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Czosnek H. Tomato Yellow Leaf Curl Virus. Encyclopedia of Virology, 5 vols. (B.W.J. Mahy and M.H.V. Van Regenmortel, Editors), pp. 138-145 Oxford:

Elsevier.

movement protein NS(M) with a heat-reversible sealing ofplasmodesmata that impairs development. Plant Journal 43:688–707.

Sherwood JL, German TL, Moyer JW, Ullman DE, and Whitfield AE(2000) Tomato spotted wilt. In: Maloy OC and Murray TD (eds.)Encyclopedia of Plant Pathology, pp. 1030–1031. New York: Wiley.

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Soellick T-R, Uhrig JF, Bucher GL, Kellmann J-W, and Schreier PH(2000) The movement protein NSm of tomato spotted wilt tospovirus(TSWV): RNA binding, interaction with TSWV N protein, andidentification of interacting plant proteins. Proceedings of theNational Academy of Sciences, USA 97: 2373–2378.

Takeda A, Sugiyama K, Nagano H, et al. (2002) Identification of a novelRNA silencing suppressor, NSs protein of tomato spotted wilt virus.FEBS Letters 532: 75–79.

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138 Tomato Spotted Wilt Virus

Author's personal copyAuthor's personal copy

Tomato Yellow Leaf Curl VirusH Czosnek, The Hebrew University of Jerusalem, Rehovot, Israel

ã 2008 Elsevier Ltd. All rights reserved.

Glossary

Agroinoculation An alternative route for viral

infection; the viral genome is cloned, usually as a

head-to-tail dimer, in the T-DNA of Agrobacterium

tumefaciens and is delivered to plants by inoculation.

Introgression Incorporation of chromosomal

segments of wild tomato species in the domesticated

tomato by crosses and selection; introgression lines

are used to localize genes to the tomato

chromosomes.

Rolling circle Mechanism of replication followed by

many viral DNA and by begomoviruses in particular.

Viruliferous whitefly Insect that has acquired virus

from an infected plant and is ready to infect other

host plants.

Whitefly Insect that belongs to the order Homoptera;

they cause damage to plants by feeding and by

vectoring plant viruses.

Introduction

In the late 1950s the tomato cultures in the Jordan valleyof Israel were unexpectedly affected by a disease ofunknown etiology. The disease was accompanied bylarge populations of whiteflies. The suspicion that thewhiteflies were the vector of a viral disease was confirmedfollowing controlled transmission experiments in the lab-oratory. The virus was named tomato yellow leaf curlvirus (TYLCV). The virus was isolated and its genomesequenced in the late 1980s.

TYLCV is a member of the genus Begomovirus of thefamily Geminiviridae, which includes viruses transmitted bythe whitefly Bemisia tabaci. Begomoviruses have a genome

Encyclopedia of Virology, Third E

either split between two circular single-stranded (ss)DNA -moleculesof approximately2700 nteachnamedDNAAandDNA B (bipartite) or with a single genomic DNA A-likemolecule (monopartite). TYLCV is monopartite. The rela-tionships between the virus, the vector, and the host tomatoplant have been the object of many studies.

From the early 1960s tomato cultures have been underthe constant threat of TYLCV-like begomoviruses world-wide. TYLCV has quickly spread to the Middle East,Central Asia, North and West Africa, Southeast Europe,the Caribbean islands, Southeast USA, and Mexico.TYLCV-related begomoviruses have been identified inItaly, the Maghreb and Western Africa, and the ArabianPeninsula. Breeding programs for resistance have startedin the mid-1970s and several commercial varieties withadequate resistance have been released. Several locitightly linked to TYLCV resistance have been assignedto the small arm of tomato chromosome 6. A variety ofstrategies have been devised based on the pathogen-derived resistance concept, which involves the expressionof functional as well as dysfunctional viral genes. RNA-mediated virus resistance based on antisense RNA andpost-translational gene silencing was efficient but washighly sequence dependent.

Virus Structure

Like all geminiviruses, TYLCV has a characteristic particleof twinned morphology of approximately 20� 30 nm insize (Figure 1(a)). The virus capsid (total m.w. 3330 kDa)consists of two joined, incomplete icosahedra, with aT¼ 1 surface lattice containing a total of 22 capsomereseach containing five units of a 260-amino-acid coat protein(30.3 kDa). TYLCVhas a single 2787 nt (totalm.w. 980 kDa)covalently closed-genomic circular ssDNA.

dition (2008), vol. 5, pp. 138-145

Figure 1 Virions, host tomato plants and whitefly vector. (a) Viral particles with twinned morphology of approximately 20� 30nm

in size. (b) Left – infected tomato plant with typical symptoms; right – noninfected tomato plant. (c) Adult B. tabaci whiteflies,

approximately 2mm in size.

Tomato Yellow Leaf Curl Virus 139


Host Range

The domesticated tomato Solanum esculentum (formerlyLycopersicon esculentum) is the primary host of TYLCV.Most of the wild tomato species such as S. chilense,S. habrochaites (formerly L. hirsutum), S. peruvianum, andS. pimpinellifolium include accessions that are symp-tomless carriers and are used as genitors in breeding pro-grams for TYLCV resistance. Several cultivated plants(bean (Phaseolus vulgaris), petunia (Petunia hybrida), andlisianthus (Eustoma grandiflorum)) are hosts of TYLCVand present severe symptoms upon whitefly mediatedinoculation. Weeds, such as Datura stramonium and Cynan-

chum acutum, present distinct symptoms, whereas others,such as Malva parviflora, are symptomless carriers. Plantsused to rear whiteflies, such as cotton (Gossypium hirsutum)and eggplant (Solanum melongena), are immune to the virus.Experimental hosts of the virus include jimsonweed(Datura stramonium). Some plants recalcitrant to whiteflymediated inoculation, such as Nicotiana benthamiana andN. tabacum, may be infected by TYLCV DNA clonesusing agroinoculation.

Transmission to Tomato

In nature TYLCV is transmitted exclusively by the white-fly B. tabaci in a persistent manner (Figure 1). Symptomsincluded growth arrest leaflets cupped inward with yellowmargins, and barely produced fruits (Figure 1). B. tabacithrives in commercial fields of cotton, tomato, eggplant,and pepper, in tropical and subtropical countries. It alsoinfests the greenhouses in these regions as well as those intemperate countries. Whiteflies may cause dramaticdamages due to feeding and the transmission of begomo-viruses. B. tabaci comprises many types (or biotypes) thatcan be distinguished by their plant host range, fertility, aswell as with molecular markers (especially from the mito-chondrial genome). Among the many biotypes, B and Q areextremely efficient vectors of TYLCV.

Encyclopedia of Virology, Third

Transmission of TYLCV to tomato by B. tabaciB biotypehas been studied thoroughly. The virus is transmitted totomato plants after vector-feeding on infected tomatoplants or alternative hosts. The incidence of the disease isdirectly correlated with the pressure of the whitefly popu-lation. One to three viruliferous insects are able to infect atomato plant. The efficient acquisition access period (AAP)is 15–30min, the latent period is 8–24 h, and the efficientinoculation access period (IAP) is at least 15min. FemaleB. tabaci are more efficient vectors thanmales. The ability ofthe whiteflies to transmit TYLCV to tomato test plantssteadily decreases with age, from 100% to 10–20% duringtheir adult life time.

Symptoms develop on inoculated seedlings 2–3weeksafter insect first inoculation feeding. In the field inocula-tion can occur immediately after transplantation.Infected seedlings remain stunted and do not yieldfruits. Infection at a later stage affects vegetative growthand fruit setting. Disease incidence increases rapidly andin severely affected regions results in yield reduction ofup to 100%.

The viral DNA replicates in the nuclei of infectedcells and is mostly phloem limited. Apart from whiteflies,TYLCV can be transmitted by grafting and agroinocula-tion. It is not mechanically transmitted and it is notpropagated by seeds.d

Genome Organization and Expression

A schematic drawing of the TYLCV genome is shown inFigure 2. It replicates according to a rolling circle mech-anism. The viral genome encodes two large open readingframes (ORFs) on the viral strand (V1 and V2), and fouron the complementary strand (C1–C4). A 313 nt longintergenic region (IR) contains a 29 nt long stem–loopstructure with the conserved nanonucleotide TAATAT-TAC which is the origin of replication (Ori) of the virus.The IR also contains the promoters of the V1, V2, C1, andC4 genes.

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1548 C3

1087

V1

IR

498

V2

3081482787/1

26212473

2177

1639 1491

C4

C1

C21232

1090

Figure 2 Genome organization of tomato yellow leaf curl virus.

The single-stranded virion DNA comprises 2787 nt. Open reading

frames (ORFs) of virion-sense and complementary-sense strand

polarity are designated (V) and (C), respectively. ORFs arerepresented by an arrow; numbers indicate first and last

nucleotide of each ORF. V1 encodes the capsid protein (CP),

V2 a movement protein, C1 the replication initiator protein (Rep),C2 a transcriptional activator protein (TrAP), C3 a replication

enhancer protein (REn), and C4 a symptom and movement

determinant. IR: intergenic region. The conserved inverted repeat

flanking the conserved nanonucleotide sequence TAATATTACis symbolized by a stem–loop; an arrow head indicates the

cleaving position of Rep in the TAATATT/AC loop; A at the cutting

site (/) is nucleotide number one, by definition.

140 Tomato Yellow Leaf Curl Virus


. V1. The V1 ORF encodes the capsid protein (CP).TheCP is a multifunctional protein: TheN- andC-terminiof CP monomers interact to form the capsid (one viralgenomic molecule is encapsidated in each geminate parti-cle). TheCPhas a nuclear localization signal (NLS) and it isable to shuttle the viral genomic DNA in and out of thenucleus. It is essential for infectivity, and it is the only viralprotein recognized by the insect vector.

. V2. The V2 ORF has properties analogous to thoseof a movement protein and in some cases mutants affectsymptom expression.

. C1. The C1 ORF encodes the replication initiatorprotein (Rep). It is the only viral protein necessary forreplication. The functional protein is an oligomer. TheRep protein recognizes the Ori located in the IR andspecifically cleaves the nanonucleotide TAATATTACbetween nucleotides 7 and 8. Together with plant hostpolymerase(s) it initiates viral DNA replication accord-ing to the rolling-circle model. Short inverted repeatslocated in the IR upstream the stem–loop structure arerecognized by the Rep protein and also involved in thereplication process. Rep also interacts with another viral


protein, the viral replication enhancer protein (REn),encoded by ORF C3 and with a variety of cellular pro-teins such as a retinoblastoma-like protein, an interactionthat may enhance plant cell replication and thereby viralmultiplication.

. C2. The ORF C2 encodes a transcriptional activatorprotein (TrAp). Both ORFs C2 and C3 are transcribedfrom a promoter located in the 30 end of the C1 ORF.TrAp enhances transcription of the viral strand promoter.It is able to bind to viral genomic DNA and possesses anNLS. In addition, the C2 gene product acts as silencingsuppressors.

. C3. The ORF C3 encodes the replication enhancerprotein (REn). This protein interacts with itself to formoligomers. REn interacts with Rep and with cell-cycleassociated host proteins to increase the amount viralDNA (genomic and double-stranded) in the infectedplant.

. C4. The ORF C4 encodes a protein not essentialfor infectivity but contributes to the spread of the virus inthe plant and induction of symptoms. The protein mayalso act as a silencing suppressor, but this has not beendefinitively proved.

Geographical Distribution

The name TYLCV was coined in the early 1960s todescribe a virus transmitted by the whitefly B. tabaci thataffected tomato cultures in Israel. Early diagnosis ofTYLCV was essentially based on symptom observation,although symptoms vary greatly as function of soil,growth conditions, and climate. Serology has been oflimited use because whitefly transmitted geminivirusesshare many epitopes. The analysis of DNA sequenceshas become the tool of choice, allowing one to accuratelyidentify the virus and to evaluate its relationship withother TYLCV isolates. TYLCV has been reported in themid- and late 1970s in Cyprus, Jordan, and Lebanon. Ithas been identified in Egypt and Turkey in the early1980s. The virus has spread to Turkey, Iran and theAsian republics of the former USSR, and to Saudi Arabiaand Yemen during the mid–late 1990s. Two TYLCVisolates closely related to the Middle Eastern virus havebeen described in Japan in the late 1990s. In China,TYLCV isolate TYLCVs has been identified in the south-west province of Guangxi. In the early 1990s two virusisolates belonging to a new species related to the MiddleEastern TYLCV, named tomato yellow leaf curl Sardiniavirus, have been identified in Sardinia (TYLCSV-Sar)and in Sicily (TYLCSV-Sic), Italy. The Sardinian isolateTYLCSV-Sar has been discovered in Spain in the early1990s. By he mid-1990s the Middle Eastern TYLCV wasfound in Portugal and in Spain; in the latter country, ittended to displace the previously established Italian virus.

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Recombinants between the two viruses have been found.TYLCV has invaded North Africa, possibly from Spainand Italy. In Morocco, both the Italian and the MiddleEastern strain were discovered in the early 2000s. InTunisia the Italian virus was identified in the early 2000s.TYLCV appeared in Southern France in 1999. In 2000,the Middle Eastern strain of TYLCV was identified inCrete, Attiki, and Southern Peloponnesus in Greece. InEast Africa, TYLCV was present in Sudan as early as thelate 1970s. In Tanzania a virus distinct from the Mediter-ranean isolates has been sequenced. In the Reunion Islandthe virus was detected in the late 1990s. The MiddleEastern strain of TYLCV has appeared in the WesternHemisphere in the mid-1990s in the Caribbean Islands,first in the Dominican Republic, then Cuba, Jamaica,Puerto Rico, and the Bahamas. From there, the virushas reached the USA, identified first in Virginia in thelate 1990s, then in Florida, Georgia, Louisiana, NorthCarolina, and Mississippi. It seems that TYLCV is nowfound in several regions of Mexico.

Hence during the last decade TYLCV has spreadextremely fast and constitutes a major limiting factor totomato cultivation, worldwide. In many regions, theinvading Mediterranean strain of TYLCV coexists withlocal TYLCV strains, but in several cases it has almostreplaced them, as in Southern Spain. The Sardinian iso-late of TYLCSV has been recently detected in Jordan andin Israel, indicating that the expansion of TYLCSV is notunidirectional, from the Eastern Mediterranean region toother parts of the world as thought not long ago.

Taxonomy and Classification

TYLCV is the name of the virus originally isolated inIsrael. Sequence comparisons of TYLCV-like viruses ana-lyzed worldwide have revealed that the name TYLCVwas used mistakenly to name a complex of closely aswell as distantly related begomoviruses affecting tomato.Viruses with nucleotide sequence homology of more than89% have been considered to be strains of the samespecies while viruses with homologies of less than 89%have been considered as belonging to different virus spe-cies. Accordingly, the begomoviruses affecting tomatohave been classified into several species: all the TYLCVisolates known today have a monopartite genome.

The members of the TYLCV species, as well as mem-bers of species closely related to TYLCV updated as ofDecember 2006, are listed in Table 1; the acronym andthe GenBank accession number of the DNA sequence areprovided.

This classification is rendered even more complicatedby the recent discovery that recombination betweenmembers of different species of geminiviruses happensrelatively frequently. For example, a naturally occurring


recombination has been recently found in the Almeriaregion, Spain, between TYLCVand TYLCSV. The recom-binant virus, coined tomato yellow leaf curl Malaga virus(TYLCMalV-[ES], AF271234), probably occurred becausethe two virus species have coexisted in the tomato plantsgrown in the greenhouse.

Additional begomoviruses that infect tomato cultureshave not been assigned to the TYLCV and are discussedelsewhere in this encyclopedia. These viruses clearly dif-fer from the various TYLCV isolates in the symptomsthey induce on tomato, in their host range, and in theirnucleotide sequence.

Virus–Vector Relationship

Path of the Virus in the Insect

Like all begomoviruses TYLCV follows a definite path inits B. tabaci vector. Whiteflies feed when their stylets reachthe virus-rich phloem of infected leaves. TYLCV can bedetected in the insect head approximately 10min afterfeeding started. From the esophagus the virus reaches themidgut where it can be detected approximately 30minafter it was first found in the head. At this point, some ofthe viruses might be excreted through the hindgut. Thecrossing of TYLCV from the midgut to the hemolymph issurprisingly fast. The virus reaches the hemolymph 30minafter it was first detected in the midgut, 90min after thebeginning of the AAP. The crossing of the gut is likely to bean active process involving specialized unknown receptors.To avoid degradation in the hemolymph, geminivirusesinteract with a GroEL-like chaperonin produced by theinsect endosymbiotic bacteria and excreted in the hemo-lymph. TYLCV can be detected in the salivary glandsapproximately 5.5 h after it was first detected in the haemo-lymph, 7 h after the beginning of the AAP, approximately1 h before the insects are able to infect tomato plants. Oncethe virus reaches the salivary gland, crossing several cellwalls that may constitute selective receptor-mediated bar-riers, it is almost immediately excreted into the salivarypump and from there into the plant together with the saliva.The capsid (and the coat protein) is the only begomoviralstructure recognized by the would-be receptors and by theendosymbiotic chaperonin.

Retention of TYLCV in the Insect Vector

The virus can be detected in every stage of vector de-velopment. Following a 48 h AAP on TYLCV-infectedtomato, viral DNA remains associated with B. tabaci for theentire adult life of the insect while infectivity decreases withtime, but not entirely. Various TYLCV isolates presentsometimes different parameters of interactions with theirwhitefly host. For example, the maximum retention period

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Table 1 List of 59 virus isolates (written in black) used in this article belonging to 15 different strains (written in red) and six different

species of the Tomato yellow leaf curl virus cluster (written in green). The accession numbers of the complete A component sequence is

indicated in the second column and the abbreviation of the name of the virus isolates and strains is indicated in the third column

Tomato leaf curl Sudan virus

Tomato leaf curl Sudan virus – Gezira ToLCSDV-Gez

Tomato leaf curl Sudan virus – Gezira [Sudan:Gezira:1996] AY044137 ToLCSDV-Gez[SD:Gez:96]

Tomato leaf curl Sudan virus – Shambat ToLCSDV-ShaTomato leaf curl Sudan virus – Shambat [Sudan:Shambat:1996] AY044139 ToLCSDV-Sha[SD:Sha:96]

Tomato leaf curl Sudan virus – Yemen ToLCSDV-YE

Tomato leaf curl Sudan virus – Yemen [Yemen:Tihamah:2006] EF110890 ToLCSDV-YE[YE:Tih:06]Tomato yellow leaf curl Axarquia virus

Tomato yellow leaf curl Axarquia virus – [Spain:Algarrobo:2000] AY227892 TYLCAxV-[ES:Alg:00]

Tomato yellow leaf curl Malaga virus

Tomato yellow leaf curl Malaga virus – [Spain:421:1999] AF271234 TYLCMaIV-[ES:421:99]Tomato yellow leaf curl Mali virus

Tomato yellow leaf curl Mali virus – Ethiopia TYLCMLV-ET

Tomato yellow leaf curl Mali virus – Ethiopia [Ethiopia:Melkassa:2005] DQ358913 TYLCMLV-ET[ET:Mel:05]

Tomato yellow leaf curl Mali virus – Mali TYLCMLV-MLTomato yellow leaf curl Mali virus – Mali [Mali] AY502934 TYLCMLV-ML[ML]

Tomato yellow leaf curl Sardinia virus

Tomato yellow leaf curl Sardinia virus – Italy TYLCSV-IT

Tomato yellow leaf curl Sardinia virus – Italy [Italy:Sardinia:1988] X61153 TYLCSV-IT[IT:Sar:88]Tomato yellow leaf curl Sardinia virus – Sicily TYLCSV-Sic

Tomato yellow leaf curl Sardinia virus – Sicily [Israel:Henryk:2005] DQ845787 TYLCSV-Sic[IL:Hen:05]

Tomato yellow leaf curl Sardinia virus – Sicily [Italy:Sicily] Z28390 TYLCSV-Sic[IT:Sic]Tomato yellow leaf curl Sardinia virus – Sicily [Tunisia:Bkalta 3:2002] AY736854 TYLCSV-Sic[TN:Bk3:02]

Tomato yellow leaf curl Sardinia virus – Spain TYLCSV-ES

Tomato yellow leaf curl Sardinia virus – Spain [Spain:Almeria 2:1992] L27708 TYLCSV-ES[ES:Alm2:92]

Tomato yellow leaf curl Sardinia virus – Spain [Spain:Canary] AJ519675 TYLCSV-ES[ES:Can]Tomato yellow leaf curl Sardinia virus – Spain [Spain:Murcia 1:1992] Z25751 TYLCSV-ES[ES:Mur1:92]

Tomato yellow leaf curl Sardinia virus – Spain[Morocco:Agadir:2002] AY702650 TYLCSV-ES[MA:Aga:02]

Tomato yellow leaf curl virus

Tomato yellow leaf curl virus – Gezira TYLCV-GezTomato yellow leaf curl virus – Gezira [Sudan:1996] AY044138 TYLCV-Gez[SD:96]

Tomato yellow leaf curl virus – Iran TYLCV-IR

Tomato yellow leaf curl virus – Iran [Iran] AJ132711 TYLCV-IR[IR]Tomato yellow leaf curl virus – Israel TYLCV-IL

Tomato yellow leaf curl virus – Israel [Australia:Brisbane:2006] 1934a TYLCV-IL[AU:Bri:06]

Tomato yellow leaf curl virus – Israel [China:Shangai 2:2005] AM282874 TYLCV-IL[CN:SH2:05]

Tomato yellow leaf curl virus – Israel [Cuba] AJ223505 TYLCV-IL[CU]Tomato yellow leaf curl virus – Israel [Dominican Republic] AF024715 TYLCV-IL[DO]

Tomato yellow leaf curl virus – Israel [Egypt:Ismaelia] AY594174 TYLCV-IL[EG:Ism]

Tomato yellow leaf curl virus – Israel [Egypt:Nobaria:1991] EF107520 TYLCV-IL[EG:Nob:91]

Tomato yellow leaf curl virus – Israel [Israel:Rehovot:1986] X15656 TYLCV-IL[IL:Reo:86]Tomato yellow leaf curl virus – Israel [Italy:Sicily:2004] DQ144621 TYLCV-IL[IT:Sic:04]

Tomato yellow leaf curl virus – Israel [Japan:Haruno:2005] AB192966 TYLCV-IL[JR:TosH:05]

Tomato yellow leaf curl virus – Israel [Japan:Misumi:Stellaria] AB116631 TYLCV-IL[JR:Mis:Ste]Tomato yellow leaf curl virus – Israel [Japan:Miyazaki] AB116629 TYLCV-IL[JR:Miy]

Tomato yellow leaf curl virus – Israel [Japan:Omura:Eustoma] AB116630 TYLCV-IL[JR:Omu:Eus]

Tomato yellow leaf curl virus – Israel [Japan:Omura] AB110217 TYLCV-IL[JR:Omu]

Tomato yellow leaf curl virus – Israel [Japan:Tosa:2005] AB192965 TYLCV-IL[JR:Tos:05]Tomato yellow leaf curl virus – Israel [Jordan:Tomato:2005] EF054893 TYLCV-IL[JO:Tom:05]

Tomato yellow leaf curl virus – Israel [Lebanon:Tomato:2005] EF051116 TYLCV-IL[LB:Tom:05]

Tomato yellow leaf curl virus – Israel [Mexico:Culiacan:2005] DQ631892 TYLCV-IL[MX:Cul:05]

Tomato yellow leaf curl virus – Israel [Morocco:Berkane:2005] EF060196 TYLCV-IL[MO:Ber:05]Tomato yellow leaf curl virus – Israel [Puerto Rico:2001] AY134494 TYLCV-IL[PR:01]

Tomato yellow leaf curl virus – Israel [Spain:Almeria:Pepper:1999] AJ489258 TYLCV-IL[ES:Alm:Pep:99]

Tomato yellow leaf curl virus – Israel [Tunisia:2005] EF101929 TYLCV-IL[TN:05]

Tomato yellow leaf curl virus – Israel [Turkey:Mersin:2004] AK812277 TYLCV-IL[TR:Mer:04]Tomato yellow leaf curl virus – Israel [US:Florida] AY530931 TYLCV-IL[US:Flo]

Tomato yellow leaf curl virus – Mild TYLCV-Mld

Tomato yellow leaf curl virus – Mild [Israel;1993] X76319 TYLCV-Mld[IL;93]Tomato yellow leaf curl virus – Mild [Japan:Aichi] AB014347 TYLCV-Mld[JR:Aic]

Continued


Encyclopedia of Virology, Third Edition (2008), vol. 5, pp. 138-145


Table 1 Continued

Tomato yellow leaf curl virus – Mild [Japan:Atumi] AB116633 TYLCV-Mld[JR:Atu]

Tomato yellow leaf curl virus – Mild [Japan:Daito] AB116635 TYLCV-Mld[JR:Dai]

Tomato yellow leaf curl virus – Mild [Japan:Kisozaki] AB116634 TYLCV-Mld[JR:Kis]Tomato yellow leaf curl virus – Mild [Japan:Osuka] AB116636 TYLCV-Mld[JR:Osu]

Tomato yellow leaf curl virus – Mild [Japan:Shimizu] AB110218 TYLCV-Mld[JR:Shi]

Tomato yellow leaf curl virus – Mild [Japan:Shizuoka] AB014346 TYLCV-Mld[JR:Shz]

Tomato yellow leaf curl virus – Mild [Japan:Yaizu] AB116632 TYLCV-Mld[JR:Yai]Tomato yellow leaf curl virus – Mild [Jordan:Cucumber:2005] EF158044 TYLCV-Mld[JO:Cuc:03]

Tomato yellow leaf curl virus – Mild [Jordan:Homra:2003] AY594175 TYLCV-Mld[JO:Hom03]

Tomato yellow leaf curl virus – Mild [Jordan:Tomato:2005] EF054894 TYLCV-Mld[JO:Tom:03]

Tomato yellow leaf curl virus – Mild [Lebanon;LBA44:05] EF185318 TYLCV-Mld[ILB;LBA44:05]Tomato yellow leaf curl virus – Mild [Portugal:2:1995] AF105975 TYLCV-Mld[PT:2:95]

Tomato yellow leaf curl virus – Mild [Reunion:2002] AJ865337 TYLCV-Mld[RE:02]

Tomato yellow leaf curl virus – Mild [Spain:72:1997] AF071228 TYLCV-Mld[ES:72:97]

Tomato yellow leaf curl virus – Mild [Spain:Almeria:1999] AJ519441 TYLCV-Mld[ES:Alm:99]

aAustralian accession.

Species names are in italic fonts and strain and isolate names are in roman fonts.



of isolates of TYLCSV (TYLCSV-[IT:Sar]) was 8 days fromthe end of the AAP compared to 5weeks for TYLCV.

Both TYLCV and TYLCSV can be detected in theeggs and in adult progeny of viruliferous whiteflies in lowincidence. However while the TYLCV progeny was ableto transmit the virus to tomato plants, the TYLCSVprogeny did not. Although the question of the possiblereplication of TYLCV in its insect vector remains contro-versial, transcripts of viral genes V1, V2, and C3 accumu-lated in B. tabaci long after transfer of viruliferouswhiteflies on nonhost cotton plants. In contrast to TYLCV,transcripts of the bipartite begomovirus ToMoV did notaccumulate in the whiteflies.

Deleterious Effects of TYLCV on LifeExpectancy and Fertility of theWhitefly Vector

Three-day-old insects raised on eggplants (a TYLCVnonhost) following a 48 h AAP on TYLCV-infected to-mato plants showed a reduction of 17–23% in their lifeexpectancy compared to insects that have not acquiredthe virus, and to a 40–50% decrease in the mean numberof eggs laid. These deleterious effects, in addition to theinvasion of the reproductive system, suggest that TYLCVhas some features reminiscent of an insect pathogen.

Sexual Transmission

TYLCV can be transmitted among whiteflies in asex-dependent manner, in the absence of any other sourceof virus. TYLCV was transmitted from viruliferous malesto females and from viruliferous females to males, but notamong insects of the same sex. The recipient insectswere able to efficiently inoculate tomato test plants. Inthe recipient insects TYLCV was first detected in the


hemolymph, but not in the head as in the case of acquisi-tion from infected plants. Therefore the virus follows, atleast in part, the circulative pathway associated withacquisition from infected plants. Insect to insect virustransmission was instrumental in increasing the numberof whiteflies capable of infecting tomato test plants in awhitefly population. Accordingly, a plant virus can besexually transmitted among its insect vector.

Breeding Tomato for Resistance to TYLCV

Incorporation of Resistance Trait from WildTomato Species

The domesticated tomato S. esculentum is extremely sus-ceptible to TYLCV. Breeding tomato for resistancestarted in the early 1960s and is going on since then. Ithas been initially observed that some accessions of wildtomato species exhibited resistance to the virus and couldbe crossed with the domesticated tomato. The first suc-cessful breeding program was initiated with S. peruvianum.Although this type of resistance was controlled by threeto five recessive genes, a first hybrid with acceptableresistance was released in 1988. Advanced breeding linesand commercial varieties containing this type of resis-tance were released subsequently. Resistance genes fromseveral different accessions of the wild tomato speciesS. chilense have been incorporated into breeding programsin the early 1990s. For each S. chilense accession, resistanceis determined by a different semidominant gene and sev-eral minor genes. The wild tomato species S. habrochaiteshas been used in the late 1990s to produce breeding linesin which resistance is under the control of a major domi-nant locus.

After more than 25 years of effort, the best resistantcultivars and breeding lines give far higher yields upon

Edition (2008), vol. 5, pp. 138-145

Figure 3 TYLCV-infected tomato fields planted with

susceptible and resistant tomato genotypes. Note that the

susceptible plants are stunted, and they will not produce fruits;for comparison, the resistant plants will remain symptomless,

or have mild symptoms, and will yield.



infection than those of susceptible cultivars; diseasesymptoms are absent or mild but all of them containvarious amounts of virus (Figure 3). It is interesting tonote that in many cases (especially when the resistanceoriginates from certain accessions of S. chilense and ofS. habrochaites), the tomato lines are resistant to TYLCVand also to a number of begomoviruses in very differentparts of the world, some of them monopartite and othersbipartite. For example, line Lh902 that originated fromS. habrochaites is resistant to TYLCV in the Mediterraneanregion as well as to a wide range of bipartite geminivirusesin Central America.

Genetically Engineered Tomato for Resistance

A variety of strategies have been devised based on theexpression of functional as well as dysfunctional viralgenes such as coat protein and Rep protein. A tomatointerspecific hybrid expressing the TYLCV coat proteingene under the control of the 35S CaMV promoterresponded upon whitefly mediated TYLCV inoculationshowed expression of delayed disease symptoms andrecovery from disease. Tomato inbred lines have beentransformed with a 30 truncated Rep gene (two-fifths ofthe gene) and the virus intergenic region from the Floridaisolate of TYLCV (TYLCV-[US:Flo]). Resistance wasachieved upon whitefly mediated inoculation in fieldconditions. However, these plants were susceptible tothe bipartite begomovirus ToMoV from Florida. Simi-larly, tomato plants transformed with the Rep gene ofTYLCSV (TYLCSV-[IT-Sar]) truncated in its 30 end(leaving 210 amino acids out of 257) exhibited resistanceto TYLCSV-[IT:Sar] but were susceptible to the relatedstrain from Spain TYLCSV-ES[ES]. The viral Repgene altered in the NTP-binding site crucial for virus


replication has been used as trans-dominant proteins toblock virus replication.

RNA-mediated virus resistance was highly sequencedependent. Expression of antisense sequence of theTYLCV-[IT-Sar] Rep gene in transgenic N. benthamiana

resulted in repression of nearly all virus replication. Theincorporation of a ribozyme structure into the antisenseconstruct did not increase the efficiency of the system.Resistant tomato plants have been developed whichexploit the mechanism of post-transcriptional genesilencing via double-stranded RNA sequences. Noncod-ing conserved regions from the genomes of TYLCV,TYLCV-mild (TYLCV-Mld[IL]), and from the TYLCVstrains from Egypt (TYLCV-[EG:Ism]), and TYLCSVfrom Sardinia (TYLCSV-[IT:Sar]) and Spain (-TYLCSV-ES[ES]) were used to design a construct thatcan trigger broad resistance against the differentTYLCVs. A high level of resistance was obtained whenplants were inoculated with TYLCV-[EG:Ism], TYLCV-Mld[IL], and TYLCSV-ES[ES]. A positive correlationbetween resistance and the accumulation of virus-specificsiRNAs was observed in silenced plants.

Localization of Loci Linked to Resistance toTYLCV in Tomato for Possible Use inMarker-Assisted Breeding

Mapping genes in tomato has been facilitated by the devel-opment of saturated maps based on DNA polymorphism(RFLP, AFLP, SSR, SCAR, etc.). A TYLCV-resistancegene originating from S. chilense accession LA 1969, Ty-1,has been mapped to tomato chromosome 6 using RFLPmarkers. Three additional loci linked to resistance againstTYLCV have been mapped to chromosome 6 using resis-tant tomato inbreds derived from S. chilense accessionsLA1932, LA2779, and LA1938. Another resistant geneoriginating from S. pimpinellifolium has been mapped, usingRAPD markers, also to chromosome 6 but to a locusdifferent from Ty-1. It can be noted that a locus conferringresistance to a nonrelated TYLCV isolate belonging to thespecies tomato leaf curl Taiwan virus from Taiwan, origi-nating from L. hirsutum LA1777, has been located in chro-mosome 11 using RFLP markers.

See also: African Cassava Mosaic Disease; Bean GoldenMosaic Virus; Beet Curly Top Virus; Emerging Gemini-viruses; Tomato Leaf Curl Viruses from India; SatelliteNucleic Acids and Viruses.

Further Reading

Czosnek H (ed.) (2007) Tomato Yellow Leaf Curl Virus Disease:Management, Molecular Biology, Breeding for Resistance.Dordrecht: Springer.

dition (2008), vol. 5, pp. 138-145

Tombusviruses 145


Lapidot M and Friedmann M (2002) Breeding for resistance towhitefly-transmitted geminiviruses. Annals of Applied Biology 140:109–127.

Nakhla MK and Maxwell DP (1998) Epidemiology and management oftomato yellow leaf curl disease. In: Hadidi A, Khetarpal RK, and

Tombusviruses

S A Lommel and T L Sit, North Carolina State University

ã 2008 Elsevier Ltd. All rights reserved.

Glossary

Modular evolution Evolution of viral genomes

involving the combination of common genes/gene

families.

Movement protein A plant viral protein that

potentiates viral cell-to-cell movement through

plasmodesmata.

Origin of assembly Unique RNA sequence and

structure that specifically binds CP to initiate capsid

assembly.

Polycistronic The characteristic of a given RNA

containing more than one gene (open reading

frame).

Quasiequivalence Capsid protein subunits

arranged so that they are in somewhat equivalent

environments with respect to their adjacent subunits.

(Silencing) suppressor Virally encoded product

that inhibits a stage in the host RNA silencing

pathway.

Subgenomic RNAs Less-than-full-length RNAs that

are produced during replication, usually to express

internal open reading frames.

Introduction

The Tombusviridae is a relatively large and diverse family ofsingle-stranded, positive-sense, RNA plant viruses withcommon morphological, structural, molecular, and geneticfeatures. Due to their small size and extremely high virustiter in experimental hosts, viruses in the family areparticularly well characterized in terms of virion struc-ture, replication, gene expression strategies, local and sys-temic movement, suppression of host gene silencing andassociated satellite viruses, and defective interfering RNAs.

The family is constituted based on a unifying phylogeneticand biological feature. The RNA-dependent RNA polymer-ase of tombusviruses is highly conserved in terms of sequence


Koganezawa H (eds.) Plant Virus Disease Control, pp. 565–583.St. Paul, MN: APS Press.

Pico B, Diez MJ, and Nuez F (1996) Viral diseases causing the greatesteconomic losses to tomato crop. Part II: The tomato yellow leafcurl virus – A review. Scientia Horticulturae 67: 151–196.

, Raleigh, NC, USA

identity, genomic structure, and gene expression and function.Biologically, tombusviruses share the property of being pri-marily soil transmitted, often without a biological vector, andaccumulate to high levels in the roots of infected plants.Beyond these constants the family is remarkably diverse inbiology, pathology, host range, and genome organization.

Many of the viruses now comprising the familyTombusviridae have been studied for a number of decades.Viruses like tomato bushy stunt virus (TBSV), carnationringspot virus (CRSV), carnation mottle virus (CarMV),and cymbidium ringspot virus (CymRSV) were firstdescribed and virions purified and characterized in the1940s. The taxonomic and phylogenetic relatedness ofmany of the viruses now comprising this family was notresolved until the mid-1980s, when genomes of theseviruses were first cloned and sequenced.

Taxonomy, Phylogeny, and Evolution

The family Tombusviridae of plant viruses is composed ofthe genera Aureusvirus, Avenavirus, Carmovirus, Diantho-virus, Machlomovirus, Necrovirus, Panicovirus, and Tombus-

virus, with more than 43 species and 15 tentative speciesrecognized. Several genera are represented by many spe-cies whereas three genera are monotypic. The typespecies of the genus Aureusvirus is Pothos latent virus. Thisgenus is quite similar to the genus Tombusvirus but isdistinguished by having significantly different sizedmovement and silencing suppressor proteins. The typespecies of the monotypic genus Avenavirus is Oat chloroticstunt virus. This species constitutes a separate genusbecause the genome organization is intermediate betweenthose of the genera Carmovirus and Tombusvirus. Further-more its capsid protein (CP) is significantly larger thanthose found in other genera whose CPs have a protruding(P) domain. Carnation mottle virus is the type species of thegenus Carmovirus. This genus is distinguished by havingtwo small proteins associated with virus movement and aCP with a P domain. The genus Dianthovirus, of which

Edition (2008), vol. 5, pp. 138-145

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