Resistance to pathogens and host ... - Wiley Online Library

Review

Blackwell Publishing Ltd

Tansley review Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom

Author for correspondence: Eric Galiana Tel: +33 492 38 64 72 Fax: +33 492 38 65 87 Email: [email protected]

Marie-Pierre Develey-Rivière and Eric Galiana UMR1064 Interactions Plantes–Microorganismes et Santé Végétale, INRA-Université Nice Sophia-Antipolis-CNRS, F 06903 Sophia Antipolis Cedex, France

Received: 22 February 2007 Accepted: 18 April 2007

Contents Summary

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I.

Introduction

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II.

The many forms of developmental resistance

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III.

Molecular mechanisms of developmental resistance

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IV.

Relationships between defense and development in plants

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V.

Concluding remarks

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Acknowledgements

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References

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Summary Key words: disease resistance, host development, plant kingdom, plant– pathogen interactions.

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 plant–pathogen 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 developing hosts and may have practical applications, making it possible to reduce pesticide 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: 405–416 No claim to original French government works. Journal compilation © New Phytologist (2007) doi: 10.1111/j.1469-8137.2007.02130.x

I. Introduction Plant disease resistance depends on many factors, including environmental conditions, the nature of the infected tissue

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

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in this factor being largely ignored in molecular analysis. Thus the influence of plant development on disease resistance is a crucial break in our understanding of plant–pathogen interactions. Nonetheless, in many plant–pathogen interactions, the expression of resistance depends on the developmental stage at which the plant is infected. Plants are generally more susceptible to disease in early than in late phases. This may reflect an increase in resistance over time, with plants already resistant to a pathogen increasing their ability to control infection and colonization at a precise growth phase. Alternatively, a host plant susceptible to a virulent pathogen at early stages of growth may acquire disease resistance during its development. This increase or acquisition of resistance to pathogenic infections as a function of plant development has been given several names: ‘ontogenic resistance’, ‘developmental resistance’, ‘mature seedling resistance’, ‘adult seedling resistance’ and ‘age-related resistance’ (Whalen, 2005). This pluralism in denomination reflects the fact that different laboratories have studied this form of resistance independently. However, it also indicates the polymorphic nature of the phenomenon and the various stages associated with resistance, depending on the plant–pathogen interaction considered. This type of resistance may also be referred to as ‘flowering-induced resistance’ or ‘senescence-induced resistance’, depending on the timing of 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 physiological process or developmental stage. However, this generic term can be used to cover all forms of resistance positively correlated with host plant development, despite phenotypic and molecular variations. This term has the advantage of distinguishing developmental resistances from all other forms of resistance. It is also consistent with the available data showing that the mechanisms involved in ARR differ in nature or in aspects of regulation from the mechanisms used in response to infection in the well-known two-branched innate plant defense system (Chisholm et al., 2006; Jones & Dangl, 2006) which result in the hypersensitive response (HR), systemic acquired resistance (SAR) or induced systemic resistance (ISR). However, it has the drawback of reducing the resistance–development relationship in plants to a single form of resistance, thereby masking its considerable diversity. Many studies have been published on this phenomenon within the plant kingdom, testifying to its extent. Resistance acquisition during development has been reported for a large number of model and crop plants, both monocotyledons and dicotyledons (Table 1). The developmental stage at which resistance occurs depends on the plant considered but, once induced, this resistance generally persists throughout the rest of the life cycle of the plant. It may provide protection against a specific pathogen or have broad-spectrum activity. This resistance is thus of clear agronomic interest, but remains little used. This is largely a result of a lack of understanding of the

New Phytologist (2007) 175: 405–416

genetic, molecular and cellular mechanisms leading to the establishment of a form of resistance related to plant development (Panter & Jones, 2002; Whalen, 2005). The few studies devoted to this subject to date have either investigated the functional 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 possible approaches emerge: to characterize some important aspects of agonistic or antagonistic connections between defense and development pathways; to reveal the diversity of defense reactions which remain to be explored in the different botanical families; and to elucidate what causes pathogen growth arrest in 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 host development has only just begun. Current knowledge is based on detailed, precise phenomenological description at the plant level for many hosts of different botanical families (Table 1), which has revealed various characteristics of these forms of resistance (Fig. 1). 1. Resistance and developmental transitions Resistance to diseases may develop gradually during the life of the plant but is often associated with major transitions occurring during the plant life cycle (Poethig, 2003; Bäurle & Dean, 2006). Thus, resistance may be established at the time of the juvenile/adult transition during vegetative growth, at the flowering transition or with the onset of senescence. Mechanisms controlling developmental transitions may also govern the expression of resistance. The genetic demonstration of such causal relationships is an important step towards understanding the processes of induction of these forms of resistance and an essential element of studies of links between defense and development. Maize (Zea mays) is one of the rare plant species for which a genetic study has shown a direct effect of a developmental transition (juvenile/adult) on a susceptibility/resistance transition. In the Corngrass1 mutant (Cg1), the juvenile-vegetative phase is extended, and adult resistance to common rust (Puccinia sorghi) is delayed. Cg1 mid-whorl leaves continue to display juvenile traits and their susceptibility to P. sorghi is similar to that in Cg1 and wild-type seedling leaves, whereas wild-type mid-whorl leaves are resistant (Abedon & Tracy, 1996). The expression of adult characteristics is therefore necessary for leaf resistance to P. sorghi in maize. The acquisition of resistance during the vegetative phase has also been described for soybean (Glycine max; Paxton & Chamberlain, 1969; Lazarovits et al., 1980), bean (Phaseolus vulgaris; Bateman &

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No claim to original French government works. Journal compilation © New Phytologist (2007) www.newphytologist.org

Table 1 Examples of developmental resistance in different botanical families (the host plant, the pathogen and the developmental context associated with the onset of resistance are indicated) Host plant

Pathogen

Onset of resistance

References

Poaceae

Rice (Oryza sativa)

Xanthomonas oryzae pv. oryzae

Vegetative phase

Xanthomonas campestris pv. oryzae Pyricularia oryzae

Vegetative phase Vegetative phase

Wheat (Triticum aestivum)

Puccinia graminis f.sp. tritici

Maize (Zea mays)

P. recondita f.sp. tritici Puccinia sorghi

Flowering transition or juvenile/adult transition Vegetative phase Juvenile/adult transition

Mazzola et al. (1994); Century et al. (1999); Wang et al. (2006) Koch & Mew (1991) Andersen et al. (1947); Kahn & Libby (1958) Sunderwirth & Roefls (1980); Knott (1971) Pretorius et al. (1988) Headrick & Pataky (1987); Abedon & Tracy (1996)

Grape (Vitis vinifera)

Uncinula necator

Fruit ripening

Vitis labruscana

Guignardia bedwellii; Botrytis cinerea

Fruit ripening

Delp (1954); Chellemi & Marois (1992); Tattersall et al. (1997) Salzman et al. (1998)

Soybean (Glycine max) Common bean (Phaseolus vulgaris) Cowpea (Vigna unguiculata)

Phytophthora sojae Phytophthora sojae Rhizoctonia solani Uromyces vignae

Vegetative phase Vegetative phase Vegetative phase Vegetative phase

Lazarovits et al. (1980) Paxton & Chamberlain (1969) Bateman & Lumsden (1965) Heath (1994)

Rosaceae

Strawberry plant (Fragaria) Apple tree (Malus atrosanguinea)

Botrytis cinerea Venturia inaequalis

Vegetative phase Leaf maturity

Cooley et al. (1996) Li & Xu (2002)

Brassicaceae

Arabidopsis thaliana

Turnip (Brassica rapa) Cabbage (Brassica oleracea) Rape (Brassica napus)

Pseudomonas syringae pv. tomato Pseudomonas syringae pv. maculicola Cauliflower mosaic virus Hyaloperonospora parasitica Emco5 Cauliflower mosaic virus Hyaloperonospora parasitica Leptosphaeria maculans

Vegetative/flowering transition Vegetative/flowering transition Vegetative/flowering transition Vegetative phase Vegetative phase Juvenile/adult transition Juvenile/adult transition

Kus et al. (2002) Kus et al. (2002) Leisner et al. (1993) McDowell et al. (2005) Leisner et al. (1992) Coelho et al. (1998) Ballinger & Salisbury (1996)

Malvaceae

Cotton (Gossypium hirsutum)

Rhizoctonia solani

Vegetative phase

Hunter et al. (1977)

Solanaceae

Tobacco (Nicotiana tabacum)

Phytophthora parasitica Hyaloperonospora tabacina

Flowering transition Flowering transition or vegetative phase Flowering phase Vegetative phase Flowering transition or vegetative phase

Hugot et al. (1999) Reuveni et al. (1986); Wyatt et al. (1991) Yalpani et al. (1993a,b) Kim et al. (1989) Panter et al. (2002); Parniske et al. (1997)

Vitaceae

Fabaceae

Pepper (Capsicum annuum) Tomato (Lycopersicon esculentum)

Tobacco mosaic virus Phytophthora capsici Cladosporium fulvum

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Fig. 1 Developmentally regulated responses controlling plant–pathogen interactions. The ontogenic transition leading to the acquisition of resistance to a pathogen is indicated for each host plant. When known, developmental (Corngrass1 (CG1)) or resistance genes (Xanthomonas 21 (Xa21), resistance to Peronaspora parasitica (RPP31), Cladosporium fulvum9B (Cf-9B)) and signaling elements regulating developmental responses are also mentioned.

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 was discussed 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), has shown that the establishment of resistance to Phytophthora parasitica occurs between 70 and 75 d after seed germination, at the time of floral transition (Hugot et al., 1999). Studies using several ecotypes of Arabidopsis and various photoperiod conditions have shown that the transition from the vegetative phase to the floral phase is correlated with the induction of resistance to cauliflower mosaic virus (CaMV) and to Pseudomonas syringae (Leisner et al., 1993; Rusterucci et al., 2005). In both cases, a delay in flowering is accompanied by a delay in the expression of resistance. Floral transition was shown to be required for acquired resistance to CaMV by analysis of the terminal flower 1 (tfl1) mutant. TFL1 encodes a protein that plays an important role in floral induction and in maintenance of the floral identity of the apical meristem (Shannon & Meeks-Wagner, 1991). Its inactivation leads to early flowering and early resistance to CaMV (Leisner et al.,


1993). As in maize, changes in developmental stage disturb the expression of resistance in Arabidopsis. Other studies have suggested that resistance may be correlated with the onset of leaf senescence. However, in Arabidopsis, ARR to P. syringae is not correlated with induction of senescenceassociated gene 13 (SAG13), a marker of the prechlorotic stage of senescence (Weaver et al., 1998). Thus, mature Arabidopsis plants express ARR before the occurrence of senescence (Kus et al., 2002). 2. Resistance and tissue maturity Several plant species develop resistance that is restricted to a given tissue or organ, as a function of the maturity of that tissue or organ. For example, in soybean, resistance to Phytophthora sojae in hypocotyl varies with tissue maturity (Lazarovits et al., 1980). Tissues formed later in development are highly susceptible, whereas the older tissues remain asymptomatic. Fruit maturation may also be directly correlated with the induction of resistance. This phenomenon has been studied in particular detail for grapevine (Vitis vinifera, V. labruscana). Uncinula necator, the grape powdery mildew fungus, like other ascomycetes, is unable to initiate new infections of the berry during ripening (Delp, 1954; Tattersall et al., 1997; Salzman et al., 1998). A kinetic study has shown that resistance is expressed only when sugar


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concentrations in the grape reach a threshold value (Chellemi & Marois, 1992), and that this involves an enhancement of the antifungal activity of defense-related proteins (cf. Tattersall et al., 1997; Salzman et al., 1998). Many other studies have demonstrated 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 between leaf maturity and leaf rank. Indeed, it is clear that leaves of different ranks and maturities have different physiological characteristics, which may interfere with the expression of resistance. For example, leaf maturity in rice (Oryza sativa) has no effect on the degree of resistance to Xanthomonas campestris pv. 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 the fungus P. sorghi, whereas leaves with adult features (from node 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 the juvenile stage to the adult stage also delays the acquisition of resistance (Abedon & Tracy, 1996). Most studies on other plant species have evaluated plant resistance in leaves of different 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 could account for the influence of leaf rank on the expression of resistance. Zeier (2005) reported age-dependent variations in the local and systemic defense responses of Arabidopsis leaves to an avirulent strain of P. syringae. Younger leaves of Arabidopsis generally invested in more pronounced inducible defenses than older leaves, although both ended up with similar levels of resistance. However, in this study, the agerelated resistance was not active in the exanimate plants. 3. Increased or acquired resistance and plant development Host plants may acquire resistance or display an increase in resistance with development (Fig. 2). Thus, in adult rice plants, resistance to different isolates of Xanthomonas oryzae pv. oryzae or Xanthomonas campestris pv. oryzae increases in a non-race-specific manner at later growth stages (Mew et al., 1981; Mazzola et al., 1994; Century et al., 1999). Similar increases have been observed in the resistance of wheat (Triticum aestivum) and tomato (Lycopersicon esculentum) to various fungi (Knott, 1968, 1971; Sunderwirth & Roefls, 1980; Parniske et al., 1997; Panter et al., 2002) and in that of tobacco to tobacco mosaic virus (TMV) (Yalpani et al., 1993b). Several plants also acquire resistance to virulent pathogens during the course of development. For example, ecotypes of N. tabacum, G. max and Arabidopsis that are susceptible to the oomycetes Peronospora tabacina, Phytophthora sojae and


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Fig. 2 Illustration of increased (a) and acquired (b) resistance during tobacco (Nicotiana tabacum) development. (a) Leaves from 8-wk-old (left) or 12-wk-old (right) N. tabacum cv. xanthi nc. NN plants (bearing the N gene, which confers resistance to tobacco mosaic virus) were inoculated on the same day with a suspension of viral particles (100 µg ml–1) of tobacco mosaic virus. Five days after inoculation, fewer and smaller hypersensitive response-associated necrotic 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 a suspension (100 cells µl–1) of Phytophthora parasitica zoospores (agent of black shank disease). Five days after inoculation, the acquisition of resistance to the oomycete at late developmental stages results in the absence (black arrow) or a reduction (80%) of disease symptoms (white arrow).

Hyaloperonospora parasitica, respectively, gradually become resistant to these pathogens during the course of their development (Bhattacharyya & Ward, 1986; Reuveni et al., 1986; Rusterucci et al., 2005). A similar phenomenon is observed in wheat and rice for the expression of resistance to 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 several pathogens, a particular pathovar or a given strain or race of pathogen. In cases of race-specific resistance, the expression of resistance is generally associated with the functional regulation of plant resistance (R) genes. The influence of development on


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race-specific resistance genes has been studied in detail in rice and wheat, to assist breeders in their decision-making processes. The effects of plant age on resistance were therefore first described in 1947 for rice (Andersen et al., 1947) and in 1959 for wheat (Samborski & Ostapyk, 1959). Several R genes conferring resistance to Xanthomonas have been identified in rice. Two of these genes, Xa6 and Xa21, confer developmentally controlled resistance to Xanthomonas campestris pv. oryzae and to X. oryzae pv. oryzae, respectively (Koch & Mew, 1991; Mazzola et al., 1994; Century et al., 1999). In wheat, several varieties harbor genes conferring resistance to certain species of the Puccinia genus. In the leaf rust (Lr) and stem rust (Sr) gene families, only a few genes confer developmental resistance to P. recondita f.sp. tritici (Pretorius et al., 1988) and Puccinia graminis f.sp. tritici (Knott, 1968, 1971; Sunderwirth & Roefls, 1980), respectively. The resistance conferred by the other Lr and Sr genes is not influenced by plant development. Similar observations have been reported for tomato. Thus, the homolog of Cladosporium resistance genes Hcr9-9A, Hcr9-9B and Hcr9-9th confer resistance to different strains of Cladosporium fulvum expressed only at specific developmental phases (Parniske et al., 1997; Hammond-Kosack et al., 1998; Panter et al., 2002). The other genes of this family confer constitutive resistance. In Arabidopsis, the developmental regulation of resistance to the Emco5 isolate of H. parasitica has been reported for the Colombia (Col-0) ecotype, but not for the Wassilewskija (WS-0) ecotype. The inoculation of Col-0 with another virulent strain of H. parasitica, Ahco2, leads to the development 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 resistance involves 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 two different oomycetes, Peronospora tabacina and Phytophthora parasitica (Reuveni et al., 1986; Wyatt & Kuc, 1990; Hugot et al., 1999), and TMV (Yalpani et al., 1993b). After the onset of ripening, grape berries express resistance to three ascomycetes (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 similarly be altered in mature tissues, although this remains to be demonstrated. The importance of control of the infectious cycle has been highlighted for the resistance of two crucifers, Arabidopsis and turnip (Brassica rapa), to CaMV (Leisner et al., 1992, 1993). In these two host plants, long-distance transport of the virus occurs in the phloem. During the course of host development, sink–source relationships change and the region of plants that CaMV can invade is progressively reduced, leading to resistance. In both plants, resistance results from the control of viral migration. Thus, the ability of other viruses using the same strategy of migration via the


phloem to colonize parts of the plant may also be restricted at later stages of plant development. Finally, race-specific and nonspecific resistance may have additional effects. Developmental resistance in tobacco harboring the N gene for resistance to TMV leads to decreases in both HR lesion size and infection efficiency (Fig. 2). Thus, mechanisms other than those involved in HR and functional regulation of the N gene are involved. Similarly, in soybean, race-specific ARR to race 4 of P. sojae (Lazarovits et al., 1980) and nonspecific ARR to other races of P. sojae, which does not depend on the developmental regulation of a resistance gene (Paxton & Chamberlain, 1969), are additive.

III. Molecular mechanisms of developmental resistance 1. Developmental induction of defense mechanisms If we consider the well-known sequential triptych of perception– transduction–expression which governs the induction of plant defense responses to pathogen infection (for a review, see Yang et al., 1997), influences of developmental stage at each of the main three steps of the cascade have been reported in relation to expression of resistance in different plant species (Fig. 1). Developmental resistance may initially involve the functional regulation of R genes. Studies of rice resistance to X. oryzae pv. oryzae and of tomato resistance to C. fulvum conferred by Xa21 and Hcr9-9B, respectively, have shown that the developmental regulation of R gene promoters is not important. Indeed, the expression of Xa21 is independent of rice developmental stage, wounding or infection with X. oryzae pv. oryzae (Century et al., 1999). The Xa21 gene encodes a receptor-like protein kinase, which may be involved in recognizing a pathogen ligand and activating an intracellular kinase, leading to a defense response (Song et al., 1995). The autophosphorylation of Ser686, Thr688 and Ser689 of XA21, which functions to stabilize XA21 against developmentally controlled proteolytic activity (Xu et al., 2006), and the XA21 binding protein 3 ubiquitin ligase XB3 (Wang et al., 2006) contribute to Xa21-mediated resistance. Similarly, the Hcr9-9B promoter is also functional at stages of development during which tomato plants are susceptible to C. fulvum (Panter et al., 2002). These studies indicate that developmental regulation of the resistances mediated by the Hcr9-9B and Xa21 genes is controlled post-transcriptionally or by other factors, as has been suggested for the N. tabacum–TMV (Yalpani et al., 1993b) and G. max–P. sojae (Bhattacharyya & Ward, 1986) interactions. For the signal transduction step, the establishment of ARR in N. tabacum and Arabidopsis may require the activation of a salicylic acid (SA)-dependent pathway (Fig. 1). A strong correlation between the degree of resistance to TMV and SA concentrations in the leaves of flowering tobacco plants has been reported (Yalpani et al., 1993b). Studies on NaHG


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tobacco plants, expressing the bacterial salicylate hydroxylase Nahg gene and unable to accumulate SA (Gaffney et al., 1993), led to delineate the requirement for SA of developmental resistance to P. parasitica. Mechanisms controlling infection efficiency are induced by an SA-independent pathway, whereas mechanisms controlling intercellular colonization are induced by an SA-dependent pathway (Hugot et al., 1999). Thus, while SA is necessary and sufficient for SAR establishment (Malamy et al., 1990; Metraux et al., 1990; Rasmussen et al., 1991; Ward et al., 1991; Gaffney et al., 1993), activation of the SA cascade alone is not sufficient for expression of all the features of ARR. The activation of several different transduction pathways may be necessary for the expression of all the resistance characteristics for a given pathogen. In Arabidopsis, SA has been shown to have a variable influence on the expression of ARR to different pathogens. SA is required for effective resistance against the bacterium P. syringae and the oomycete H. parasitica Emco5 (Kus et al., 2002; Cameron & Zaton, 2004; McDowell et al., 2005), but is not essential for the expression of ARR to H. parasitica Noco2 (Rusterucci et al., 2005). Moreover, analyses of mutants affected in the SA-dependent pathway have shown that the function of NPR1 (nonexpressor of pathogenesis related (PR) genes) is required for the establishment of SAR (Dong, 2004) and ISR (Pieterse et al., 1996), and for ARR to H. parasitica Emco5 (McDowell et al., 2005), but not for ARR to P. syringae (Kus et al., 2002; McDowell et al., 2005). There are therefore clearly several different pathways contributing to developmental resistance, at least in Arabidopsis and tobacco. Concerning the last step of the triptych of perception– transduction–expression for plant defense responses, many studies have reported the accumulation of pathogenesisrelated PR proteins during development, independently of infection. PR gene expression (including PR-1a and PR-2, two molecular markers for SAR) has been observed in the flowers (Lotan et al., 1989; Neale et al., 1990), leaves (Fraser, 1981) and roots (Neale et al., 1990) of healthy tobacco. In various plants, PR protein accumulation is often correlated with the expression of resistance. In particular, in tobacco and grapevine, 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. tabacina is associated with the developmental expression of β-(1→3)-glucanases, chitinases and peroxidases (Wyatt et al., 1991), whereas resistance to TMV and P. parasitica is correlated with the PR-1a and PR-2 proteins (Yalpani et al., 1993b; Hugot et al., 1999). In addition, whereas pathogen-induced systemic acquired resistance leads mainly to the up-regulation of defense-related genes (Maleck et al., 2000), developmental resistance involves the up-regulation not only of defense-related genes but also of genes involved in modifying or strengthening the cell wall to prevent pathogen invasion (Hugot et al., 2004). In grapevine,


Review

resistance is associated with expression of the genes encoding PR-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 antifungal proteins is strictly coordinated with hexose accumulation, and this accumulation constitutes a developmentally controlled defense response (Fig. 1). Indeed, the activity of antifungal proteins in vitro is increased by glucose (Salzman et al., 1998). These authors suggested that the observed enhancement of antifungal protein activity by sugars may be a result of the disruption of fungal gene regulation by sugar repression (Ronne, 1995). The sugar repression of genes involved in pathogenesis or virulence might be facilitated by the putative membrane pore-forming activities of proteins of the PR-5 family (Roberts & Selitrennikoff, 1990; Abad et al., 1996), enhancing the uptake of sugars into the cell. Transcriptome analysis has characterized two waves of developmental defense activations in the early and late phases of barley (Hordeum vulgare) embryo development that may determine crucial defenses against pathogens. The early wave of activation takes place when the embryo is still developing, in parallel with up-regulation of the 9-LOX (lipoxygenase) pathway. The second wave of activation is initiated before grain desiccation, with the up-regulation of several PR genes and of genes encoding proteins with antioxidant responses (Nielsen et al., 2006). In Arabidopsis, PR-1 gene expression is transiently induced in leaves and this expression begins in the prefloral phase, but there is no correlation between the ARR response and expression of this molecular marker for SAR (Rusterucci et al., 2005). All these studies highlight our lack of knowledge concerning the exact role of plant defense responses in the expression of developmental resistance. They also demonstrate the need for further studies to elucidate the influence of developmental stage on the activation of plant defenses. They also clearly show, as illustrated in the next section, that there are uncharacterized mechanisms of plant defense and that further studies of the cellular and molecular basis of the various forms of resistance are required. 2. Unexplored regulation of plant–pathogen interactions Once a plant has fully developed its defense mechanisms, how does it control the colonization of resistant tissues by pathogens? The dissection of hypersensitive and induced resistance responses has shown that plants employ a panoply of defense strategies, from the sacrifice of some cells to save the plant as a whole to the development of antimicrobial compounds. Compounds accumulating in late phases of host plant development may enable the plant to inhibit the infectious cycles of certain pathogens. At the moment, it would be difficult to draw up a complete list of these compounds, to determine their role in resistance and to evaluate their role in controlling the initiation of infection or colonization by


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pathogens. However, the great diversity of situations in which resistance is acquired during development in the host plant suggests that a great number of processes or molecules may disturb the growth of various pathogens in planta. During tobacco and Arabidopsis development, the transition from susceptibility to resistance to P. parasitica and P. 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 in tobacco was characterized based on in vitro survival and assays of P. parasitica zoospore germination. This activity was detected in intercellular fluids from healthy tobacco leaves committed to flowering and was correlated with the control of infection observed once resistance has been established. It seems to constitute a developmentally regulated mechanism inhibiting the early steps of pathogen invasion by causing the death of P. parasitica cells. This cytotoxic activity was not detected in intercellular fluids from susceptible plants or from plants in which SAR had been induced, whereas it was detected in NahG transgenic plants that did not accumulate salicylic acid. In Arabidopsis, antibacterial activity (present in intercellular fluids from mature plants previously inoculated with P. syringae and subsequently displaying ARR) significantly inhibited the growth of P. syringae by 20–46% (Kus et al., 2002). In this plant, SA accumulation in the intercellular space is critical for antibacterial activity, as shown by the inhibition of Pseudomonas syringae in vitro and the in planta rescue of ARR-defective mutants by SA management (Cameron & Zaton, 2004). There are therefore two important differences in intercellular cytotoxic activity between tobacco and Arabidopsis: SA accumulation does not involve pathogen-induced responses in tobacco and does not reflect an increase in the requirement for SA. In addition to providing opportunities for characterizing new and diverse host molecules influencing pathogen growth in planta, analyses of the relationship between resistance and host development may bring to light new aspects of plant–pathogen interactions that have yet to be explored. With a view to characterizing the apoplastic molecules required for cytotoxic activity in tobacco, the form of host-induced cell death has been described in P. parasitica. Apoplastic molecules have been shown to induce a form of vacuolar cell death in the oomycete. The single-celled zoospores undergo a form of cell death characterized by dynamic membrane rearrangements, cell shrinkage, the formation of numerous large vacuoles in the cytoplasm and the degradation of cytoplasmic components followed by plasma membrane disruption. Phytophthora parasitica cell death requires protein synthesis but not caspase activation, and is associated with the production of intracellular reactive oxygen species (Galiana et al., 2005). Thus, the activation of programmed cell death processes in a pathogen, like host hypersensitive cell death, is involved in regulating plant–pathogen interactions. The importance of pathogen cell death in the regulation of a plant–pathogen interaction has been confirmed by studies on the rice blast


fungus Magnaporthe grisea, which requires autophagic cell death for rice infection (Veneault-Fourrey et al., 2006).

IV. Relationships between defense and development in plants The expression of resistance to disease during host development is only one aspect of the connection between defense and development processes in plants. A second is the involvement of plant hormones in many aspects of plant development and plant–pathogen interactions (Raskin, 1992; Johnson & Ecker, 1998; Mayda et al., 2000; Mauch-Mani & Mauch, 2005). SA, jasmonic acid, ethylene and abscisic acid have been studied in detail, to determine their effects on the expression of resistance. However, each of these hormones is known to play a crucial role in various development processes. For example, endogenous SA has been shown to be involved in 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 development and defenses concerns the molecular conservation of transduction pathways governing various processes. Thus, different members of the same family may be involved in defense responses or developmental processes. Structural and functional similarities between R gene products and developmental proteins have raised the possibility of overlapping functions, cross-talk and a possible evolutionary relationship between the receptors and their associated pathways (Jeong et al., 1999; Ellis et al., 2000; Dangl & Jones, 2001; Whalen, 2005). To illustrate this point, the Toll/interleukin-1 receptor– nucleotide binding site–leucine-rich repeat (TIR-NBS-LRR)type gene is of particular interest. Studies in Arabidopsis established that interactions with pathogens and developmental responses to neighbour plants share core-signaling components. Indeed, the analysis of the constitutive shade-avoidance mutant csa1 (displaying shade-avoidance responses in the absence of shade) implicates TIR-NBS-LRR proteins in photomorphogenic development. RPS4, conferring resistance to P. syringae pv tomato strain DC3000 (avrRps4) (Gassmann et al., 1999), complements the csa1 developmental mutant phenotype which is caused by a mutation in CSA1, the closest homolog of RPS4. Thus, the dual role of the TIR domain implicated in both development and immunity in Drosophila melanogaster and Caenorhabditis elegans appears to be conserved in Arabidopsis (Faigon-Soverna et al., 2006). Downstream in the signaling cascades, mechanisms similar to those formally associated with plant defenses also seem to be used to control developmental patterning. Two NPR1-like genes 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. Like NPR1, BOP2 is found in both the nucleus and the cytoplasm and interacts preferentially in yeast with the transcription


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factor encoded by PERIANTHIA (PAN). PAN belongs to the same family as TGA2, TGA3, TGA6, and TGA7, which interact with NPR1, controlling PR1 expression during SAR. This indicates that there may be a regulatory mechanism common to plant morphogenesis and plant–pathogen interactions (Hepworth et al., 2005). The available data thus converge to suggest that there are similarities in the regulation of cell–cell communications in the pathological and developmental contexts. However, little is known about the molecular support for putative cross-talk and functional overlap in the signal transduction network. The two NPR1 homologs BOP1 and BOP2 are probably not involved in disease resistance signaling as bop1 bop2 mutants are neither more susceptible 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 defense responses and plant development. Losses and gains of TGA2.1 and TGA2.2 function have shown that TGA2.2 is of major importance for SA-inducible gene expression, whereas TGA2.1 (which interacts with tobacco NPR1) is dispensable for SA-inducible gene expression, but plays a regulatory role in correct stamen development (Thurow et al., 2005). More generally, several examples of Arabidopsis mutants in defense-related genes with developmental effects or in developmental genes with effects on defense have been reported (for a review, see Whalen, 2005). However, not enough is known in this emerging field about the way in which developmental function may influence defense function and vice versa in plants.

V. Concluding remarks Studies on developmentally acquired resistance have provided new insight into basic mechanisms regulating plant–pathogen interactions and into agrosystem monitoring. The polymorphic character of developmental resistance makes it necessary to study the various forms of this resistance in as many current and alternative model organisms as possible. Such studies should provide a more exhaustive evaluation of the levels of plant defense operating during host development and of the diversity of plant defenses, which remains to be explored in most botanical families. They will also advance our knowledge of the complex antagonistic or agonist relations between development and defense programs. A precise definition of the defense and resistance potential of each host plant throughout its life cycle is a key element for the control of pathogen infection, and is essential to ensure high crop yields. In the context of integrated crop management, developmental resistance is considered as an important factor in the rationalization of cultural practices for vines and is being evaluated for use in several other crop species (Cooley et al., 1996; Ficke et al., 2002). The occurance of an effective resistance in the field should make it possible to refine models for forecasting plant disease epidemics and for optimizing farm


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practices in terms of pesticide application, so that pesticides can be applied for shorter periods of high host susceptibility and the most effective treatments can be used (Gadoury et al., 2003; Kennelly et al., 2005; Fletcher et al., 2006). The many examples of relationships between resistance to pathogens and host development should be examined in an evolutionary context (Dobzhansky, 1973). These relationships may partly account for the organization of defense networks according to a Darwinian selection process. The earliest phases of angiosperm evolution were characterized by extensive developmental experimentation, structural lability (Friedman, 2006) and acclimation to stresses, enabling the plants to cope with environmental changes. The identification of similar transduction pathways governing various developmental or defense processes in different plants suggests that these pathways have been conserved through evolution. Plants may therefore have acquired some capacity to resist pathogens by adaptation or exaptation (the acquisition by a protein of a function other than that for which it was originally selected; Gould & Vrba, 1982) of physiological or developmental functions. Different components of defense responses may therefore not only defend the plant against stresses, in addition to those exerted by plant pathogens, but also play other roles in plant development, structure and function (Heath, 1991).

Acknowledgements Profound thanks go to the former and present members of our research group at UMR1064 IPMSV Sophia-Antipolis for their substantial contributions to our work. Marie-Pierre Rivière-Develey was supported by a fellowship from INRA and the Association pour la Recherche sur les Nicotianées.

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