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Zucchini tigré mosaic virus is a distinct potyvirus in the papaya ringspot virus cluster: molecular and biological insights

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Abstract

In recent years, three new potyviruses have been described in the papaya ringspot virus (PRSV) cluster. In addition, two types of PRSV are recognized, type W, infecting cucurbit plants, and type P, infecting papaya and also cucurbits. A third type, PRSV-T, was also partially described in Guadeloupe. Complete genome sequencing of four PRSV-T isolates showed that this virus is a related virus that is distinct from PRSV, and the name zucchini tigré mosaic virus (ZTMV) is proposed, in reference to the typical symptoms observed in zucchini squash. Eleven other viral isolates from different geographic origins were confirmed as ZTMV isolates using the complete sequence of the cylindrical inclusion (CI) coding region, whereas pairwise sequence similarities in the coat protein (CP) coding region did not unambiguously distinguish ZTMV isolates from PRSV isolates. The use of the CI coding region for species demarcation appears more suitable than the CP coding region for closely related viruses. Principal coordinates analysis based on the biological behavior of the viral isolates studied clustered PRSV-P, PRSV-W and ZTMV isolates into three different groups. Therefore, ZTMV is different from PRSV in its molecular and biological properties.

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References

  1. Adams MJ, Antoniw JF, Beaudoin F (2005) Overview and analysis of the polyprotein cleavage sites in the family Potyviridae. Mol Plant Pathol 6:471–487

    Article  CAS  PubMed  Google Scholar 

  2. Adams MJ, Antoniw JF, Fauquet C (2005) Molecular criteria for genus and species discrimination within the family Potyviridae. Arch Virol 150:459–479

    Article  CAS  PubMed  Google Scholar 

  3. Adams MJ, Carstens EB (2012) Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2012). Arch Virol 157:1411–1422

    Article  CAS  PubMed  Google Scholar 

  4. Adams MJ, Zerbini FM, French R, Rabenstein F, Stenger DC, Valkonen JPT (2012) Potyviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, London, pp 1069–1089

    Google Scholar 

  5. Ali A, Natsuaki T, Okuda S (2004) Identification and molecular characterization of viruses infecting cucurbits in Pakistan. J Phytopathol 152:677–682

    Article  CAS  Google Scholar 

  6. Arocha Y, Vigheri N, Nkoy-Florent B, Bakwanamaha K, Bolomphety B, Kasongo M, Betts P, Monger WA, Harju V, Mumford RA, Jones P (2008) First report of the identification of Moroccan watermelon mosaic virus in papaya in Democratic Republic of Congo (DRC). Plant Pathol 57:387

    Article  Google Scholar 

  7. Atreya PL, Atreya CD, Pirone TP (1991) Amino acid substitutions in the coat protein result in loss of insect transmissibility of a plant virus. Proc Natl Acad Sci USA 88:7887–7891

    Article  CAS  PubMed  Google Scholar 

  8. Baker CA, Lecoq H, Purcifull DE (1991) Serological and biological variability among papaya ringspot virus type W isolates in Florida. Phytopathology 81:722–728

    Article  Google Scholar 

  9. Bateson MF, Lines RE, Revill P, Chaleeprom W, Ha CV, Gibbs AJ, Dale JL (2002) On the evolution and molecular epidemiology of the potyvirus Papaya ringspot virus. J Gen Virol 83:2575–2585

    CAS  PubMed  Google Scholar 

  10. Bejerman N, Guiolitti F, de Breuil S, Lenardon S (2010) Molecular characterization of Sunflower chlorotic mottle virus: a member of a distinct species in the genus Potyvirus. Arch Virol 155:1331–1335

    Article  CAS  PubMed  Google Scholar 

  11. Blanc S, Ammar E-D, Garcia-Lampasona S, Dolja VV, Llave C, Baker J, Pirone TP (1998) Mutations in the potyvirus helper component protein: effects on interactions with virions and aphid stylets. J Gen Virol 79:3119–3122

    CAS  PubMed  Google Scholar 

  12. Bohn GW, Kishaba AN, McCreight JD (1980) WMR29 muskmelon breeding line. HortScience 15:539–540

    Google Scholar 

  13. Carstens EB (2012) Introduction to Virus Taxonomy. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, London, pp 3–7

    Google Scholar 

  14. Chen J, Chen J, Adams MJ (2002) Characterization of potyviruses from sugarcane and maize in China. Arch Virol 147:1237–1246

    Article  CAS  PubMed  Google Scholar 

  15. Chen KC, Chiang CH, Raja JA, Liu FL, Tai CH, Yeh S-D (2008) A single amino acid of NIaPro of Papaya ringspot virus determines host specificity for infection of papaya. Mol Plant Microbe Interact 21:1046–1057

    Article  CAS  PubMed  Google Scholar 

  16. Clark MF, Adams AN (1977) Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. J Gen Virol 34:475–483

    Article  CAS  PubMed  Google Scholar 

  17. Colinet D, Kummert J, Lepoivre P (1998) The nucleotide sequence and genome organization of the whitefly transmitted sweetpotato mild mottle virus: a close relationship with members of the family Potyviridae. Virus Res 53:187–196

    Article  CAS  PubMed  Google Scholar 

  18. Desbiez C, Justafre I, Lecoq H (2007) Molecular evidence that zucchini yellow fleck virus is a distinct and variable potyvirus related to papaya ringspot virus and Moroccan watermelon mosaic virus. Arch Virol 152:449–455

    Article  CAS  PubMed  Google Scholar 

  19. Desbiez C, Girard M, Wipf-Scheibel C, Lecoq H (2010) A novel natural mutation in HC-Pro responsible for mild symptomatology of Zucchini yellow mosaic virus (ZYMV, Potyvirus) in cucurbits. Arch Virol 155:397–401

    Article  CAS  PubMed  Google Scholar 

  20. Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2011) InfoStat versión 2011. InfoStat Group, College of Agricultural Sciences, National University of Cordoba, Argentina. http://www.infostat.com.ar

  21. Fernandez-Rodriguez T, Rubio L, Carballo O, Marys E (2008) Genetic variation of papaya ringspot virus in Venezuela. Arch Virol 153:343–349

    Article  CAS  PubMed  Google Scholar 

  22. Gal-On A, Raccah B (2000) A point mutation in the FRNK motif of the potyvirus helper component-protease gene alters symptom expression in cucurbits and elicits protection against the severe homologous virus. Phytopathology 90:467–473

    Article  CAS  PubMed  Google Scholar 

  23. Gibbs A, Mackenzie A (1997) A primer pair for amplifying part of the genome of all potyvirids by RT-PCR. J Virol Methods 63:9–16

    Article  CAS  PubMed  Google Scholar 

  24. Gonsalves D (1998) Control of papaya ringspot virus in papaya: a case study. Ann Rev Phytopathol 36:415–437

    Article  CAS  Google Scholar 

  25. Ha C, Coombs S, Revill PA, Harding RM, Vu M, Dale JL (2008) Design and application of two novel degenerate primer pairs for the detection and complete genomic characterization of potyviruses. Arch Virol 153:25–36

    Article  CAS  PubMed  Google Scholar 

  26. Huet H, Gal-On A, Meir E, Lecoq H, Raccah B (1994) Mutations in the helper component protease gene of zucchini yellow mosaic virus affect its ability to mediate aphid transmissibility. J Gen Virol 75:1407–1414

    Article  CAS  PubMed  Google Scholar 

  27. Inoue-Nagata AK, de Mello Franco C, Martin DP, Marques Rezende JA, Ferreira GB, Dutra LS, Nagata T (2007) Genome analysis of a severe and mild isolate of Papaya ringspot virus-type W found in Brazil. Virus Genes 35:119–127

    Article  CAS  PubMed  Google Scholar 

  28. Janzac B, Fabre M-F, Palloix A, Moury B (2009) Phenotype and spectrum of action of the Pvr4 resistance in pepper against potyviruses, and selection for virulent variants. Plant Pathol 58:443–449

    Article  CAS  Google Scholar 

  29. Lecoq H, Lot H, Pitrat M (1982) First identification of Watermelon mosaic virus type-1 (WMV-1) in Southeastern France. Agronomie 2:787

    Google Scholar 

  30. Lecoq H, Desbiez C (2012) Viruses of cucurbit crops in the mediterranean region: an ever-changing picture. Adv Virus Res 84:67–126

    Article  PubMed  Google Scholar 

  31. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC (1999) Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73:152–160

    CAS  PubMed Central  PubMed  Google Scholar 

  32. Mansilla PJ, Moreira AG, Mello APOA, Rezende JAM, Ventura JA, Yuki VA, Levatti FJ (2013) Importance of cucurbits in the epidemiology of Papaya ringspot virus type P. Plant Pathol 62:571–577

    Article  Google Scholar 

  33. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463

    Article  CAS  PubMed  Google Scholar 

  34. Olarte-Castillo XA, Fermin G, Tabima J, Rojas Y, Tennant PF, Fuchs M, Sierra R, Bernala AJ, Restrepoa S (2011) Phylogeography and molecular epidemiology of Papaya ringspot virus. Virus Res 159:132–140

    Article  CAS  PubMed  Google Scholar 

  35. Pitrat M, Lecoq H (1983) Two alleles for watermelon mosaic virus 1 resistance in melon. Cucurbit Genetic Coop Annual Report 6:52–53

    Google Scholar 

  36. Purcifull DE, Edwardson JR, Hiebert E, Gonsalves D (1984) Papaya ringspot virus. CMI/AAB Description of plant viruses, p 292

  37. Quiot-Douine L, Purcifull DE, Hiebert E, De Meija MVG (1986) Serological relationships and in vitro translation of an antigenically distinct strain of papaya ringspot virus. Phytopathology 76:346–351

    Article  Google Scholar 

  38. Quiot-Douine L, Quiot J-B, Labonne G (1986) Description préliminaire d’un potyvirus isolé de courgette (Cucurbita pepo L.) en Guadeloupe. Agronomie 6:227–233

    Article  Google Scholar 

  39. Quiot-Douine L, Lecoq H, Quiot J-B, Pitrat M, Labonne G (1990) Serological and biological variability of virus isolates related to strains of papaya ringspot virus. Phytopathology 80:256–263

    Article  Google Scholar 

  40. Romay G, Lecoq H, Geraud-Pouey F, Chirinos DT, Desbiez C (2013) Current status of cucurbit viruses in Venezuela and characterization of Venezuelan isolates of Zucchini yellow mosaic virus. Plant Pathol. doi:10.1111/ppa.12072

    Google Scholar 

  41. Shukla DD, Ward CW (1989) Identification and classification of potyviruses on the basis of coat protein sequence data and serology. Arch Virol 106:171–200

    Article  CAS  PubMed  Google Scholar 

  42. Spetz C, Taboada AM, Darwich S, Ramsell J, Salazar LF, Valkonen JPT (2003) Molecular resolution of a complex of potyviruses infecting solanaceous crops at the centre of origin in Peru. J Gen Virol 84:2565–2578

    Article  CAS  PubMed  Google Scholar 

  43. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  Google Scholar 

  44. Xia X (2000) Data analysis in molecular biology and evolution. Kluwer Academic Publishers, Boston/Dordrecht/London

    Google Scholar 

  45. Yakoubi S, Desbiez C, Fakhfakh H, Wipf-Scheibel C, Marrakchi M, Lecoq H (2008) Biological characterization and complete nucleotide sequence of a Tunisian isolate of Moroccan watermelon mosaic virus. Arch Virol 153:775–781

    Article  Google Scholar 

  46. Yakoubi S, Lecoq H, Desbiez C (2008) Algerian watermelon mosaic virus (AWMV): a new potyvirus species in the PRSV cluster. Virus Genes 37:103–109

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Prof. Dan Purcifull and Dr. Carlye Barker for kindly providing reference isolate Q10 of ZTMV. We thank Dr. Michel Pitrat, INRA-Avignon, for kindly providing melon accession seeds for biological tests. This work was partially supported by the cooperation agreement between the Venezuelan Foundation Fundayacucho and the Embassy of France in Venezuela, with a scholarship to GR.

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Correspondence to C. Desbiez.

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705_2013_1798_MOESM1_ESM.docx

Supplementary material 1 (DOCX 14 kb) Supplementary Table S1. Host and geographic origins of viral isolates analyzed in this study

705_2013_1798_MOESM2_ESM.docx

Supplementary material 2 (DOCX 16 kb) Supplementary Table S2. Primers used for amplification and sequencing of ZTMV and PRSV

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Romay, G., Lecoq, H. & Desbiez, C. Zucchini tigré mosaic virus is a distinct potyvirus in the papaya ringspot virus cluster: molecular and biological insights. Arch Virol 159, 277–289 (2014). https://doi.org/10.1007/s00705-013-1798-0

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