonalo pcpride rriggers physiologicat reactions lharare chrracterisdc 1() thc wound response. Changes in plasma lnclnbmne pelme-abiliiy aÍe ànroDg dre earliest cellular responses to lre.ttnenl wirh sysremin andoligogàlàcturnide eLicirors of the wound rcsponsc. The idlDx ol calcirn rndprolons ànd the efl1ux of polassirn ánd chlo de ions lead ro an incrcasc thccybplasmic free calcium conccn(ration, iDtracellular acidiÍication, dcpolaizationof the plasmn men$tànc, and alkalinization of the apoplast (Fclix and Botler.t995t Thanr eLal., 1995i Moyenand Johannes, 1996t Moyenelat.. 1998: Scha er.1998). These early events árc csscntirlly indislinguishable frolrl those lriggcrcdin plant cells afieÍ parbogcn recognition or cliciraiion (Conrath er xl., l99t: Ebelnnd Mithófèr, 1998; Scheel, 1998; Katz et al., 2002). In borh wound ênd pathogendetènse responses. these ion fluxes were shown 10 be neccssary and sulïcienríbr the strbsequent activation of dclcnsc gencs (Fukudà, 1996i Jabs et al.. 1997iSchallef and Oecking, 1999: Blume et a1..2000; Sch.riler and Fr.$son,200l).

8.4 Systemins: Peptide Signals in The Systemic Wound Response I7'7

Both woundins ànd slstemin stinulate the accumulation of calnoduln as wellas of polygalacMonase. phospholipêse, and protein kinase activities which mayall contribute to the transducrion ol the wound signal in tonaro (Conconi er al.,1996;Stankovic àndDavies, 1997; Stratmam and Ryan, 199?;Beqey and Ryan.1999; Bergey et al., 1999; NaÍváez-Vásquez et al., 1999: Chico er.il., 2002) andother planr species (e.9., seo età1., 1995;Vian e1xl., 1996i I-€e et aL., 1997; Roioe1à1., 1998; Seo et al., 1999: Dhondl €t al., 2000i Jonak et a1.,2000; Wang er al..2000i Isbigurc et al., 2001). Both wounding and sysremin stimulate the synlhesisand trarsient accunulation of JA (Pena-CoÍés et a1., 1993;Doárcs et a1.. 1995à).arolher inducer of defense gene exFession (Farmer and Ryan, 1990; F'aÍncr et al.,i991). This finding places thc ociadecanoid palhway for JA biosynthesis downslrean o[ bolh wounding and systemin in the signaling pan\way that ]eads to theexpression of wound-responsive genes (Farner and Ryan, 1992). Consislently, arapid and transient induction of JA biosynthetic enzymes is observed nfter wound-irg or systemin teatment and is lbllowed by a delayed and more suslained in-duction of SWRPS wift a diÍect role in detering insect herbivores (Ryan, 2000iStrassner el a1., 2002). The production of ET is triggered by wouding and sys-temin treatment (Felix and Boller, 1995;O'Donnell eial., 1996), and both ET andJA were shown 1o be required for SWRP gene activation (O'Donnell et al., 1996).Firaily, a local and systemic pÍoduction of HzO2 was observed in tomato planisupon wounding and systemin lrea1ment rd was $hown to depend on a llnctionaloct8decmoid pathway. Hence, a role for HrO, as a second messenger downstreamoI JA was pÍoposed (Orozco-Cardenas and Ryan, 1999; Ororco-Cáfdenas, 2000).

8.4.3 The Role ofTonato Systemín in WoundSígnal Transductíon

The aclivities elucidared for tomato sysiemin are essentially consistent with amodel of wound signàling originally pÍoposed by Farmer l|nd Ryrm (1992). Ac-coÍding to this model, systemin is released fÍom prosystemin às a consequenceof wounding, translocated throughout the aeriêl parls of the plant, and then interacts with a ccll-sufface receptor in the target tissue. This inleraction resultsjn tbe activation of a lipase, which release, linolenic acid frorn membrane lipidsto serve as a substrate o[ thc octadecànoid pilhway for the bjosynthesis of JAwhich, in lum, àclivales defênse genes (Farmer and Ryan, 1992). The modelwas lalêr reÍined to accouni lbr the requirement of BT for SW.I?P gene activa-tion (O'Donnell et al., 1996), the defense signaling activity of oxylipins other thanJA (Stintzi et al.. 2(}{)l), the action ofH2O2 as a second messengeÍ downstream ofJA (Orozoo Cárdenàs, 2000), ànd Lhe involvemenl of ion fluxes across the plasmamembrane ànd reversiblê Folein phosphorylàtion in wound signaling (Schaller,1999; Ryàn,2000: Schaller,2001). lmportant suppoÍt for this nodel includes thechàÍàcterization of a cel-suÍfàce binding site fbr systemin erhibiting charnclcr'istics of a tunciionêl systemin receptor (Meindl et al., 1998; Scheer and Ryan,1999: Stratmann et al., 2000i Scheer and Ryan, 2002). as well as data derived Èomthe analysis of transgenic and mutànl tomato plants. Transgenic tonato plants

178 8. Sigraling in Pldt Rcsistancc Rcslorses

in which the expression of Fosyslenin was supplrssed by the antisense RNAte€hnology werc impaired in both the wound-induced accumlation of PIs andrcsistance b insect laffae demonstrating àn absolute rcquirement of prosysteminlbr the aclivarion of the wound response in tomato plants (MccuÍl et al., I992;Orozco-Carden$ et al., I 993). ln a converse manner, constilrtive accumrlàtion ofSWRPS was obserled ft tomato plarts overexpressing Fosystenin under controlof the conslilutive CaMV 35S promoter (McGu et al.. 1994). Exrragenic sup-pressoÍs of the .l5sr?rí,r)srediz-mediàted SWRP accLmularion were identifiedand chancterized, demonstrating that woundirg and systennr induce defense geneexpression through a cormnon signaling pathw.ry (Howe el al., 1996; Howe àndRyan, I 999). S urprisnrgly, when ectopically cxpressed. prosystemin appeàrs 1() besumcienl1() lriggcr defense gene activation and, thus, wounding is no longer rc-quircd. In prosyslenrnr'overexprcssirg plants, untnnely processing ofprosysleminmay occur or the eclopic cxpíession of prosystemin cven aueviates Íre need lorprocessi.g, as 1ull-length prosystemin was írown to be as active as systemin inthe inducrion of JWnP gene expression whcn srpplied ro lomnto planrs via thctÍ{nspiÍrli{ slream (DoDbrowski et al., 1999; Vetsch er a1., 2000). Cra ing ex-pernnsnts wcfe ped(rned using 35s..rpruryríe,??ir-expressing plants as the roolstock and wild-typc lolnato as the scior SWRPS worc found to accumulale in thescion. denonstraling dral the overexpression ofpÍosystenrin is sufÍicienr to gener-ate à graft-transmissiblc signal for defense gene acrivnlion. Similarly. addition ofsystemin orprosystenin to wound sitcs on leaves ol prcsystcnlilr mtisense planrscaused,Sl44?P gene activation in the distrl unwolrnded ieÀves (Donrbrcw$ki er al.,1999). These obseryalions arc consistent with systemin irsell bciDg lhe mobilcsignal. (Pro)systemin-induced syrthcsis of another! às yet lrnidentiÍied signAlingmolecllle, however, cannot be exchdcd.

A micrcaÍray compfisirg 235 cDNAs w.rs used to analyze the rel live chêngesin geoe expression in wounded and distàI, unwornded leaves oÍ krn:rto plants.While transcripts fbr SWRPS with diÍcctdclcnse function (i.e., the "lêtc" defcnsegenes, e.9., those fbr Pls; Ryan, 2000) acc mulated to hlgh ievels in bolh lissues,the coordimle indrction of genes foÍ octadccanoid paihway enzlnes dcdicatedto JA biosynthesis ("early" dclènsc gencs; Ryan. 2000) was obscrvcd loc.rlly butnot syslemically (StrassDer cla1..2002). lD this study, JÀ nDd ils precu|.sor 12-oxophytodicnoic acid accumulated iD ihe damflged, bLrl nor in distal, leaves ofwornded plants (Strussner et al., 2002) which is consislenl with previous repoÍsoflin1iLed syslenricJA accunutation(Bowles, 1998i Rotocl nl., 1999;Zieglereral.,2001). Hence, synthesis rnd accunulàlion of JA nr systemic leaves do noL secmto be required for defensc gcne rclivation. However. this does no! nccessxrilyÍnply rhat systcnic SW]?P gene activation. as suggèsted by Bowles (1998), isJA independcnt: A recent study showed thal sysLenic wound signaling requiÍesthc capaciLy to synthesize JÀ in Èc woundcd leaf, whereas Èe abiliLy 1() percciveJA is feqrired in the sysLcmic leaves. Elegart grafting expeÍincnts were perfo nedusirg tomato Irlulánls thar eirher fail to synáesize (.?r 2t Howe and Àyan, 1999)or perceivc (idi 1 i Li er À1., 2001) rhe JA signal. When grafted plants were woxndedbetorv the graftiunction. activation of thc wóund response in the scion deDended

8.5 ll -ADinobutync A.id Aorivarcs Resislance licslonses r79

on the abiljty to perceive JA. Wound or (pro)sysleÍnnr ird ced acÍvalion of theJA biosyndË1ic pathway, on the other hÀnd, was rectuired in rhe lower parl oftlre plant fbr the genoation of a gral't transmissible signal, bu1 rot for delènsegene rcrivadon in the scion (Li e1a1.,2002). The dala srygest that the aclivirloI (pro)systemin is requiÍed jn lhe wounded leaf to promote the pÍoduction of asysren c signal, possj bly JA or anolher ocradccanoid-derived nrotccu le. Therelbre,the nodel oÍ wound signaling origiually p.oposed by Fanner and Ryan ( 1992) nr.tydcscribe locnl rafief than systenic wound sigDal trdnsdrctron events. Thirry yeàrsafrer rhe initial report on thc phenomenon (creen and Ryaq 1972), rhc idendty ofthe systemic signal moiecule in thc wounrl response of planrs is srill unclear.

AnotheÍ lcvet of complexity is added by the cell-lypc,spccific expression oïgcncs involved in the wound responsc, which is ceÍainly highly relevant foÍthe processes learling to Lroth local and sysrenic activation of delensc genes."Early genes". i.e., thoscr.pidlyiffluccd afterwounding, ircludinglhoseencodirgprosystenin and solnc ofthe JA biosyntbetio enzymes, à.c expÍesscd in vasculalbundles (Jacinto ei à1., I 997 i Kubigsrelrig et al.. 1999; Hause et àt., 2000), ivhereas''late genes', i.e-, thosc forSWRPS wirh à diÍeot role in plnntd€tense, areexpressedin palisade and adj.rcenl sporgy mesophyllcells (ShumwrLy et al.! 1976i Walker-Simmons .rnd Rylllr, 1977i Ryan. 2000). The tempoÍally aod spatially separaredexpression oflhe two classes ol gone$ led to the suggcstion thar wound-signalingevcrlsn y initiallybe activatcd in thevascularbundlcs to produce second messel]-gers Octrdco.rnoids, OGAS. HrOr) that will then induce delènse gene expressionin mesophyll cclls (Orozco-Cárdenas, 2000; Ryan, 2000). Some of 1he secondmessengers nlny cxeÍt theireffècts over long disrances and conlribure 10 systeDricsignal íarNducrion.

F0Íher work is nccded to precisely unde$tand syslemin Íction nd ttnciionin tomàto plants. Obviously, rhcse shdies will bave k) be ext€nded to other plmrryecies, particlrlaÍly to Á/4rjílr1rrl.Í. The plethora of signaling mnlants vailableir Arabidopsit wlll bÊ vseiul 10 advance o r undersl nding of the complcxilyof wound signal trÀnsdxclion às wcll as the interaction ol lhc systemin signáltrànsduction prlhw.ry wiih other delÈnse sigll.rling palhways (see bclow).

8.5 B-Aminobutyric Acid Activates Resistance Responses

i3 Alninobulyric acid (llABA) is a nonplolc arnino acid, which is only rárelylbund in nature. BABÀ hrs been described as part oI a snrall, g-kjlodalron Foleinaceous inhibitor of tÍypstu an.l nicrubiêl serine proteinascs isolated tionl y"fí;rld

tseutlotuhe rculo, is (B\rÍseva and Kofanova. 1996). ln addilion, BABA w.rs foundnr root cxudntes oí tomato plants grown in solarized soil (Camlicl ard Katdn,1992). DespiLe ils mre occurrence, BABA is nn i eresting conlpóund. This isbêcàtrse oI its close strLcnual similaÍity 1() à highly bioactive subsnnce, thencuÍ!transmitteÍ GÀBA, wlrose Dêtural occurreÍce is wcll documented in plants (ShclperaL, 1999). Also, BABA is a potent inducer of àcqui'ed disease rcsistance (Jakàbe! ê1.. 2001). Applied as eilhcr a soil dfench or lblinr sprày, BABA has a hoad

180 8. Sismling in Plant Resitrancè Responses

spe.trum of activity agàinst viruses, bacteÍia, oomycetes, fungi, and nemalodes(Jakab et al., 2001). This wide range of activity sxpports a role for BABA as aninducer olacquncd disease resistance. especially since the substance was shownnor to be directly toxic to microorganisms Geviewed by Jal(ab et al., 2001). AsBABA is highly water soluble it is rcadily taken up by plani roots and lhen dis-tdbuted tlfouglout the plànt (Cohen and Gisi, 1994; Jakab et a1.. 2001).

8. 5. 1 S-Amin<tbutyric Acid-Induced. Priming

Depending on the mefiod of àpplication, mild phylotoxic effects of BABA lravcbeen observed. BABA has been spnyed on leaves, iniected inlo slcms ofplanls,sÍpplied via petiole dip, or applied as a soil drench to the root system. when appliedas a lbliar spray to tobacco plaDts, BABA, and to a lesseÍ exient oí-aminobutyricac.d. DUt not CABA. sere phl l , ' ro\ ic:rr u concerur l ion o. l0t , Lrg Inl-r ,cr.I m'nolnr) (CoheÍ, 1994). Small nccrolic lcsiols stnded to fonn on h ealed leàvcstwo days alteÍ spÍaying. A rapid induclion of necrolic lesions in tobacco was àlsoobserved by SiegÍisr et al. (2000) afier tbliar trearmenl wilh l0 mmolar BABA.Localizcd necrosis was accompanied by the lbrmation oI reaclive oxygen species,lipid pcLoxidation. callose deposition around the lesions, and nn increÁse in theSA contcnl olthe lcaves (Siegrisl et al.,2000). No such ellects wcre observed irplants lreÍted widr GABA. even a! concentmdons as high as 2000 Ég nl-'(ca.20 mmolar) (Coben, i994; Siegrist et al., 2000)

IB Arubidopsis,spt^yingBABA onk) lcÀvcs Al$o lcads to the formrtion ol'smAllrecrolic lesjons and to an accumulation oí P.R gonc transcripts, with a pnltom thniis similafto the oneobserved whcn SA is used to induoc rcsistrnce. Howcvcr. whcnsupplied vialhe roolsystem, BABA concentrations suíncicntto induce resistrroc.do noi induce defense geneexpression in /rariír"Íir (Znnmcrli et r1.,2000). Thisobservation suggesis thrt the indusli{)n of rcsistancc by BABA i Arubidopsílis not primarily based on a prcvious àccuumlati()r ol dcíensc genc transcripts.Rather, an addiiional nrechanisn of resislancc irduoti{ seerns 1o be prcsent inB AB A,-ÍrcÁed Arabidopsí\ plants. This conclusion is supported by the observationthat BABA induces resistance against the oomyceÍe PetDnoVJan parcsicita irwild-type Á.arlldprir plants as weli as in plants that are impaired in defensegene êxprcssion (Zinmerli et al., 2000), such as the nprl, jarl, or ettl m\tÍafis(B lcckcr cl al., I 988 i Sràswick et à1., 1992; Cao cl ai., 1994), and NdrG rransgenicAfarraolrir plants (Dela.cy ct à1.. 1994). ln this case, resislancc is indcpendent()1 lhc presence of SA and P,R or otber dclbnse gene àclivatión. Common to theBABA mediated deferse nechanism ot servcd lhc diíferent mutart ,$d !fildtype plants is a more ràpid and stronger deposition of callose-containing papillaeal the site of infecrion by P parasititd (Zitnrr,e et al., 2000). BABÁ primesAruhidopsi! ro effe.tiyely rcàLt to P pansitica itection wilh pnpillae dcposition,thus rïaking fuÍher defense responses obsolete since ingress by P pdldrtricd hasrlrcady been stopped ar this point. lnterestingly. a sinilar observation was nadewith ,VaáG tobacco chàlle.gcd v,,ith downy mildew: fiere was no difference in theprotection by BABA berween NaÀ6 itnd wild lypc pilnls (Cohcn cr à1., 2000). Ir is

3.6 Crc$-T. | [ BÍuccn sLetr i l ingPith$i)s l8 l

probablethn!also rD this case pfinring for polenliàled induclion ol S^-nrdcpcndcntdelense mechanisns is responsible for the observod prolection.

When BABA-pl eteated Ámtidolrir plants are chÀUcnged with a virulert sÍairof Prr. prjming becomes appàrcn L as à strong potendarion of PR- 1 gene cj(pÍcssion(Zirnmedi etal.,2000). lr this case, the indLrclion kinctics are vcry snnilar !o tholeobseÍved in response to aviruient zrr (Zilnmerii et al., 2000). lr the interactionbetween.,lr.1óido/rir rnd Prt, pÍiming by BABA is dependent on an idact SAsignaling pathway, b|Í indeperdent on a lunctnnring JA,ET pathwry as evidcnlfiom experiments \ri$ the same defensc rcsponsc mulants as dcscibed above(Zinnnerli e1al., 2000). Interestingly, ln theÁrdri.Jopr;r ,. cirer€a i eraction. iti! PR 1 thàt agrin sbows stongly poleniiated expression (Zimnedi et ai., 2001)ard not PDFJ.2 (l}lollxna e! al.. 1998) iral is.ommonly thoughl loplay a Íolc indelènse against B. cin.rr.eí.

In contast io other inducers of SAR, snch as SA or BTH (tuhler et al., 2002),BABA itselïdoes not induce PR genc oxpression (Zinnnefli et al.,2000). UsingBABA, il is possible lherelbre to cleAfly separaie priming and defense gere ac,tiv:rlion. Thjs will grcally ilcililatc the futrue analysi$ of priming phenomena in

8.6 Cross-Talk Between Signaling Pathways

Over the past yeam, evidence has acclrmr ated indicating rhAt rhe SA-, JA-, U1'-,and syslenin-dependent deLènse palhways cao afLèct each orher, cither positivelyor negatively. Allhough the obscrvcd prthway inleractions vary between speciesancl lhe type ol rttAoker used, i1 is beoonring hrcrcasingly cleaÍ tlr0t cÍoss-tnlkbetween $igoaling prthways is ill]portrDt ior the plant to fine-tune its delense re-sponses. Fbr €xrmplc, JA Ilnd El havc beeD shown to êct synergislically in therctivatior oí gencs encoding delcnsc-rclatcd plànl proteins, such lls Pls and de-icusins (O'DoDncll c1 al., 199ó; Pcnninckx el al., I998). Moreovcr, JA And tj l' h.ivebccn shown 10 suppoÍt the action of SA resulting inenhanced PÀ gcnc cxprcssion(Lawron er al., 1994; Xu et al., 1994; Schweizer et al., 1997). on ràc olher hand,SA, lNA, àndBTH suppress JA-dependentdetènse gene expression (Doheíyetà1.,1988; Peíê-Cortés et al., 1993; Bowling et nl., 1997;Niki et a1., 1998r Fidanlsefet al.. 1999i Van Wees et al.. l9S9). possibly Lhrougb inhibition ofJAbiosynthesisand action eena-Cortés et al., 1993; Doarcs et à1., 1995b; Harms et al.. 1998).Corsisrcnl wilh this, PÍesb et al. (1999) demonslrated Lhàr TMV infccted ro-bÀcco plants displnying SAR are unable to express noÍnlai JA-medircd wound re-sponses, plobably due to inljbitionofJA signaling by nrcreased SA levels resultingtiom the TMV infèction. Also, in thc,4rdrtdoprtr !sl2 mutanl rhe SA-dependentsignaling pathway is conslitutively aclivaLod. \i/hi Lc lA-dependen! sigDaling is sup-pressed (Kachroo et al., 2001). ConvcrsclÍ in palhogen-inocuLated Nard planls,wlicl are unable to àccumtrlale significa t SA levels, cxpr€ssrcn of the JA,ETresponsivc dcfcnsin gene PDF].2 was at least twoÍbld highcr thàn in wild lypeplanls (Penninckx et al.. 1996). Inhibjtory effects of sêlicylates on ET biosynthesis

lla2 8. Signaling in Plant Resistance Rèslonses

have also been rcported (rcviewed by Shah and Klessis, 1999). Thus, activaling

the SA pêthway confers resistance to a broad spechlm of microbial pall1ogens

but. ar the sane timc, may have detrimental effects on the JA/GTdependcnl signai

trànsduction mechanism that confeN rcsistarce agairst insccls and ccfain groups

of pathogens.An additional levei of nntagonistic rcgrlation of wound- and palhogen-induced

defense responses is provided by lhe prolon eleclrochemical gÍadieni across theplasma membrane. In tomato and tobacco plants, activation of the plasma men1-bráne Hr- ATPase by the tungal toxin fusicoccin (FC) induces the accumulationof both basic and acidic PR proteins (Fukuda. 1996; Roberts md Bowies, 1999:Schallcr and Oecking, 1999i Frick nnd Schrller 2002). Also, exprcssion ofa bac-terial FotoD pump induced a lesion mimic plrcnotype, activated muhiple defensercsponses, and ircreNed the r€sistmcc 10 midobial pathogens in transgenic tGbacco andpotatoplanls (Mitdere1al.. 1995i Abad etal., 1997; Riz.hsky andMittlcr,200I ). Ir .ddilion 10 activating pa$ogen delènse responses, fte hyperpolarizationof tho plasma membrane by Fc{rcahnent resulted in .r supprcssion of wound-,sysrcrin-, OGA-, and JA"induced JWÀP gcns sxprission (DoheÍy and Bowles,1990: Schaler, 1999; Frick and Schallor, 2002). Bolh lhe aclivation ofpathogenrcsponse genes and the represshn of wound-induced genes by Fc werc shownro be at least paÍly independonl of SA, as they (i) weÍe incompatibie with thctiming of Fc-ind ccd SA accunulation in tomato leaves. a d (ii) occ rl cd undcrconditions of inbibitcd SA biosynthesis (Schaller et ai., 2000). Furthe norc, FCinduosdPl? gene expression in Nír, O tobacco and tomalophnt$, i.o. plants urablero Aocunn alc signilicant amoullls ofsA (sohÀller st A].,2000;Friok ard schaller,2002).

while rclivrlion oJ the H+'ATPase induced Pft gene cxprcssion ànd SWRPgene sutrcssion. inhibitors of tl1e plasma lnembrane Hr-ATPl|"tc rclivity andionophorcs thnl dissipale the proton electlochemical gràdient induccd SWRPgenes in ton]à1o (Schaller and Oecking, 1999i Schaller and Fliisson. 2001).Octadec.rnoid-dcpendent signÍrli g wÀs írlsotrigger€d by thc iur-channcl-ibrminSpeptjde alamcthich (EngetbeÍh et al., 2001), and, rnorc gcncrally, a role lor thepore-forming prcpc4jes ofelicitoÍs in ihe induction of deferse rcspoDscs hàs beendiscussed (KlÍsenerand Wdlcr 1999). Apparently, wound and pathogen dcfcnsÈsignàling pàthways rc diflcrcnliàlly allècled by changes in the proton electÍ'chenical gndient. Therefore, the plasma membrane H+-ATPase may act as aswitch activàting either wound or pathogcD dcfcnse rcsponses.

Scvcul sl dies hxve pÍovided evidence lor tradc o1Is belwecn SA-dependentpathogen resis!àncc md JA-dependent irsect rcsist.noe, indicàting that the activa-rion of apêÍicular defensc nrccb.mism can Íeduce lhe €sjstance to ceÍanr groupsofpathogens oÍ herbivorous insects. Forntstàncc, Moran (1998) demonsirated th.t!SAR in cucuÍrber agàinst CoLLetotrit h wn orbicularc was associaled wilh reducedresistance agáirst icedirrgby spotted cxcumberbeedes(Diabrotica ut|tucíntunc'tata hoh,aftti) ànd enhrnced reproduclion of melon aphids íÁplir sorrytt). As"nilêr phenomcDon was observed by Prcslon cL rl. (1999) who denonstratedthal TMv-in1èctcd tobacco plants induced for SAR displ,ty higlrcr scnsitility to

E.7 Lun.!m,r1r. A ' i \n,on ^t Indufc ' l Ob.óe Re i . r rn.e Mcc[ | : 0. 183

tobacco homworm (Mand&ca r...t,a) grazing when compared wilh onirducedcortrol plarts. Furthermore, it has been shown fia1 transgenic tobacco planrs withreduced SA levels, causcd by silencnrg of the PÀl gene, cxhibir reduccd SARagajnsf TMV but enhanced herbivore induced resistance ro Heliothit rircscenslarvae (Felton elal., 1999). In a conveffe manner, PÁt{verexpressing tobaccodisplays a shong reductioD oÍ herbivore-induced insect

'esistance, while TMV-

induced SAR was enhanced in these plants.Tlre SAR inducer BTH has in some cases À1so been shown 1() red ce insect

resistance. Exogenons appljcation of BTH to tomato plants enhanced lhe level ofrcsisiance against Prr, but inproved the suitability of lomato 1bÍ f€eding by leafchewinglarvae ofÉe corn eal.worll,(Hetícowrya zea) (Stor'le1aI., 1999). A similarpheDomcnon wàs observed by Thaler et ai. (1999) who repoted comFomisedrcsistarce to the beet armyworm(Spodopteru exigua) upon applicalion of BTH toIield-gro\vn lomato plànls. In most cases, the rcduced insect resistance of SAR-exFessing plants oould bc àttribuled to the inhibition of JA productior by eitherBTH or increased SA levels.

8.7 Concomitant Activation of Induced DiseaseResistance Mechanisms

Though negAtivc interacrions between the SA- and JA/BT-dependent signd trans-duction pathwáys have clearly been shown, oiher strdiss rrguc ngdnst such anegative relêlionship. A genetic scre€n for ihe isolation of,4ríridoprtr signoltransductioD mutants that constitutively cxpress tbc JA/ET-responsive 71H12. J geneyiêlded two mutants. which showedconcomitrnt induolion ofboih lhe SA- and theJA-depcndent signaling pathways (Hi\rertet rl.,2001). The íinding that some genetrrDscripts whichincrease ti et A. brcssicicolailltecrion of,4rÍ*iilo/rrir leaves alsoacoumulate Lrpon trealÍen! wiih SA, JA, and ET, also points to 40 overlAp of thediffbrent signaling pathways, al leasr in A/'dbldaprl.i (Schent et aI.,2000).In lhiscontext, jt is woÍhwhilê to mention that apre-treÀhent with syíemir was shownto prime tómib cell suspênsion cultures for Augmented induction of the HrO,burst induoed by the àddition ofOGAS or water (Stennis et il.. 1998). In a similArmanner, preincubaling cultured parsley cells witb JA polenlialed l}le subsequeDtactivalion oI phenylpropanoid dcfensc rcsponscs by a P rojdr cell wall elicitor(Kauss elal., 1992b). Also, p nnng Á.artloëir plants with BTH (Kohler et al.,2002) or BABA (Jakàb et r1.,2001) enlanced the subsequent indnction of deÍenseresponses agairst biotic and abiotjc stresses. Thus, priln g lilcly represents amolecular mcchàÍism aÍ which the system . JA/ET. BABA, and SA signaling

Fêilure 1() demonstmte a negalive relalionship between signaling mechanisnswas also reported on the level oipàthogen or insect ÍesistaDce. For instêDcc, iÍ-oculaling lower leaves ol tobncco plants with TMV does not affect the growthof tobacco aphid (M)r,s

"i.ottande) populations (Ajlan and Potlêr, 1992). In a

similar manner, thcre is no negative effect of BTH applicalion on the population

184 8. Sigml ing in Pldt Resistànce Responsès

growth ofwhiteflies (R"' ia alsentifulii) andleaÍminers (Zi.ioft)za spp.) (Inbalet al., 1998). lnteresringly. Stout et al. (1999) have demonslralod thdt jnoculàtion

of tomato leavcs with Prl induced resistance to bolh Psí and thc cont eàrwonn(.Helicoverya .ea) \tld\stai pads of the PrÊinocula.ed plants. Convcrsely, feedingby 11. zed induced resistance against both Prr and 11. rsa. A nice demonslÍadon ofsimultaneous pathogen ànd insect resistance in the Íield was provided by Zehnderet al. (2001). The authors observed that rhizobacteria-mediated ISR of cucumberagainst insect-transmitred bêcierial wilt disease, causedhy Et"winia tracheiphila,was associated with re.duced feeding of the cucumber bcctle vector lt appeàredlhal induction of ISR was associated with reduced concenhrions of cocurbilacin.a secondary metabolite and powerful feeding stimulant ibr crcumber bee es.In-ductron ofrhizobacteria mediated ISR aga;nst t r,"acáe,pntla was also elïectivein tle absence oI bectle vectors, suggesting that ISR prctects cucumber againstbaclerial wilt notonly by reducing beede feedirg and pathogen transmission, butalso tbrough induction of defense rcsponses that act against the brct€r;àl pàthogcn.These observations indicate that negative interactions between induced palhogen-and insect resistance afe by no means geneÍal,

The questioD of whetber SA- and JA/ET"dependert resistance againsr micro-bial patbogens can be expressed simullaneously was Íecendy addressed by VanWees et al. (2000), In ,4/dr;do1.rh, SA-dependent. necrosis-biggered SAR and,lAlET-dependent, rhizobActeriarnediated ISR nre each effective against vaÍiouspathogens, allhough their spectrum of eÍfeciiveness partly diverges (Ton et nl.,2002b). Both SAR and ISR are eflective against P!1. Simultaneous aotivalim oíboth types oI induced resislance resulled in an addilive effect on the level oí in-duced proleclion against $is palhogen. In Ardàrzolrtr gsnotypes that flre blockedin eitheÍ SAR oÍ ISR, this addilive eflèct was Ítbsenl. MoÍeover, induction ofISRdid not afiect expression of the SAR màÍker gcne PR-/ in plants expressing SAR.Together, xhese observadons demonsíaue that the sign: iDg pêthways involved inboth types ofinduced resistance can be compatible àlld thal therc is not reccssaFily significant cross-talk betwe€n them. Therefbre, combining SAR a d ISR cdnprovide rn attractive tool for inFoving disease contÍol in planh.

References

Abad, M.S., l lakirni, S.M., Krnie$'iki, WK., Ronóens, C.M.T., Shuldêv. V,I"am, E., andSh.h. D.M. 1997. Chàractdizoiion of rcquired resiÍtancc in lesionrnimic t.ansgenicpoLàto expiesing baclerio-ots|n. Mol. PLnntMi.nbe lttte,r.t. 101635 645.

Abeles, F.8., Morga\PW,odSallveil, M.E.J. i 992. trr)/" h. in t'Lant Biolog!.s^nDiÊga,CA:^cadcDric Pres.

Ajlan, A.M., ánd Poitor D.A. I 992. Láck oï efibct oftobácco mosric virdsindnced systemicacquired rsisiance or aÍhropod hèrbivores iD tobá.co. P, ltopathabsr 82:647 -651 .

Bakker, P.A.H.M.. Van Peer, R., and Schippe6, B. I 991. SuppÍessjon of soil'bome flànrta$ogen! by 0uorescent psendononàdsr nohanisns and prospccts.In l?ir,i. /rÍ.r4.ttions and loil-Rame Diseaser, eds. A.B.R. Recmster, G.I. Bollen, M. Geda8h, M.^.Ruissen, B. Schippes, ènd A. TÈnpel. pp. 217 230. Amsterdam. Tlr Nethedands:Elsevier Scientiíc PublishcN.

185

""1,.ïi."i1".;I,),. ll";;;;:;: ;;1):ï;,i:; :'1" lil,l.'1,'i:;lÏ'liïlïïil:

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t " ' " ' .

* ' " t . "*

r l ' r 'Mo' a 'o l /0 81s 8-r '

":';l*:*Íjr:*'*:u;,kL;'ilïi1"Ïl; lïl.Ï")i,f;'lïi;,," :iÍ;

"r3iiJ,l'^.i13""", t.^ , sonemirre. c., and Kende, H re88 rnsensivitv to cthvrene

"'."ïi"""á t"

" --**Íl"

Í^\i[iaAtabidoPsis thati'nd scic"e 241:1086 1089

''*:*l*':*'{nm";;'* ï:1 i"ïï:.',ï.31,'l;}ffiïïï1il1JJiï:Ëi"."tíi1.'i]#:;i,ï:r, -"be!r!on,

r.1.. Lddin, r'c ' and Ktí\cr' B N lees Anarvsis*;;;.i.";;;r:*'.'.d'"'.d

deten\e rcrponse" in Aro'iroP' I lÍar'dld prinr' ccn) 'ns

a

;r;1,t":ïi"Ïllí"t1,Ïl iïíJlïJiÍ;l-i,:'l::''"ï*" ou"* "'u"'"^R. S,. l5 l :1495 l5 i0

'*Í*í*;'*,lJ;*;ï, :::1:l;i :;.H;::;Ïi Jll?ï:ïï,,lÏ1"1'Ï:::Pla nt Cell 6t1845-185'7

"rÏïi;jt *Íx,HïJ1,1Ëïitu3*'ilï?ï"i;1;lï?l;,i'l"iïJ''#il.ï1ce 9tt5'13-1584

"':*l;l;l;,lll,ni";hH;,1,',i,f;.T.lii-iiiJiï,Li1i'-1ïïïlliÏ,ïïl'iïÏÏ#"rliíl*,

o , nt,,"n*. * tansnsa R sjmons G worrcr' M Frirtch A vsnDlcren"'*,"*lj:.;'* llgvf*"",1ïlil8'i",1; Iïili; i""l"i ."";'i.""ruï,1;

Dathoqen resislaÍce. Cell 88:6S5-705 '

"T:ïïÏn' jï:ï"Y"r.'",,,ï$:;ïiitiï*$#ifr#ïrï;ïil;"ffi Ïilïffi f iï-ÏàÍi"

non 4 s s" i n 8 4e P t

"trÏJ,"** ;*r:**"ï,i;; ïli"?,ïl* f;,,','.j;i'ii'l;ïï"Xïij":l#ï;

",i"Í,1,i']iï;ii33*,,u*'t*:^yT:lti,ïl'i;ï"ïi'llï;iiïii'ï1,,',iËil'#pÍotcin kinde is svitemic'll) iduced opoD wol

"r,i1ï.1ï..tíil;- t.t,

'-und. s r', Jones I B ' starr' R E ' ànd Krec' It r' 2000. Re-

' : ; ; ; ; ; ; i ; ; ; ; ; ; " , ,ape'aspv.va.o,o, iaÍ 'om"'o,1vo' I \e ' rcF'ra ' ioruÍc ' Ihv 'É*

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P/dnr Plui ' l l l \ '81-02'

.lll*j ;lll: hr : l;ïïï;;::ffi'":: li,'"ïï 'iïl#l:":lÏi;

..P."1 ""iiïl-Jilíiií;:' j. i",ill"lji;*.*.,e.nËn. e "s'h' ppr dov a'd

taba,ta PhJsrol Unl Pta4t Pathol ^4'13

'N!'

I li6 8. Signalins in Plant ResistaDce Responset

Cohcn, Y, md Cisi, U. 1994. Sltemic auslocaLion of 11C DL l-aninobutyrlc acid intomato plants in relation to induced resistoce against PftIíophthon iaJèsídns. PhlsíolMol. Plant PathoL. 45:441446.

Cóhen, Y, Ovadia, 4., and Oka. Y 2000. Is irduced Êsisrancc levestble? The BABAcase. (^rrÍráct), ItJ/ Irl.ru d tiohdl S!tupoÍiun ok lnrluced Resittanc. ta ptant Direases.IslaÍd ofcortu. Crcece,22 27 May 2000, p.68.

Conconi, A., Miqrcl. M., Browse, J.A.. and Rym, C.^ 199ó.lniraceitular lerels of freehxnenic and iinoleic acids increase in ronato leaves in reslonse to wouDding. p/anlPhltiol.111,:797 803.

Conrath, U., Jobljck, W., and Kauss, I.I. 1991. The prcGnr kiDase inhibitort K 252a, decrea\eselicitoÊinducedCa:+ uptake and K+ rclcase, ud increascs coumadn syDthesislnpasteycells. ? EBS 1"ft. 2191 11-144.

Conmth. U.. Che\ 2., Ricisliaro, J.R., and Klè!sis. D.F. 1995. ï\'o inducen ohlant dcièDse.erponscs, 2,6-dichloroisonicotir c acid aíd sdljcylic acid, nnribit catalase àcLivny intoba.có. Pmc. Nad. A.dd. Sti. USA 92:7143 :7141.

Conralh, U., PieteÍsci C.M.J., ard Máuch,Moi, 8. 2002. priming in plárt-pdihogen inrelÀ.Íions. Trundx Pldat Sr:i. 51210116.

CoÍstrbcl, C.P. 1999. A surley oïherbivory n uciblc defensive prÍcins aMtphyiocheÍri-c ls. tn hducetl Plunt Dafuhs.' Aeai$t Parhdsh! ant t-teóivoft!. Biacheniltry, ELot-ogy dn t A sticrlture, eds. A.A. Agraval, S. Tuzun. and E. Bcrr, pp. | 37- I 66. Sr. paul.MNTAPS Press

Conslabel, PC., Yip, L., ànd Ryan, C.A. I 998. A.olyíemin lïom porfllo. blÀck nightshade,and bell pepper: prinÍuy slructuN and biologicrl l1crivily ofprrdicrcd syslemir polypcp-ti'Jee. Pld l4al. Biol.36:55 62.

de Bruxellcs, C.t,., nnd Roberh. M.lt. 2(l0l . Signírls rcgut ing DnÍ1ipte rcsponses ro wornd-iDg rnd herbivolcs. Cil. À.?r PhhtS.i 20t487-521.

Dc LÀítl. A. M.M., and VrD Loon. L C. I 98 L Regulnlion (t, crhytcne biosynrhcsis in viflrs-i'Íbct€d tobaoco lcales. I. D€remrnr4li{rr of (he rclc ol rucrhionhre

^s a prrcunor of

c\\y)ene. Pktnt P h! \iol. 68: 256-260.Dclarcy, T.11, Ukne$, S., Vcrnooij, 8., Fnednch, L., Weymdnn, K., Negrotto, D.. Càthcy,

T., Cut'Rella, M., Ke$mdnn, H.,Ward, E, dndRysh,J. 1994. A ccnr rotcotsrlicyticacid tu plinx disease LesiÍarcc. S.ience26611247-1250.

Delancy, T.P, Ffiedrich. L., und Ryals, J. 1995. Á.aàiddprir lignul lransduciion muLruÍdcièctivc in chedcllly ànd biologically inducod discase resiNt|mce. ptoc. Nat. A.xttt.S.i. USA 92:6602-6646.

Dompscy, D.A, Sl'0h, J., ard Klc$ig, D.F. 1999. Salicylic rci.l rnd discase resiÍLrncc nrplaDts. crt. Àcr /14d,5r.i. l8:547 575.

Dhondt, S., GeoiTtuy, P, Stehnach, 8.A., LÈgrald. M., .nd Hejrz, T. 2000. Sotrbtc |hosfholilase A2 àctility is iNluced bèfore orylitjn accumulation nr tobacco frosajc lirusinÍècted tobac.o lcaves lDd is cootihred by patatin tile enzynes. ptant .t. 231431

Díaz. J., Ten llavc, A.. and Vaó KÀn,.r.A.1,.2002. The role of erhytcne and wdund siSnalirgin rcsistance of tomaro lo a,Íttiscí erea. Pldht PhrtioL.129:131,1-lt15.

Dodês. S.H., Syovers. ]t. Wejler E.W, ard Ryan, C.^. t995a OtigogaiacÍrcnides andchttosan activate planl delcnsive genes rhrough thc ocradecanoid parhway. pm.. ry4rlÁ.ad. ,t ;. usrt 92:4095 4098.

Doares, S.H., Narváer-Vásqrez, J., C.Íc.ni, À, ard Ryan, C.^. 1995b. Sdicylic acidiMibits synthcsis of protenràse nnribitors nr tomrro teavei hduced by íyÍ€min andja$onic acid. P/znr pt)jdt. r0rj:t74t 174ó.

187

Dohdry, H.M.. ard Borles, D.J. 1990. The Íole ofpH ánd io! trMspoí in oligosacchadde-induccd proteinàsè inhibitor acctrmulation in iomàlo llants . Plant Cell Envircn. l3:a5l855.

DoheÍq', H.M.. selvendro, R.R.. od Bowles, D.J. i988. Tïe wourdrcsponse of iomàtoplets cm be lnhibited by aspirin md relaled hydroxy b€lzoL

^c;ds. Physial. MoL Planr

Pdthal. 33.37'1 i84.Doke, N., Miua, Y, Sanchez, L.M., Pdt. H.J., Noritake, T., Yoshioia, H., and Katakit.l,

K. 1996. Tïe oxidative bu6t lrotects plets lgalnst pàthogen àtt&k mecbanism aÍdrole rs ar enelgency sigMl lbr plant bio dciènccr d reviev. Gene 119:45 51.

Donibrowski. J.E., Pearce,G., andRtd, C.A. 1999. P.dei !e inhibitor-inducing aciivityof fte prohormone FosysteDin Íèsides exclusivoly h thc C-tenninal systemin domaln.Prcc. NatL. Acad. S.i. USA 96: \2947-12952

Ebel, J., ard Mithóter, A. 1998. Early elenls in the elicitation of plaDt defence. Pldnia20ó:335-34Ii.

Ëngelbedh, J., Koch, T., Schueler, C.,Bachmann, N..Rechtenbacb,J., atld Boland, W.2001.Ion chamel-ibÍming alamethicin is a polenL elicitor of voialile biosynihcsis md tendrilcoiling. Cross tàlk betweenjasmonatc and talicylaLe si8naling h linu bean. Plonr Piryr,ol.125369-37'7.

l-amer, 8.E., md Rytu. C.. A. 1990. lntealánt Communicationr AiÍbomc Nothyl jasmonÀle

induces synrhesis of proteinase inhibito$ in plnnt leaves. Prcc. Nan. Aca.l. Sci. USA87t7713J'716.

Farmer, E.8., and ltyan, C.A. 1992. Ocladecdoid pr€cursoru of jasmonic acid áctivAte ftesynrhciJis of wornd-iDdLrcible prolciíase iDhibitors. Pl4tr Cell 4t 12y134.

Faflner E.8., Johtson, R.R., and RyaD, C.A. 1991. Rceulation of èxplession of pro-Leinase inhibitor ecnes by merhyljmmonflte 0ndj&smotric

^cid Planl Phtsiol 9S:995-

1002.Fauth, M., Menen, A., Hahn, M.G., Jeblick, W, and Kduss, H. 1996 Comlelence for

eliciration ofIlrO, in hypocotyls ofoucumberis induced by bÍeaching the cuticle and i$enhanccd by s4licylic acid. PLaLt Physial tt0:347-354

Felix, G., bd Boller, T. 1995. Syslemininduces rapid ionfluxes lnd ethylene biosynthesisln Lycowtsicon pe ruvidkun oell$. Pldrr J ?r381-389.

Felton, G.W., Kofth, K.L" Bi,J.L., Wesley, S.V. Hrhmdn, D V, Mà$ews, MC,MurPhy,J.B.,Llmb, C., lDd Diïon,R.A. l999 Inverse relalionship between syslemic resistÀnceofllants fo micÍoorganisms dd to inseci herbivory. Crlr liol.9:317 320

Feys, 8.J., MoisÀn, L.I., Newmann, M.A., and Plrke! J.E. 2001. Direct internclon be'twccn rhe Árdàldoprir diseaso resistan e sigualing ProteinÊ, EDS I and làD4 EMBO t20:5400-541L

Fidanlsef, A.L., Stout. M.J., Th.ler, J.S.. Duiley, S.S., andBostock,R.M. l999 Signal in-teÍáctions in pàLhogen rnd inscct atlackr elpression of lipoxygcna\c, Pdeimse inhibíorII, and plihogènesis{elatcd protêin P4 in the lomato, L).oP etsicor elcalèhtutu Phtsiol.Mol. Plant. Pathol. 54197-114.

nick. U.8., ud Sohaller, A. 2002 CDNA nicrcmày ualysis offusicoocin-induced cbangcsin genc cxpression in tomalo pl!aIs. PLanta 216:83 94.

Frye, c.A.. and Imes, R.w 1998. An Á/dàidrpsB nutàn! virh enhanced resistdce topowdery nildew- Plar, Cell 10:947 95ó.

FD,e, c.A., Teg, D., and Innes, R.w 2001. Negarive regulation of dcfense resPór'ses inpldnls by a conser!Èd MAPKK kinase. Pro.. Na,l A./d. S.i USÁ 98:373-378.

Fukudà, Y 1996. CooÍdimted etivatioÍ of chitirase Senes ad extràcell d rlkalidzationin suspension-cDlturcd tobac.o cells. Biosci. Biote.h Biachen 60:2005 2A1O

rt

lr88 8. Sigaljng i! Plant Resistànce Re$po$es

caïfÍev. T.. ftiednch, L. Vemooij. B. Negrotto. D, Nve, C, Uknes, S' Wdd' E'

Kesinann. H.. rnd Ryal$, J lgg3 Requiremenr of saLicvlic Àcid for lhe inductjoÍ of

s\{eni . x.qrr . . ( ,1re ' ' d1re S r"n 'P 20l -5d- <6

Cu.ili"t,.q., "nA

r"ton, t tSg2 llfluence ofseed dd rool exudrtes on fluorescent Pse!

domona\ and 1uryi iÍ soldiz cd sóil. Phttaryttunos! 82t120 327

covn[ E.M., and IÀine, A 2000 TlF h]lèreeNilive leá.tion facililates plant inf4tion

tv the rccÍotrophic fungus aotJtis cincrca Curr Riol lO:751J51

cratram. rl., anrl Grahar, M Y 1994 Wold'asÍrciàted conpetencv factoÍs de rcquitd

lor thè proxnnal ccll responscs 01'soybcan to the Pà.t'roPlrfi,fa roJde wàll Slucan elicitorl

Plant Phrsiol. 105 :57 1 51 4c!@n, T.R., ard Ryrn, C.A. 1972 Wound_idlced PÍotei.asc iliribitor in plant leave$: A

po$ible defcnse mechanis agairtt insects. ,t ie,'/ 175:776-777

Gudldch, H., MueUer MJ., Kutcbln, T M., and zcnk, M H I992 Ilsnonic àcid jt a siSnal

qansduccr iÍ elicibÉjnduccd plant coll critures Pft. N.tl Á.a.í S'i U!'4 89:2389-

2393.Uamrcrs.hmi<l!, R, and KuÍ,l lg82 Lignincadon rs a meclànism for induced svstènic

rcsistànce ilr cucumbd PbrioL PLdf,t PathoL 20:61 71

HainrcBcbnidt, R., Métraux, J.P., and van Loon, LC.200l lnducing ÍeÍstarce: a sunÈ

mary of plrpeÍs pfcsented attheFinl Int mdtion^l Slltqbsiu onltttlu'ed Rctltun'e t')

Ptuht Distdscs, Con!,MAy 2OO0 EuÍ I I'tunt PothóL lD7tl-O

llanl1s, K.,ltan:riez, L. andPefra_CoÍós, H 1998.ldribition ofwound_iiduced acct1nrula_

tio,r ol'auenc orkle sy hrse tÉnscdpts in 1fux leaves by aïirin and salicvlic ffid Ptunl

Pr l r i . t . 11811057-10ó5.I-Iàuse, 8., Slen/-el. L, Mierscb, O , Mauchen H., Krlrhcll' lt, Zc8lcÍ. J , a d Waíetndck'

B. 2000. Tissue-$Pccinc oxylidn signdurc of lomoto nowcrs: rllene_oxide cyclo$e is

highly cxpresscd in disti,rct nolver organs ard uscr rlár bundlcs flo' l 24r 1 13- 1 2Ó

rlc, i , \ i 'orcn, R.F, Zhao, T, shao, l , Zhu,L. ,Trns.X,a, \dZho,J-M 200l overcx-

pÍessidr of PTl5 in lomdto potcnliales pr$og4'nrduccd delènsc gcnc expresÍr'on flno

enhmces tliscusc r esisrunce t o Preutlanlohas ryfini!4 p\ ' tunab Mot Pl1nt Mi( roh?

I a I e nct. l4t1 453-1 45'7Hilpcí. 8., Bohlnmn, H.. Op dcn Canp R. PÍzvbvla, D., Mie$ch. O, Buoh^la,

^ ';nd A!cL, K. 2001. lÍ)ld1on and chiractcrizalior of signal transduclion nutmts of

Arabitlopsis tholiaha th^r .onstilLrtivclv trcdvate thc octadecanoid palhwav Ànd lonn

nccro(ic nicr)lesions. Pll,r J 26:135446Hotlnan.T, Schnidi LS .Zheng, X., lddBcn!,A.F 1999.1íol'tioD olethvletrc irsensrtive

soylrean mutànts that are àLtercd in pathogen susceptibilnv rnd gene-foFgene diseaso

rcsistance. Plarr l'l,rsiol. I l9:935-949HowqO.A.,.ndRyan,CA lggg Sunpresos ofsvstemin ÍignaliDg identifv ecnes in arc

lonratd wouil responsc Pathwry Ga'cll.s l5lrl411 l42l

Howe. O.A., LiShtner, L. Brosse, J., ànd Rvan. C A 1996' A! ocladecanoid lltLhwa)mulnnt (JL5 of tonalo is compromised h sig lnrg for dèfense agairsl irsccl allack

PlanÍ CdL a:2067 -20'11 .Inbar. M., Doost laf, H., Sonoda, R.M . Leibee, G L., Mdver, R T l 998 Elicitos of flLnt

dofensive syíens tcducè insecl densilics nnd diseasc irci dencc J.Ch'k1 E oL 24:135

hhigdÍo, S., Kawri-Oda, A., Nishida, l . md Otadn, K 2OO) . rhe .leJè.tivc ih afih't de

Àir.c,.? / gène encodes a novèl pliosPhotipasc À I catalvzing the idtill step ofjasnorc

àci.l biosynthesis, which synchionizes Plien maturdtion anther dehiscence. ard ilowel

opedng in Áró rprir. Piarí Czl| l3:2t9122tt9

I li9

Jabs, T.,'Ischiipe. M., Colling,C., HabLbrcck, K., and Scleel. D. 1997. ElicitoFstitnulatedioD fllxcs and O; fron the oxidadve bust are escntial oonponents in tigSering defeDse

Scnc activatio! and phytoalexln bioslnlhesis p.slcy. P,,.. Nal. Á.dd. J.l USÁ94:4800 4805.

Íacinto, T.. Mccurl, 8., FraDcesch. V, Delano Frcie., J.. and Ryan, C.A. 1997. Tomato

lroslsleDin pronoter confers wound inducible, vasculd bundle specinc exp|e$ion ofrlie l3-glucuroniddle gene in trarsgenic tomato !lan!s. Planíd 203:406412.

J.kab. G., Coiti€a V, Toquin. V, Risoli, G., zimDedi L.. Métnux, J.P, and Mauch'Mánl.B. 2001. l3-lminobutyric acid-irdtrced.e$istatrce ln plant!. Eax .1. Plant Pathol. 141:29 i1.

JiÍage. D.. Zhou. N., Cooper, 8., Cldkc. J.D., Dong. X., and OlazebÍook, J.2001. ConsLi'tuti.ye ldlicyllc acid dependent signallng nr .?f/ and.tpí mutanls rcqui.cs PAD4. PldtJ. 26.395-407 .

Jonak, C., Beisrelner, D.. Beyetly, J., and Hnt, ft. 2000. Wound-induced expt!$ion ardactivdíon of WlG, a novel glycogen synthase klndre 3. Plaht Ce l2t146'7-1475.

Kacluoo. P., Slàíllin, J, Shah, J., Whiltle, U.J., and Klesig. D.F. 2001. A fatty aciddesaturase modÍlates Lhe acLivalion ofdetense signlling pathways jn platrts. Prc.. Ndrl.lcad. S.,. US,4 98:9448 9453.

Karban, R., and Baldwií, l-T. 1991 . Inttucetl Revonseí to H.ráivory Chicagor Universiiy

Katz, V^., Thulkc, O.U., dnd Connth, U. 1998. À benzolliadiazole pfimes parslcy cellsfor AugNcnled elicnation ol defense responses. Plzrt Pl')rbL. )1711333-1339.

Katz, VA., Fuchs, A., ànd C('n!alh. lJ. 2002. PrcrreÀhentwith salicylic ncid pdmes puÍsleycclls l'or enhanced ion lrmspoí following elicitalion. aÉ35 I/u.520153-5'1.

Kàuss. H., and Jeblick, W 1995. PremaÍ ont of pa|xlcy suspcnsion oulrurcs wilh sdioylicucid ênhnnces spontancous and elicited prcduction oltlroz. PLdnt Phr\iol. 108)l7l-I l?8.

Krusc. H., Thcjsin8or-Hir1kel, E., MtudeuÍann. R., ald ConÍdó, U. 1992a. Dichloroison-icorinic r|]d salicylic ucid, inducers of systeÍuc ncquired resistDcc, cDheucc ltrngllelicilor rcspon$cs in p.rrsley cells. P/.'nl "/. 21655-óó0.

Kauss, H., Krause. K., and Jeblick, W 1992b. Medryl iasmonate condition$ I,tlrsley sus-peDsion oells for increased elicilati(D of phenylpropAnoid defense responses. Aio.*?/r.Aiophls. Ret. Cohn. 189:3lJ4-308.

Kauss, H., Franle, R., Krause, K., Coffalh, U., Jeblick, W, Crimig,8., An.l Malem. U.1993. Conditioning otparsley P.trcselinun citpun) s$pensjon cells inorea$es elicitor-induced incoÍpoÍntion of celL sall lhenolics. Plart /hIt ol. 1021459466.

Kauss. H., Jeblick, W, Zicglcr, J., and Krdbler, W. 1994. Prereament of pdsley (Per-nsclinun ctispuh L.) s$pension culLDres with melhyl jasmonatÊ enhances clicirdionof .cliv.ted oxygen species. Plzrt Pbriol 105:89-104.

Klessig, D.E, and Màlany, J. 1994. fte salicylio acid sign{l tu plan$. PlartMol Ë,o1.26) 439-1445.

Kllisener, B., dd Weiler, E. W. | 999. Pore-Ïorming propeíies of clicito6 of planl defbnsoreacnons aDd celluktyric èn4tus. FEBS Leu. 459:263266.

Knoestcr M., Vdn Lnon, L.C., Van den Heuvel. J.. Hennig, L, Bol. I.R. md Linihorst,H.J.M. 1998. Elhylene'insensitilc tobacco l&ks nonhosr resisLance rgainst soil-borrcfv9| Pmd NatL Aca.l. Sci. USA 95:1933-1937.

KnocÍèi,M.,Li ho6t, H.J.M., Bol, J.F', and Vd Loon, L.C.2001.Involvement ofcthyl€nein lesion develolmenl.nd syslemic acquircd rcsistance in tobdcco during Èè hypeÍsensirive rerctior to tobacco mos^i. liÍtrs. Phlsiol. MoL Plant Pathol. 59:45 57 .

190 8. Signaling h Plant Resistan.e Responses

Kohler. A.. Schwindliry. S., dd Cotrath. U. 2002. Benrcthiadiazole-induced prining forpoteÍirted responses to prthoSen írfectio!, wounding, dd inliftrátion of wald intÍrleavès reqni€s the NPÁ1,4r'lMl Beie n\ Ardbidopsis. Plant Phrriot 128:1046 105Ó.

Kubigsreltig. L, Laddert. D., and Wcile\ E.W 1999. StÍucture and regularion oftheÁ/a_bi.lnps^ thdLiant alleae oxida synthasè gene. 1'lazta 208:463 -'171.

Kuó, L 1987. Translocatcd signdls ntr pia imunization. AnL N Y. A.ad sci 494:221223.

Latunde-Dada,4.O., and Lucas, LA.2001. The plant defense nctivator acibonzold-s_nethyl pnnès cowpea [visra

"4sli."lata (L.) Walp.] seedlings for rapid induction of

le${bn.e. Pri,',,/. Mol Ptn4 rath"l.58.lae 208.Lawtdr, K.A., Poltcr, S.L., Uknes, S., aldRyals,J.1994. Acquired Íesistance siSral rans_

duclion inÁrarldorri' is elhylene independcnt. Plant Cd[ 6:581 588.Lee, S., Suh, S., Kim, S., Crair, R.C., Kwdt, LM., Nàn, H. G., and Lec, Y. 1997 syíemic

ele'atioÍ ol phosphatidic acid ànd lysophospholipid levels in woundcd planls. /'ldrr I12:547 556.

Leenan, M., var Pclt, J.A., Herddclc\, M.I., Schel,d, lt.J.. Bakkea PAH.M., àndSclipFrs, B. I 995. Bioconnoi oflLrs{rimr will ot rádish in comnerci!l ErccnhoNe trahby íced treatmenr with Pserdannna\ luorcsdhs WCS314. Phrta4tholosr 85:l30l'1305.

tÊóÍ. J., Rojo, E., and Sínchez-SeÍaro, LL 2001. Wolnd tignalling i'r planls ./ try. Aol52:1-9.

Li, L., a d llowe, C.A. 2001. AL(cmalivc idicing of prosyslemin prc-nRNA pÍ)ducestiÍo isofbnns llrar are ncLivo ns si8oàls in the wound respo$e pa \Nl!y. Pldkt Mol Bial

Li, L., Li. C., aM Hosc, G.A. 200 L G€netic analysis ofsound signuling in tomato Ef idcncclin ad alrolc ofjos,nonio &id in defense a,rd lbnalc ls tiliry l'Ltnt Phrsiol l2ll4l+14t1.

Li, L., Li, C., Lcc, C.]., and Ítowe, C.A. 2002. Dislinct toles for jnsmonntc synthesi$ andnction iulhe syícmio wo$nd rcsponscol t(NÀto. P/rc. Ndtl. Aca.l. Sci. US^ 99:6416-6421

Lund, S.ï, S1àll, R.E., and Klec, HJ 1998. Ethylenc regnlatcs dlc susocltible rssponse iopathogcn nriection in tomato. PLont Ccll 10:3'11-382.

Malany, J.. and Klessig, D.n 1992. s licyllc .ci.l and pltnt discasc rcsiítlÍlce. ./'llrur I2 643454.

Mauch, n, Iladwiger, L.A., and Bollo!, .I. 1994. Ethylene: synptom, not signil for thcmduction ol chi(inrse and l3' 1,3 eluc$dso in pea póds by prdrogcns and cljcitos PtunlPlrysiaL. '76:6t17-61 t .

Mcconn, J., Crcclnàn, R.A., Bell, E., Mullel,.Í.E., and Brosse, J. 1997. JaÉmonÀle isesenr ia l fof insecldelenseinAtubi t lopsis.ProN.N4.Acd. l .Sci .USA94:541)-5411

McGu,8., lndRya!,C.A. i992.TheorgaDizat i {nrot lheprosyÍeDingeDc.Pl4rrMD,Biín.2lt:405409.

McCuÍ1, B., Pcarcc, c., Oró7rd-Càrdenas, M., aDd Ryan, (1. A. I 992. Stnctutt. expre|sionaid dÍisense nrbibitiotr ofthe syíemin precu6or genc. S.;.mc 255:1570 1573.

McCurl,0., Orozco'Cardenas, M., Pedre, G.. Àdd Ryan. C.A. 1994. OvetexpÍesion of thc

rosystcmin gene ln lrarsgenic tomato planLs Senerates a systcmic sigDalthal constit!tively induces proLeinase bhibitor syntlicsis. Pm.. Nul Ánl S.i. USA 9 | 9799-9802

MeiDdl. T., Boiter. T., and leIiÍ, G 1998. Thc plant wound bomone syÍemin binds withthe N-tcn Dal pm tó its .ècèptor bui needs tlic C lrmiràl paÍ to rctivatc it. Plant Czll10:1561 1570

l9 l

Miltler, R., :nd Lan, E. 1996. Sadince in the face of ibes I pàlhosen-ild&ed proeralmedcell death ln plarN. ?'/d,Á Mictubiol. 4110-\5.

_ Mitder, R., Shulne\ V, and LaÍ1, E. 1995. Coordinated activaÍon of plogllrlmed cell deathanddelènscmechoismsiníesge c tobacco llmts expre$ing a bacterial protor pump.Pldnt Ccll7:29 42.

Moran, P 1998. Plant medlaled irtdactions betweer iÍrecLs Ànd tmgal plànt pathogeD andthc role of chenjcal respoNes to infecton. (recolrStd I l5:5 13-530.

Moyen, C.. and Johànnes, E. 1996. Slsletrin hansieDd) depoldizes the romato mesolhyllce]l niembrmc md dt{tsonizes tusicolcirÈinduced extracei]uld acidif,cation of meso-phyllÍi,ssne. Plont CelL Envircn. 191464470.

Moyen, C., HanDond-Kosack. K.E.,Jones, J., Knight. M.R.. andJohannes, E. 1998. Sy$,emrn'dBteFrn.ncrea.eolc) !p lc,miccxlc i , rnrnrom.,rooc,uphyl lcel l \ . ( r 'mohllization from i Ía and extracellultr compdments. Pturr C.ll Enrinn.21:) l0l-l 11l.

Mui, L.A.J., Brown, LR., Ddbx R.M., Bestwick, C.S., Bi, Y-M., MàÍslield, J.W, àndDmpor L 1996. Sàlicylic acid potentiates defens€ gene expresstun ir tissue extibitingacquiÍed resistÀnce to patho8en attack. lldrÍ "/. 9:559-57 L

Mur, L.4., Brown, LR., Dtrby, R.M.. Bestwick, C.S., Bi, Í-M., Mans$eld, J.W, Dràper, L2000. A loss of resisLatue Lo avirulent bacterial pathogens in lobncco is {snociaièd withthe attenmtior ol a salicylic acid-poÈntiAted oxidative bursL PLdnt J. 231609-62) .

Nafláez-Vásquez. J., Florin-Christense., J., íhd Ryan. C.A. I 999. Positional spaificity ola phostholipase A Àctivily induced by wou ing. systemin, and oligorracchàride elicilosin rolaÀro 1èà\es. Plant CeU llt2249-2260.

Niki, T., MiLsuhara, L, Seo, S.. Ohlsr.tbo, N., and Ohnshi. Y 1998. Antagonistic eflèct ofsalioylic írcid and jasmonic acid on the expÍession of parhosen$h{êllited (PR) proteingeÍes in woundod matule toba.co lellfics. PLa t Cêll Phts,oi. 39:50È507.

NoÍman-Settoftlad, C., Vidrd, S., sDd PÀl!a. T. E. 2000. JntcrÀcrine signal patlways contÍoldcfense geDeerpressior iD Á rdbi.t ?rti iD response to cell wAll-degnrding enzymes liomErwinia cantovora, Mol. Plaat Micnbe Intetuct. 131430-!38.

O'Donnell, P.L, Calvert, C., Atzorn. R., WAslemack, C., Leyser, H.M.O., andBowles, D.J.1996. Ethylenê As A signal mediating the wound Íesponse of bmato plírnh. "Sc,?rce2'7 411914-1917 .

Orczco'Cárdems, M.L. 2000. Hydrcgen p€ruiide rcts as I second mcssengcr tbr thc i'Èductrotr of dcleDse gene$ in romalo plants in Íesponse to í)ounding, systemin, atrd rnethylja$monàte. Plat Ccll l3rl79-191.

Orozco-CarAenas, M., andRyan, C.A. 1999. Hydrosen looxide is seneratcd systemiclllyjn llmt leÀves by wourding ànd systemin via the octddccanojd pathway. P,?.. Ndtl.Á(d,L S.r. USA 96:6551 6557.

orozco-cadenas. M., McCuÍI, B., flnd Ryan, C.4. 1993. Exlression of an antisense prosys-tcmin gene in tomnto plonts ieduces the resistance towdd Ma ndu.a lettd laÍlàe. Pbc.Natl. A.ad. Sci. USA90:8273 8276.

Pedce, C., Snydom, D., John$n, S., Ànd RyAn, C.A. 1991. A polypeptide rlon (omtoleavcs induce$ would-inducible proDinàse inhibitorlrotelns.,Lien.? 253:895-898.

Pearce, G., Moum, D.S., SÍatmaN, J., and Ryan, C.A.2001. Produclion of multiplc planthormones fron r siryle polyprctenr precu6oi Narure 4111817 820.

Peía-CoÍés, H-, Albrecht, T.. Pru! S., Weiler, E.W,:rnd Willmitzer. L. 1993. Aslirinpevents wound-induced gele elpressión in tomalo leaves by blocking jasnonic acidbiosvrtbesis. Pl@ra I 91 : i23-128.

Ponninckx, I.A.M.A., Eggemort, K.. TeÍas, F.R.G., Thoma, B.PH.L, De Samblanx,C.W., BDclala, 4., Métraux, J.-P., Mannds, J.M.. and BDkaeÍ, WF. 199ó.

192 8 S,gnaling in PhnrRe3istuce Re3ponses

Pàthosetr-induc€d systemic activation of a llànt dofensi! gerc in Átuàidopr6 tollows àsalicylic acid-indepedent paÍhw

^!. P L1 it C. I I 812309 -2323 -

Penrtnclc, LA.M.A-, Thom, B.P.H.J., Buchala, 4., ànd Métrux. J.'P 1998. Concomitant stivÀtion ofjarnonàte and ethylerc reslonse pàthways is requirod for iduction ofa plant defensin gene in Á/dridopsis. PlMt CeU lO:2103 2113.

PieteBe, C.M.J., Vm Wees. S.C.M., Hoffland, E., Vu Pelt, J.A., md Vd Loon. L.C. 199ó.Systemic @sistance io Á/aàdoprir induced by biocontrol beteria is indepddenl ofsalicyliceidaeunulationándpathogercsis-relaiedgeneeqressiq.PIa Ce A:1225,tz37.

Pietese, C.M.J.. Van Wees, S.C.M., Van Pe1t, J.4., Ktroester, M., Len. R., cenits, H.,Weisbeek, P.J., atld Van t on, L.C. 1998. A novèl signaling panlway cotrlrolling indu@dsystemic ÍesistanceinÁ.ardopris. Plant Ce 10tl5'l|-1580.

Piete.se, C.M.J., Vd Pelt, J.4., Ton. J., Parctxnm, S., Muellea M.J., Buchala, A.J.,Mét€ux, J.-P., atrd Van Iron, L-C. 2000. Rhizobacreria,nediared induced systemicËsistancc (ISR) itr ,,1/ar,í./,pris r{uires sènsitiviry io ja$nonaie aÍd ethyleíe but is norac.ompanied by ar nrcÍease in their production. Pr)0iiol. MoL Plait Pothol. 57tlz3-134.

Piêíerse, C.M.J.. Van Wees. S.C.M., Ton, J., Van Pelt, J.A., and Vu Loon, L.C, 2002.Signàling in rhizobacteria-induced sysienic resistance in Arubi.kpsis thaliana. PldktBiol.41535-544.

Preston, C.4., trwandowski, C., Enyedi, A.J., and Baldwin, LT. 1999. Tobacco mosnicvirus inoculstion inhibits wound-itrduced jasmonic acid-mediate.l responses within trutnot belween plànts. Pldrtd 209:87-95.

Raskin, I. 1992. Role of salicylic acid in plot$., nra. rR€, Plant PhysioL. Plant MoL Bid.431439-463.

Roymond, P., Weber, H., Damond. M., and Farmer, B.E. 2000. Diffêrential gene expres-sion in r€spome i,o mechanical wounding and insect f@di\\s in Anbidapsis. Plant CêU12t'70'7J 19.

Rizhsky, L., ánd Mittler, R. 2001. Inducible expressioÍ of bacterio-opsin in transgenictobacco and tomato plang. Plant Mo|. Biol. 461313-323.

Robeís, M.R., ànd Bowlês, D.L 1999. Fusicoccin, 14-3-3 pÍoteins, and dêfense responsesin tonato plants. Pidu t Pirls iol. 119:lU3-1250.

Rojo, Ê.. TilaÍenko. 8., León, J., B€rser, s., vdcann€yt, c., and Sánchez-SeÍano, J.J. I 998.Reversible pmtein phosphorylation resulates jasmonic acid-dependent aÍd -independent

',vound signal transduclion pathways i\\ Arabidopsis thaliana. Plakt J. 131)53-165.

Rojo, 8., Leór, J., and Sánchez-Senaío, I.J. 1999. Cross-talk between wound sisnaltinspdhwàys detemines locái ve$us systemic gene expression ia Arabidopsis thaliana.Pldnt J. 20.135-\42.

Ryals, J.4., Neucnschwande\ U.H., Willits, M.G., Molina, A., SteiÍel. H.-Y. and Hunt.M.D. 1996. Systemic acquned resistance. Pturr C?ll8rl809-1819.

Rym, C.A. I 992. The seuch for the proteinase inhibilor-inducing factor, Pm P/aÍt Mól.Biol. 19123 133.

RyaL C-4. 2000. The syslemjÍ signÀlirg pathway: dilïerential aclivátion of plant def€nsiveEenes. aiochitu. Bíophys. Acta 1477:112 l2l.

Schaler, A. 1998. Action of proteolysis-resistant systemin analoguei in wouDd signallng.P ht tó c h e mi s t r ! 4'1 t60 5 -612.

Schaller, A. 1999. Oligolepnde signalling and the acrion of sysÍemjl. Plaht Mol. Biol.40:'/63-:169.

193

Schaller, A. 2001 Bloacdve leptides as signal motecntes in liaDt defelse, Srowth, àn.lderclopment. In aiod.rir. Ndturcl ptuttu.re, cd. Nr^UtRahman, Vot. 25, pp. 3ó7,,+ 1 l Amsterdan, The Nedreíands: Elsevier

Schaller, A., and Frason, D. 2001. IndncLion of round responsc gene cx!ression in romatoleÀves by ionophores. /lard 212:431-435.

Schaller. A., and Oecting, C. 1999. Modularion oi piasma neDrbraÍe H rmpase aotiviLydilïerentially acriratcs wourd and parhogen deièDse responses in tomàro plants. p/drlCeU 1l:263 212.

Schalle., 4., and Ryan, C.A. 1995. Sysremin-a polypeptide delcnse sigDlt ir llants. Bt Er_r,lr 18:27-33.

Schaller, A., Roy, P, md Àmhein, N. 2000. Saticylic acid indepcndenl iDdtrcrion ofpatlrogcnesis relared scne expÈssnnr by fusicocciÍ. ptd, kt 2101599 606.

Scheel, D.1998. Resirtarceresponselhysiology andsignal tÍ^nsÁn Íior.Cu Opin. ptunlAtol. 1:305 310

ScheeÀ J.M., and Ryan, C.A. 1999. A 160 kDa systemin íeceptor on the cell sud.aceof Llcapc^icon perwiokun suspension cutrurEd celts: kinetic analyses, iMucrion bymcthyl jasmonatc lnd lbotoaÍnniry labetitr8. Ptad Ca, I l:1525-1535.

Schcor,J.M., ard RyÀ\ C.A.2002 The sysremin reccptoÍ SRt60holi. Llc.petsicokpeiriard,í is a membeÍ of rhe LRR recoptor kln$e famity. pnc Not. Acd.í. Sci. USA99r9585-9590.

Scncnk, P.M., Kazal, K., Wilson.l., Anderson, J.p, Richmond, T., Someraitre, S.C.. andManDers, J.M. 2000. Coordinaled plmt deíense rcsponses. in ArcbiLtops\ rc\crted by

'nicroaray nnalysis. P/r?. Nai. Acdd. Sci.97:t t655-11660.

SchNele, L, Ànd Kruss, H. 1990. Enhanced ocrivity ol thc plírsmr menbratre locatiz.cdcnllose synthose in cLrcumber.)caves ]rirh induced ÍesisLance. phlsiol Mot. ptont pathoL.3'7 t22l-228.

Schwcizer, P., B challi, A , and Mélraux, J.-F. 1997. Ccne expression panems ànd levolsofjasnonic acjd in rice nc$cd with the rcsisranceinducer 2,6-dichtoroisonicorinio acid.Plakt Pht! iol. 1l5t6l-7O

Seo, S., Okdtnoto, M., Sero, 1.1., Isbjzuk{ K.. Sano, H., nnd Ohashi, y | 995. Tobacco MApKnase: A posiblc mediatorin wourd signnl r'ansduction pdhwoys. Sct4r.e 270i1988-1992.

Sco, S., Sano,H., md Ohtrshi, Y 1999. Jasmonsre-bmedwound signaltransducrion requjrcsactivation of WIPK, a robeco miotogen,activarei p(Íei\ Urnasè. ptaht Ce ph:t4iot.1t1289-298.

Sh{h, J., nnd Klcssig, D.R 1999. S.ticylic ltoid: signfll perccption and traDsdDcrion.li Bbthemistry dnd Moletulat Bialoq! oJ plaht Hèmorrr eds. pp.J. Hooykaás,M-4. H.11, md K.R. l,ibbengr, pp.513 541. AmiteÍdam, The Ncirerl.ndsr Èlsevicr

Shrh, J., TNui. n. and Kle$js, D.n 1997. Characterizátion oia salicylic acid-insensirivemDtrnt írdt/ óf á rabidoprir /,{atda, idendned in a selecrivc sorecn urilizing rhe SAinducible expresion ot tbe IMS2 senÈ. Mol. Pllut Micrcbe Interací. 10.69-jB.

Shelp, 8.J., Bown, A.w, and Mclern, M.D. 1999. Mehtbolism md funorion of grnrna-ádinobutyric ácid. ?rzdr PLant Sci. 4t446452.

Shinsu, K., Nakajima. H., Rdjasekhtu, K., Dixon, R.A., ànd Lamb, C. 1997. Salicylicacd polènliates an agodsrdependent gai! conlrol that amplilies lathoeen signals in rheactivation ol defonse mcchmisns. Plant Cell 9:261-270.

Shumway, L.K., Yans, VV, dd Ryb, C.A. 1976. Evidèncc for the piesencc of lroteindseinhibitor I in vacuolar bodies of plart cÈlt|. Ptan," 129: I 6 | 165

194 8. Signaling in Plant Resislancc RespoÍses

siesrist,J., Orcbcr M.,.rd BuclÉraner. H.2000. Ê-aminobutydc acid nediated enhancemènlol resjstarce i! robàcco to robacco mosaic vins depcnds on rhe accunulation ofsalicylic acid. PÀ)siol Mdl. PlanÍ. Pdthot. 56:95,106.

Stankovic,8., rnd Davies. E. 1997.Intercellula. comunicaLion in ptatrts:elechicd siim_urafi on of lroteiíase nrhibitor gene expressioo in lomato. ?r Ianta 2021402 406.

StÀswick, P.8., Su, WP, ànd Howell, S.H. 1992. Melhyt jasmonite inhibilion of rcor gÍowLhed inductioD of a leaf pnÍci! are decrcased in an Á/drido, sis thaliana i\Áànr. pto..Natl. Acal Sci. UitA 89:6a31-4a40.

sLrswick, PE., Yuer, c.Y, and Leinnan, C.C. 1998. Jasrnonate signatins mutants ofÁ/a-à a/,ri r are suscepLilrle to the kJil iungus p!rá,!n i/f.3" tare. ptant J. 15:j 47,7 51.

Slcnnis, M.J., ChandÍa, S., Ryaq C.A., and Low' p lt)98. SyÍerin porerriares ihe oxidativebursr in cultu.cdtonrato cclls. Pktht phrsiol ll7:t03\-1036.

Sticter. L., Mauct-Mani, B., aÍd Mónaux, J.-p I 997. Sysrenric acqui.cd rcsist nce. Á,&.Rey Ph!1opdth. 35:235 270.

Sti!Ízj. 4., Webcr, H., ReymoDd. P, Browse, L, and Frnne., E.E. 2001 ptanr dctcnse intlie absence of.ia$nonic

^cid: ttc rcle oÍctclopenlenorcs. ptuc. Natt. Acad. sci. USA

9il:i2837-12842.Stoul, M.J., I,idantsel, A.L., Duffey, S.S., and Bostock, R.M. t999. SignÀl i oractions in

prrlrogen ord jnsecr rtucki sysrenic ptrnrDredjalcil ifteracri(ms betweeÍ fÍlrlrogens andlrcrbivorcs ol'thc tomato, L)r. npe$icoft èlatlent kt. phtsial Mot ptdnl t tthoL. 54t115-t : t0.

Strassler, J., Schallcr n, llick, U.8., Howc, c.A., Wciler B.W, Antrhetu, N.,Macbe(rx, P., and Schrllcf, A. 2002. Choracterizorion and cDNA-nicrcáray expressi{r)0nalysis oÍ'12-oxophytodicDoale rcducrascs rcvedts diiïerenrirt roles lbr ocrldccanoidhiosynthesis in the localversus ílc sysremic wound rcsponse. plarlJ.32:585 60r.

SLr$hnanr, J.W, rud Ryan, C.A. 1997. Myelin bAíic prDtciD kinNc activir) in lol)rotoIc0vcs is nrduccd syíenicrliy by wornding d incrcuscs in respo0se ro syÍeniD lndoljgosncchrride eliciton. Ptr).. Narl..tcarí S./: UJi4 9:t:11085-t 1089.

Stràt'n.nn,J.,SchecrJ., lld Rfdn, C.À. 2000. Suraurin inhjbns i tilttion of defense signAL-nrg by sysLenrin, chiLoslrn, and I f'-ghcan elicitor in Nustcnsion-culLurcd. ,)..?a.rt o,t)?tuyhnun .ells. lt t:. Nqtl. Acdi. S.i. USA 97:aa62-8867 .

S1umm. D., lnd ceiÍlcr C. 1986. ltotc of papill@ tn Lh€ induccd sysromic rcsisLanceof oucu'nbe$ ignirsl Cdk,oitiNhu lagaluiuht plrtio!. Mat. pt4nt p\thot.2}AAS-4t0.

'Ih.rin, J.P, cubb,1.R., drd Wildon, D.C 1995. DcpohrizLÍion of romlto lc.f.elti byoligogalacturonidc clicitos t,L\nt Cell Ehni hn. ta:2lt -2t4.

Thalc\ J.S., Fidrntscl A.L., Dl|1.ey, S.S., and Bosrock, tt M. 1999 .ftrdc oïIs in plarldciinse againÍ ltlhoecns aid he rivorcs: a Íeld dcnoníuLior of chcm ical elcnorÍ dt.nduced resiitdncc.I CÀzn. Eol 25:159'1 t60.)

ThoDna, B.P.H.J., ng8erDonL. K., Pcnnnrckx, l.^M.A., Mauch-M$i, 8., Vogèlsxng,R., Canmue, B PA, and Brcckaerr, WF t998. Sepautc jasnoDatc depeidenr ardsalicylare-dependenr defeDse rcsponse paíhways in Arabi.topsís .re esenLiLn bf fcÍstrDcc to distiÍcl microbirl p.lrhogens. Ptu.. Nan. A.dd. S.i. U.tÁ95:1510?,1511t.

Thotmr4 B.PH.J., Eggenonr, K., ficrcns. K.HM., and Brlckaeí, WF. 1999. Reqntre-denr offuncLionat.rÀ)tcnr-;rr.rrirÀ,s 2 Sene fof eficieDt rcsjslance of,,l/.àil.)P\N k)infeclidr by a,rr.rtr ./u,rca . phtt phrlid. t21:1093- 1102.

lhulke, O.U.. ard Cormh, LJ. 1998 Salicytic aci.t has a dual tule jn rhe acLiv ionofdcfense{clared gcnes in parslcy. pt ní.t. t4:3542.

195

Ton, J., Davison, S., Var Wees. S.C.lvL, Van l.oon, L C., ind Piete$e. C.M..Í. 2001. The,4rrórlrprr /,!? / locns conlntlittg Èizobacteda mediated induced syíeni. resistanceis invohcd iD elhylène signalln5. Plànt Phlsial. 125:652 66).

'ron, J., De Vos, M., Robben. C., Blchala, 4.J., Mélralx. L P. Van l-ooD, L.C.. and Pictene,C.M.J.2002a. Clidacte satiotr of,{fabidrpr;r enhanced diseasc susceptibiliLy mutanlsthal {e aflecLed in systemically indDced resjítan.e. Pldr-l.29r11 21.

Ton,1., Van Pelt,.l.A., Vm Loon. L.C.. and Piolese. C.M.J.2002b. Ditrerenlial eftbctivene$ of saticylate-detendenr and jàsnonate/cthylcnc{cpendonl iDduced resistancc jn

Attbila?sh. Mal. Plant Micrcbe tntentt.15:21 34.van Loon, L C., and van Sxien, D.^. | 999. the faDilies of pathogenesis rclated poteiN.

their activities, and compdative amlysis of PR 1 lype p|otei$. Prlriol. Mal Pldrr

van LooD, I-.C., Bal<keÍ, PA.H.NI., and Pietcrse. C.M.J. | 998. systemic tesistance itrducedby rhizoslhclc bacteria. A'ru. Rev. Phltopatl@l. 36t153483.

Van Wees, S.C.M., PieteÍse, C.M.i.. TriFsÈMat 4., V$ 't WeÍende. Y.AM.. Htutog, E,and Vm Loon, L.C. I 997. Ditferential induction of systerjc tesiÍance in ArrDidopsi tby biocoDt ol baclena. M'l Pldnl Mittube ldencí. lt:tt 1tOJ24.

Van Wees, S.C.M.. Luijend,jk, M., Snioorcnburg, L. lrn Loon. L.C., and PieteNc, C.M.r'1999. Rhizobàcteria-mediated indDced systcnic rcsistaÍce (lSR) in Á/arildzrd is notasocirlcd wiLh a diÍecleÍfecr on knovn dciensc-gcnes bu1 $limulates the expression ofthejaÍnonak'n ucible gene Áinv,tP ulon cfi0lleÍge. Pla,lt I|oL. Bkn.1l:537-549.

Van wocs, S.C.M., De Swad, E.A.M., van Pclt, .1.A., Van Loon, L.c, and Pieteltc,C.M.J. 2000 EnhancemenL oi induccd disca$e rcsisrmce by sim{llaneors activltbnof salicllrre- dd jasmonate-depe dcnt dclbÍse pÀthwAys ln A l,ilotlit thtli<uLo. P tóc.Natl. Acd4. S.i. USA 91 187 | \-81 | 6.

Vlnacken H., L$, H., Ratc, D.N., rÍd Creenberg, J.l 200I À rolc th salicyllc rc andNPRI in rcguhdng ccll grcw t\ in Afttlrilats is. Purtt J.281209-216.

Vctsch, M., Jffzik, Í.. dnd Sch^llcr, A 2000. Chaructcrizxlion ol pÍ)ryíemjn Èxprcsscd inthe baculovirus/insccL oell slstem rcvcals bnnogical AoLivity ol nro systcmh Prccusor

Villn, A.,llenry-Vim, C , Sch0ntz, R., Ledoigt, G., I'IrcIissc, J.-M., Dcsbiez. M -O , andJulicr,.l.-L. 1996. Is ncnbfanc potentièl involvcd i'l crlDodulin gdc extrerrioD aiicrcxternd srimuldtior ir pl!$ts? FEBS Lzu.380t93 96

vidal, S., Poncc dc Léon, L, DÈnecke, J., and Palvd, T.E. I 997. S aLicylic .cid and thc PlunLp Ího9cn Etuini| qtutorott indDcc dcilnse gcdes vir iogonistic falhways Pr,z/I11115 t23.

Vijayan, P., Shockey, J., lrvcsltD, C.A., Cook, R.J., and BroNsc..l. 1998 A rolc 1bfjasmonaLe in prlhogcn dc1è è trt Atubitlopsh. Ptoc. Naíl. AuIl. Sti UJx 95:7209-1214.

walker Sinmors, M.K., ^nd

Ryan, C.^. I 97?. lnnnDological identiÍiolrion ol rÍoleirascinbibit()rs I and lIiniso]atcdlenl !àcuoles PlariPl]sioi Ó0:6|{3.

Walling. L.L.2000. The mynrd platrr rcsponses to herLr\laÈs. J. PLult Gtu\|íh Rcsutl9:195 216.

wdng, c., Zicn, c.A., Alitlhile, M.. wclri, R., HildebraÍd, D.F.. md wang, x. 2000. Itrvolvcnrcnl ol phospholipasc D in woud-induced accumllalion ofjxsbonic acld nrAnbi.lop\js. Plant C?11 12:2237-2246.

WeyNnnr K., Hunl, M., likncs. S., Neuenschwander. U.. Lawton, K., Steine!, U. Y, xndRyals, J. 1995. Slppressjon ald restauratun of lesion fomnrion in,l,?Óid,l'r;s kln\tants. PLafi C.ll lt20l3 2022.

196 8. Siglaling in Pldt Resistdce Responses

Xu, Y, Chatrg, P.-F- L., Liu. D.. NamiDhu, M.L., Raghothama, K.G., Hsegaw4 P.M.,and BÍossàn, R.A. 1994. Ptmt defense genês de syneÍgbtically irduced by ethylene ardnethyl jasmonate. Pldrr Cell 611077-1085.

Z€hnder, c.W. Murphr J.F., Sikom, E.J., and Kloeppea J.w 200i. Application of Íhi-zobrcleria ïor induced resisbn.e. Eut J. Pla í Pathol. 107:39-50.

ziesler, J., Keinànen, M., ard Baldwin, 1 2001 . Heóivore'induced allene oxjdê synthasetranscripts ánd jdlnonic acid ií Nicoíiána dtteMaía. Pb)tochefritjtry 581'7291X4

ZiÍmerli, L., JÀkab. G.. MéÍaux, J.P., aod Mauch-Mani, B. 2000. Potentiation ofpathogen-lpecific defeffe nechanism, inÁ/artdopris by betá"animburyÍi,c

^cid. Proc. NatL Acad

Sc i. USA 97 112920-12925.Zimmorll L., Méhaux, J.P., ard Mauch-Mani, B. 2001. Ê-aminobutyri. Àcid-in&crd pro-

ieation of àEridoprts agaiÍst lhê necro$ophic tunels Batryns ciwrea. Plaht Phyiol.126:517-523.

Sadik TuzunElizabeth Bent(Editors)

Multigenic and InducedSystemic Resistance in Plants

à Springer

Delartment of Entomologysíd PlaDt Pathology

USA

Elizateth BetrtDepaÍlÍnent of Plant PathologyUliversity of CalifomiaRiveside, CA 92521USA

LibrÀry of CongB$ Cotrfol Nunbd: 2004063216

IsBN-lor 0-387-23265-6 e.rsBNr tr387-23266.4 printêd on rcid-f!.e papq.lsBN-13r 9?8"038?-23265-2

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