Journal of Plant Pathology

, Volume 101, Issue 4, pp 1067–1075 | Cite as

Molecular diversity of main cucurbit viruses in Syria

  • Mohamad Chikh-AliEmail author
  • Tomohide Natsuaki
  • Alexander V. Karasev
Original Article


Cucurbits are among the main crops and vegetables grown in Syria, including cucumber (Cucumis sativus), melon (C. melo), watermelon (Citrullus lanatus), and various squash species (Cucurbita pepo, C. moschata, and C. maxima). Cucurbit virus diseases are responsible for significant yield and quality losses to cucurbit crops. In the current study, we investigated the etiology of cucurbit virus diseases, and assessed the molecular diversity of the causal viruses in three major regions of cucurbit production of Syria. Out of 12 viruses and virus groups investigated, zucchini yellow mosaic virus (ZYMV), watermelon mosaic virus (WMV),cucumber mosaic virus (CMV), cucurbit aphid-borne yellows virus (CABYV) and a new member of the genus Polerovirus, pepo aphid-borne yellows virus (PABYV) were detected in various cucurbit crops from plants displaying virus-like symptoms. Syrian ZYMV isolates were closely related and shared low diversity suggesting a relatively recent introduction. A diverse population of WMV with four classical and two emerging isolates of WMV were identified, which complicates the control program. Two CMV isolates were closely related to CMV isolates, reported previously from other crops in the same regions, which may indicate frequent movements of CMV among different hosts. The finding of an isolate of PABYV, a newly described species of the genus Polerovirus, reveals a wider distribution of this virus that may represent a potential emerging problem to cucurbit production.


ZYMV PABYV Emerging viruses WMV CABYV CMV 



This research was partially funded by the Japan Society for the Promotion of Science (JSPS) who granted a postdoctoral fellowship to the first author from 2009 to 2011.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Research involving human participants and/or animals

This manuscript does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Not applicable.


  1. Abou-Jawdah Y, Sobh H, El-Zammar S, Fayyad A, Lecoq H (2000) Incidence and management of virus diseases of cucurbits in Lebanon. Crop Prot 19:217–224Google Scholar
  2. Ali A, Kobayashi M (2010) Seed transmission of cucumber mosaic virus in pepper. J Virol Methods 163:234–237PubMedGoogle Scholar
  3. Cèlia GA, Antonio JM, Montserrat S, Ronan XC, Jordi GM, Ana MH (2014) The complex resistance to cucumber mosaic cucumovirus (CMV) in the melon accession PI161375 is governed by one gene and at least two quantitative trait loci. Mol Breed 34:351–362Google Scholar
  4. Chikh Ali M, Maoka T, Natsuaki KT (2007) The occurrence and characterization of new recombinant isolates of PVY displaying shared properties of PVYNW and PVYNTN. J Phytopathol 155:409–415Google Scholar
  5. Chikh Ali M, Maoka T, Natsuaki KT (2008) The occurrence of potato viruses in Syria and the molecular detection and characterization of Syrian potato virus S isolates. Potato Res 51:151–161Google Scholar
  6. Chikh Ali M, Maoka T, Natsuaki KT (2009) Biological and molecular characterization of two zucchini yellow mosaic virus isolates from Syria. EPPO Bulletin 39:99–104Google Scholar
  7. Chikh Ali M, Maoka T, Said Omar AM, Natsuaki KT, Natsuaki T (2012) Characterization of potato and tobacco isolates of cucumber mosaic virus from Syria and the first report on CMV satellite RNA from potato. Phytopathol Mediterr 51:3–10Google Scholar
  8. Choi SK, Choi JK, Park WM, Ryu KH (1999) RT-PCR detection and identification of three species of cucumoviruses with a genus-specific single pair of primers. J Virol Methods 83:67–73PubMedGoogle Scholar
  9. Corrêa RL, Silva TF, Simões-Araújo JL, Barroso PAV, Vidal MS, Vaslin MFS (2005) Molecular characterization of a virus from the family Luteoviridae associated with cotton blue disease. Arch Virol 150:1357–1367PubMedGoogle Scholar
  10. Desbiez C, Wipf-Scheibel C, Lecoq H (2002) Biological and serological variability, evolution and molecular epidemiology of zucchini yellow mosaic virus (ZYMV, Potyvirus) with special reference to Caribbean islands. Virus Res 85:5–16PubMedGoogle Scholar
  11. Desbiez C, Joannon B, Wipf-Scheibel C, Chandeysson C, Lecoq H (2009) Emergence of new strains of watermelon mosaic virus in south-eastern France: evidence for limited spread but rapid local population shift. Virus Res 141:201–208PubMedGoogle Scholar
  12. Dovas CI, Efthimiou K, Katis NI (2004) Generic detection and differentiation of tobamoviruses by a spot nested RT-PCR-RFLP using dI-containing primers along with homologous dG-containing primers. J Virol Methods 117:137–144PubMedGoogle Scholar
  13. Fujiie A, Omar AS, Sawas AB, Abbas A, Abdul Hadi M, Sawas E, Barakat A, Naser M, Takahashi S (2008) Survey of aphid infestation and viral infection of potatoes in Syria. J ISSAAS 14:46–59Google Scholar
  14. Gibbs MJ, Armstrong JS, Gibbs AJ (2000) Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582PubMedPubMedCentralGoogle Scholar
  15. Haj Kassem AA, Abdul Halim K, Rifai OEG, Warrak W (2005) The most important of viruses affecting cucurbits in Syria. Arab J Plant Protect 23:1–6Google Scholar
  16. Ibaba JD, Laing MD, Gubba A (2015) Incidence and phylogeny of viruses infecting cucurbit crops in KwaZulu-Natal, Republic of South Africa. Crop Prot 75:46–54Google Scholar
  17. Ibaba JD, Laing MD, Gubba A (2017) Pepo aphid-borne yellows virus: a new species in the genus Polerovirus. Virus Genes 53:134–136PubMedGoogle Scholar
  18. Kamberoglu MA, Desbiez C, Caliskan AF (2015) Characterization of an emerging isolate of watermelon mosaic virus in Turkey. Int J Agric Biol 17:211–215Google Scholar
  19. Knierim D, Tsai WS, Maiss E, Kenyon L (2014) Molecular diversity of poleroviruses infecting cucurbit crops in four countries reveals the presence of members of six distinct species. Arch Virol 159:1459–1465PubMedGoogle Scholar
  20. Kone N, Coulibaly A, Koita O, Kone D, Bediako EA, Knierim D, Menzel W, Winter S (2015) First report of Pepo aphid-borne yellows virus on zucchini in cote d'Ivoire. New Disease Reports 31:27Google Scholar
  21. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874Google Scholar
  22. Lecoq H, Desbiez C (2012) Virus of cucurbit crops in the Mediterranean region: an ever-changing picture. In: Loebenstein G, Lecoq H (eds) Viruses and virus diseases of vegetables in the Mediterranean Basin. Adv. Virus res, vol 84. Elsevier, USA, pp 67–126Google Scholar
  23. Lecoq H, Katis N (2014) Control of cucurbit viruses. Adv Virus Res 90:255–296PubMedGoogle Scholar
  24. Lotos L, Efthimiou K, Maliogka VI, Katis NI (2014) Generic detection of poleroviruses using an RT-PCR assay targeting the RdRp coding sequence. J Virol Methods 198:1–11PubMedGoogle Scholar
  25. Lotos L, Maliogka VI, Katis NI (2016) New poleroviruses associated with yellowing symptoms in different vegetable crops in Greece. Arch Virol 161:431–436PubMedGoogle Scholar
  26. Martin DP, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563PubMedPubMedCentralGoogle Scholar
  27. Mnari-Hattab M, Gauthier N, Zouba A (2009) Biological and molecular characterization of the cucurbit aphid-borne yellows virus affecting cucurbits in Tunisia. Plant Dis 93:1065–1072PubMedGoogle Scholar
  28. Moreno IM, Malpica JM, JA D-P’n, Moriones E, Fraile A, Garcia-Arenal F (2004) Variability and genetic structure of the population of watermelon mosaic virus infecting melon in Spain. Virol 318:451–460Google Scholar
  29. O’Keefe DC, Berryman DI, Coutts BA, Jones RAC (2007) Lack of seed coat contamination with cucumber mosaic virus in lupin permits reliable, large-scale detection of seed transmission in seed samples. Plant Dis 91:504–508PubMedGoogle Scholar
  30. Padidam M, Sawyer S, Fauquet CM (1999) Possible emergence of new geminiviruses by frequent recombination. Virology. 265:218–225PubMedGoogle Scholar
  31. Papayiannis LC, Ioannou N, Boubourakas IN, Dovas CI, Katis NI, Falk BW (2005) Incidence of viruses infecting cucurbits in Cyprus. J Phytopathol 153:530–535Google Scholar
  32. Perotto MC, Celli MG, Pozzi EA, Luciani CE, Conci VC (2016) Occurrence and characterization of a severe isolate of watermelon mosaic virus from Argentina. Eur J Plant Pathol 146:213–218Google Scholar
  33. Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 98:13757–13762PubMedPubMedCentralGoogle Scholar
  34. Romay G, Lecoq H, Geraud-Pouey F, Chirinos DT, Desbiez C (2014) Current status of cucurbit viruses in Venezuela and characterization of Venezuelan isolates of Zucchini yellow mosaic virus. Plant Pathol 63:78–87Google Scholar
  35. Roossinck MJ (2002) Evolutionary history of cucumber mosaic virus deduced by phylogenetic analyses. J Virol 76:3382–3387PubMedPubMedCentralGoogle Scholar
  36. Salminen MO, Carr JK, Burke DS, McCutchan FE (1995) Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res Hum Retrovir 11:1423–1425PubMedGoogle Scholar
  37. Shang QX, Xiang HY, Han CG, Li DW, Yu JL (2009) Distribution and molecular diversity of three cucurbit-infecting poleroviruses in China. Virus Res 145:341–346PubMedGoogle Scholar
  38. Simmons HE, Dunham JP, Zinn KE, Munkvold GP, Holmes EC, Stephenson AG (2013) Zucchini yellow mosaic virus (ZYMV, Potyvirus): vertical transmission, seed infection and cryptic infections. Virus Res 176:259–264PubMedPubMedCentralGoogle Scholar
  39. Smith JM (1992) Analyzing the mosaic structure of genes. J Mol Evol 34:126–129PubMedPubMedCentralGoogle Scholar
  40. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA: molecular evolutionary genetics analysis software version 4. Mol Biol Evol 24:1596–1599PubMedGoogle Scholar
  41. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple-sequence alignment aided by quality analysis tools. Nucleic Acids Res 22:4673–4680Google Scholar
  42. Trkulja V, Vasić J, Vuković B, Stanković I, Vučurović A, Bulajić A, Krstić B (2014) First report of watermelon mosaic virus infecting melon and watermelon in Bosnia and Herzegovina. Plant Dis 98:1749PubMedGoogle Scholar
  43. Wintermantel WM, Hladky LL (2010) Methods for detection and differentiation of existing and new crinivirus species through multiplex and degenerate primer RT-PCR. J Virol Methods 170:106–114PubMedGoogle Scholar
  44. Yakoubi S, Desbiez C, Fakhfakh H, Wipf-Scheibel C, Fabre F, Pitrat M, Marrakchi M, Lecoq H (2008) Molecular, biological and serological variability of zucchini yellow mosaic virus in Tunisia. Plant Pathol 57:1146–1154Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Entomology, Plant Pathology and NematologyUniversity of IdahoMoscowUSA
  2. 2.Laboratory of Plant Pathology, School of AgricultureUtsunomiya UniversityTochigiJapan
  3. 3.Bioinformatics and Computational Biology ProgramUniversity of IdahoMoscowUSA

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