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Resistance to pathogens and hostdevelopmental stage: a multifacetedrelationship within the plant kingdom

Marie-Pierre Develey-Rivire and Eric Galiana

UMR1064 Interactions PlantesMicroorganismes et Sant Vgtale, INRA-Universit Nice

Sophia-Antipolis-CNRS, F 06903 Sophia Antipolis Cedex, France

Contents

Summary 405

I. Introduction 405

II. The many forms of developmental resistance 406

III. Molecular mechanisms of developmental 410resistance

IV. Relationships between defense and 412development in plants

V. Concluding remarks 413

Acknowledgements 413

References 413

Author for correspondence:

Eric Galiana

Tel: +

33 492 38 64 72

Fax: +33 492 38 65 87

Email: [email protected]

Received: 22 February 2007

Accepted: 18 April 2007

Key words:

disease resistance, host

development, plant kingdom, plant

pathogen interactions.

Summary

The induction of resistance to disease during plant development is widespread in the

plant kingdom. Resistance appears at different stages of host development, varies

with plant age or tissue maturity, may be specific or broad-spectrum and is driven

by diverse mechanisms, depending on plantpathogen interactions. Studies of these

forms of resistance may help us to evaluate more exhaustively the plethora of levels

of regulation during development, the variability of the defense potential of devel-

oping hosts and may have practical applications, making it possible to reduce pesti-

cide applications. Here, we review the various types of developmental resistance in

plants and current knowledge of the molecular and cellular processes involved in

their expression. We discuss the implications of these studies, which provide new

knowledge from the molecular to the agrosystem level.

New Phytologist(2007) 175: 405416

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Journal compilation New Phytologist(2007)

doi: 10.1111/j.1469-8137.2007.02130.x

I. Introduction

Plant disease resistance depends on many factors, includingenvironmental conditions, the nature of the infected tissue

and the genotypic combination of the host species and thepathogen. Plant development is just as important, but is farless frequently taken into account. The necessary simplificationof biological models for analysis and exploitation has resulted


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in this factor being largely ignored in molecular analysis. Thusthe influence of plant development on disease resistance isa crucial break in our understanding of plantpathogeninteractions. Nonetheless, in many plantpathogen interactions,the expression of resistance depends on the developmentalstage at which the plant is infected. Plants are generally moresusceptible to disease in early than in late phases. This may

reflect an increase in resistance over time, with plants alreadyresistant to a pathogen increasing their ability to controlinfection and colonization at a precise growth phase.

Alternatively, a host plant susceptible to a virulent pathogenat early stages of growth may acquire disease resistance duringits development.

This increase or acquisition of resistance to pathogenicinfections as a function of plant development has been givenseveral names: ontogenic resistance, developmental resist-ance, mature seedling resistance, adult seedling resistanceand age-related resistance (Whalen, 2005). This pluralism indenomination reflects the fact that different laboratories have

studied this form of resistance independently. However, it alsoindicates the polymorphic nature of the phenomenon and thevarious stages associated with resistance, depending on theplantpathogen interaction considered. This type of resist-ance may also be referred to as flowering-induced resistanceor senescence-induced resistance, depending on the timingof its onset. The denomination age-related resistance (ARR)

was one of the first to be proposed (Lazarovits et al

., 1980; Kus

et al

., 2002), and does not relate to any particular physiolog-ical process or developmental stage. However, this genericterm can be used to cover all forms of resistance positively cor-related with host plant development, despite phenotypic and

molecular variations. This term has the advantage of distin-guishing developmental resistances from all other forms ofresistance. It is also consistent with the available data showingthat the mechanisms involved in ARR differ in nature or inaspects of regulation from the mechanisms used in response toinfection in the well-known two-branched innate plantdefense system (Chisholm et al

., 2006; Jones & Dangl, 2006)which result in the hypersensitive response (HR), systemicacquired resistance (SAR) or induced systemic resistance(ISR). However, it has the drawback of reducing the resist-ancedevelopment relationship in plants to a single form ofresistance, thereby masking its considerable diversity.

Many studies have been published on this phenomenon

within the plant kingdom, testifying to its extent. Resistanceacquisition during development has been reported for a largenumber of model and crop plants, both monocotyledons anddicotyledons (Table 1). The developmental stage at whichresistance occurs depends on the plant considered but, onceinduced, this resistance generally persists throughout the restof the life cycle of the plant. It may provide protection againsta specific pathogen or have broad-spectrum activity. Thisresistance is thus of clear agronomic interest, but remains littleused. This is largely a result of a lack of understanding of the

genetic, molecular and cellular mechanisms leading to theestablishment of a form of resistance related to plant develop-ment (Panter & Jones, 2002; Whalen, 2005). The few studiesdevoted to this subject to date have either investigated thefunctional regulation of resistance (

R

) or defense genes (Century

et al

., 1999; Hugot et al

., 1999; Panter et al

., 2002; McDowell

et al

., 2005) or proposed new mechanisms that have yet to be

explored (Hugot et al

., 1999, 2004; Kus et al

., 2002; Galiana

et al

., 2005). From these studies (Fig. 1), several possibleapproaches emerge: to characterize some important aspects ofagonistic or antagonistic connections between defense anddevelopment pathways; to reveal the diversity of defense reac-tions which remain to be explored in the different botanicalfamilies; and to elucidate what causes pathogen growth arrestin resistant plants ( Jones & Dangl, 2006).

II. The many forms of developmental resistance

The genetic and molecular dissection of the mechanisms

underlying the emergence of disease resistance during hostdevelopment has only just begun. Current knowledge is basedon detailed, precise phenomenological description at the plantlevel for many hosts of different botanical families (Table 1),

which has revealed various characteristics of these forms ofresistance (Fig. 1).

1. Resistance and developmental transitions

Resistance to diseases may develop gradually during the lifeof the plant but is often associated with major transitionsoccurring during the plant life cycle (Poethig, 2003; Burle &

Dean, 2006). Thus, resistance may be established at the timeof the juvenile/adult transition during vegetative growth, atthe flowering transition or with the onset of senescence.Mechanisms controlling developmental transitions may alsogovern the expression of resistance.

The genetic demonstration of such causal relationships isan important step towards understanding the processes ofinduction of these forms of resistance and an essential elementof studies of links between defense and development. Maize(

Zea mays

) is one of the rare plant species for which a geneticstudy has shown a direct effect of a developmental transition(juvenile/adult) on a susceptibility/resistance transition. Inthe Corngrass1

mutant (

Cg1

), the juvenile-vegetative phase is

extended, and adult resistance to common rust (

Pucciniasorghi

) is delayed. Cg1

mid-whorl leaves continue to displayjuvenile traits and their susceptibility to P. sorghi

is similar tothat in

Cg1

and wild-type seedling leaves, whereas wild-typemid-whorl leaves are resistant (Abedon & Tracy, 1996). Theexpression of adult characteristics is therefore necessary forleaf resistance to P. sorghi

in maize. The acquisition of resist-ance during the vegetative phase has also been describedfor soybean (

Glycine max

; Paxton & Chamberlain, 1969;Lazarovits et al

., 1980), bean (

Phaseolus vulgaris

; Bateman &


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Lumsden, 1965), cowpea (Vigna unguiculata; Heath, 1994),cabbage (Brassica oleracea; Coelho et al., 1998) and cotton(Gossypium hirsutum; Hunter et al., 1977). However, the

correlation of resistance with the juvenile/adult transition wasdiscussed only for cabbage.A correlation between floral transition and resistance has

been reported in Nicotiana tabacum (Wyatt et al., 1991;Hugot et al., 1999) and Arabidopsis (Leisner et al., 1993;Rusterucci et al., 2005). A kinetic analysis on tobacco plants,aged 50 d (vegetative phase) to 120 d (flowering phase), hasshown that the establishment of resistance to Phytophthora

parasiticaoccurs between 70 and 75 d after seed germination,at the time of floral transition (Hugot et al., 1999). Studiesusing several ecotypes of Arabidopsis and various photoperiodconditions have shown that the transition from the vegetativephase to the floral phase is correlated with the induction of

resistance to cauliflower mosaic virus (CaMV) and to Pseu-domonas syringae (Leisner et al., 1993; Rusterucci et al.,2005). In both cases, a delay in flowering is accompanied bya delay in the expression of resistance. Floral transition wasshown to be required for acquired resistance to CaMV byanalysis of the terminal flower 1 (tfl1) mutant. TFL1 encodesa protein that plays an important role in floral induction andin maintenance of the floral identity of the apical meristem(Shannon & Meeks-Wagner, 1991). Its inactivation leads toearly flowering and early resistance to CaMV (Leisner et al.,

1993). As in maize, changes in developmental stage disturbthe expression of resistance in Arabidopsis.

Other studies have suggested that resistance may be correlated

with the onset of leaf senescence. However, in Arabidopsis, ARRto P. syringaeis not correlated with induction of senescence-associated gene 13 (SAG13), a marker of the prechloroticstage of senescence (Weaver et al., 1998). Thus, mature

Arabidopsis plants express ARR before the occurrence ofsenescence (Kus et al., 2002).

2. Resistance and tissue maturity

Several plant species develop resistance that is restricted toa given tissue or organ, as a function of the maturity ofthat tissue or organ. For example, in soybean, resistance toPhytophthora sojae in hypocotyl varies with tissue maturity

(Lazarovits et al., 1980). Tissues formed later in developmentare highly susceptible, whereas the older tissues remainasymptomatic. Fruit maturation may also be directlycorrelated with the induction of resistance. This phenomenonhas been studied in particular detail for grapevine (Vitisvinifera, V. labruscana). Uncinula necator, the grape powderymildew fungus, like other ascomycetes, is unable to initiatenew infections of the berry during ripening (Delp, 1954;Tattersall et al., 1997; Salzman et al., 1998). A kinetic studyhas shown that resistance is expressed only when sugar

Fig. 1 Developmentally regulated responsescontrolling plantpathogen interactions.The ontogenic transition leading to theacquisition of resistance to a pathogen isindicated for each host plant. When known,developmental (Corngrass1 (CG1)) orresistance genes (Xanthomonas21 (Xa21),resistance to Peronaspora parasitica (RPP31),Cladosporium fulvum9B (Cf-9B)) andsignaling elements regulating developmentalresponses are also mentioned.


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concentrations in the grape reach a threshold value (Chellemi& Marois, 1992), and that this involves an enhancement ofthe antifungal activity of defense-related proteins (cf. Tattersallet al., 1997; Salzman et al., 1998). Many other studies havedemonstrated an effect of leaf maturity. For example, in apple(Malus atrosanguinea) trees, leaf maturity is positively correlated

with resistance to the fungus Venturia inaequalis(Li & Xu,

2002). In such analyses, it is important to distinguish betweenleaf maturity and leaf rank. Indeed, it is clear that leaves ofdifferent ranks and maturities have different physiologicalcharacteristics, which may interfere with the expression ofresistance. For example, leaf maturity in rice (Oryza sativa) hasno effect on the degree of resistance toXanthomonas campestrispv. oryzae, whereas leaf rank does have an effect (Koch & Mew,1991). During vegetative growth, maize leaves expressing

juvenile traits (first five to six nodes) are susceptible to thefungus P. sorghi, whereas leaves with adult features (fromnode 8 to the terminal tassel) express resistance to this fungus(Hooker, 1985; Headrick & Pataky, 1987; Poethig, 2003). A

genetic study has shown that delaying transition from thejuvenile stage to the adult stage also delays the acquisition ofresistance (Abedon & Tracy, 1996). Most studies on otherplant species have evaluated plant resistance in leaves ofdifferent ranks rather than in leaves differing in maturity(Hooker, 1985; Headrick & Pataky, 1987; Pretorius et al.,1988; Roumen et al., 1992; Yalpani et al., 1993b; Kus et al.,2002). These studies have generated few data that couldaccount for the influence of leaf rank on the expression ofresistance. Zeier (2005) reported age-dependent variations inthe local and systemic defense responses of Arabidopsis leavesto an avirulent strain of P. syringae. Younger leaves of

Arabidopsis generally invested in more pronounced inducibledefenses than older leaves, although both ended up withsimilar levels of resistance. However, in this study, the age-related resistance was not active in the exanimate plants.

3. Increased or acquired resistance and plantdevelopment

Host plants may acquire resistance or display an increase inresistance with development (Fig. 2). Thus, in adult riceplants, resistance to different isolates ofXanthomonas oryzaepv. oryzaeorXanthomonas campestrispv. oryzaeincreases in anon-race-specific manner at later growth stages (Mewet al.,

1981; Mazzola et al., 1994; Century et al., 1999). Similarincreases have been observed in the resistance of wheat(Triticum aestivum) and tomato (Lycopersicon esculentum) tovarious fungi (Knott, 1968, 1971; Sunderwirth & Roefls,1980; Parniske et al., 1997; Panter et al., 2002) and in that oftobacco to tobacco mosaic virus (TMV) (Yalpani et al., 1993b).Several plants also acquire resistance to virulent pathogensduring the course of development. For example, ecotypes ofN. tabacum, G. maxand Arabidopsis that are susceptible tothe oomycetes Peronospora tabacina, Phytophthora sojae and

Hyaloperonospora parasitica, respectively, gradually becomeresistant to these pathogens during the course of theirdevelopment (Bhattacharyya & Ward, 1986; Reuveni et al.,1986; Rusterucci et al., 2005). A similar phenomenon isobserved in wheat and rice for the expression of resistanceto the pathogenic fungi Puccinia recondita f.sp. tritici and

Pyricularia oryzae (Andersen et al., 1947; Kahn & Libby,1958; Pretorius et al., 1988; Roumen et al., 1992).

4. Specific and broad-spectrum resistance

Age-related resistance may be effective against severalpathogens, a particular pathovar or a given strain or race ofpathogen. In cases of race-specific resistance, the expression ofresistance is generally associated with the functional regulationof plant resistance (R) genes. The influence of development on

Fig. 2 Illustration of increased (a) and acquired (b) resistanceduring tobacco (Nicotiana tabacum) development. (a) Leaves from8-wk-old (left) or 12-wk-old (right) N. tabacum cv.xanthi nc. NNplants (bearing the N gene, which confers resistance to tobaccomosaic virus) were inoculated on the same day with a suspension ofviral particles (100 g ml1) of tobacco mosaic virus. Five days afterinoculation, fewer and smaller hypersensitive response-associatednecrotic spots are present on the leaf taken from a flowering plant(arrows). (b) Two leaves from 6-wk-old (left) or 10-wk-old (right)N. tabacum cv.xanthi nc. NN plants were inoculated with asuspension (100 cells l1) of Phytophthora parasitica zoospores(agent of black shank disease). Five days after inoculation, theacquisition of resistance to the oomycete at late developmentalstages results in the absence (black arrow) or a reduction (80%)of disease symptoms (white arrow).


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race-specific resistance genes has been studied in detail in riceand wheat, to assist breeders in their decision-makingprocesses. The effects of plant age on resistance were thereforefirst described in 1947 for rice (Andersen et al., 1947) and in1959 for wheat (Samborski & Ostapyk, 1959). Several Rgenes conferring resistance toXanthomonashave been identifiedin rice. Two of these genes, Xa6andXa21, confer develop-

mentally controlled resistance toXanthomonas campestrispv.oryzaeand toX. oryzaepv. oryzae, respectively (Koch & Mew,1991; Mazzola et al., 1994; Centuryet al., 1999). In wheat,several varieties harbor genes conferring resistance to certainspecies of the Pucciniagenus. In the leaf rust (Lr) and stemrust (Sr) gene families, only a few genes confer developmentalresistance to P. reconditaf.sp. tritici(Pretorius et al., 1988) andPucciniagraminisf.sp. tritici(Knott, 1968, 1971; Sunderwirth& Roefls, 1980), respectively. The resistance conferred by theother Lrand Srgenes is not influenced by plant development.Similar observations have been reported for tomato. Thus, thehomolog ofCladosporiumresistance genes Hcr9-9A, Hcr9-9B

and Hcr9-9th confer resistance to different strains ofCladosporium fulvumexpressed only at specific developmentalphases (Parniske et al., 1997; Hammond-Kosacket al., 1998;Panter et al., 2002). The other genes of this family conferconstitutive resistance. In Arabidopsis, the developmentalregulation of resistance to the Emco5 isolate ofH. parasiticahasbeen reported for the Colombia (Col-0) ecotype, but not for the

Wassilewskija (WS-0) ecotype. The inoculation of Col-0 withanother virulent strain ofH. parasitica, Ahco2, leads to the devel-opment of identical symptoms on both young and mature plants.These results indicate that the resistance to H. parasitica(Emco5) developed by the Col-0 ecotype is race-specific. By

crossing Col-0 and Ws-0, it has been shown that resistanceinvolves a recessive resistance gene (McDowell et al., 2005).Some lines of evidence indicate that major developmental

changes also induce effective broad-spectrum resistance.During flowering growth, tobacco expresses resistance to twodifferent oomycetes, Peronospora tabacina and Phytophthora

parasitica(Reuveni et al., 1986; Wyatt & Kuc, 1990; Hugotet al., 1999), and TMV (Yalpani et al., 1993b). After the onsetof ripening, grape berries express resistance to three ascomy-cetes (Delp, 1954; Chellemi & Marois, 1992; Tattersall et al.,1997; Salzman et al., 1998). For pathogens of the same family(Oomycetes or Ascomycetes), the infectious cycle may simi-larly be altered in mature tissues, although this remains to be

demonstrated. The importance of control of the infectiouscycle has been highlighted for the resistance of two crucifers,

Arabidopsis and turnip (Brassica rapa), to CaMV (Leisneret al., 1992, 1993). In these two host plants, long-distancetransport of the virus occurs in the phloem. During the courseof host development, sinksource relationships change andthe region of plants that CaMV can invade is progressivelyreduced, leading to resistance. In both plants, resistanceresults from the control of viral migration. Thus, the ability ofother viruses using the same strategy of migration via the

phloem to colonize parts of the plant may also be restricted atlater stages of plant development.

Finally, race-specific and nonspecific resistance may haveadditional effects. Developmental resistance in tobacco har-boring the Ngene for resistance to TMV leads to decreases inboth HR lesion size and infection efficiency (Fig. 2). Thus,mechanisms other than those involved in HR and functional

regulation of the Ngene are involved. Similarly, in soybean,race-specific ARR to race 4 ofP. sojae(Lazarovits et al., 1980)and nonspecific ARR to other races ofP. sojae, which does notdepend on the developmental regulation of a resistance gene(Paxton & Chamberlain, 1969), are additive.

III. Molecular mechanisms of developmentalresistance

1. Developmental induction of defense mechanisms

If we consider the well-known sequential triptych of perception

transductionexpression which governs the induction of plantdefense responses to pathogen infection (for a review, see Yanget al., 1997), influences of developmental stage at each of themain three steps of the cascade have been reported in relationto expression of resistance in different plant species (Fig. 1).

Developmental resistance may initially involve the functionalregulation ofRgenes. Studies of rice resistance to X. oryzaepv. oryzaeand of tomato resistance to C. fulvumconferredbyXa21 and Hcr9-9B, respectively, have shown that thedevelopmental regulation ofRgene promoters is not im-portant. Indeed, the expression ofXa21 is independent of ricedevelopmental stage, wounding or infection with X. oryzae

pv. oryzae (Century et al., 1999). The Xa21 gene encodes areceptor-like protein kinase, which may be involved in reco-gnizing a pathogen ligand and activating an intracellularkinase, leading to a defense response (Song et al., 1995). Theautophosphorylation of Ser686, Thr688 and Ser689 of XA21,

which functions to stabilize XA21 against developmentallycontrolled proteolytic activity (Xu et al., 2006), and the XA21binding protein 3 ubiquitin ligase XB3 (Wang et al., 2006)contribute toXa21-mediated resistance. Similarly, the Hcr9-9Bpromoter is also functional at stages of development during

which tomato plants are susceptible to C. fulvum (Panteret al., 2002). These studies indicate that developmental regu-lation of the resistances mediated by the Hcr9-9BandXa21

genes is controlled post-transcriptionally or by other factors,as has been suggested for the N. tabacumTMV (Yalpaniet al., 1993b) and G. maxP. sojae (Bhattacharyya & Ward,1986) interactions.

For the signal transduction step, the establishment of ARRin N. tabacumand Arabidopsis may require the activationof a salicylic acid (SA)-dependent pathway (Fig. 1). A strongcorrelation between the degree of resistance to TMV and SAconcentrations in the leaves of flowering tobacco plants hasbeen reported (Yalpani et al., 1993b). Studies on NaHG


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tobacco plants, expressing the bacterial salicylate hydroxylaseNahggene and unable to accumulate SA (Gaffneyet al., 1993),led to delineate the requirement for SA of developmentalresistance to P. parasitica. Mechanisms controlling infectionefficiency are induced by an SA-independent pathway, whereasmechanisms controlling intercellular colonization are inducedby an SA-dependent pathway (Hugot et al., 1999). Thus, while

SA is necessary and sufficient for SAR establishment (Malamyet al., 1990; Metraux et al., 1990; Rasmussen et al., 1991; Wardet al., 1991; Gaffneyet al., 1993), activation of the SA cascadealone is not sufficient for expression of all the features of ARR.The activation of several different transduction pathways maybe necessary for the expression of all the resistance character-istics for a given pathogen. In Arabidopsis, SA has been shownto have a variable influence on the expression of ARR to dif-ferent pathogens. SA is required for effective resistance againstthe bacterium P. syringaeand the oomycete H. parasiticaEmco5(Kus et al., 2002; Cameron & Zaton, 2004; McDowell et al.,2005), but is not essential for the expression of ARR to

H. parasiticaNoco2 (Rusterucci et al., 2005). Moreover, ana-lyses of mutants affected in the SA-dependent pathway haveshown that the function ofNPR1 (nonexpressor of patho-genesis related (PR) genes) is required for the establishmentof SAR (Dong, 2004) and ISR (Pieterse et al., 1996), and for

ARR to H. parasiticaEmco5 (McDowell et al., 2005), but notfor ARR to P. syringae (Kus et al., 2002; McDowell et al.,2005). There are therefore clearly several different pathwayscontributing to developmental resistance, at least in Arabidopsisand tobacco.

Concerning the last step of the triptych of perceptiontransductionexpression for plant defense responses, many

studies have reported the accumulation of pathogenesis-related PR proteins during development, independently ofinfection. PRgene expression (including PR-1aand PR-2,two molecular markers for SAR) has been observed in theflowers (Lotan et al., 1989; Neale et al., 1990), leaves (Fraser,1981) and roots (Neale et al., 1990) of healthy tobacco. Invarious plants, PR protein accumulation is often correlated

with the expression of resistance. In particular, in tobacco andgrapevine, the accumulation of defense proteins is correlated

with resistance to viruses (Fraser, 1972; Takahashi, 1972), fungi(Tattersall et al., 1997; Salzman et al., 1998) or oomycetes(Reuveni et al., 1986; Wyatt et al., 1991; Hugot et al., 1999).The resistance of tobacco to P. tabacinais associated with the

developmental expression of-(13)-glucanases, chitinasesand peroxidases (Wyatt et al., 1991), whereas resistance toTMV and P. parasiticais correlated with the PR-1a and PR-2proteins (Yalpani et al., 1993b; Hugot et al., 1999). In addition,

whereas pathogen-induced systemic acquired resistanceleads mainly to the up-regulation of defense-related genes(Malecket al., 2000), developmental resistance involves theup-regulation not only of defense-related genes but also ofgenes involved in modifying or strengthening the cell wall toprevent pathogen invasion (Hugot et al., 2004). In grapevine,

resistance is associated with expression of the genes encodingPR-5 (thaumatin-like or osmotin), lipid transfer protein(LTP) and chitinases (Tattersall et al., 1997; Salzman et al.,1998). During fruit ripening, the accumulation of antifungalproteins is strictly coordinated with hexose accumulation, andthis accumulation constitutes a developmentally controlleddefense response (Fig. 1). Indeed, the activity of antifungal

proteins in vitrois increased by glucose (Salzman et al., 1998).These authors suggested that the observed enhancement ofantifungal protein activity by sugars may be a result of thedisruption of fungal gene regulation by sugar repression(Ronne, 1995). The sugar repression of genes involved inpathogenesis or virulence might be facilitated by the putativemembrane pore-forming activities of proteins of the PR-5family (Roberts & Selitrennikoff, 1990; Abad et al., 1996),enhancing the uptake of sugars into the cell. Transcriptomeanalysis has characterized two waves of developmental defenseactivations in the early and late phases of barley (Hordeumvulgare) embryo development that may determine crucial

defenses against pathogens. The early wave of activation takesplace when the embryo is still developing, in parallel withup-regulation of the 9-LOX (lipoxygenase) pathway. Thesecond wave of activation is initiated before grain desiccation,

with the up-regulation of several PR genes and of genesencoding proteins with antioxidant responses (Nielsen et al.,2006). In Arabidopsis, PR-1 gene expression is transientlyinduced in leaves and this expression begins in the prefloralphase, but there is no correlation between the ARR responseand expression of this molecular marker for SAR (Rusterucciet al., 2005).

All these studies highlight our lack of knowledge concerning

the exact role of plant defense responses in the expression ofdevelopmental resistance. They also demonstrate the need forfurther studies to elucidate the influence of developmental stageon the activation of plant defenses. They also clearly show, asillustrated in the next section, that there are uncharacterizedmechanisms of plant defense and that further studies of thecellular and molecular basis of the various forms of resistanceare required.

2. Unexplored regulation of plantpathogen interactions

Once a plant has fully developed its defense mechanisms, howdoes it control the colonization of resistant tissues by pathogens?

The dissection of hypersensitive and induced resistance responseshas shown that plants employ a panoply of defense strategies,from the sacrifice of some cells to save the plant as a whole tothe development of antimicrobial compounds.

Compounds accumulating in late phases of host plantdevelopment may enable the plant to inhibit the infectiouscycles of certain pathogens. At the moment, it would bedifficult to draw up a complete list of these compounds, todetermine their role in resistance and to evaluate their rolein controlling the initiation of infection or colonization by


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pathogens. However, the great diversity of situations in whichresistance is acquired during development in the host plantsuggests that a great number of processes or molecules maydisturb the growth of various pathogens in planta.

During tobacco and Arabidopsis development, the trans-ition from susceptibility to resistance to P. parasiticaandP. syringae(Fig. 1) is correlated with the accumulation of antioomycete

and antibacterial activities, respectively, in intercellular fluids(Hugot et al., 1999; Kus et al., 2002). Cytotoxic activity intobacco was characterized based on in vitrosurvival and assaysof P. parasitica zoospore germination. This activity wasdetected in intercellular fluids from healthy tobacco leavescommitted to flowering and was correlated with the control ofinfection observed once resistance has been established. Itseems to constitute a developmentally regulated mechanisminhibiting the early steps of pathogen invasion by causing thedeath of P. parasitica cells. This cytotoxic activity was notdetected in intercellular fluids from susceptible plants or fromplants in which SAR had been induced, whereas it was

detected in NahG transgenic plants that did not accumulatesalicylic acid. In Arabidopsis, antibacterial activity (present inintercellular fluids from mature plants previously inoculated

with P. syringaeand subsequently displaying ARR) significantlyinhibited the growth of P. syringae by 2046% (Kus et al.,2002). In this plant, SA accumulation in the intercellularspace is critical for antibacterial activity, as shown by theinhibition ofPseudomonas syringae in vitroand the in plantarescueof ARR-defective mutants by SA management (Cameron &Zaton, 2004). There are therefore two important differencesin intercellular cytotoxic activity between tobacco and Arabi-dopsis: SA accumulation does not involve pathogen-induced

responses in tobacco and does not reflect an increase in therequirement for SA. In addition to providing opportunitiesfor characterizing new and diverse host molecules influencingpathogen growth in planta, analyses of the relationshipbetween resistance and host development may bring to lightnew aspects of plantpathogen interactions that have yet to beexplored. With a view to characterizing the apoplastic mole-cules required for cytotoxic activity in tobacco, the form ofhost-induced cell death has been described in P. parasitica.

Apoplastic molecules have been shown to induce a form ofvacuolar cell death in the oomycete. The single-celled zoosporesundergo a form of cell death characterized by dynamic membranerearrangements, cell shrinkage, the formation of numerous large

vacuoles in the cytoplasm and the degradation of cytoplasmiccomponents followed by plasma membrane disruption. Phy-tophthora parasiticacell death requires protein synthesis butnot caspase activation, and is associated with the productionof intracellular reactive oxygen species (Galiana et al., 2005).Thus, the activation of programmed cell death processes in apathogen, like host hypersensitive cell death, is involved inregulating plantpathogen interactions. The importance ofpathogen cell death in the regulation of a plantpathogeninteraction has been confirmed by studies on the rice blast

fungus Magnaporthe grisea, which requires autophagic celldeath for rice infection (Veneault-Fourreyet al., 2006).

IV. Relationships between defense anddevelopment in plants

The expression of resistance to disease during host

development is only one aspect of the connection betweendefense and development processes in plants. A second is theinvolvement of plant hormones in many aspects of plantdevelopment and plantpathogen interactions (Raskin, 1992;

Johnson & Ecker, 1998; Mayda et al., 2000; Mauch-Mani &Mauch, 2005). SA, jasmonic acid, ethylene and abscisic acidhave been studied in detail, to determine their effects on theexpression of resistance. However, each of these hormones isknown to play a crucial role in various development processes.For example, endogenous SA has been shown to be involvedin the flowering of thermogenic plants (Raskin et al., 1987),flowering time regulation in Arabidopsis (Martinez et al., 2004),

and SAR signaling and disease resistance (Ryals et al., 1996).A third aspect of the relationship between plant develop-

ment and defenses concerns the molecular conservation oftransduction pathways governing various processes. Thus,different members of the same family may be involved indefense responses or developmental processes. Structural andfunctional similarities between Rgene products and develop-mental proteins have raised the possibility of overlappingfunctions, cross-talk and a possible evolutionary relationshipbetween the receptors and their associated pathways (Jeonget al., 1999; Ellis et al., 2000; Dangl & Jones, 2001; Whalen,2005). To illustrate this point, the Toll/interleukin-1 receptor

nucleotide binding siteleucine-rich repeat (TIR-NBS-LRR)-type gene is of particular interest. Studies in Arabidopsisestablished that interactions with pathogens and developmentalresponses to neighbour plants share core-signaling components.Indeed, the analysis of the constitutive shade-avoidancemutant csa1 (displaying shade-avoidance responses in theabsence of shade) implicates TIR-NBS-LRR proteins in photo-morphogenic development. RPS4, conferring resistance toP. syringae pv tomato strain DC3000 (avrRps4) (Gassmannet al., 1999), complements the csa1 developmental mutantphenotype which is caused by a mutation in CSA1, the closesthomolog ofRPS4. Thus, the dual role of the TIR domainimplicated in both development and immunity in Drosophila

melanogasterand Caenorhabditis elegansappears to be con-served in Arabidopsis (Faigon-Soverna et al., 2006).

Downstream in the signaling cascades, mechanisms similarto those formally associated with plant defenses also seem tobe used to control developmental patterning. Two NPR1-likegenes from Arabidopsis, blade-on-petiole 1 (BOP1) and BOP2,have redundant functions in controlling growth asymmetry,an important aspect of patterning in leaves and flowers. LikeNPR1, BOP2 is found in both the nucleus and the cytoplasmand interacts preferentially in yeast with the transcription


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factor encoded byPERIANTHIA(PAN). PAN belongs to thesame family as TGA2, TGA3, TGA6, and TGA7, whichinteract with NPR1, controlling PR1 expression during SAR.This indicates that there may be a regulatory mechanismcommon to plant morphogenesis and plantpathogen inter-actions (Hepworth et al., 2005). The available data thus con-verge to suggest that there are similarities in the regulation of

cellcell communications in the pathological and develop-mental contexts. However, little is known about the molecularsupport for putative cross-talk and functional overlap in thesignal transduction network. The two NPR1 homologsBOP1 and BOP2 are probably not involved in disease resist-ance signaling as bop1 bop2mutants are neither more suscep-tible nor more resistant than wild-type plants to challenge

with P. syringae pv. maculicola ES4326 (Hepworth et al.,2005). Tobacco transcription factors of the TGA family(TGA2.1 and TGA2.2) play different roles in plant defenseresponses and plant development. Losses and gains ofTGA2.1 and TGA2.2function have shown that TGA2.2 is of

major importance for SA-inducible gene expression, whereasTGA2.1 (which interacts with tobacco NPR1) is dispensablefor SA-inducible gene expression, but plays a regulatory rolein correct stamen development (Thurowet al., 2005).

More generally, several examples of Arabidopsis mutants indefense-related genes with developmental effects or in develop-mental genes with effects on defense have been reported (fora review, see Whalen, 2005). However, not enough is known inthis emerging field about the way in which developmentalfunction may influence defense function and vice versa in plants.

V. Concluding remarks

Studies on developmentally acquired resistance have providednew insight into basic mechanisms regulating plantpathogeninteractions and into agrosystem monitoring. The polymor-phic character of developmental resistance makes it necessaryto study the various forms of this resistance in as many currentand alternative model organisms as possible. Such studiesshould provide a more exhaustive evaluation of the levels ofplant defense operating during host development and of thediversity of plant defenses, which remains to be explored inmost botanical families. They will also advance our know-ledge of the complex antagonistic or agonist relations betweendevelopment and defense programs.

A precise definition of the defense and resistance potentialof each host plant throughout its life cycle is a key element forthe control of pathogen infection, and is essential to ensurehigh crop yields. In the context of integrated crop manage-ment, developmental resistance is considered as an importantfactor in the rationalization of cultural practices for vines andis being evaluated for use in several other crop species (Cooleyet al., 1996; Ficke et al., 2002). The occurance of an effectiveresistance in the field should make it possible to refine modelsfor forecasting plant disease epidemics and for optimizing farm

practices in terms of pesticide application, so that pesticidescan be applied for shorter periods of high host susceptibilityand the most effective treatments can be used (Gadouryet al.,2003; Kennellyet al., 2005; Fletcher et al., 2006).

The many examples of relationships between resistance topathogens and host development should be examined in anevolutionary context (Dobzhansky, 1973). These relation-

ships may partly account for the organization of defense net-works according to a Darwinian selection process. The earliestphases of angiosperm evolution were characterized by extensivedevelopmental experimentation, structural lability (Friedman,2006) and acclimation to stresses, enabling the plants to cope

with environmental changes. The identification of similartransduction pathways governing various developmental ordefense processes in different plants suggests that these path-

ways have been conserved through evolution. Plants maytherefore have acquired some capacity to resist pathogens byadaptation or exaptation (the acquisition by a protein of afunction other than that for which it was originally selected;

Gould & Vrba, 1982) of physiological or developmentalfunctions. Different components of defense responses maytherefore not only defend the plant against stresses, inaddition to those exerted by plant pathogens, but also playother roles in plant development, structure and function(Heath, 1991).

Acknowledgements

Profound thanks go to the former and present members of ourresearch group at UMR1064 IPMSV Sophia-Antipolis fortheir substantial contributions to our work. Marie-Pierre

Rivire-Develey was supported by a fellowship from INRAand the Association pour la Recherche sur les Nicotianes.

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