Journal of Plant Pathology

, Volume 101, Issue 4, pp 1143–1150 | Cite as

Genetic diversity and phylogenetic analyses of tomato chlorosis virus isolates using the coat protein gene sequences

  • Nevin Yeşilyurt
  • Bayram ÇevikEmail author
Short Communication


Since the first report of tomato chlorosis virus (ToCV) in 2008, yellowing symptoms were observed in major tomato production areas of Turkey. Therefore, surveys were conducted in Antalya, Burdur, Isparta and Muğla provinces where 329 symptomatic tomato samples were collected from greenhouses and open fields. Testing all samples by RT-PCR using primers specific for ToCV coat protein (CP) gene revealed that 113 of 329 tomato samples resulted in positive amplification of this virus. While ToCV was not detected in Isparta and Burdur, more than 50% of the samples collected from Antalya tested positive. The CP genes of 12 selected ToCV isolates from different areas were cloned, sequenced and compared with each other and the full-length CP genes of isolates from other countries. Genetic diversity and phylogenetic analysis showed that the Turkish ToCV isolates have low genetic diversity and they are closely related, clustering in the same phylogenetic group. On the other hand, the CP genes of ToCV isolates from different countries showed greater diversity than the Turkish isolates and were phylogenetically divided into three groups.


Tomato ToCV Genetic diversisty Phylogenetic analysis CP gene 



This study was supported by Suleyman Demirel University Scientific Research Project Coordination Unit (BAP) Project No: 2255-D-10.

Supplementary material

42161_2019_297_MOESM1_ESM.docx (324 kb)
ESM 1 (DOCX 324 kb)


  1. Abou-Jawdah Y, El Mohtar C, Atamian H, Sobh H (2006) First report of Tomato chlorosis virus in Lebanon. Plant Dis 90:378PubMedGoogle Scholar
  2. Accotto GP, Vaira AM, Vecchiati M (2001) First report of Tomato chlorosis virus in Italy. Plant Dis 85:1208PubMedGoogle Scholar
  3. Albuquerque LC, Villanueva F, Resende RO, Navas-Castillo J, Barbosa JC, Inoue-Nagata AK (2013) Molecular characterization reveals Brazilian Tomato chlorosis virus to be closely related to a Greek isolate. Trop Plant Pathol 38:332–336Google Scholar
  4. Anonymous (2013) PM 7/118 (1) Tomato chlorosis virus and tomato infectious chlorosis virus. OEPP/EPPO Bull 43:462–470Google Scholar
  5. Barbosa JC, Costa H, Gioria R, Rezende JAM (2011) Occurrence of Tomato chlorosis virus in tomato crops in five Brazilian states. Trop Plant Pathol 36:256–258Google Scholar
  6. Barbosa JC, Rezende JA, Armando-Filho B (2013) Low genetic diversity suggests a single introduction and recent spread of tomato chlorosis virus in Brazil. J Phytopathol 161:884–886Google Scholar
  7. Çevik B, Erkış G (2008) First report of Tomato chlorosis virus in Turkey. Plant Pathol 57:767Google Scholar
  8. Dalmon A, Bouyer S, Cailly M (2005) First report of Tomato chlorosis virus and Tomato infectious chlorosis virus in tomato crops in France. Plant Dis 89:1243PubMedGoogle Scholar
  9. Dolja VV, Kreuze JF, Valkonen JP (2006) Comparative and functional genomics of closteroviruses. Virus Res 117:38–51PubMedGoogle Scholar
  10. Dovas CI, Katis NI (2002) Multiplex detection of criniviruses associated with epidemics of a yellowing disease of tomato in Greece. Plant Dis 86:1345–1349PubMedGoogle Scholar
  11. Font MI, Juarez M, Martinez O, Jorda C (2004) Current status and newly discovered natural hosts of Tomato infectious chlorosis virus and Tomato chlorosis virus in Spain. Plant Dis 88:82PubMedGoogle Scholar
  12. Fortes IM, Navas-Castillo J (2012) Potato, an experimental and natural host of the crinivirus tomato chlorosis virus. Eur J Plant Pathol 134:81–86Google Scholar
  13. Freitas DMS, Nardin I, Shimoyama N, Rezende JAM (2012) First report of tomato chlorosis virus in potato in Brazil. Plant Dis 96:593PubMedGoogle Scholar
  14. Gharsallah C, Halima AB, Fakhfakh H, Gorsane F (2015) Insights into the genetic diversity and the phylogenetic analysis of Tunisian isolates of Tomato chlorosis virus. Phytoparasitica 43:87–96Google Scholar
  15. Hanssen IM, Lapidot M, Thomma BPHJ (2010) Emerging viral diseases of tomato crops. Mol Plant-Microbe Interact 23:539–548PubMedGoogle Scholar
  16. Hirota T, Natsuaki T, Murai T, Nishigawa H, Niibori K, Goto K, Hartono S, Suastika G, Okuda S (2010) Yellowing disease of tomato caused by Tomato chlorosis virus newly recognized in Japan. J Gen Plant Pathol 76:168–171Google Scholar
  17. Jacquemond M, Verdin E, Dalmon A, Guilbaud L, Gognalons P (2009) Serological and molecular detection of Tomato chlorosis virus and Tomato infectious chlorosis virus in tomato. Plant Pathol 58:210–220Google Scholar
  18. Karasev AV (2000) Genetic diversity and evolution of closteroviruses. Annu Rev Phytopathol 38:293–324PubMedGoogle Scholar
  19. Kataya AR, Stavridou E, Farhan K, Livieratos IC (2008) Nucleotide sequence analysis and detection of a Greek isolate of Tomato chlorosis virus. Plant Pathol 57:819–24Google Scholar
  20. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedPubMedCentralGoogle Scholar
  21. Lee YJ, Kil EJ, Kwak HR, Kim M, Seo JK, Lee S, Choi HS (2018) Phylogenetic characterization of tomato chlorosis virus population in Korea: evidence of Reassortment between isolates from different origins. Plant Pathol J 34(3):199–207PubMedPubMedCentralGoogle Scholar
  22. Lett JM, Hoareau M, Reynaud B, Saison A, Hostachy B, Lobin K, Benimadhu SP (2009) First report of Tomato chlorosis virus in tomato on Mauritius Island. Plant Dis 93:111PubMedGoogle Scholar
  23. Li R, Mock R, Huang Q, Abad J, Hartung J, Kinard G (2008) A reliable and inexpensive method of nucleic acid extraction for the PCR-based detection of diverse plant pathogens. J Virol Methods 154:48–55Google Scholar
  24. Louro D, Accotto GP, Vaira AM (2000) Occurrence and diagnosis of tomato chlorosis virus in Portugal. Eur J Plant Pathol 106:589–592Google Scholar
  25. Lozano G, Moriones E, Navas-Castillo J (2004) First report of sweet pepper (Capsicum annuum) as a natural host plant for Tomato chlorosis virus. Plant Dis 88:224PubMedGoogle Scholar
  26. Lozano G, Moriones E, Navas-Castillo J (2007) Complete sequence of the RNA1 of a European isolate of tomato chlorosis virus. Arch Virol 152:839–841PubMedGoogle Scholar
  27. Marco CF, Aranda MA (2005) Genetic diversity of a natural population of cucurbit yellow stunting disorder virus. J Gen Virol 86:815–822PubMedGoogle Scholar
  28. Navas-Castillo J, Camero R, Bueno M, Moriones E (2000) Severe outbreaks in tomato in Spain associated with infections of tomato chlorosis virus. Plant Dis 84:835–837PubMedGoogle Scholar
  29. Nei M, Kumar S (2000) Molecular evolution and Phylogenetics. Oxford University Press, OxfordGoogle Scholar
  30. Orfanidou CG, Dimitriou C, Papayiannis LC, Maliogka VI, Katis NI (2014) Epidemiology and genetic diversity of criniviruses associated with tomato yellows disease in Greece. Virus Res 186:120–129PubMedGoogle Scholar
  31. Orilio AF, Fortes I M Navas-Castillo J (2014) Infectious cDNA clones of the crinivirus Tomato chlorosis virus are competent for systemic plant infection and whitefly-transmission. Virology 464–465C:365–374 PubMedGoogle Scholar
  32. Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  33. Papayiannis LC, Ioannou N, Dovas CI, Maliogka VI, Katis NI (2006) First report of Tomato chlorosis virus (ToCV) on tomato crops in Cyprus. Plant Pathol 55:567Google Scholar
  34. Rubio L, Ayllón MA, Kong P, Fernández A, Polek M, Guerri J, Moreno P, Falk BW (2001a) Genetic variation of Citrus tristeza virus isolates from California and Spain: evidence for mixed infections and recombination. J Virol 75:8054–8062PubMedPubMedCentralGoogle Scholar
  35. Rubio L, Abou-Jawdah Y, Lin HX, Falk BW (2001b) Geographically distant isolates of the crinivirus cucurbit yellow stunting disorder virus show very low genetic diversity in the coat protein gene. J Gen Virol 82:929–933PubMedGoogle Scholar
  36. Segev L, Polston JE, Lapidot M (2004) First report of Tomato chlorosis virus in Israel. Plant Dis 88:160Google Scholar
  37. Solórzano-Morales A, Barboza N, Hernández E, Mora-Umaña F, Ramirez P, Hammond RW (2011) Newly discovered natural hosts of Tomato chlorosis virus in Costa Rica. Plant Dis 95:497PubMedGoogle Scholar
  38. Tairo F, Mukasa SB, Jones RA, Kullaya A, Rubaihayo PR, Valkonen JPT (2005) Unravelling the genetic diversity of the three main viruses involved in sweet potato virus disease (SPVD), and its practical implications. Mol Plant Pathol 6:199–211PubMedGoogle Scholar
  39. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729PubMedPubMedCentralGoogle Scholar
  40. Velasco L, Simon B, Janssen D, Cenis JL (2008) Incidences and progression of Tomato chlorosis virus disease and Tomato yellow leaf curl virus disease in tomato under different greenhouse covers in Southeast Spain. Ann Appl Biol 153:335–344Google Scholar
  41. Wintermantel WM, Wisler GC (2006) Vector specificity, host range, and genetic diversity of tomato chlorosis virus. Plant Dis 90:814–819PubMedGoogle Scholar
  42. Wintermantel WM, Polston JE, Escudero J, Paoli ER (2001) First report of Tomato chlorosis virus in Puerto Rico. Plant Dis 85:228PubMedGoogle Scholar
  43. Wintermantel WM, Wisler GC, Anchieta AG, Liu HY, Karasev AV, Tzanetakis IE (2005) The complete nucleotide sequence and genome organization of tomato chlorosis virus. Arch Virol 150:2287–2298PubMedGoogle Scholar
  44. Wisler GC, Duffus JE, Liu HY, Li RH (1998a) Ecology and epidemiology of whitefly-transmitted closteroviruses. Plant Dis 82:270–280PubMedGoogle Scholar
  45. Wisler GC, Li RH, Liu HY, Lowry DS, Duffus JE (1998b) Tomato chlorosis virus: a new whitefly-transmitted, phloem-limited, bipartite closterovirus of tomato. Phytopathology 88:402–409PubMedGoogle Scholar
  46. Zhao RN, Wang R, Wang N, Fan ZF, Zhou T, Shi YC, Chai M (2013) First report of tomato chlorosis virus in China. Plant Dis 97(8):1123–1123PubMedGoogle Scholar

Copyright information

© Società Italiana di Patologia Vegetale (S.I.Pa.V.) 2019

Authors and Affiliations

  1. 1.Faculty of Agriculture, Department of Plant ProtectionSüleyman Demirel UniversityIspartaTurkey
  2. 2.Faculty of Education, Department of Mathematic and ScienceHakkari UniversityHakkariTurkey
  3. 3.Faculty of Agricultural Sciences and Technologies, Department of Plant ProtectionIsparta University of Applied SciencesIspartaTurkey

Personalised recommendations