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Identification and Characterization of a Host Reversibly Glycosylated Peptide that Interacts with the Tomato leaf curl virus V1 Protein

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Abstract

Monopartite geminiviruses of the genus Begomovirus have two virion-sense genes, V1 and V2. V2 encodes the viral coat protein, but the function of V1 is largely unknown, although some studies suggest that it may play a role in cell-to-cell movement. Yeast two-hybrid technology was used to identify possible host binding partners of V1 from Tomato leaf curl virus (TLCV) to better understand its function. A protein closely related to a family of plant reversibly glycosylated peptides, designated SlUPTG1, was found to interact with V1 in yeast and in vitro. SlUPTG1 may function endogenously in the synthesis of cell wall polysaccharides, since a bacterially expressed form of the protein acted as an autocatalytic glycosyltransferase in␣vitro, a SlUPTG1:GFP fusion protein localized to the cell wall, and expression of SlUPTG1 appeared to be highest in actively dividing tissues. However, expression of SlUPTG1 in a transient TLCV replication assay increased the accumulation of viral DNA, suggesting that this host factor also plays a role in viral infection. Together, these data provide new insight into the role of V1 in TLCV infection and reveal another host pathway which geminiviruses may manipulate to achieve an efficient infection.

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Abbreviations

ACMV:

African cassava mosaic virus

AD:

activation domain

CaMV:

Cauliflower mosaic virus

CAT:

chloramphenicol acetlytransferase

CBP:

calmodulin-binding peptide

ER:

endoplasmic reticulum

GFP:

green fluorescent protein

GUS:

ß-glucuronidase

Ni-NTA:

nickel-nitriloacetic acid

ORF:

open-reading frame

Pd:

plasmodesmata

PM:

plasma membrane

RGP:

reversibly glycosylated peptide

TLCV:

Tomato leaf curl virus

TYLCSV:

Tomato yellow leaf curl Sardinia virus

UPTG:

UDP-glucose:protein transglucosylase

References

  • D.M. Benko R.S. Haltiwanger G.W. Hart W. Gibson (1988) ArticleTitleVirion basic phosphoprotein from human cytomegalovirus contains O-linked N-acetylglucosamine Proc. Natl. Acad. Sci. USA. 85 2573–2577 Occurrence Handle2833746 Occurrence Handle1:CAS:528:DyaL1cXitFOqu7o%3D Occurrence Handle10.1073/pnas.85.8.2573

    Article  PubMed  CAS  Google Scholar 

  • S.N. Bocca R. Kissen J.A. Rojas-Beltran F. Noel C. Gebhardt S. Moreno P. du Jardin J.S. Tandecarz (1999a) ArticleTitleMolecular cloning and characterization of the enzyme UDP-glucose: protein transglucosylase from potato Plant Physiol. Biochem. 37 809–819 Occurrence Handle1:CAS:528:DC%2BD3cXlsFequw%3D%3D Occurrence Handle10.1016/S0981-9428(99)00117-5

    Article  CAS  Google Scholar 

  • S.N. Bocca A. Rothschild J.S. Tandecarz (1999b) ArticleTitleInitiation of starch biosynthesis: purification and characterization of UDP-glucose:protein transglucosylase from potato tubers Plant Physiol. Biochem. 35 203–210

    Google Scholar 

  • D.A. Brummell A. Camirand G.A. Maclachlan (1990) ArticleTitleDifferential distribution of xyloglucan glycosyl transferases in pea Golgi dicytosome and secretory vesicles J. Cell Sci. 96 705–710 Occurrence Handle1:CAS:528:DyaK3cXmt1Oqurg%3D

    CAS  Google Scholar 

  • I.J. Delgado Z. Wang A. Rocher Particlede K. Keegstra N.V. Raikhel (1998) ArticleTitleCloning and characterization of AtRGP1. A reversibly autoglycosylated arabidopsis protein implicated in cell wall biosynthesis Plant Physiol. 116 1339–1350 Occurrence Handle9536051 Occurrence Handle1:CAS:528:DyaK1cXisFyqsbs%3D Occurrence Handle10.1104/pp.116.4.1339

    Article  PubMed  CAS  Google Scholar 

  • D.P. Delmer (1999) ArticleTitleCellulose biosynthesis: exciting times for a difficult field of study Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 245–276 Occurrence Handle15012210 Occurrence Handle1:CAS:528:DyaK1MXkt1yksb8%3D Occurrence Handle10.1146/annurev.arplant.50.1.245

    Article  PubMed  CAS  Google Scholar 

  • K.S. Dhugga S.C. Tiwari P.M. Ray (1997) ArticleTitleA reversibly glycosylated polypeptide (RGP1) possibly involved in plant cell wall synthesis: purification, gene cloning, and trans-Golgi localization Proc. Natl. Acad. Sci. USA 94 7679–7684 Occurrence Handle9207152 Occurrence Handle1:CAS:528:DyaK2sXksFylsbk%3D Occurrence Handle10.1073/pnas.94.14.7679

    Article  PubMed  CAS  Google Scholar 

  • A. Driouich L. Faye L.A. Staehelin (1993) ArticleTitleThe plant Golgi apparatus: a factory for complex polysaccharides and glycoproteins Trends Biochem. Sci. 18 210–214 Occurrence Handle8346556 Occurrence Handle1:CAS:528:DyaK3sXlslOmsbg%3D Occurrence Handle10.1016/0968-0004(93)90191-O

    Article  PubMed  CAS  Google Scholar 

  • Y.P. Duan C.A. Powell D.E. Purcifull P. Broglio E. Hiebert (1997) ArticleTitlePhenotypic variation in transgenic tobacco expressing mutated geminivirus movement/pathogenicity (BC1) proteins Mol. Plant-Microbe Interact. 10 1065–1074 Occurrence Handle9390421 Occurrence Handle1:CAS:528:DyaK2sXnslait7o%3D

    PubMed  CAS  Google Scholar 

  • I.B. Dry J.E. Rigden L.R. Krake P.M. Mullineaux M.A. Rezaian (1993) ArticleTitleNucleotide sequence and genome organization of tomato leaf curl geminivirus J. Gen. Virol. 74 147–151 Occurrence Handle8423446 Occurrence Handle1:CAS:528:DyaK3sXltlalsr8%3D Occurrence Handle10.1099/0022-1317-74-1-147

    Article  PubMed  CAS  Google Scholar 

  • I. Dry L. Krake P. Mullineaux A. Rezaian (2000) ArticleTitleRegulation of tomato leaf curl viral gene expression in host tissues Mol. Plant-Microbe Interact. 13 529–537 Occurrence Handle10796019 Occurrence Handle1:CAS:528:DC%2BD3cXislOjtLs%3D

    PubMed  CAS  Google Scholar 

  • B.L. Epel J.W.M. Lent Particlevan L. Cohen G. Kotlizky A. Katz A. Yahalom (1996) ArticleTitleA 41 kDa protein isolated from maize mesocotyl cell walls immunolocalizes to plasmodesmata Protoplasma 191 70–78 Occurrence Handle1:CAS:528:DyaK28XjvFOrsbo%3D Occurrence Handle10.1007/BF01280826

    Article  CAS  Google Scholar 

  • C.M. Fauquet D.P. Maxwell B. Gronenborn J. Stanley (2000) ArticleTitleRevised proposal for naming geminiviruses Arch. Virol. 145 1743–1761 Occurrence Handle11003482 Occurrence Handle1:CAS:528:DC%2BD3cXnt1WhtL8%3D Occurrence Handle10.1007/s007050070089

    Article  PubMed  CAS  Google Scholar 

  • M.R. Fernandez-Fernandez E. Camafeita P. Bonay E. Mendez J.P. Albar J.A. Garcia (2002) ArticleTitleThe capsid protein of a plant single-stranded RNA virus is modified by O-linked N-acetylglucosamine J. Biol. Chem. 277 135–140 Occurrence Handle11606576 Occurrence Handle1:CAS:528:DC%2BD38XjslCruw%3D%3D Occurrence Handle10.1074/jbc.M106883200

    Article  PubMed  CAS  Google Scholar 

  • Frangioni, J.V. and Neel, B.G. 1993. Solubilization and purification of enzymatically active glutathione S-transferase (pGEX) fusion proteins. Anal. Biochem. 210: 179–187.

    Google Scholar 

  • P.M. Frey N.G. Scharer-Hernandez J. Futterer I. Potrykus J. Puonti-Kaerlas (2001) ArticleTitleSimultaneous analysis of the bidirectional African cassava mosaic virus promoter activity using two different luciferase genes Virus Genes 22 231–242 Occurrence Handle11324760 Occurrence Handle1:CAS:528:DC%2BD3MXivFyjt7w%3D Occurrence Handle10.1023/A:1008183827072

    Article  PubMed  CAS  Google Scholar 

  • A.P. Gleave (1992) ArticleTitleA versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome Plant Mol. Biol. 20 1203–1207 Occurrence Handle1463857 Occurrence Handle1:CAS:528:DyaK3sXltlaquw%3D%3D Occurrence Handle10.1007/BF00028910

    Article  PubMed  CAS  Google Scholar 

  • Goffard, A. and Dubuisson, J. 2003. Glycosylation of hepatitis C virus envelope proteins. Biochimie 85: 295–301.

    Google Scholar 

  • N. Grimsley T. Hohn J.W. Davies B. Hohn (1987) ArticleTitleAgrobacterium-mediated delivery of infectious maize streak virus into maize plants Nature 325 177–179 Occurrence Handle1:CAS:528:DyaL2sXpslegsQ%3D%3D Occurrence Handle10.1038/325177a0

    Article  CAS  Google Scholar 

  • L. Hanley-Bowdoin S.B. Settlage B.M. Orozco S. Nagar D. Robertson (1999) ArticleTitleGeminiviruses: models for plant DNA replication, transcription, and cell cycle regulation Crit. Rev. Plant Sci. 18 71–106 Occurrence Handle1:CAS:528:DyaK1MXht12qtL8%3D

    CAS  Google Scholar 

  • Y.M. Hou R. Sanders V.M. Ursin R.L. Gilbertson (2000) ArticleTitleTransgenic plants expressing geminivirus movement proteins: abnormal phenotypes and delayed infection by Tomato mottle virus in transgenic tomatoes expressing the Bean dwarf mosaic virus BV1 or BC1 proteins Mol. Plant-Microbe Interact. 13 297–308 Occurrence Handle10707355 Occurrence Handle1:CAS:528:DC%2BD3cXht1ymtbc%3D

    PubMed  CAS  Google Scholar 

  • Hull, R. 2002. Matthews' Plant Virology. Academic Press, London.

  • D.J. Ingham E. Pascal S.G. Lazarowitz (1995) ArticleTitleBoth bipartite geminivirus movement proteins define viral host range, but only BL1 determines viral pathogenicity Virology 207 191–204 Occurrence Handle7871727 Occurrence Handle1:CAS:528:DyaK2MXjslCmt78%3D Occurrence Handle10.1006/viro.1995.1066

    Article  PubMed  CAS  Google Scholar 

  • Jin, H., Axtell, M.J., Dahlbeck, D., Ekwenna, O., Zhang, S., Staskawicz, B. and Baker, B. 2002. NPK1, an MEKK1-like mitogen-activated protein kinase kinase kinase, regulates innate immunity and development in plants. Dev. Cell 3: 291–297.

    Google Scholar 

  • A. Kheyr-Pour M. Bendahmane V. Matzeit G.P. Accotto S. Crespi B. Gronenborn (1991) ArticleTitle Tomato yellow leaf curl virus from Sardinia is a whitefly-transmitted monopartite geminivirus Nucleic Acids Res. 19 6763–6769 Occurrence Handle1840676 Occurrence Handle1:CAS:528:DyaK3sXpsFensw%3D%3D

    PubMed  CAS  Google Scholar 

  • Klinkenberg, F.A., Ellwood, S. and Stanley, J. 1989. Fate of African cassava mosaic virus coat protein deletion mutants after agroinoculation. J. Gen. Virol. 70: 1837–1844.

    Google Scholar 

  • S.M. Langeveld M. Vennik M. Kottenhagen R. Wijk Particlevan A. Buijk J.W. Kijne S. Pater Particlede (2002) ArticleTitleGlucosylation activity and complex formation of two classes of reversibly glycosylated polypeptides Plant Physiol. 129 278–289 Occurrence Handle12011358 Occurrence Handle1:CAS:528:DC%2BD38XjvFSmsrk%3D Occurrence Handle10.1104/pp.010720

    Article  PubMed  CAS  Google Scholar 

  • H. Lodish A. Berk L. Zipursky P. Matsudaira D. Baltimore J. Darnell (2000) Molecular Cell Biology W.H. Freeman New York

    Google Scholar 

  • K.G. Mullis R.S. Haltiwanger G.W. Hart R.B. Marchase J.A. Engler (1990) ArticleTitleRelative accessibility of N-acetylglucosamine in trimers of the adenovirus types 2 and 5 fiber proteins J. Virol. 64 5317–5323 Occurrence Handle2120471 Occurrence Handle1:CAS:528:DyaK3MXhvFKmtw%3D%3D

    PubMed  CAS  Google Scholar 

  • M. Padidam R.N. Beachy C.M. Fauquet (1996) ArticleTitleThe role of AV2 (“precoat”) and coat protein in viral replication and movement in tomato leaf curl geminivirus Virology 224 390–404 Occurrence Handle8874500 Occurrence Handle1:CAS:528:DyaK28Xmt12gs7g%3D Occurrence Handle10.1006/viro.1996.0546

    Article  PubMed  CAS  Google Scholar 

  • Padidam, M., Beachy, R.N. and Fauquet, C.M. 1999. A phage single-stranded DNA (ssDNA) binding protein complements ssDNA accumulation of a geminivirus and interferes with viral movement. J. Virol. 73: 1609–1616.

    Google Scholar 

  • E. Pascal P.E. Goodlove L.C. Wu S.G. Lazarowitz (1993) ArticleTitleTransgenic tobacco plants expressing the geminivirus BL1 protein exhibit symptoms of viral disease Plant Cell 5 795–807 Occurrence Handle8364356 Occurrence Handle1:CAS:528:DyaK2cXhtVags7w%3D Occurrence Handle10.1105/tpc.5.7.795

    Article  PubMed  CAS  Google Scholar 

  • J.E. Rigden I.B. Dry P.M. Mullineaux M.A. Rezaian (1993) ArticleTitleMutagenesis of the virion-sense open reading frames of Tomato leaf curl geminivirus Virology 193 1001–1005 Occurrence Handle8460471 Occurrence Handle1:CAS:528:DyaK3sXit12rsLc%3D Occurrence Handle10.1006/viro.1993.1215

    Article  PubMed  CAS  Google Scholar 

  • J.E. Rigden I.B. Dry L.R. Krake M.A. Rezaian (1996) ArticleTitlePlant virus DNA replication processes in Agrobacterium: insight into the origins of geminiviruses? Proc. Natl. Acad. Sci. USA 93 10280–10284 Occurrence Handle8816791 Occurrence Handle1:CAS:528:DyaK28XlslGktbs%3D Occurrence Handle10.1073/pnas.93.19.10280

    Article  PubMed  CAS  Google Scholar 

  • M.R. Rojas H. Jiang R. Salati B. Xoconostle-Cazares M.R. Sudarshana W.J. Lucas R.L Gilbertson (2001) ArticleTitleFunctional analysis of proteins involved in movement of the monopartite begomovirus, Tomato yellow leaf curl virus Virology 291 110–125 Occurrence Handle11878881 Occurrence Handle1:CAS:528:DC%2BD3MXovFGgsr4%3D Occurrence Handle10.1006/viro.2001.1194

    Article  PubMed  CAS  Google Scholar 

  • G. Sagi A. Katz D. Guenoune-Gelbart B.L. Epel (2005) ArticleTitleClass 1 reversibly glycosylated polypeptides are plasmodesmal-associated proteins delivered to plasmodesmata via the Golgi apparatus Plant Cell 17 1788–1800 Occurrence Handle15879561 Occurrence Handle1:CAS:528:DC%2BD2MXlsVynsr0%3D Occurrence Handle10.1105/tpc.105.031823

    Article  PubMed  CAS  Google Scholar 

  • Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.

    Google Scholar 

  • M. Seemanpillai I. Dry J. Randles A. Rezaian (2003) ArticleTitleTranscriptional silencing of geminiviral promoter-driven transgenes following homologous virus infection Mol. Plant-Microbe Interact. 16 429–438 Occurrence Handle12744514 Occurrence Handle1:CAS:528:DC%2BD3sXjsVylt7c%3D

    PubMed  CAS  Google Scholar 

  • L.A. Selth S.C. Dogra M.S. Rasheed H. Healy J.W. Randles M.A. Rezaian (2005) ArticleTitleA NAC domain protein interacts with Tomato leaf curl virus replication accessory protein and enhances viral replication Plant Cell 17 311–325 Occurrence Handle15608335 Occurrence Handle1:CAS:528:DC%2BD2MXotlamsA%3D%3D Occurrence Handle10.1105/tpc.104.027235

    Article  PubMed  CAS  Google Scholar 

  • L.A. Selth J.W. Randles M.A. Rezaian (2004) ArticleTitleHost responses to transient expression of individual genes encoded by Tomato leaf curl virus Mol. Plant-Microbe Interact. 17 27–33 Occurrence Handle14714865 Occurrence Handle1:CAS:528:DC%2BD2cXivVSltr8%3D

    PubMed  CAS  Google Scholar 

  • Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876–4882.

    Google Scholar 

  • A. Turner B. Wells K. Roberts (1994) ArticleTitlePlasmodesmata of maize root tips: structure and composition J. Cell Sci. 107 3351–3361 Occurrence Handle7706391 Occurrence Handle1:CAS:528:DyaK2MXivFyrtrg%3D

    PubMed  CAS  Google Scholar 

  • M.H. Regenmortel Particlevan M.A. Mayo C.M. Fauquet J. Maniloff (2000) ArticleTitleVirus nomenclature: consensus versus chaos Arch. Virol. 145 2227–2232 Occurrence Handle11087105 Occurrence Handle10.1007/s007050070053

    Article  PubMed  Google Scholar 

  • F.A. Wald R. Kissen P. du Jardin S. Moreno (2003) ArticleTitleCharacterization of UDP-glucose protein transglucosylase genes from potato Plant Mol. Biol. 52 705–714 Occurrence Handle13677461 Occurrence Handle1:CAS:528:DC%2BD3sXmtVentLk%3D Occurrence Handle10.1023/A:1025061324856

    Article  PubMed  CAS  Google Scholar 

  • M. Whitford P. Faulkner (1992) ArticleTitleA structural polypeptide of the baculovirus Autographa californica nuclear polyhedrosis virus contains O-linked N-acetylglucosamine J. Virol. 66 3324–3329 Occurrence Handle1583718 Occurrence Handle1:CAS:528:DyaK38XltVKls7s%3D

    PubMed  CAS  Google Scholar 

  • J. Zhou Y.-T. Loh R.A. Bressan G.B. Martin (1995) ArticleTitleThe tomato gene Pti1 encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response Cell 83 925–935 Occurrence Handle8521516 Occurrence Handle1:CAS:528:DyaK2MXhtVSnu7bI Occurrence Handle10.1016/0092-8674(95)90208-2

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Horticulture Unit, CSIRO Plant Industry, P.O. Box 350, 5064, Glen Osmond, SA, Australia

    Luke A. Selth, Satish C. Dogra, M. Saif Rasheed & M. Ali Rezaian

  2. School of Agriculture and Wine, The University of Adelaide, 5005, Adelaide, SA, Australia

    Luke A. Selth, Satish C. Dogra, M. Saif Rasheed & John. W. Randles

  3. National Institute for Biotechnology and Genetic, Engineering (NIBGE), Jhang Road, P.O. Box 577, Faisalabad, Pakistan

    M. Saif Rasheed

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  1. Luke A. Selth
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  2. Satish C. Dogra
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  3. M. Saif Rasheed
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  5. M. Ali Rezaian
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Correspondence to M. Ali Rezaian.

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Selth, L.A., Dogra, S.C., Rasheed, M.S. et al. Identification and Characterization of a Host Reversibly Glycosylated Peptide that Interacts with the Tomato leaf curl virus V1 Protein. Plant Mol Biol 61, 297–310 (2006). https://doi.org/10.1007/s11103-006-0028-5

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