Virus Resistence

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Journal of Plant Pathology (2008), 90 (2), 153-171
Edizioni ETS Pisa, 2008
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INVITED REVIEW PLANT RESISTANCE RESPONSES TO VIRUSES

P. Palukaitis1 and J.P. Carr2
1 Scottish 2 Department
Crop Research Institute, Invergowrie, Dundee, DD2 5DA, UK of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK
SUMMARY
Plants have developed numerous approaches to resist infection by viruses. On the other hand, in many instances viruses have evolved to overcome these various resistance responses and barriers. The extent to which viruses can overcome some or all of these responses and barriers determines the extent to which they are able to colonize plants of a given genotype or species. Resistance against plant viruses occurs at different levels and by various mechanisms, most of which largely remain uncharacterized. Here, we will consider these various levels of resistance, as well as the types of resistance responses, the isolated genes involved in resistance, the signalling pathways that have been described, and the various resistance factors that have been implicated in resistance to specific viruses.
cells. With one exception, these are still the major forms of resistance that occur against virus infection (rev. by Bruening, 2006). Besides these various levels described below, resistance also occurs via the surveillance mechanism designated RNA silencing or RNA inhibition (RNAi). We will not consider RNAi in detail here, as it has been covered in many reviews in recent years (Brodersen and Voinnet, 2006; Burgyn, 2006; Li and Ding, 2006; Vaucheret, 2006; Ding and Voinnet, 2007). Nevertheless, the effects of RNAi may also be a contributing factor to either the various types of induced resistance or the barriers to infection described below.
TYPES OF RESISTANCE
INTRODUCTION
Francis Holmes (1946) made some poignant observations concerning the types of resistance plants have to viruses, when he examined the host range of Tobacco etch virus (TEV) and Tobacco mosaic virus (TMV) and showed that (besides whether or not the plants showed local or systemic symptoms) the plants responses could be divided into four categories (Table 1). He found that many plant species did not show detectable virus multiplication in the inoculated leaves, while other species did; however, there was also differentiation amongst the latter group as to whether the plant species become infected systemically or not. The proportion of plant species in each category differed between the two viruses. Four decades later, Zaitlin and Hull (1987) described resistance operating at four levels: inhibition of replication, cell-to-cell movement, and systemic infection (long-distance movement), as well as defense responses restricting infection to a limited number of
Corresponding author: P. Palukaitis Fax: +44. 1382.568523 E-mail: Peter.Palukaitis@scri.ac.uk
Complete resistance in a plant to virus infection is referred to as immunity (reviewed by Bruening, 2006). In plants that convey immunity to viruses in one genotype of a species but not another, the immunity is usually manifested in preventing virus replication. Usually, this is assessed in isolated, single cells (protoplasts), or multiple leaf cells co-infected by agroinfiltration of DNA expressing viral genomes. If immunity occurs against all biotypes of a pathogen and in all cultivars or accessions of a particular plant species the situation is referred to as non-host resistance. For viruses, this is a largely an unexplored area, although some strides are being made in understanding non-host resistance operating against fungi (reviewed by Ellis, 2006; Bittel and Robatzek, 2007; Hckelhoven, 2007; Wise et al., 2007; Hadwiger, 2008). Some resistance genes have been described as conveying extreme resistance (ER). In some cases these may actually convey immunity, in that no virus multiplication could be detected (Barker and Harrison, 1984; Watanabe et al., 1987) while in the case of Potato virus X (PVX), replication occurred to a limited extent and then an induced resistance occurred, leading to prevention of further replication (Khm et al., 1993). In cowpea (Vigna unguiculata) cv. Arlington, where a dominant resistance limiting accumulation of Cowpea mosaic virus (CPMV) in protoplasts was described, the resistance was due to inhibition of the polyprotein processing of this virus (Ponz et al., 1988).
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Resistance to viruses
In those instances where replication of viruses occurred at normal levels, but the virus was prevented from moving outside of the inoculated cells, a subliminal infection was said to occur (Sulzinski and Zaitlin, 1982) and further infection was thought to be inhibited by either a dysfunctional viral-encoded movement protein for that plant genotype or some barrier in that plant genotype that prevented the normal function of the viral movement protein (reviewed by Waigmann et al., 2004; Ueki and Citovsky, 2006). In some cases, specific resistance genes of the plant have been identified in blocking or preventing viral cell-to-cell movement, with corresponding changes occurring in mutants of those viruses that can overcome the resistance gene (reviewed by Kang et al., 2005a; Bruening, 2006). In some plant genotypes the virus can move cell-to-cell to a limited extent, before a multicellular hypersensitive response (HR) occurs, which first activates defense responses preventing the infection from spreading further and then kills the cells within the infected zone (reviewed by Gilliland et al., 2006a; Loebenstein and Akad, 2006). The ER and HR are referred to as types of innate resistance. Both are associated with dominant resistance genes (reviewed by Bruening, 2006; Maule et al., 2007). Plants undergoing an HR also induce a state of pathogen-nonspecific resistance called systemic acquired resistance (SAR) (reviewed by Gilliland et al., 2006a). SAR is activated by defense signalling responses and will be considered below. If no ER or HR occurs, then the virus may continue to spread cell-to-cell throughout the leaf, as well as into and within the vasculature. If the virus cannot spread to upper leaves of the plant, then it is likely that there is a barrier to infection preventing the virus from ingressing into the sieve elements of the phloem (Waigmann et al., 2004; Bruening, 2006; Ueki and Citovsky, 2006). This barrier may prevent movement into one or more of the cell types within the vasculature: bundle sheath cells, vascular or phloem parenchyma cells, and/or companion cells. Ingress into
the sieve element from the companion cells also may be blocked, as might egress from the sieve elements to companion cells, and then to other vascular cells, although data from grafting experiments tend to suggest that ingress rather than egress is the major barrier (Bruening, 2006). The above observations are consistent with the work of Holmes (1946) on the extent of virus infection in 310 species of plants infected by TMV vs. TEV (Table 1). He showed that infectivity could not be recovered from the inoculated leaves by back inoculation to a susceptible host from 111 of 310 plant species inoculated with TMV and 227 of 310 plant species inoculated with TEV; i.e., they were immune or possibly had a subliminal infection. On the other hand, infectivity could be recovered from the inoculated leaves, but not from the upper leaves of 127 (TMV) and 22 (TEV) inoculated plant species, while infectivity could be recovered from all leaves of 72 (TMV) and 61 (TEV) inoculated plant species. Infection of upper leaves may be limited to a few leaves, before the plant recovers. This may be a manifestation of age-related resistance, which appears to be a salicylic acid (SA)-mediated form of innate resistance (Garcia-Ruiz and Murphy, 2001), or may be due to the inability of the virus to completely block RNAi (Ji and Ding, 2001). Most viruses probably encode RNA silencing suppressors, which prevent one or more steps associated with RNAi (Li and Ding, 2006). In plants showing recovery from infection by nepoviruses and tobraviruses, recovery is due to a failure of the virus to prevent RNAi from being established ahead of the virus infection in upper, newly formed leaves (Ratcliff et al., 1997, 1999). This recovery from infection also occurs in some hosts after infection by Cauliflower mosaic virus (CaMV) (Covey et al., 1997). Tolerance is a manifestation of resistance in which the plants may show only mild or no symptoms as a function of infection (Bruening, 2006). In the experiments described by Holmes (1946), virus also could be
Table 1. Susceptibility types to Tobacco mosaic virus (TMV) and Tobacco etch virus (TEV) in 310 plant species tested.
Plant response No symptoms No recovered virus No symptoms Virus in inoculated leaves only Local symptoms Virus in inoculated leaves only No symptoms Virus in upper leaves Systemic symptoms Virus in inoculated leaves Inoculation with TMV No. of species 111 100 27 15 57 Inoculation with TEV No. of species 227 15 7 8 53
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recovered from various leaves of different plant species, whether they showed symptoms or not (Table 1). Where genes conferring tolerance have been delimited, multiple, recessive genes are involved (reviewed by Fraser, 1990, 1992; Kang et al., 2005a; Bruening, 2006; Maule et al., 2007). In addition, in most cases examined, tolerance is usually associated with a reduced titer of virus in the plants. The relationship between recovery and tolerance has not been investigated in detail, although in one instance, tolerance specified by two or three specific genes against Cucumber mosaic virus (CMV) in cucumber could be overcome by co-infection with Zucchini yellow mosaic virus (ZYMV), which increased CMV replication in the upper leaves (Wang et al., 2004). This suggests that tolerance may be a manifestation of RNAi operating against a specific virus.
RESISTANCE GENES
Many resistance genes have been described operating against specific viruses in particular crop species (reviewed by Fraser, 1990, 1992; Kang et al., 2005a; Bruening, 2006). Most of these resistance genes have not been isolated and so remain uncharacterized. Many more resistance genes operate as quantitative traits loci and thus function additively in conferring resistance (Maule et al., 2007). Nevertheless, in the past 15 years, more than 20 resistance genes have been isolated and characterized (Maule et al., 2007); most of them fall into two main groups in terms of common features, while the resistance genes that do not, appear quite different from the rest in form and presumably function. There is a general assumption that a dominant resistance gene reflects an encoded positive effect limiting or blocking a virus, while the allele for susceptibility does not have such a role. By contrast, a recessive resistance gene is thought to be one where the encoded protein is unable to function to promote virus infection, while its dominant allele conveying susceptibility can do so. Dominant resistance. Most of the resistance genes isolated are dominant genetically and are involved in resistances manifested by an HR or an ER (Maule et al., 2007). The proteins encoded by these resistance genes show considerable similarity in their organization, in which three functional domains have been defined: an N-terminal domain similar to either a Toll/interleukin-1 receptor (TIR) domain or a coiled-coiled (CC) protein domain; a nucleotide binding domain (NB); and a leucine-rich repeat (LRR) domain. These proteins are similar to those associated with resistance to bacteria, fungi, insects and nematodes (Jones and Dangl, 2001, 2006). They are all considered to be involved in activating defense signalling responses. A list of the virus resistance genes that encode such proteins is shown in
Table 2. These include several resistances operating against specific tobamoviruses, for which resistancebreaking strains have been isolated (Pelham, 1972; Hall, 1980; Tbis et al, 1982; Watanabe et al., 1987; Padgett and Beachy, 1993). Resistance-breaking strains have also been identified for the Rx gene operating against PVX (Moreira et al., 1980) and the Sw-5 gene conferring resistance to Tomato spotted wilt virus (TSWV) (Aramburu and Mart, 2003; Ciuffo et al., 2005). The dominant resistance genes that do not encode such defense signal response activation proteins include the Tm-1 gene from tomato and the genes associated with resistance to systemic infection by TEV in Arabidopsis thaliana. The Tm-1 gene product was found to block virus replication of both TMV and Tomato mosaic virus (ToMV) in protoplasts (Motoyoshi and Oshima, 1977; Fraser and Loughlin, 1980; Watanabe et al., 1987; Meshi et al., 1988; Ishibashi et al., 2007). The encoded protein, designated p80GCR237, is unrelated to any protein with a known function, but contains a TIM barrel structure identified in a wide variety of enzymes (Ishibashi et al., 2007). The resistance of some ecotypes of Arabidopsis thaliana to the systemic movement of TEV requires three genes designated RTM1, RTM2 and RTM3 (Chisholm et al., 2000), the last of which was not characterized. The RTM1 gene was shown to encode a protein similar to the lectin jacalin (Chisholm et al., 2000), while the RTM2 gene was shown to encode a 41 kDa protein similar to small heat-shock proteins, although its expression was not stimulated by heat nor did it function in thermotolerance (Whitham et al., 2000). Both the RTM1 and RTM2 genes were expressed exclusively in phloem-associated cells and the corresponding proteins localized to sieve elements (Chisholm et al., 2001). Therefore, these proteins presumably function in preventing long-distance movement of TEV in A. thaliana, by a yet unknown mechanism. Recessive resistance. Using a candidate gene approach, several laboratories have isolated recessive resistance genes (Table 2) conferring resistance against particular potyviruses (Ruffel et al., 2002, 2005, 2006; Nicaise et al., 2003; Gao et al., 2004; Kang et al., 2005b; Bruun-Rasmussen et al., 2007), the carmovirus Melon necrotic spot virus (MNSV) (Nieto et al., 2006), the bymoviruses Barley mild mosaic virus (BMMV) and Barley yellow mosaic virus (BYMV) (Kanyuka et al., 2005; Stein et al., 2005), and the sobemovirus Rice yellow mottle virus (RYMV) (Albar et al., 2006). These resistance genes all encode translation factors involved in the formation of the 40S ribosome complex required to initiate translation of RNAs (reviewed by Robaglia and Caranta, 2006). The resistance to various potyviruses is associated with the translation initiation factors eIF4E and eIF(iso)4E, while resistances to the bymoviruses and MNSV are associated with eIF4E only, and resistance to RYMV is associated with the trans-
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Table 2. Cloned genes conferring resistance to viruses.
Resistance genes Dominant genes N Rx1 Rx2 Sw-5 HRT RCY1 Y-1 Tm-2 Rsv1 Tm-2 RT4-4 RTM1 RTM2 Tm-1 PvVTT1 Recessive genes pvr1/pvr2 mol1/mol2 sbm1 rym4/5 pot-1 rymv1 nsv pvr2 + pvr6 C. annuum L. sativa P. sativum H. vulgare S. lycopersicum O. sativa C. melo C. annuum PVY, TEV LMV
2
Plant species
Virus targets
Reference
N. tabacum S. tuberosum S. tuberosum S. lycopersicum A. thaliana A. thaliana S. tuberosum S. lycopersicum G. max S. lycopersicum P. vulgaris A. thaliana A. thaliana S. lycopersicum P. vulgaris
TMV, ToMV a PVX PVX TSWV, TCSV, GRSV TCV CMV PVY ToMV, TMV SMV ToMV, TMV CMV TEV TEV TMV, ToMV BDMV
Whitham et al., 1994 Bendahmane et al., 1999 Bendahmane et al., 2000 Brommonschenkel et al., 2000 Cooley et al., 2000 Takahashi et al., 2002 Vidal et al., 2002 Lanfermeijer et al., 2003 Hayes et al., 2004 Lasfermeijer et al., 2005 Seo et al., 2006 Chisholm et al., 2000 Whitham et al., 2000 Ishibashi et al., 2007 Seo et al., 2007
Ruffel et al., 2002; Kang et al., 2005b Nicaise et al., 2003 Gao et al., 2004; Bruun-Rasmussen et al., 2007 Kanyuka et al., 2005; Stein et al., 2005 Ruffel et al., 2005 Albar et al., 2006 Nieto et al., 2006 Ruffel et al., 2006
PSbMV, BYMV BaMMV, BaYMV PVY, TEV RYMV MNSV PVY, TEV
(a) Virus names: Barley mild mosaic virus (BaMMV); Barley yellow mosaic virus (BaYMV); Bean dwarf mosaic virus (BDMV); Bean yellow mosaic virus (BYMV); Cucumber mosaic virus (CMV); Groundnut ringspot virus (GRSV); Lettuce mosaic virus (LMV); Melon necrotic spot virus (MNSV); Pea seed-borne mosaic virus (PSbMV); Pepper veinal mottle virus (PVMV); Potato virus X (PVX); Potato virus Y (PVY); Rice yellow mottle virus (RYMV); Soybean mosaic virus (SMV); Tobacco etch virus (TEV); Tobacco mosaic virus (TMV); Tomato chlorotic spot virus (TCSV); Tomato mosaic virus (ToMV); Tomato spotted wilt virus (TSWV); Turnip crinkle virus (TCV).
lation initiation factor eIF(iso)4G. The eIF4E translation initiation factor has been shown to interact with the VPg of several potyviruses viruses while the allelic mutants conveying resistance usually, but not always, failed to interact (Kang et al., 2005b; Michon et al., 2006; Beauchemin et al., 2007; Yeam et al., 2007; Charron et al.,
2008). A number of A. thaliana mutants that showed resistance to potyviruses also were associated with changes to eIF4E and eIF(iso)4E, while mutants conveying recessive resistance to CMV in A. thaliana were identified as being due to changes in eIF4E and eIF4G (reviewed by Robaglia and Caranta, 2006).
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DEFENSIVE SIGNALLING PATHWAYS IN RESISTANCE
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The occurrence of salicylic acid and its derivatives, during incompatible and compatible interactions with viruses. SA (2-hydroxybenzoic acid) plays a central role in the signal transduction pathway that results in SAR and it is required for localization of viral and other pathogens during the HR (reviewed by Alvarez, 2000). SA is required for the expression of a group of proteins that collectively are referred to as pathogenesis-related (PR) proteins (reviewed by Murphy et al., 1999; van Loon and van Strien, 1999). The ones described from tobacco do not appear to have any role in resistance to viruses, but are often used as markers of SAR. During virus-induced HR lesion development, SA biosynthesis occurs initially in and around the developing lesions, but later throughout the entire plant (Malamy et al., 1990; Mtraux et al., 1990; Huang et al., 2006; Nobuta et al., 2007; Strawn et al., 2007). Most of the SA produced is converted to a glucose conjugate (SA-2-O--D-glucoside; SAG) that accumulates within cell vacuoles (Enyedi et al., 1992; Hennig et al., 1993; Dean and Mills, 2004). It has been suggested that in SAR-expressing tissues, SAG represents a storage form of SA from which free, biologically active SA can be released in response to further infection (Hennig et al., 1993). The induction of SAR and, to some extent, maintenance of basal resistance to pathogen infection depends on SA-mediated signalling. Consequently, if SA accumulation is inhibited by engineering plants to express the salicylate-degrading enzyme SA hydroxylase (nahGtransgenic plants; Gaffney et al., 1993; Mur et al., 1997), or if SA production is decreased by mutation of SA biosynthetic genes (Nawrath and Mtraux, 1999; Wildermuth et al., 2001), plants are not able to express SAR and are super-susceptible to both virulent and avirulent pathogens. SA can be detected in phloem sap (Mtraux et al., 1990; Rasmussen et al., 1995), consistent with a role in the spread of SAR induction to all parts of the plant. However, results, sometimes conflicting with each other, obtained from grafting experiments with different nahG-transgenic tobacco lines (Vernooij et al., 1994; Darby et al., 2000) cast doubt on the idea that SA is necessarily an essential translocated signal in SAR induction. Subsequently, the isolation of the A. thaliana dir1 mutant, defective in a gene encoding a lipid transfer protein, suggested that a lipid or lipid-derived substance, possibly jasmonic acid (JA), could be the translocated SAR-inducing signal (Maldonado et al., 2002; Truman et al., 2007). Recently, work from the Klessig laboratory showed that transgenic plants silenced for the gene encoding a SA-binding (SABP2) were compromised in gene expression of PR proteins and SAR induction (Park et al., 2007). SABP2 is an es-
terase that can convert methyl salicylic acid (Me-SA) into SA (Kumar et al., 2006). Me-SA is produced in tissues undergoing an HR (Shulaev et al., 1997). It is a volatile chemical that can diffuse into the air and even induce SAR in nearby, non-infected plants (Shulaev et al., 1997). Taken together these studies provided evidence suggesting that Me-SA is an important long-distance signal in the induction of SAR following a HR. Although SA is needed for the maintenance of basal resistance, successful pathogen localization during the HR and the establishment of SAR, an increase in its biosynthesis can occur during a compatible interaction with certain virulent pathogens. With respect to virus infection, systemic, non-necrotizing infections do not normally trigger biosynthesis of SA and the consequent induction of SA-responsive genes (PR genes etc.) (Malamy et al., 1990; Whitham et al., 2003). However, SA-responsive gene expression has been observed in A. thaliana (Whitham et al., 2003; Huang et al., 2005) and increased SA accumulation was observed in potato (Krecic-Stres et al., 2005) and tobacco (A.M. Murphy and J.P. Carr, unpublished data), during systemic infections with CMV and potyviruses [Turnip mosaic virus (TuMV) in A. thaliana and Potato virus Y (PVY) in potato]. These results appear to be paradoxical. For example, in the case of CMV, elevation in SA levels in the host, due to treatment with exogenous SA or induction of endogenous SA biosynthesis by an avirulent pathogen prior to infection with CMV, will inhibit the systemic movement of the virus (Naylor et al., 1998; Ji and Ding 2001; Mayers et al., 2005) (see below). However, elicitation of SA biosynthesis by CMV infection is a slow process that is only apparent after systemic movement of the virus to all parts of the plant has already occurred (Ji and Ding 2001; Whitham et al., 2003). Because of the counter-defensive action of the CMV 2b protein, continued replication or local movement of CMV in systemically infected tissues of the plant will be unaffected by increased SA levels (Naylor et al., 1998; Ji and Ding 2001; Murphy and Carr 2002). It remains to be seen how the induction of what is nominally a defensive response can benefit CMV. Jasmonic acid and ethylene. The relationship between SA and signalling mediated by JA and its volatile ester methyljasmonic acid is intriguing. JA is an oxygenated fatty acid (oxylipin) that is a signal in resistance to certain bacterial and fungal pathogens and against insect pests (Reymond and Farmer, 1998; Thaler et al., 2004). Together with the gaseous plant hormone ethylene (ethene), JA also regulates a systemic resistance pathway inducible by non-pathogenic microbes [induced systemic resistance (ISR)] that primes resistance to fungi and bacteria in A. thaliana (Ton et al., 2002). However, based on studies with Turnip crinkle virus (TCV), it appears that ISR is not effective against virus
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infection (Ton et al., 2002). The interplay, or cross-talk, between the pathways and the choice made between expression of SA-induced, anti-microbial gene products (e.g., PR proteins) versus JA-induced antimicrobial gene products (e.g., defensins) is regulated at several levels. In A. thaliana, the products of the PAD4 and EDS1 genes promote SAmediated gene induction and repress gene expression induced by JA. These regulatory proteins are themselves negatively regulated through phosphorylation catalyzed by a protein kinase (Brodersen et al., 2006) (see next section). Additional points for cross-talk between SA- and JAmediated signalling pathways are provided by antagonistic effects on the re-localization of WRKY transcription factors from the cytoplasm to the nucleus (Balbi and Devoto, 2007; Miao and Zentgraf, 2007). Various members of this large family of transcription factors (characterized by the amino acid sequence motif WRKYGQ/KK) are up-regulated during defense responses mediated by both SA and JA and the promoters of many defense-related inducible genes (including PR genes) contain W-boxes for WRKY binding (Du and Chen, 2000; Balbi and Devoto, 2007; van Verk et al., 2008). In A. thaliana, two members of this family, WRKY53 and WRKY70 appear to act as crucial nodes in a network that maintains the equilibrium between SA- with JA-mediated signalling and that regulate the responses of these pathways to either pathogen attack or the developmental and environmental cues that trigger senescence (Balbi and Devoto, 2007; Li et al., 2004). Although the JA and SA pathways are viewed predominantly as being mutually antagonistic, pioneering transcript profiling work revealed significant positive as well as negative cross-talk between the two pathways (Schenk et al., 2000). Other work has shown that JA is synthesized transiently in the earliest stages of a TMVinduced HR and may play a minor role in localization (Kenton et al., 1999; Liu et al., 2004), and a recent study suggests that JA plays a role in SAR induction, which until recently was considered a JA-independent process (Truman et al., 2007). Ethylene is produced copiously during the HR and is a strong inducer of certain PR genes. Ethylene-dependent signalling is indispensable for the maintenance of basal resistance to fungi and bacteria (van Loon and van Strien, 1999; Geraats et al., 2007). However, ethylene does not appear to be essential for the induction of resistance to viruses, although since its biosynthesis from 1-aminocyclopropane-1-carboxylic acid results in the release of cyanide (Siegien and Bogatek, 2006), it is conceivable that this may contribute to the induction of resistance to viruses via the mitochondrial signalling pathway (se below). It is also possible that ethylene plays a role as a negative regulator of SA-mediated resistance to viruses. It has been proposed that this may explain a de-
crease in susceptibility to infection with CaMV observed by Milner and colleagues in the ethylene signalling mutant etr1 in A. thaliana (Love et al., 2007). Reactive oxygen species, calcium signaling, nitric oxide and protein kinase activation. Reactive oxygen species (ROS) have long been recognized as signals in defense, most notably during the oxidative burst or bursts that occur very early in the HR during a gene-forgene response (Heath, 2000) or during recognition of microbe- or pathogen-associated molecular patterns (MAMPS or PAMPS, respectively) in basal resistance (see Mackey and McFall, 2006 and references therein). MAMPS have been investigated most extensively in studies of basal resistance to bacterial pathogens, leading to the identification of factors such as bacterial flagellin, which trigger basal or innate immunity (GomezGomez and Boller, 2000). However, the triggering of transient or even sustained ROS and ethylene production by TMV coat protein (Allan et al., 2001), amino acid sequences within the coat proteins of potexviruses (Baurs et al., 2008), or by CaMV gene products (Love et al., 2005) in susceptible hosts, suggests that certain viral gene products can function as MAMPS. The oxidative burst, which occurs in cells in the immediate vicinity of the infection site, is due predominantly to the activation of NADPH oxidase associated with the plasma membrane. In a gene-for-gene interaction, the burst is biphasic, with an initial small burst (probably wound- or MAMP-induced), followed later by a sustained burst that is often associated with the onset of host cell death (reviewed by Torres and Dangl, 2005). In A. thaliana, there are ten NADPH genes, of which two (AtrbohD and F) encode enzymes that function during the HR; the rest play roles in other plant functions such as development (Foreman et al., 2003). NADPH oxidase catalyses the formation of superoxide (O2-) anions that are readily converted to other ROS, including the perhydroxyl radical (.HO2) and hydrogen peroxide (H2O2), via non-enzymatic and enzymatic mechanisms (Lamb and Dixon, 1997). ROS have several roles during the HR, but from the signalling point of view, perhaps two are the most important. Firstly, the oxidative burst activates Ca2+ ion influx across the plasma membrane via cyclic nucleotide-gated channels, in addition to mobilization of Ca2+ ions from intracellular stores (Torres and Dangl, 2005; Ma and Berkowitz, 2007). The cytoplasmic domains of the NADPH oxidase proteins have EF-hand motifs, characteristic of proteins regulated by Ca2+ ion levels (Keller et al., 1998). This permits changes in Ca2+ flux to function both upstream and downstream of ROS production, resulting in a positive feedback on ROS production and, in concert with nitric oxide (NO), helping to drive cell death in the HR (see below). A second effect of alterations in Ca2+ ion concentra-
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tions in the cytoplasm is triggering of the activity of calcium-dependent protein kinases, as well as highly complex mitogen-activated protein kinase (MAPK) cascades. MAPKs are activated through phosphorylation by MAPK kinases (MAPKKs) that are in turn activated by upstream protein kinases, MAPKK kinases (MAPKKKs), and so on (Ma and Berkowitz, 2006). MAPK cascades function in plant defense responses and probably the best studied of these are the wound- and SA-induced protein kinases (WIPK and SIPK; Zhang and Klessig, 1998). From studies in a variety of plant species, it is clear that MAPK cascades play roles in tissues within and beyond the infection site and participate in the control of cell death, regulation of ROS production, PR gene induction and establishment of induced resistance (Pedley and Martin, 2006). Nevertheless, although MAPK cascades have been studied intensively, it is not always clear how they control defense, especially with respect to defense against viral pathogens. However, there are a few examples in which their roles have been revealed. In A. thaliana, MAPK4 is an important regulator of the antagonism between SA- and JA-mediated defensive signalling (see above). Thus, knockout of the gene for MAPK4 results in constitutive expression of genes controlled by the SA-regulated pathway and knockout of responses to treatment with JA (Brodersen et al., 2006). The identities and functions of the protein substrates for defense-related MAPKs remain elusive. Although proteomic studies have revealed likely substrates for MAPKs (Merkouropoulos et al., 2008), only one in vivo substrate with a clear role in defense has been identified: the ethylene biosynthetic enzyme 1aminocyclopropane-1-carboxylate synthase, which in A. thaliana is the substrate for MAPK6, the equivalent (orthologue) to the tobacco SIPK (Liu and Zhang, 2004). With respect to a role in resistance to viruses for MAPK cascades, no specific substrates have been identified. Nevertheless, several studies using over-expression or virus-induced gene silencing of candidate genes in either tobacco or N. benthamiana plants expressing a transgene for the N resistance gene indicate that MAPK activity is required for TMV localization in the HR (reviewed by Caplan and Dinesh-Kumar, 2006). Thus, WIPK, SIPK and an upstream MAPKK are needed for full N gene-mediated resistance to TMV. SIPK, but not WIPK, is required for cell death induction during the HR, indicating a branch in the MAPK-mediated signalling pathway (Yang et al., 2001; Jin et al., 2003; Liu et al., 2004). In many cases, the phosphorylation targets for defense-related MAPKs are likely to be transcription factors. In tobacco and pepper, increased expression of genes for TGA, Myb and WRKY transcription factors occurred after a TMV-induced HR or following treatment with SA (Yang and Klessig, 1996; Chen and Chen, 2000; Liu et al., 2004; Park et al., 2006; van Verk et al., 2008). The connection between these factors and virus
resistance is unclear. Although members of the transcription factor families are known to be involved in the induction of PR gene expression, there is no evidence that the PR proteins are involved in virus resistance (reviewed by Murphy et al., 1999). Nevertheless, silencing of expression of specific WRKY and Myb factors in tobacco did decrease the efficiency of N gene mediated resistance to TMV, suggesting that new classes of defense gene await identification (Liu et al., 2004). Calcium flux regulates biosynthesis of NO in animal cells and is thought likely to be a strong influence on NO production during plant defense responses. NO is an important defensive signal and probably exerts a positive feedback on Ca2+ flux by enhancing calcium release from endomembrane stores (Ma and Berkowitz, 2007; Hong et al., 2008). However, at present, the available data on the mechanism(s) of NO production in plants are confusing (reviewed by Hong et al., 2008). The relative tissue levels of NO and H2O2 appear to regulate programmed cell death during an HR (Delledone et al., 2001). NO regulates defense gene expression both at the point of infection and in distal tissues, in part by inducing the biosynthesis of SA (Song and Goodman, 2001). NO may exert some of its effects via modulation of cyclic nucleotide-based signalling (Wendehenne et al., 2004) and by the S-nitrosylation of protein targets (Hong et al., 2008). However, NO also may stimulate changes in nuclear gene expression and defensive signalling indirectly through inhibition of cytochrome oxidase (Huang et al., 2002). This process can lead to changes in mitochondrial redox and the induction of specific sets of defense related genes (Maxwell et al., 2002). This mode of action may prove to be more important directly in resistance to viruses (see below). Cell death and the hypersensitive response. Programmed host cell death (PCD) accompanies many gene-for-gene interactions and the term HR is used often, though inaccurately, to describe this correlative feature of resistance. Although hypersensitive cell death has been studied scientifically for almost a century, we still do not understand its significance in resistance particularly with respect to viruses (Mur et al., 2008). There also exists uncertainty about the nature of the PCD that occurs during the HR. The process has sometimes been described as a variant of apoptosis. For example, caspases are aspartate-specific cysteine proteases that are important effectors of apoptosis in animal cells and several groups have reported increased cysteine protease activity during the HR (reviewed by Birch et al., 2000; Lam and del Pozo, 2000). Furthermore, Bax, an animal PCD effector protein, induced PCD when expressed from a viral vector (Lacomme and Santa Cruz, 1999). However, there is no evidence that plant genomes encode either orthologues of animal caspases or Bax-type proteins, while other characteristics of apoptosis, such as DNA
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laddering, are not clearly apparent during the HR (Mur et al., 2008). Additionally, plant metacaspases, which are similar in several respects to animal caspases, do not cleave caspase substrates and it is not thought that they are involved in the HR (Bonneau et al., 2008). Perhaps the nearest functional analog of a caspase found to be associated with the HR was discovered by Chichkova and colleagues (2004). This enzyme cleaves only a single bond in a model substrate for caspase (the virD2 protein of Agrobacterium tumefaciens) while human caspase cleaves at two sites, suggesting a greater degree of specificity than its mammalian equivalents. An inhibitory peptide synthesized to mimic this cleavage site retarded the appearance of HR-associated cell death in the TMV:N gene interaction (Chichkova et al., 2004). Recent work with the N gene-mediated HR in tobacco suggests that defensive PCD is a form of autophagy (Liu et al., 2005; Mur et al., 2008). In other words, cell death in the HR involves breakdown and re-cycling of cellular materials, rather than their outright destruction. In other systems autophagy is used to remove defective structures or as a means of rapidly providing intermediates for energy generation (reviewed by Bassham, 2007). The process of autophagy involves the compartmentalization of cytoplasmic material into double-membrane bound vesicles (autophagosomes) that fuse with either the vacuole (in A. thaliana) or small lysosomes (in tobacco), where degradation occurs (Bassham, 2007). Significantly, given the likely role of the vacuole and related structures in the autophagy, vacuolar processing enzymes (VPEs) with caspase-like activity have been reported in Nicotiana spp. and A. thaliana, and appear to contribute both to cell death during the HR and to inhibition of pathogen spread (Hatsugai et al., 2004; Rojo et al., 2004). Work with a cysteine protease from tomato, with 94 % similarity to the tobacco VPE, suggested that these proteins may have the capability of acting on the promoter of the gene for the ethylene biosynthetic enzyme 1-aminocyclopropane-1-carboxylic acid synthase (Matarasso et al., 2005). How an apparently vacuolar localized protein influences the activity of nuclear DNA is puzzling. Matarasso and colleagues (2005) proposed that a posttranslational modification of tomato VPE allowed a proportion of the protein synthesized to migrate to the nucleus. Interestingly, from the point of view of plant-virus interactions, expression of the A. thaliana VPE (VPE) was enhanced during a compatible infection with TuMV in which no HR-type necrosis occurred (Rojo et al., 2004). Taken together with the observations of Whitham et al. (2003), who showed increased expression of SA-inducible genes by this virus, this suggests that VPE expression is stimulated by SA and may be part of a delayed resistance response. Consistent with this idea, knockout of VPE gene expression causes a modest increase in the accumulation of TuMV (Rojo et al., 2004).
There is no direct evidence from any system showing that cell death is an absolute requirement for the limitation of virus spread during an HR. Although host cell death is a prominent feature of N gene-mediated resistance to TMV, several studies indicate that it is dispensable. Weststeijn (1981) exploited the temperature-sensitive nature of necrotic lesion formation and TMV localization in tobacco containing the N resistance gene to show that increased temperature could facilitate the escape of virus from lesions for up to 12 days following the first appearance of TMV-induced lesions. Santa Cruz and colleagues (Wright et al., 2000) used genetically engineered TMV expressing green fluorescent protein to confirm that virus remained in living cells at the periphery of the HR lesion for several days following the appearance of the HR in NN genotype Nicotiana edwardsonii. Mittler et al. (1996) grew NN genotype tobacco plants in an oxygen depleted atmosphere to inhibit ROS formation and cell death following inoculation with TMV, and more recently, Kirly et al. (2008) applied antioxidant agents to inhibit TMV-induced ROS generation. In both studies plants were still able to inhibit the spread of the virus, confirming that cell death induction and virus localization are separate processes. Studies in other systems have shown that cell death is either not required for resistance or can be separated from resistance on a genetic basis (Schoelz et al., 2006). Thus, in potato, the gene-for-gene resistance to PVX, conditioned by the Rx gene and the viral coat protein, does not normally elicit cell death and appears to be an extreme form of resistance (ER; see above). Only when the coat protein was expressed using agroinfiltration in large swathes of leaf tissues in Rx-containing potato plants was HR-associated cell death induced (Bendahmane et al., 1999). Cell death and resistance can be induced by separate domains within a single viral elicitor molecule. Thus, a study of HR-type resistance to CMV in cowpea showed that specific and distinct amino acids within the viral RNA polymerase sequence were responsible for the induction of virus localization and the elicitation of cell death (Kim and Palukaitis, 1997). Furthermore, cell death and resistance induction triggered by CaMV in Nicotiana species are controlled by separate host genes (Cole et al., 2001). Consistent with the idea that cell death and resistance are separate processes it was observed during the study of a caspase-like activity in tobacco that while pharmacological inhibition of its activity slowed the cell death process, it did not prevent localization of TMV in NN genotype tobacco (Chichkova et al., 2004). Similarly, silencing of a newly discovered HRinduced, jasmonate-regulated F-box protein in tobacco inhibited N gene associated cell death but did not inhibit N gene mediated restriction of TMV infection (van den Burg et al., 2008).
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RESISTANCE FACTORS
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Achievement of dominant gene-mediated resistance usually involves factors and components at the beginning and at the end of pathways activated by the dominant resistance genes. These components include various transcription factors (described above) and enzymes involved in various processes, including, kinases, proteinases, RNA polymerases, RNases, replication inhibitors, and cellular responses to ROS. Various examples of such factors are described below. In addition to those listed below, plants have been shown to produce other antiviral factors that either when added to virus inocula or previously applied to plants can inhibit virus infection to various degrees. These include the pokeweed antiviral protein, a ribosome-inactivating protein, the action of which has been studied extensively (reviewed by Nielsen and Boston, 2001; Park et al., 2004a), and others that have been reported but not assessed further. Alternative Oxidase (AOX) and mitochondrial redox signalling. Although, so far, we have considered ROS as products of the oxidative burst, ROS are produced at all times as by-products of normal metabolic activity (Noctor and Foyer, 1998). Within mitochondria the respiratory electron transport chain constantly gives rise to ROS as a by-product of its activity (Yip and Vanlerberghe, 2001). Plant mitochondria can minimize ROS generation while maintaining efficient electron flow into and through the respiratory chain using an enzyme called the alternative oxidase (AOX). AOX is the sole component of a distinct branch of the respiratory pathway, the so-called alternative or cyanide-resistant pathway, which connects oxidation of the ubiquinol/ ubiquinone (UQ) pool directly to the reduction of oxygen to water. By engaging AOX, excess electrons flowing into the UQ pool are dissipated. Although no ATP is generated by the alternative respiratory pathway, its activity ensures that respiratory metabolism can continue under conditions of stress (Maxwell et al., 1999; Affourtit et al., 2001, 2002; Yip and Vanlerberghe, 2001; Moore et al., 2002; Pasqualini et al., 2007). In addition, strong evidence exists to indicate that the ability of AOX to modulate the levels of ROS in the mitochondrion allows it to regulate ROS-mediated signal transduction and indirectly, nuclear gene expression (Maxwell et al., 2002). Among the genes affected in this way are some of those encoding members of the Aox gene family themselves (Norman et al., 2004). AOX is synthesized in the cytoplasm and is posttranslationally translocated into the mitochondrion (Vanlerberghe and McIntosh, 1997). In all plants examined to date, AOX is encoded by a small family of nuclear genes, a subset of which are inducible. For example, A. thaliana has at least four Aox genes, of which
one, Aox 1a, is inducible by chemicals such as cyanide or antimycin A, which inhibit electron flow through the cytochrome pathway, causing an increase in mitochondrial ROS levels (Wong et al., 2002; Singh et al., 2004). Increased Aox gene expression and AOX activity is also triggered by natural and synthetic inducers of pathogen resistance such as SA, NO and 2,6-dichloroisonicotinic acid (Rhoads and McIntosh, 1993; Chivasa et al., 1999; Huang et al., 2002). These chemicals probably induce changes in Aox gene expression by inhibition of electron flow through the cytochrome pathway (Xie and Chen, 1999; Huang et al., 2002; Norman et al., 2004). Aox gene expression also increased in tobacco (Lennon et al., 1997; Chivasa and Carr, 1998) and A. thaliana (Lacomme and Roby, 1999; Simons et al., 1999) in tissues undergoing a HR induced by viruses or other pathogens. The Aox 1a promoter from tobacco has certain sequence motifs in common with the promoters of genes encoding PR protein (Rhoads and McIntosh, 1993). Nevertheless, it cannot be regulated by the same signalling pathway as the PR proteins since its expression is not dependent upon NPR1, the key regulator of SA-induced PR gene expression (Wong et al., 2002). Studies of the potential role of AOX in pathogen resistance led to the discovery that SA-induced resistance to viruses is mediated in part by a pathway that appears to involve signals transduced through changes in redox or ROS in the mitochondria. Moreover, this pathway is separate from the NPR1-dependent pathway required for SA-induced PR gene expression and resistance to fungi and bacteria (Chivasa et al., 1997; Murphy et al., 1999; Wong et al., 2002; Singh et al., 2004). Initial evidence for this included observations that resistance to replication and/or movement of CMV, PVX and TMV in tobacco, as well as of Turnip vein clearing virus in A. thaliana, can be induced with non-toxic levels of antimycin A or cyanide (Chivasa and Carr 1998; Wong et al., 2002). Similar findings with respect to the DNA virus CaMV in A. thaliana have been reported (Love et al., 2005, 2007; Gilliland et al., 2006b). Evidence for the existence of a mitochondrial signalling pathway regulated by AOX came from studies using transgenic plants or viral vectors to alter alternative pathway capacity (Gilliland et al., 2003; Murphy et al., 2004). Increasing the capacity of the alternative pathway to scavenge mitochondrial ROS compromised resistance to TMV induced by antimycin A, and resistance induction by SA or antimycin A was enhanced in transgenic tobacco plants with decreased alternative pathway capacity. This suggested that AOX acts as a negative regulator of induced resistance to viruses (Gilliland et al., 2003). However the work also indicated that SA can activate additional AOX-independent resistance mechanisms against TMV, including RNAi mediated by RDR1 (Gilliland et al., 2003). The effects of altering alternative pathway capacity on chemically-induced resistance to TMV were
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subtle. In contrast, high-level expression of wild-type and mutant AOX proteins from a TMV-derived vector greatly enhanced the susceptibility of N. benthamiana to virus infection (Murphy et al., 2004). However, in more recent work it has been found that even the relatively small changes in alternative pathway capacity, which can be produced by constitutive expression of Aox-derived transgenes in tobacco (Gilliland et al., 2003; Pasqualini et al., 2007), can have dramatic effects on the ability of plants to resist viruses other than TMV (R. Fu, J. Verchot-Lubicz, W.S. Lee and J.P. Carr, unpublished data). Other recent experiments with Aox-transgenic tobacco indicate that, whereas it was thought that NO induced resistance to TMV via an SA-dependent mechanism (Song and Goodman, 2001), it now appears that NO can induce resistance rapidly via an additional, AOXregulated, SA-independent mechanism (W.S. Liang and J.P. Carr, unpublished data). Tobacco ethylene response factor 5 (NtERF5). ERF5 is a tobacco transcription factor, so named because it resembled ERF1 from A. thaliana in sequence and there were four other tobacco ERFs previously identified, even though NtERF5 gene expression did not respond to ethylene (Fischer and Drge-Laser, 2004). NtERF5 gene expression was enhanced by infection with TMV, but its natural expression was temperature sensitive, with little expression at 32C. Transgenic over-expression of NtERF5 was found to reduce TMV accumulation in the inoculated leaves, and to prevent systemic infection of TMV in tobacco plants expressing the N gene at 32C, when the N gene, SA-mediated defense response is inactive against TMV. NtERF5 is also not activated by either SA or JA (Fischer and Drge-Laser, 2004), and therefore represents an independent defense response against TMV from that activated by the SAdependent defense pathway. RNA-dependent RNA polymerase (RdRp1). Infection of tobacco and numerous other species by viruses had been shown to induce an RNA-dependent RNA polymerase (RdRp) (reviewed by Fraenkel-Conrat, 1986) now designated RdRp1 (reviewed by Wassenegger and Krczal, 2006). Its exact role in virus infection was not known, although at one time there was speculation that it might be involved in virus infection (Fraenkel-Conrat, 1983). A cDNA clone of a gene transcript encoding an RdRp (RDR) was isolated from tomato (Schiebel et al., 1998). Work on defining genes involved in RNAi in Neurospora crassa and A. thaliana identified a gene in each case resembling the tomato RDR gene (Cogoni and Macino, 1999; Dalmay et al., 2000; Mourrain et al., 2000). Interrogation of the A. thaliana genome identified six genes with similarities to the tomato RDR gene (Yu et al., 2003). Thus, based on phylogenetic analysis, the tomato gene was designated
RDR1 and the A. thaliana RDR gene shown to be involved in RNAi was designated RDR6. Silencing the RDR1 gene was shown to affect infection by TMV and PVX in N. tabacum (Xie et al., 2001), and by Tobacco rattle virus (TRV) and TMV-Cg in A. thaliana (Yu et al., 2003). RDR1 gene expression was stimulated in both tobacco and A. thaliana by SA (Xie et al., 2001; Yu et al., 2003) and silencing RDR1 gene expression in A. thaliana did not affect RNAi (Yu et al., 2003), indicating that the RdRp1 was not required for RNAi, at least not against the viruses tested. In tobacco, the stimulation of RDR1 gene expression by SA, independent of the AOX pathway (Gilliland et al., 2003), and silencing of tobacco RDR1 did not prevent the SA-mediated resistance from being induced (Xie et al., 2001), indicating that RdRp1 was one of several components acting against TMV during the SA-mediated defense response. N. benthamiana was shown to express a translationally defective RDR1 gene, which was thought to explain the susceptibility of this host to many viruses (Yang et al., 2004). However, constitutive expression of a Medicago truncatula RDR1 orthologue of NtRDR1 in transgenic N. benthamiana altered the disease resistance profile after infection by several tobamoviruses tested, but not against CMV or PVX (Yang et al., 2004). Thus, the role of RdRp1 in virus resistance appears to be limited to specific viruses. Whether or not RdRp1 functions though a separate RNAi pathway is not clear. RdRp1 does not require primers for complementary RNA synthesis (Fraenkel-Conrat, 1983, 1986) and may function by making regions of single-stranded viral RNA templates double-stranded, thus masking regulatory signals and preventing them from functioning in translation or replication. The inhibitor of TMV replication, p80GCR237. The Tm-1 gene encodes an 80-kDa protein, designated p80GCR237, that binds to the 126 and 183 kDa proteins of both TMV and ToMV and prevents them from assembling into the active replicase complex. However, once the replicase complex has been formed, the 126 and 183 kDa proteins cannot bind to p80GCR237 (Ishibashi et al., 2007). These data also suggest that p80GCR237 functions stoichiometrically and not catalytically and therefore can be saturated or lead to resistance breakdown allowing delayed infection to occur with time, which in fact was described (Fraser and Loughlin, 1980). Nevertheless, in other instances, the Tm-1 gene has been shown to provide resistance in the field, although resistance-breaking strains have been identified (Pelham, 1972; Hall, 1980; Watanabe et al., 1987), with mutations in the viral-encoded 126 kDa protein (Meshi et al., 1988; Hamamoto et al. 1997). The success of this resistance gene may reflect the fact that the 126 kDa protein is also the RNA silencing suppressor of ToMV and TMV and is involved in virus movement and activation of defense responses
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(Kubota et al., 2003; Ding et al., 2004). Thus, a reduced availability of the 126 kDa protein may have more than one effect on virus accumulation. Tobacco inhibitor of virus replication (IVR). A protein induced by TMV infection in N gene tobacco was isolated and was found to inhibit the accumulation of TMV (reviewed by Loebenstein and Akad, 2006). Although IVR was induced by the N gene-mediated response against TMV, the IVR was not target-specific in its interference; IVR applied to leaf discs or leaves could inhibit accumulation of CMV, PVX or PVY (Gera and Loebenstein, 1983). Constitutive expression of IVR, either in transgenic tobacco (Akad et al., 2005) or naturally in a hybrid Nicotiana derived from a cross between N. glutinosa x N. debneyi (Loebenstein et al., 1990), gave enhanced resistance to TMV. The mode of action of IVR is not clear, but as it can be applied to protoplasts infected with TMV 4 to 18 h after inoculation and still reduce virus accumulation, it apparently interferes with virus replication (Loebenstein and Gera, 1981). Whether it also can interfere with subsequent steps in virus infection is not know. IVR does not have singlestranded RNase activity (Gera and Loebenstein, 1983), although whether it has double-stranded RNase activity has not been evaluated. Since it accumulates in the intercellular spaces (Spiegel et al., 1989), IVR probably is not a transcription factor. It is not known by what pathway transcription of the tobacco IVR gene is induced, although it was not stimulated by exogenously applied SA (M. Takeshita and P. Palukaitis, unpublished). Tobacco antiviral factor (AVF). AVF is a family of phosphorylated glycoproteins stimulated in TMV-infected N-gene tobacco that when mixed with TMV, prior to inoculation, led to inhibition of virus accumulation (Sela and Appelbaum, 1962; Sela, 1981). Both AVF and human -interferon stimulated plants to produce nucleotides with antiviral activity (Reichman et al., 1983). AVF was purified using antibodies to human -interferon; however, the purified proteins did not resemble interferon in sequence (Edelbaum et al., 1990, 1991). The two purified glycoproteins, pg35 and gp22, appeared to be a -1,3-glucanase and an isoform of PR-5 (Edelbaum et al., 1991). Resistance factors induced in Capsicum annuum. In Capsicum spp., resistance to several tobamoviruses is controlled by the allelic genes L1-L4 (reviewed by Grube et al., 2000; Sawada et al., 2004). Pathotypes of the tobamoviruses TMV and Pepper mild mottle virus (PMMV) can break resistance conferred by specific L genes (Alonso et al., 1991; Tsuda et al., 1998; Grube et al., 2000; Hamada et al., 2002; Genda et al., 2007). In addition, several factors have been identified that may play key roles in resistance to tobamoviruses in Cap-
sicum spp. These include PR-10 and the Tin2 gene product, both of which were found to be induced during an incompatible reaction between TMV-P0 and C. annuum cv. Bugang carrying the L2 resistance gene (Shin et al., 2003; Park et al., 2004b). Other pepper genes that appear to be involved in the defense response were shown to be induced during this incompatible response, such as genes encoding a lipid transfer protein (CaLTP1) (Park et al., 2002) and an alanine aminotransferase (CaAlaAT1) (Kim et al., 2005), but their roles in the defense against virus infection are not known. Transcription of the gene encoding PR-10 (CaPR-10) was induced in leaves during the incompatible response elicited by TMV-P0, but not during a compatible reaction between TMV-P1,2 and hot pepper carrying the L2 resistance gene. By contrast, CaPR-10 was expressed constitutively in roots and was not upregulated by infection with TMV0. CaPR-10 was shown to be an 18 kDa RNase with no apparent sequence specificity, capable of degrading both TMV RNA and plant RNA. During induction of CaPR-10 in leaves, the encoded protein was phosphorylated, which increased its specific activity; the RNase PR10 present in roots was also a mixture of phosphorylated and non-phosphorylated protein. CaPR-10 transcription was induced by SA, JA, ethylene, sodium chloride and the herbicide methyl viologen (MV; also known as paraquat), which generates superoxide radicals (Park et al., 2004b). The C. annuum, TMV-induced gene (CaTin2) encodes a mature 23 kDa protein that contains little sequence similarity to other cell wall proteins, except for the 26amino acid signal peptide. However, fluorescently-tagged CaTin2 appeared to localize to the cell wall in cells transiently expressing this fusion protein, and in common with other cell wall proteins, CaTin2 was expressed preferentially in leaves and roots, as well as to a lesser extent in flowers, but not detectably in stems or fruit. Interestingly, constitutive expression of CaTin2 in transgenic tobacco resulted in some resistance against TMV or CMV, between one and two weeks after inoculation, although the resistance was lost by one month after inoculation. This suggested that the expression of the CaTin2 cell wall protein probably was limiting virus movement and accumulation. CaTin2 was induced during the incompatible response elicited by TMV-P0, but not by the compatible response elicited by TMV-P1,2. CaTin2 also was induced by treatment with SA, ethylene, JA, and more slowly by ABA, sodium chloride, and MV (Shin et al., 2003).
CONCLUDING REMARKS
Since the initial experiments done by Holmes (1946) demonstrating different levels of resistance to two viruses, considerable progress has been made in understanding the nature of resistance and in isolating resistance
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genes. Over the last 15 years there has been immense progress in understanding defensive signalling in resistance to viruses and other pathogens, although much still remains to be determined. We still do not fully understand the exact pathway of resistance, or the mechanism by which any resistance gene inhibits virus accumulation or spread. However, in some cases, we know how the resistance gene is triggered to activate the signalling pathway and some components of the signalling pathway have been identified. Some aspects of the interaction of a resistance gene products and a viral-encoded protein also have been identified. This is particularly the case for recessive resistance genes operating against potyviruses, although the exact mechanism by which virus infection is inhibited is still not clear. Compared to these areas, relatively little progress has been made in understanding how resistance responses inhibit virus replication, cell-to-cell and long-distance movement (see Zaitlin and Hull, 1987). In many cases, these resistance responses have not been correlated with the presence of specific genes, while in other cases where specific genes have been identified, the mechanisms by which they affect the above process has not been determined. This is particularly true with respect to specific blocks in long-distance movement. In some cases these may be due to RNAi, although these then would have to be aspects of RNA silencing that occur in one genotype of a species but not another. Although we know that RNAi plays a part in induced and basal resistance and that many aspects of the mechanism of RNAi have been elucidated, other mechanisms remain elusive. With the tools now available to isolate genes, interrogate plant genome sequences, analyse changes in the expression of multiple genes or their encoded proteins, and functional genomics, we can expect to see progress in gaining a better understanding of the identity of specific resistance factors and the mechanisms by which they confer resistance to the infection process by specific viruses. It is also hoped that some progress will be possible in the largely unexplored area of non-host resistance, which may provide new sources of potentially broad-spectrum, durable resistance that can be exploited. As we become more familiar with the effects of climate change on the durability of the current array of deployed natural resistant genes, new sources of resistance that are thermotolerant may also be required. Thus, understanding how resistance mechanisms operate to block virus infection at the different levels is critical to safeguarding the food supply against the effects of infection by viral pathogens.
the Rural and Environment Research and Analysis Directorate (RERAD) (PP), and by grants from the Biotechnology and Biological Sciences Research Council (BBSRC) and the Cambridge University Newton Trust (JPC).
REFERENCES Affourtit, C., Krab K., Moore A.L., 2001. Control of plant mitochondrial respiration. Biochemica et Biophysica Acta Bioenergetics 1504: 58-69. Affourtit C., Albury M.S.W., Crichton P.G., Moore A.L., 2002. Exploring the molecular nature of alternative oxidase regulation and catalysis. FEBS Letters 510: 121-126. Akad A., Teverovsky E., Gidoni D., Elad Y., Kirshner B., RavDavid D., Czosnek H., Loebenstein G., 2005. Resistance to Tobacco mosaic virus and Botrytis cinerea in tobacco transformed with complementary DNA encoding an inhibitor of viral replication-like protein. Annals of Applied Biology 147: 89-100. Albar L., Bangratz-Reyser M., Hbrand E., Ndjiondjop M.N., Jones M., Ghesquire A., 2006. Mutations in the eIF(iso)4G translation initiation factor confer high resistance of rice to Rice yellow mottle virus. Plant Journal 47: 417-426. Allan A.C., Lapidot M., Culver J.N., Fluhr R., 2001. An early tobacco mosaic virus-induced oxidative burst in tobacco indicates extracellular perception of the virus coat protein. Plant Physiology 126: 97-108. Alonso E., Garca-Luque I., de la Cruz A., Wicke B., AvilaRincn M.J., Serra M.T., Catresana C., Daz-Ruz J.R., 1991. Nucleotide sequence of the genomic RNA of pepper mild mottle virus, a resistance-breaking strain in pepper. Journal of General Virology 72: 2875-2884. Alvarez M.E., 2000. Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Molecular Biology 44: 429-442. Aramburu J., Mart M., 2003. The occurrence in north-east Spain of a variant of Tomato spotted wilt virus (TSWV) that breaks resistance in tomato (Lycopersicon esculentum) containing the Sw-5 gene. Plant Pathology 52: 407. Balbi V., Devoto A., 2007. Jasmonate signalling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios. New Phytologist 177: 301-318. Barker H., Harrison B.D., 1984. Expression of genes for resistance to potato virus Y in potato plants and protoplasts. Annals of Applied Biology 105: 539-545. Bassham D.C., 2007. Plant autophagy-more than a starvation response. Current Opinion in Plant Biology 10: 587-593. Baurs I., Candresse T., Leveau A., Bendahmane A., Sturbois B., 2008. The Rx gene confers resistance to a range of potexviruses in transgenic Nicotiana. Molecular Plant-Microbe Interactions 21 (in press). Beauchemin C., Boutet N., Lalibert J.F., 2007. Visualization of the interaction between the precursors of VPg, the viral protein linked to the genome of Turnip mosaic virus, and the translation eukaryotic initiation factor iso4E in planta. Journal of Virology 81: 775-782.
ACKNOWLEDGEMENTS
Work on virus resistance mechanisms in the authors laboratories was supported by Workpackage 1.5 from
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Virus Resistence

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001_JPP_Review_153

Journal of Plant Pathology (2008), 90 (2), 153-171

Edizioni ETS Pisa, 2008

INVITED REVIEW PLANT RESISTANCE RESPONSES TO VIRUSES

Corresponding author: P. Palukaitis Fax: +44. 1382.568523 E-mail: Peter.Palukaitis@scri.ac.uk

Journal of Plant Pathology (2008), 90 (2), 153-171

Journal of Plant Pathology (2008), 90 (2), 153-171

Palukaitis and Carr

Journal of Plant Pathology (2008), 90 (2), 153-171

Journal of Plant Pathology (2008), 90 (2), 153-171

Palukaitis and Carr

Journal of Plant Pathology (2008), 90 (2), 153-171

Journal of Plant Pathology (2008), 90 (2), 153-171

Palukaitis and Carr

Journal of Plant Pathology (2008), 90 (2), 153-171

Journal of Plant Pathology (2008), 90 (2), 153-171

Palukaitis and Carr

Journal of Plant Pathology (2008), 90 (2), 153-171

Journal of Plant Pathology (2008), 90 (2), 153-171

Palukaitis and Carr

Journal of Plant Pathology (2008), 90 (2), 153-171

Journal of Plant Pathology (2008), 90 (2), 153-171

Palukaitis and Carr

Journal of Plant Pathology (2008), 90 (2), 153-171

Journal of Plant Pathology (2008), 90 (2), 153-171

Palukaitis and Carr

Journal of Plant Pathology (2008), 90 (2), 153-171

Journal of Plant Pathology (2008), 90 (2), 153-171

Palukaitis and Carr

Journal of Plant Pathology (2008), 90 (2), 153-171

Journal of Plant Pathology (2008), 90 (2), 153-171

Palukaitis and Carr

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