Plant Resistance toInfection by VirusesFrederic Revers, UMR 1332 de Biologie du fruit et Pathologie, INRA, Universite de Bordeaux,

Villenave d’Ornon, France

Valerie Nicaise, UMR 1332 de Biologie du fruit et Pathologie, INRA, Universite de Bordeaux,

Villenave d’Ornon, France

Among the most devastating pathogens, plant viruses are

responsible for considerable losses of most agronomically

important crops in the fields. The development and use of

cultivars that are genetically resistant to viruses is an

efficient strategy to tackle the problems associated with

virus diseases. Recently, important advances have been

made in our understanding of the molecular nature and

mechanisms associated with natural recessive and domi-

nant resistance genes, as well as in the antiviral defence

system based on ribonucleic acids, referred to as RNA

silencing. In this review, the authors summarise current

knowledge about the defence mechanisms that prevent

or limit viral infection in plants and discuss the likely

collaboration of these different antiviral strategies

insuring the resistance of the whole plant.

Introduction

Plant infection by viruses causes physiological disordersresponsible for plant diseases of economic and agronomicsignificance in many crops. The mechanisms by which thesymptoms of disease are generated and by which plantsresist to these pathogens are still poorly understood. Usedin a important number of crops and agricultural situations,the use of varieties carrying genetic resistances to plantviruses constitutes the most effective, economical andecological measure to control viral infection. In nature,most plant species are resistant to most plant viruses.When all genotypes within a plant species are completelyresistant to a particular virus, this resistance is defined as anonhost resistance. Because this resistance cannot be stu-died by classical genetics, it remains largely unknown.When, within a plant species, some genotypes show heri-table resistance to a particular virus, whereas others are

susceptible, the resistance is a host resistance. This resis-tance has been more investigated. To date, hundreds ofnatural resistance genes to plant viruses have been reportedfrom crops and the plantmodelArabidopsis thaliana.Mosthost resistances identified are monogenically controlled,whereas the others show polygenic control. The pheno-types associated with these resistances range from com-plete immunity (no detectable viral multiplication ininoculated cells) to partial resistance, where virus is able toinvade the whole plant without disease symptom. See also:Epidemiology of Plant Virus Diseases; Viruses and PlantDisease; Virus–Plant Co-evolution

As obligatory intracellular parasites, plant virusesdepend on the host–cell machinery for multiplication andinvasion. In their simplest form, viruses consist of a geno-mic segment of deoxyribonucleic acid (DNA) or ribonu-cleic acid (RNA) harbouring a few genes and encapsulatedwith a protein shell called the capsid. Because of the exis-tence of natural physical barriers (cuticle and cell wall),they are delivered into host plant cells through wounds orthrough the action of vectors (insects, nematodes andfungi) that feed on or infect the plants. Following theirentry into a host cell and release of the viral genome, theinfectious cycle includes translation and replication of theviral genome, assembly of progeny virus particles, gen-eralised invasion of the host through cell-to-cell and long-distance movements of viral particles or ribonucleoproteincomplexes and, finally, transmission to new hosts by vec-tors. In some cases, transmission to the following genera-tion of host plant is also observed because of seed infection.See also: PlantViruses: Soil-borne; PlantVirusMovement;Plant Virus Movement and the Impact of RNA Silencing;Plant Virus Transmission by InsectsAt each step of the viral cycle, viruses have been shown to

harness cellular processes to their own needs and to recruitcellular components, notably through the formation offunctional heterocomplexes between host and virus pro-teins. The inability to establish one of these interactionsmay cause the failure of the infectious cycle, leading to apassive resistance, which represents the first level of resis-tance that operates after a virus enters into a plant. Such amechanism is expected to possess a recessive geneticdeterminism, because in a heterozygote, the presence of asingle copy of the virus-compatible allele is expected to

Advanced article

Article Contents

. Introduction

. Recessive Resistances and Host Factors Required for

Viral Infection

. Plant Defence Mechanisms

. Plant Immunity Against Viruses: One for All and All for

One

. Concluding Remarks

Online posting date: 15th August 2014

eLS subject area: Virology

How to cite:Revers, Frederic; and Nicaise, Valerie (August 2014) Plant Resistance to

Infection by Viruses. In: eLS. John Wiley & Sons, Ltd: Chichester.

DOI: 10.1002/9780470015902.a0000757.pub3

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allow the virus to complete its cycle. When viruses findcompatible host factors to multiply, a second level ofresistance based on the induction of active defencemechanisms is triggered. They concernmainly the action ofR genes, phytohormones and RNA interference. Thisarticle focuses on these natural different plant resistancesfor which important advances have been made in the pastdecade.

Recessive Resistances and HostFactors Required for Viral Infection

Two hypotheses can be proposed for the molecularmechanisms underlying recessive resistances to pathogens.The first one suggests the involvement of an inhibitor ornegative regulator of plant defence mechanisms. To date,this scenario had only been demonstrated for themlo gene,which confers resistance in barley to powdery mildew(fungi). However, recently, RYMV2, a rice recessiveresistance to Rice yellow mottle virus (RYMV), has beenassociated with a gene homologous to the A. thalianaCPR5 gene, known to be a defence mechanism regulator(Orjuela et al., 2013). Nevertheless, the most acceptedhypothesis proposes that the recessive resistance is theconsequence of the mutation or loss of a host factor spe-cifically required for the success of the infection process.For viruses, this hypothesis is consistent with the lowinformation content of viral genomes and the ensuing needto recruit host cellular components to allow the completionof the viral infection cycle. Therefore, for each stage of thevirus cycle, plant–virus compatibility depends on complexinterplays between genes encoded by the viral and hostgenomes. See also: Virus and Host Plant InteractionsMore than 80% of reported plant resistances to viruses

are monogenically controlled. As compared with othergroups of pathogens, recessive resistance genes are over-represented in the interactions between plants and viruses(approximately 50% of the known resistance genes behavein a recessive manner). The relatively high proportion ofrecessive viral resistance genes is in marked contrast tofungal or bacterial resistance where most reported resis-tances are dominant. Furthermore, most recessive resis-tances identified in crops confer protection to potyviruses,the largest and the most economically destructive genus ofplant viruses. It is, therefore, not surprising thatmost of therecent findings on recessive resistance to viruses come fromstudies on plant–potyvirus interactions. See also:Potyviridae

Plant resistances mediated by thetranslation factor eIF4E

Potyviruses have a single-stranded positive RNA genome,which is 3’-polyadenylated and covalently linked at the 5’end to a virus-encoded protein (VPg). The VPg has beenshown to be one of the viral determinants involved in

plant–virus compatibility. The search for its cellular part-ners has shown that the VPg (or its NIa precursor) ofseveral potyviruses can interact in yeast two-hybrid andin vitro binding assays with the eukaryotic translationinitiation factor 4E (eIF4E) and/or its isoform (eIF-(iso)4E). The ability to form this VPg–eIF4E complex isneeded for virus infectivity in planta, demonstrating theimportance of this interaction. These observationsprompted the search for a genetic link between knownrecessive resistance genes in crop species and the eIF4Egenes (Wang and Krishnaswamy, 2012).During the past decade, a ‘candidate gene’ approach

revealed that a large number of natural recessive resistancegenes correspond to alleles of eIF4E or eIF(iso)4E genes ofmany plant species. In addition, analysis of knockout (KO)and knockdown (silenced) plants affected in their eIF4Eand/or eIF(iso)4E gene expression showed to be resistantto viral infection, further highlighting the requirement ofthese cellular factors for successful potyvirus infection.Quickly, these observations have been extended to othervirus families, involving bymoviruses, cucumoviruses,ipomoviruses, sobemoviruses, carmoviruses and waiki-viruses (Wang and Krishnaswamy, 2012), suggesting thateIF4E contributes to a broad mechanism of plant sus-ceptibility to viruses (Table 1).

An intriguing aspect of eIF4E-mediated resistances isthat they cover a diverse range of resistance phenotypes.Although in most investigated cases they govern completequalitative resistance, they have also been shown in someinstances to provide quantitative (partial) resistance or tobe components of polygenic resistances. For instance, inpepper, the pvr2 locus controls a partial resistance to somepathotypes of Potato virus Y (PVY) and was initiallymapped as a quantitative trait locus (QTL). Similarly, inlettuce, mo11 and mo12 appear to be associated with theabsence of accumulation of Lettuce mosaic virus (LMV) atthe cellular level and reduced accumulation of LMVwithout symptom appearance, respectively.Furthermore, most eIF4E from resistant genotypes

retain their ability to bind the 5’ cap mimic m7-Guanosine-5’-triphosphate (GTP), showing that disruption of the cap-binding property of the eIF4E complex is not required forpotyvirus resistance. Therefore, the different resistancephenotypes have been proposed to result from the quan-titatively different affinities between the viral determinants(proteins and/or nucleic acids) and the alleles of eIF4Efactors (Wang and Krishnaswamy, 2012).

Plant viruses recruit the host translationmachinery

In eukaryotes, eIF4E belongs to the eIF4F complex, theprimary function of which relies on the recruitment ofribosomes to the 5’ end of cellular messenger RNAs(mRNAs) to initiate protein synthesis. The eIF4F complexincludes the eIF4E, which binds to the 5’ cap of mRNAsand eIF4G, a scaffold protein which interacts with manytranslation machinery components. In plants, a second

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Plant Resistance to Infection by Viruses

eIF4F complex, eIF(iso)4F, includes the isoforms eIF-(iso)4E and eIF(iso)4G. See also: Translation InitiationModels in Prokaryotes and Eukaryotes; TranslationInitiation: Molecular Mechanisms in EukaryotesIn rice, the two genes rym1 and tsv1 conferring resistance

to RYMV and Rice tungro spherical waikivirus, respec-tively, were shown to encode the eIF(iso)4G protein. Inagreement to these results, reverse genetics analysesdemonstrated that Arabidopsis eIF4G functions as a sus-ceptibility factor for the infection by potyviruses, cucu-moviruses and carmoviruses (Table 1). Furthermore,studies revealed that potyvirus infection requires therecruitment of eIF4E and eIF4G in a selective and

coordinated manner. Indeed, the study of ArabidopsisKOmutants has shown that potyviruses recruit either eIF4Eplus eIF4G or eIF(iso)4E plus eIF(iso)4G (Nicaise et al.,2007). This observation supports the hypothesis of a role ofthe whole eIF4F complex during the virus cycle. In spite ofsome specificities, eIF4F and eIF(iso)4F are consideredequivalent for cellular protein synthesis, as attested by thenormal phenotype shown by KO mutants disrupted insingle components of either eIF4F or eIF(iso)4F. Inter-estingly, most viruses seem to be dependent on a singleeIF4F complex. To date, only Pepper veinal mottle poty-virus (PVMV) has been shown to be able to use both eIF4Fcomplexes. Therefore, the functional redundancy between

Table 1 Resistances to viruses associated with translation factors

Viral genus Virus

Cloned locus, gene

name or gene silencing

Translation initiation

factor Plant species

Potyvirus LMV mo1 eIF4E Lettuce

PVY and TEV pot-1 eIF4E Tomato

PVY, TEV, PepYMV,

PepSMV, PepMoV,

ERV and PVV

Silencing approach eIF4E Tomato

PVY and TEV pvr1 eIF4E Pepper

TEV pvr2 eIF4E Pepper

PVMV and ChiVMV pvr2+pvr6 eIF4E +eIF(iso)4E Pepper

PSbMV, ClYVV and

BYMV

sbm1/4 (wlv) eIF4E Pea

ClYVV Bc-3 eIF4E Bean

PPV silencing approach eIF(iso)4E Plum

MWMV and ZYMV silencing approach eIF4E Melon

ClYVV At4g18040 eIF4E Arabidopsis

TuMV, LMV and TEV

and PPV

At5g35620 eIF(iso)4E Arabidopsis

ClYVV At3g60240 eIF4G Arabidopsis

LMV and PPV At5g57870 eIF(iso)4G1 Arabidopsis

TuMV At5g57870

+At2g24050

eIF(iso)4G1

+eIF(iso)4G2

Arabidopsis

TuMV At4g34110, At2g23350

and At1g49760

PABP2, PABP4 and

PABP8

Arabidopsis

Bymovirus BaMMV, BaYMV and

BaYMV2

rym4/5 eIF4E Barley

Ipomovirus CVYV Silencing approach eIF4E Melon

Sobemovirus RYMV rym1 eIF(iso)4G Rice

Tobamovirus TMV and TBSV Silencing approach eEF1A Nicotiana benthamiana

TMV and TBSV Silencing approach eEF1B N. benthamiana

Carmovirus MNSV nsv eIF4E Melon

TCV At3g60240 eIF4G Arabidopsis

Cucumovirus CMV At4g18040 eIF4E Arabidopsis

CMV At3g60240 eIF4G Arabidopsis

Waikivirus RTSV tsv1 eIF(iso)4G Rice

Abbreviations: BaMMV, Barley mild mosaic virus; BaYMV,Barley yellowmosaic virus; BYMV, Bean yellow mosaic virus; ChiVMV,Chilli veinalmottle virus; ClYVV, Clover yellow mosaic virus; CMV, Cucumber mosaic virus; CVYV, Cucumber vein yellowing virus; ERV, Ecuadorian rocotovirus; LMV, Lettuce mosaic virus; MNSV,Melon necrotic spot virus; MWMV,Moroccan watermelon mosaic virus; PepMov, Pepper mottle virus;PepSMV, Pepper severe mosaic virus; PepYMV, Pepper yellow mosaic virus; PPV, Plum pox virus; PSbMV, Pea seed-borne mosaic virus; PVMV,Pepper veinal mottle virus; PVV,Potato virus V; PVY,Potato virus Y; RTSV,Rice tungro spherical virus; RYMV,Rice yellowmottle virus; TBSV,Tomato bushy stunt virus; TCV, Turnip crinkle virus; TEV, Tobacco etch virus; TMV, Tobacco mosaic virus; TuMV, Turnip mosaic virus.

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Plant Resistance to Infection by Viruses

these iso-complexes observed for cellular translation doesnot extend to virus infection (Wang and Krishnaswamy,2012).Over the past decade, other components belonging to the

translational machinery were demonstrated to be requiredfor virusmultiplication, including the translation initiationfactor 4B (eIF4B), the translation elongation factors 1Aand 1B (eEF1A and eEF1B) and the poly(A)-bindingproteins 2, 4 and8 (PABP2, 4 and 8) (Hwang et al., 2013; Liet al., 2014; Patarroyo et al., 2013; Sasvari et al., 2011).These results suggest that crop genes encoding translationfactors may lead to new resistance sources that need to beexplored for viral disease control.Altogether, the recruitment of the host translation

machinery highlights an example of how viruses exploitcellular resources, possibly mimicking host mRNAs.Nevertheless, although these resistances establish at a veryearly infection stage, the precise role of these molecules invirus infection process (for translation and/or replicationand/or particle movement and/or genome stability)remains to be elucidated.

In search of other recessive genes

Few other susceptible host recessive resistance genes thatare not encoding translation initiation factors have beenidentified through the analysis of mutants collections and/or natural cultivated or wild species. A positional cloningstrategy exploring barley natural variability revealedrecently the key role of the PDI5–1 (Protein disulphideisomerase like 5–1) protein in the recessive resistance tobymoviruses (Yang et al., 2014). Another recessive resis-tance gene named ra blocking vascular transport of Potatovirus A (PVA) was genetically characterised in potato.Although not cloned yet, it seems to be linked to a genecluster including dominant resistance genes as Ry and Na.

In addition, from the perspective of identifying newresistance sources, A. thaliana has provided originalinsights into the genes involved in plant–virus interactions,which could be used as potentially resistance sourcesagainst viruses. For example, the recessive resistance generpv1 conferring resistance toPlum pox virus (PPV) maps ina genomic region containing no translation factor genes.The lack of co-segregationwith eIF4Eor eIF4G gene is alsotrue for dstm1, mediating resistance to Tobacco mosaicvirus (TMV) (Serrano et al., 2008) and sha3, a major QTLcontributing to systemic resistance against PPV (Pagnyet al., 2012). tom1 and tom2A Arabidopsis mutants do notsupport TMV accumulation in single cells. After furthercharacterisation, it appears that both genes encode trans-membrane proteins localised in the tonoplast and arerequired for tobamovirus replication (Ishibashi et al., 2012).

Plant Defence Mechanisms

When viruses recruit successfully host machinery toestablish their viral cycle, active defence mechanisms are

triggered, involving the action of antimicrobial compo-nents and specific defence proteins. See also: Plant Diseaseand Defence

Dominant R genes

In plants,most ofmonogenic dominant resistance genes (Rgenes) involve highly specific processes where triggereddefence mechanisms confer resistance to a given pathogen.Most R genes identified in plant–pathogen interactionsbelong to the nucleotide binding site-leucine-rich repeat(NBS-LRR) class. Members of this class have been sub-divided based on the presence of either an N-terminal tollinterleukin-1 receptor (TIR) domain or an N-terminalcoiled-coil (CC) domain. NBS-LRR R genes are not lim-ited to protection against viruses but are involved inresistance against essentially all kinds of plant pathogens.See also: Resistance Genes (R Genes) in PlantsIn plant–virus interactions, all NBS-LRRgene products

identified so far lack a transmembrane domain which isconsistent with the intracellular localisation of the viralcycle and with their role in sensing viral products (Table 2).The product of these genes is believed to participate in asensing system that specifically recognises the viral aviru-lence (avr) gene products through the establishment of theso-called ‘gene-for-gene’ interaction. If a direct physicalinteraction between the avr and R gene products had ori-ginally been suggested, the current understanding favoursthe more sophisticated ‘guard hypothesis’ model. Thisconcept proposes that a R protein (guard) is constitutivelyassociated with a host cellular protein (guardee), main-taining the complex in an inactive state in the absence ofpathogen.During amicrobial attack, the guardee perceivesthe pathogen (via the interactionwith the avr gene product)triggering the activation of the R protein in a signaltransduction cascade ultimately leading to the initiation ofresistance. See also: Avirulence GenesThe C-terminal LRR domain of R proteins is highly

variable and is implicated in determining recognition spe-cificity (Padmanabhan et al., 2009), whereas the N-term-inal part might play a role in recruiting cellular cofactorsinvolved in the activation of the R protein (Collier andMoffett, 2009). Several studies suggested that intramole-cular interactions play key roles in maintaining NBS-LRRtype R proteins in an autoinhibited state (Collier andMoffett, 2009; Kadota et al., 2010).

ManyR genes conferring resistance against viruses havebeen identified so far (Table 2). One of the best studied is thepotato Rx1 gene that encodes a typical CC-NBS-LRRprotein and mediates resistance to Potato virus X (PVX)through recognition of the PVX CP (Avr determinant).Rx1 CC domain has been shown to form a heterodimerwith the cellular ranGTPase activating 2 (ranGAP2), aninteraction required for Rx1 function (Rairdan et al.,2008). Although direct interaction between ranGAP2 andthe PVX CP has not been detected, it has been proposedthat ranGAP2 might nonetheless interact (directly orindirectly) with PVXCP, causing a conformational change

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Plant Resistance to Infection by Viruses

in the rest of the protein and leading Rx to switch to anactive state (Hao et al., 2013). Besides, theN gene product,which displays a TIR-NBS-LRR structure, interactsdirectly with the TMV avirulence factor (the helicasedomain of the viral replicase) in an ATP-dependent man-ner. In addition, Caplan and colleagues identified a Nreceptor-interacting protein 1 (NRIP1) recruited from thechloroplast to the cytoplasm and nucleus, and of which theinteraction with both replicase and N is required for fullresistance to TMV (Caplan et al., 2008).In plants, SGT1 (Suppressor of G2 allele of SKP1),

HSP90 (Heat-shockprotein) andRAR1 (Required forMlaresistance 1) form a molecular chaperone complex, whoserole is to maintain NBS-LRR proteins in a functional butinactive form. Current evidence suggests that this chaper-one complex both stabilises R factors and mediates theirdegradation, to maintain a tight cellular balance betweendefence signalling and attenuation (Kadota and Shirasu,2012).The study of the N-mediated resistance has led to char-

acterise further the R signalling cascade in plant–virusinteractions. Thus, recognition of theTMVreplicase by theN factor in Nicotiana benthamiana initiates downstreamsignalling pathways that include rapid activation of twoMAPkinases, SIPK (Salicylic acid-induced protein kinase)andWIPK (Wounding induced protein). SGT1 undergoes

specific phosphorylation by SIPK, a process that isrequired for the establishment of N-mediated resistance.Recently, it has been proposed that phosphorylation ofSGT1 regulates the nucleocytoplasmic distribution of theN receptor, a process necessary for an effective plantresistance response to TMV infection (Hoser et al., 2013).Several of these factors have been shown to be involved inthe Rx-mediated resistance as well (Boter et al., 2007).Surprisingly, the research of N-downstream signallingcomponents through a virus-induced gene silencing(VIGS) approach has identified the CC-NBS-LRRNRG1(N requirement gene 1) as a cellular factor required for theN-mediated resistance to TMV, supporting emerging evi-dence that many disease resistances recruit more than asingle NBS-LRR protein and that NBS-LRR proteins canalso act in downstream signalling pathways.Interestingly, SGT1 also interacts with multiple E3-

ubiquitin ligase components, such as SKP1 (S phasekinase-associated protein 1), the CRL (CULLIN-RINGligase) complex and the COP9 signalosome (CSN), sug-gesting a ubiquitin-mediated proteolysis in R-mediatedresistances. In tobacco, it was shown that both SGT1 andRAR1 interact with CSN3 and CSN8 to mediate the Ngene resistance against TMV (Shirasu, 2009).Most of the time, the activation of R genes is associated

with a hypersensitive response (HR), a phenomenon

Table 2 Known resistance R genes targeted viruses

Viral genus Virus Avr factor R gene Protein class Plant species

Tobamovirus TMV Replicase/

helicase

N TIR-NB-LRR Tobacco

ToMV and TMV Movement

protein

Tm-2/Tm-22 CC-NB-LRR Tomato

ToMV and TMV Replicase Tm-1 TIM-barrel

structure

Tomato

Potexvirus PVX Coat protein Rx1 CC-NB-LRR Potato

PVX Coat protein Rx2 CC-NB-LRR Potato

Potyvirus PVY ? Y-1 TIR-NB-LRR Potato

SMV Protein P3 Rsv1 CC-NB-LRR Soybean

TEV, LMV and

PPV

Coat protein RTM1 Lectin-like Arabidopsis

TEV, LMV and

PPV

Coat protein RTM2 Small heat-shock

protein

Arabidopsis

TEV, LMV and

PPV

Coat protein RTM3 Meprin/TRAF/

CC domains

Arabidopsis

Tospovirus TCSV, GRSV

and TSWV

Movement

protein

Sw5 CC-NB-LRR Tomato

Cucumovirus CMV Replicase/

helicase

RT4–4 TIR-NB-LRR Bean

CMV Coat protein RCY1 CC-NB-LRR Arabidopsis

Carmovirus TCV Coat protein HRT CC-NB-LRR Arabidopsis

Begomovirus BDMV Nuclear shuttle

protein

PvVTT1 TIR-NB-LRR Bean

Abbreviations: BDMV,Beandwarfmosaic virus; CMV,Cucumbermosaic virus;GRSV,Groundnut ringspot virus; LMV,Lettucemosaic virus; PPV,Plum pox virus; PVX, Potato virus X; PVY, Potato virus Y; SMV, Soybean mosaic virus; TCSV, Tomato chlorotic spot virus; TCV, Turnip crinklevirus; TEV, Tobacco etch virus; TMV, Tobacco mosaic virus; ToMV, Tomato mosaic virus; TSWV, Tomato spitted wilt virus.

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Plant Resistance to Infection by Viruses

involving the programmed death of the infected and oftenof neighbouring cells. Although the underlying mechan-isms are not fully understood, one of the consequences ofthe hypersensitive reaction is to confine the pathogen in oraround the hypersensitive lesion and to prevent any furtherpathogen spread in the plant. In commonwith the situationobserved with genes conferring resistance to nonviralpathogens,most of theNBS-LRRgenes involved in plant–virus interactions lead to complete resistance but are notalways associated with cell death. The best characterisedexample of such a situation is the Rx1 gene, which confersan extreme resistance associated with a very early inhibi-tion of virus replication without any sign of hypersensitivecell death. However, overexpression of the PVX avr factor(the CP) inRx-transformedNicotiana spp. or inRx potatoactivates cell death, indicating that the same underlyingprinciples are operating. A similar extreme resistancephenotype is observed with the Sw5 and Rsv1 genes intomato and soybean, respectively (Maule et al., 2007). Afunctional module that mediates HR against viruses (aswell as nonviral pathogens) requires the interaction of twolipases, EDS1 (Enhanced disease susceptibility 1) andPAD4 (Phytoalexin deficient 4) with SAG101 (Senescence-associated gene 101). In Arabidopsis, the EDS1/PAD4/SAG101 complex regulates HRT-mediated resistanceagainst Turnip crinkle virus (TCV) (Zhu et al., 2011).See also: Hypersensitive Response in Plants; Plant Pro-grammed Cell DeathAlthoughRgene function is basedonprecise and specific

molecular interactions that lead to the activation of resis-tance by pathogen avirulence determinants, some virus Rgenes appear to have a wider specificity than might beexpected. Thus,Rx genes are effective against most naturalvariants of PVX. Moreover, Sw5, Tm-2/Tm-22 and Nconfer resistance to several tospoviruses and tobamo-viruses, respectively.In contrast with the structure of the classicalR genes, the

RTM genes were the first cloned non-NBS-LRRdominantresistance genes against viruses. Genetic characterisationof naturalArabidopsis accessions andmutants showed thatat least five dominant genes, named RTM1, RTM2,RTM3, RTM4 and RTM5 (for restricted Tobacco etchvirus (TEV) movement), are involved in resistance to TEV,LMVandPPV.A singlemutation in one of theRTM genesis sufficient to abolish the resistance phenotype. RTM1encodes a protein belonging to the jacalin family, RTM2encodes a protein with similarities to small heat shockproteins andRTM3 is amember of an undescribed proteinfamily with a meprin and TRAF homology domain and aCC domain at its C-terminal end. RTM4 and RTM5 haveonly been genetically characterised (Cosson et al., 2012).Because (1) the expression of RTM1 and RTM2 arerestricted to phloem cells and (2) RTM3 interacts directlywith RTM1 in yeast and in planta, it has been recentlyproposed thatRTMmembersmay form a phloem-residentmultiprotein complex involved in the resistance mechan-isms to block the long-distance movement of potyviruses(Cosson et al., 2010). Despite the fact that mutations in CP

of potyviruses overcome the RTM resistance, no directinteraction has been detected for CP with any RTM pro-teins so far. See also: PhloemLong-Distance Trafficking ofProteins and RNAsAnother example of a non-NLS-LRR dominant resis-

tance comes from the tomato Tm-1 gene, which confersplant resistance to the tobamoviruses TMV and Tomatomosaic virus (ToMV). Crystallisation characterisationassociated to biological analyses demonstrated that Tm-1encodes a protein with a TIM-barrel-like structure, andthat a direct interaction between the viral replicase and theTM-1 protein strongly impairs the ToMV genome repli-cation, leading toplant resistance butwithout elicitingHR-associated cell death (Ishibashi and Ishikawa, 2013).

Plant hormones and systemic acquiredresistance (SAR)

Plant hormones play important roles in regulating signal-ling networks involved in plant defences. Hormones aresmall signal molecules occurring in low concentrations,essential for the regulation of plant growth, development,reproduction and survival to stresses of biotic and abioticorigin (Robert-Seilaniantz et al., 2011). On pathogenattack, the quantity, composition and timing of the phy-tohormonal blend produced by the plant depend greatly onthe lifestyle and infection strategy of the invading attacker.In the past decades, significant progress has been made inidentifying the key components and understanding the roleof phytohormones in plant responses to biotic stresses.See also: Jasmonate Synthesis andAction inHigher Plants;Salicylic Acid; Systemic Signalling in Plant DevelopmentDuring the R-mediated resistance activation, cellular

responses elicited at the infection site are emitted to distantnoninfected tissues, resulting in a resistance or in reducedsusceptibility state that can remain efficient for severalweeks. This phenomenon is referred as the SAR. In the caseof TMV-triggered HR, the response persists up to 3 weeks(Mandadi and Scholthof, 2013). How SAR can be sus-tained for so long is not clear, but epigenetics modifica-tions, such as DNA methylation and chromatinremodelling, may be critical to maintain a SAR signal(Spoel andDong, 2012).Moreover, during a viral infection(in a manner similar to nonviral infections), this long-lasting and broad-spectrum disease resistance requiresendogenous accumulation of salicylic acid (SA), resultingin transcriptional reprogramming of a battery of genesencoding pathogenesis-related (PR) proteins. In parallel,the signal emitted by the infection spot to protect theuninfected tissues against pathogen invasion circulates as aheterocomplex, wheremethyl-SA binds to lipid derivativesand lipid-transport proteins and moves through thephloem to the rest of the plant. Thus, studies on TMV-infected plants revealed that MeSA participates in theperpetuation of SAR defence (Dempsey andKlessig, 2012;Park et al., 2007).

Jasmonic acid (JA) is also strongly involved in plantdefence against viruses, and the HR response initiated by

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Avr–R protein interactions results in a modulation of SAand JA. However, if SA clearly acts as a positive regulatorof plant resistance to viruses, the role of JA is controversialand remains to be fully elucidated. Thus, JA seems toregulate negatively the local resistance to TMV in tobacco(Oka et al., 2013) but is essential for systemic resistance toTMV inN. benthamiana (Zhu et al., 2014). It is likely that abalance between endogenous JA and SA plays a key role indetermining the degree of resistance. Interestingly, exo-genous applications of JA and SA improve plant resistanceto three RNA viruses (Cucumber mosaic virus (CMV),TMV and TCV) in Arabidopsis, tomato and hot pepper.This approach has been proposed as a strong tool for cropprotection in fields (Shang et al., 2011).

Although their role in plant defence is less well studied,recent studies indicate that other hormones such as abscisicacid, auxin, gibberellic acid, cytokinin and brassinoster-oids and peptide hormones play a role in plant defencesignalling (Bari and Jones, 2009) and could be as wellinvolved in plant–virus interactions. See also: Auxin; Jas-monate Synthesis and Action in Higher Plants; SalicylicAcid

RNA silencing

Over the past decades, RNA silencing has been recognisedas an evolutionarily conserved process in most eukaryotes.This process involved the degradation of double-strandedRNAs (dsRNAs) into small interfering RNAs (siRNA) byan endonuclease, which has been named Dicer. The siR-NAs are integrated in an RNA-induced cytoplasmicsilencing complex (RISC) which then degrades RNAswithhomology to the siRNAs (Pumplin and Voinnet, 2013).In plants, silencing pathways are particularly diverse and

partially overlapping. At least three basic processes can bedistinguished: cytoplasmic RNA silencing (or post-transcriptional gene silencing) mediated by siRNAs,silencing mediated by plant-encoded microRNAs (miR-NAs) and transcriptional gene silencing (TGS) mediatedby siRNA-directed methylation of DNA and histoneproteins. Over the past few years, key components of theseRNA silencing pathways, generally encoded by small genefamilies, have been identified and shown to have animportant regulatory role for diverse aspects of growth anddevelopment. Someof themhave alsobeen shown tohave aprotective role against invading viral pathogens. See also:Gene Silencing in Plants; MicroRNAs (miRNAs) andPlantDevelopment; Plant Virus Silencing Suppressors andRNA Silencing in PlantsPlant viruses have commonly double-stranded second-

ary structure elements in their genomic RNAs or producedsRNA intermediates during their replication. Thesemolecules are targeted by the RNA-silencing machinery toproduce virus-derived small RNAs (vsRNAs). ThesevsRNAs are also produced, through unclear mechanisms,from DNA viruses. The integration of vsRNAs in theRISC complex leads to the sequence-specific degradationof viral RNAs and to the generation of a mobile-silencing

signal, which spreads between cells through plasmo-desmata and over long distances via the phloem, through arelay-amplification process. This activates RNA silencingin noninfected cells and is notably responsible for the plantrecovery phenomenon. See also: Plant Virus Movementand the Impact of RNA SilencingIn plant–virus interactions, the host RNA silencing

machinery produces viral small RNAs that target RISCcomplexes to viral genomic (Pantaleo et al., 2007). Mostvirus-derived small RNAs in Arabidopsis plants infectedwith the potyvirus, Turnip mosaic virus (TuMV), weredependent on DCL4 (Dicer-like protein 4) and RDR1(RNA-dependent RNA polymerase 1), although fullantiviral defence also required DCL2 and RDR6 (Garcia-Ruiz et al., 2010), and RNA silencing induced by PPV wasshown to be compromised in RDR6-defective plants(Vaistij and Jones, 2009).Viruses have evolved diverse mechanisms to avoid

silencing, most notably through the expression of specificviral suppressors of RNA silencing. Many unrelated virusproteins possess silencing-suppressor activities in additionto their other functions, and silencing suppressors havenow been identified for almost all types of plant viruses.Interestingly, many of the silencing suppressors had beenpreviously identified as pathogenicity determinants (factornot required for virus replication but needed for efficientviral accumulation in plant and symptoms development)or as long-distance movement factors. In turn, increasingevidences suggest that plants have as well evolved byestablishing specific defences against RNA-silencing sup-pression by pathogens, providing yet another illustrationof the never-ending molecular arms race between plantpathogens and their hosts. The known mechanisms ofRNA silencing and mode of action of the silencing sup-pressors encoded by viral genomes have been extensivelydescribed in recent reviews (Burgyan and Havelda, 2011;Pumplin and Voinnet, 2013; Wang et al., 2012). See also:Plant Virus Silencing Suppressors and RNA Silencing inPlants; RNA Silencing and its Suppressors in the Plant-virus Interplay

Plant Immunity Against Viruses: Onefor All and All for One

Over the past 15 years, a concept revolutionising theunderstanding of immunity emerged in plants. This newconcept stems from the ability of each organism to dis-criminate between self and nonself molecules through theaction of pattern recognition receptors (PRRs), perceivingspecific microbial molecular signatures, named PAMPs(pathogen-associated molecular patterns). Perception ofPAMPs by PRRs activates PAMP-triggered immunity(PTI). To counter this defence strategy, successful patho-gens deploy effectors proteins, the primary function ofwhich is to evade/interfere with PTI. In turn, some plantcultivars have evolved R proteins to block these effectors,

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Plant Resistance to Infection by Viruses

leading to effector-triggered immunity (ETI). See also:Plant Innate ImmunitySince the discoveryof PTI–ETImechanisms, theR genes

involved in plant–virus interactions (especially the onesencoding the NBS-LRR proteins) appeared to be part ofthe ETI side of plant innate immunity against viruses,known to be associated with HR. The existence of animalPRRs specific to viral PAMPs raises the question of theexistence of PRRs perceiving plant viruses. Although noPTI pathways against plant viruses has been characterisedto date, it is important to note that BAK1 (BRI1-asso-ciated receptor kinase 1), one of the key regulators of plantPTI pathways identified so far, and its closest paralogBKK1 (BAK1-like kinase 1) are required for Arabidopsisresistance to plant viruses (Kørner et al., 2013; Yang et al.,2010), suggesting these twoproteins could aswellmodulatesome immune pathways involved in plant–virus interac-tions. RNA silencing completes plant antiviral arsenal byaffecting the viral cycle at the RNA level. Altogether, thesedefence processes ensure a highly robust plant immunesystem, effective at different steps of plant colonisation: (1)during the early infection events in the first infected cell, (2)during the cell-to-cell movement of viral particles and(3) during the systemic infection of the whole organism(Figure 1).

It now seems that there might be an overlap betweenthese different sides of the immune system mediated bynucleic acids (RNA silencing) and by proteins (R gene,

SAR). Thus, it has been shown that SA, an importantcomponent of the SAR defence system, induces theexpression of RDR1 involved in antiviral RNA silencingand enhances it. Moreover, PTI and ETI networksassociate tightly with phytohormones pathways (Armijoet al., 2013; Boutrot et al., 2010; Gimenez-Ibanez andSolano, 2013). Recently, the key RNA silencing factorRDR6, initially characterised in virus resistance, has beenrevealed to modulate PTI and ETI pathways through theposttranscriptional control of disease resistance genes(Boccara et al., 2014). The precise determination of thelink(s) between these different host defence systems is a truechallenge for the future in the quest to understand betterplant defences against viruses.

Concluding Remarks

During the past years, our knowledge on plant defencesand resistances against viruses has advanced significantly.However, even if tremendous progress has been made inthe fundamental understanding of plant infection byviruses and in the exploitation of this knowledge in solvingvirus-mediated agronomic problems, plant viral diseasesstill cause serious economic losses in many major crops byreducing yield and quality. In fields, using resistant culti-vars is the most effective and economical way to controlplant virus diseases. Genetic natural sources of resistance

Translationfactors

Viral genome

Viral proteins

Avr factor

R factor

Dicer

Replication

PRR ?

PTI ? RNA silencing ETI SAR

First infected cell

Cell-to-cell movement

Systemic movement

(a) (b) (c)

Figure 1 Plant immunity against viruses: one for all and all for one. To complete their infectious cycle in plants, viruses rely mainly on the host cellular

machinery, concept illustrated so far by the plethora of natural recessive resistances encoding translation factors. In a complementary manner, a set of active

defence mechanisms ensure a highly robust plant immune system, effective at different steps of plant colonisation: (a) during the early infection events in

the first infected cell, (b) during the cell-to-cell movement of viral particles and (c) during the systemic infection of the whole organism. Altogether, the

combination of effective passive and active resistances might explain why most plants are resistant to most viruses.

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Plant Resistance to Infection by Viruses

have been exploited extensively to develop virus-resistantplants by conventional breeding. However, plant viruseshave evolved and acquired the ability to overcomemany ofthe resistances used by breeders. In parallel, the introduc-tion of viral and nonviral sequences in plants has been usedsuccessfully to engineer resistances to viruses (althoughvery few genetically engineered virus-resistant crops havebeen released for cultivation). Moreover, the emergence ofthe TILLING (targeting induced local lesions in genome)technology or eco-tilling represents a good alternative tothe use of transgenic plants, by generating or identifyingadditional variations in existing genes, instead of intro-ducing new genes in the plant genome. However, this willundoubtedly require further important research effortstowards the identification of additional susceptibility fac-tors and of their role in viral cycles to develop new recessiveresistances, combined with the understanding of the rela-tionships, at the whole plant level, of the various host plantdefencemechanisms. Thatwill have to be also coupledwithstudies on durability of such resistances, combining forinstance several resistance genes (referred as pyramidingresistances) to minimise the ability of plant viruses toovercome such resistances. See also: Plant Breeding andCrop Improvement

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