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Virome analysis of melon with yellowish symptoms reveals mixed infections of known and emerging viruses in Southern Italy

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  • Myeonghwan KWAK,
  • Cécile DESBIEZ,
  • Eui-Joon KIL,
  • Giuseppe PARRELLA
Myeonghwan KWAK
Department of Plant Medicals, Gyeongkuk National University, 36729 Andong, Republic of Korea
Cécile DESBIEZ
Institute for Agriculture, Food, and Environment (INRAe), Pathologie Végétale, F-84140, Montfavet, France
Eui-Joon KIL
Department of Plant Medicals, Gyeongkuk National University, 36729 Andong, Republic of Korea
Giuseppe PARRELLA
Institute for Sustainable Plant Protection, National Research Council (IPSP-CNR), 80055 Portici, Italy
DOI: https://doi.org/10.36253/phyto-16655
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Published 2025-12-11

Keywords

  • Cucumis melo,
  • whitefly-transmitted viruses,
  • HTS,
  • CCYV,
  • CmEV

How to Cite

[1]
M. KWAK, C. DESBIEZ, E.-J. KIL, and G. PARRELLA, “Virome analysis of melon with yellowish symptoms reveals mixed infections of known and emerging viruses in Southern Italy”, Phytopathol. Mediterr., pp. 585–596, Dec. 2025.

Copyright (c) 2025 Myeonghwan KWAK, Cécile DESBIEZ, Eui-Joon KIL, Giuseppe PARRELLA

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This work is licensed under a Creative Commons Attribution 4.0 International License.

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Abstract

New viruses and virus strains have emerged with increasing frequencies in cucurbit cropping systems, and surveillance for these pathogens requires effective techniques. Virus diversity was assessed in a melon leaf sample from one field in the Campania region of Southern Italy. Four viruses were identified in melon presenting yellowish symptoms, including: cucurbit chlorotic yellows virus (CCYV), cucumis melo endornavirus (CmEV), tomato leaf curl New Delhi virus (ToLCNDV), and cucurbit aphid-borne yellows virus (CABYV). De novo assemblies reconstructed near-complete genomes of these viruses, and using data available in GenBank, whole genome phylogenetic relationships were determined. Based on the HTS results, a virus survey was then carried out in the same melon field, using 108 symptomatic and non-symptomatic leaf samples and RT-PCR/PCR for specific virus detections. Results obtained confirmed presence of the four viruses, with incidences of 78% for CmEV, 78% for ToLCNDV, 69% for CCYV and 52% for CABYV in the field. Most samples had mixed infections, with from two to four viruses in individual samples. Multiple infections comprised 41% infected with CABYV + ToLCNDV + CCYV + CmEV, 28% with ToLCNDV + CCYV + CmEV, 9% with CABYV + ToLCNDV and 2 % of CMV+CABYV. ToLCNDV and CmEV were the most abundant virus detected. This record of CCYV and CmEV is the first for these two viruses in Italy, with CCYV detected with high incidence. CABYV also had high incidence compared to previous reports for this virus. Further research is required, including with other cucurbit hosts, to determine incidence of emerging virus complexes causing yellowing disease in melon.

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References

  1. Barba M., Czosnek H., Hadidi A., 2014. Historical perspective, development and applications of next-generation sequencing in plant virology. Viruses 6: 106–136. https://doi.org/10.3390/v6010106
  2. Bertin S., Luigi M., Parrella G., Giorgini M., Davino S., Tomassoli L., 2018. Survey of the distribution of Bemisia tabaci (Hemiptera: Aleyrodidae) in Lazio region (Central Italy): a threat for the northward expansion of tomato leaf curl New Delhi virus (Begomovirus: Geminiviridae) infection. Phytoparasitica 46: 171–182. https://doi.org/10.1007/s12600-018-0649-7
  3. Bertin S., Parrella G., Nannini M., Guercio G., Troiano E., Tomassoli L., 2021. Distribution and genetic variability of Bemisia tabaci cryptic species (Hemiptera: Aleyrodidae) in Italy. Insects 12: 521. https://doi.org/10.3390/ insects12060521
  4. Brown J.K., Zerbini F.M., Navas-Castillo J., Moriones E., Ramos-Sobrinho R., et al., 2015. Revision of Begomovirus taxonomy based on pairwise sequence comparisons. Archives of Virology 160: 1593–1619.
  5. Desbiez C., Troiano E., Kwak M., Kil E-J., Parrella G., 2023. Identification and characterization of the viruses responsible for recent epidemics on cucurbits in Southern Italy. 19th Plant Virology Conference, Aussois, France, P-17.
  6. EPPO, 2022. Cucurbit chlorotic yellows virus, an emerging virus of cucurbits spreading worldwide. EPPO Reporting Service no. 02 – 2022; Num. article: 2022/043.
  7. Gadhave K.R., Gautam S., Dutta B., Coolong T., Adkins S., Srinivasan R., 2020. Low frequency of horizontal and vertical transmission of cucurbit leaf crumple virus in whitefly Bemisia tabaci Gennadius. Phytopathology 110: 1235–1241. https://doi.org/10.1094/PHYTO-09-19-0337-R
  8. Gautam S., Gadhave K.R., Dutta B., Coolong T., Adkins S., Srinivasan R., 2020b. Virus-virus interactions in a plant host and in a hemipteran vector: implication for vector fitness and virus epidemics. Virus Research 286: 198069.
  9. Hall T.A., 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.
  10. Hasegawa M., Kishino H., and Yano T., 1985. Dating the human-ape split by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160–174.
  11. Janssen D., Simon A., Crespo O., Ruiz L., 2017. Genetic population structure of Bemisia tabaci in Spain associated with Tomato leaf curl New Delhi virus. Plant Protection Science 53: 25–31.
  12. Karasev A. V., 2000. Genetic diversity and evolution of closteroviruses. Annual Review of Phytopathology 38: 293–324.
  13. Kavalappara S.R., Milner H., Konakalla N.C., Morgan K., Sparks A.N., … Bag S., 2021. High Throughput Sequencing-aided survey reveals widespread mixed infections of whitefly-transmitted viruses in cucurbits in Georgia, USA. Viruses 13: 988. https://doi.org/10.3390/v13060988.
  14. Kumar S., Stecher G., Li M., Knyaz C., Tamura, K., 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35: 1547–1549. https://doi.org/10.1093/molbev/msy096
  15. ISTAT, 2024. Stima delle superfici e produzioni delle coltivazioni agrarie, floricole e delle piante intere da vaso. (http://dati.istat.it/index.aspx?queryid=33703#)
  16. La Tourrette K., Holste N.M., Garcia-Ruiz H., 2021. Polerovirus genomic variation. Virus Evolution 7, veab102. https://doi.org/10.1093/ve/veab102
  17. Lecoq H., Desbiez C., 2012. Viruses of cucurbit crops in the Mediterranean region: an ever-changing picture. Advances in Virus Research 84: 67–126.
  18. López‐Martín M., Sifres A., Gómez‐Guillamón M. L., Picó B., Pérez‐de‐Castro A., 2023. Incidence and genetic diversity of cucurbit viruses in the Spanish Mediterranean area. Plant Pathology 73: 431–443. https://doi.org/10.1111/ppa.13825
  19. Lu S.H., Chen M., Li J., Shi Y., Gu Q., Yan F., 2019. Changes in Bemisia tabaci feeding behaviors caused directly and indirectly by cucurbit chlorotic yellows virus. Virology Journal 16: 106. https://doi.org/10.1186/s12985-019-1215-8
  20. Lu S.H., Li J.J., Wang X.L., Song D.Y., Bai R.E., .. Yan F.M., 2017. A semipersistent plant virus differentially manipulates feeding behaviours of different sexes and biotypes of its whitefly vector. Viruses 9: 4.
  21. Luigi M., Bertin S., Manglli E., Troiano E., Davino S., Tomassoli L., Parrella G., 2019. First report of tomato leaf curl New Delhi virus causing yellow leaf curl of pepper in Europe. Plant Disease 103: 2970.
  22. Maachi A., Donaire L., Hernando Y., Aranda M.A., 2022. Genetic differentiation and migration fluxes of viruses from melon crops and crop edge weeds. Journal of Virology 96: e00421–e00422.
  23. Maina S., Donovan N.J., Plett K., Bogema D., Rodoni B.C., 2024. High-throughput sequencing for plant virology diagnostics and its potential in plant health certification. Frontiers in Horticulture 3: 1388028. https://doi.org/10.3389/fhort.2024.1388028
  24. Manglli A., Murenu M., Sitzia M., Tomassoli L., 2016. First report of Cucurbit yellow stunting disorder virus infecting cucurbits in Italy. New Disease Report 34: 23.
  25. Moriones E., Praveen S., Chakraborty S., 2017. Tomato leaf curl New Delhi virus: an emerging virus complex threatening vegetable and fiber crops. Viruses 9: 264. https://doi.org/10.3390/v9100264
  26. Muhire B.M., Varsani A., Martin D.P., 2014. SDT: A virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE 9: e108277. https://doi.org/10.1371/journal.pone.0108277
  27. Nei M., Kumar S., 2000. Molecular evolution and phylogenetics. Oxford University Press, New York.e.0108277 https://doi.org/10.1093/oso/9780195135848.001.0001
  28. Okuda M., Okazaki S., Yamasaki S., Okuda S., Sugiyama M., 2010. Host range and complete genome sequence of Cucurbit chlorotic yellows virus, a new member of the genus Crinivirus. Phytopathology 100: 560–566.
  29. Orfanidou C.G., Baltzi A., Dimou N.A., Katis N.I., Maliogka V.I., 2017. Cucurbit chlorotic yellows virus: insights into its natural host range, genetic variability, and transmission parameters. Plant Disease 101: 2053–2058. https://doi.org/10.1094/PDIS-02-17-0164-RE
  30. Orfanidou C., Katsiani A., Papayiannis L., Katis N.I., Maliogka V.I., 2021. Interplay of cucurbit yellow stunting disorder virus with cucurbit chlorotic yellows virus and transmission dynamics by Bemisia tabaci MED. Plant Disease 105: 416–424.
  31. Orílio A.F., Navas-Castillo J., 2009. The complete nucleotide sequence of the RNA2 of the crinivirus tomato infectious chlorosis virus: isolates from North America and Europe are essentially identical. Archives of Virology 154: 683–687. https://doi.org/10.1007/s00705-009-0354-4
  32. Panno S., Caruso A.G., Troiano E., Luigi M., Manglli A., .. Davino S., 2019. Emergence of tomato leaf curl New Delhi virus in Italy: estimation of incidence and genetic diversity. Plant Pathology 68: 601–608.
  33. Parrella G., Scassillo L., Giorgini M., 2012. Evidence for a new genetic variant in the Bemisia tabaci species complex and the prevalence of the biotype Q in southern Italy. Journal of Pest Science 85: 227–238. https://doi.org/10.1007/s10340-012-0417-2
  34. Parrella G., Nappo A.G., Manco E., Greco B., Giorgini M., 2014. Invasion of the Q2 mitochondrial variant of Mediterranean Bemisia tabaci in southern Italy: possible role of bacterial endosymbionts. Pest Managment Science 70: 1514–1523. https://doi.org/10.1002/ps.3686
  35. Parrella G., Troiano E., Formisano G., Accotto G.P., Giorgini M., 2018. First report of tomato leaf curl New Delhi virus associated with severe mosaic of pumpkin in Italy. Plant Disease 102: 459. https://doi.org/10.1094/PDIS-07-17-0940-PDN
  36. Parrella G., Troiano E., Lee S., Kil E.-J., 2020. Tomato leaf curl New Delhi virus found associated with eggplant yellowing disease in Italy. Plant Disease 104: 10.1094.
  37. Parrella G., Troiano E., Desbiez C., 2023. First report of pepo aphid-borne yellows virus on courgette in Italy. New Disease Report, 47: e12144. https://doi.org/10.1002/ndr2.12144
  38. Radouane N., Ezrari S., Belabess Z., Tahiri A., Tahzima R., … Lahlali R., 2021. Viruses of cucurbit crops: current status in the Mediterranean Region. Phytopathologia Mediterranea 60: 493–519. https://doi.org/10.36253/phy-to-12340
  39. Rubio L., Abou-Jawdah Y., Lin H.X., Falk BW., 2001. Geographically distant isolates of the crinivirus Cucurbit yellow stunting disorder virus show very low genetic diversity in the coat protein gene. Journal of General Virology 82: 929–933. https://doi.org/10.1099/0022-1317-82-4-929
  40. Sabanadzovic S., Wintermantel W.M., Valverde R.A., McCreight J.D., Aboughanem-Sabanadzovic N., 2016. Cucumis melo endornavirus: genome organization, host range and co-divergence with the host. Virus Research 214: 49–58. https://doi.org/10.1016/j.virusres.2016.01.001
  41. Tomassoli L., Lumia V., Siddu G.F., Barba M, 2003. Yellowing disease of melon in Sardinia (Italy) caused by Beet pseudoyellows virus. Journal of Plant Pathology 85: 59–61.
  42. Tomassoli L., Meneghini M., 2007. First report of Cucurbit aphid-borne yellows virus in Italy. Plant Pathology 56: 720.
  43. Troiano E., Parrella G., 2023. First report of tomato leaf curl New Delhi virus in Lagenaria siceraria var. longissima in Italy. Phytopathologia Mediterranea 62: 25–28. https://doi.org/10.36253/phyto-14147
  44. Utili D., 2023. Melone, aree e volumi in calo: le strategie per il futuro del comparto. Corriere Ortofrutticolo, 25 ottobre 2023. (http://www.corriereortofrutticolo.it)
  45. Vo T.T.B., Lal A., Ho, P.T., Troiano E., Parrella G., Kil E.-J., Lee S., 2022a. Different infectivity of Mediterranean and Southern Asian tomato leaf curl New Delhi virus isolates in cucurbit crops. Plants 11: 704. https://doi.org/10.3390/plants11050704
  46. Vo T.T.B., Troiano E., Lal A., Hoang P.T., Kil E.-J., Lee S., Parrella G., 2022b. ToLCNDV-ES infection in tomato is enhanced by TYLCV: evidence from field survey and agroinoculation. Frontiers in Microbiology 13: 954460. https://doi.org/10.3389/fmicb.2022.954460
  47. Vo T.T.B., Tabassum M., Nattanong B., Qureshi M.A., Im H.-J., Parrella G., Kil E—J., Lee S., 2025. The insidious threat: assessing the dangers and spread of tomato leaf curl New Delhi virus. Plant Pathology Journal 41: 1–16. https://doi.org/10.5423/PPJ.RW.11.2024.0177
  48. Wintermantel W.M., Cortez A.A., Anchieta A.G., Gulati-Sakhuja A., Hladky L.L., 2008. Co-infection by two criniviruses alters accumulation of each virus in a host-specific manner and influences efficiency of virus transmission. Phytopathology 98: 1340–1345. https://doi.org/10.1094/PHYTO-98-12-1340

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