Abstract
Watermelon mosaic virus (WMV; genus Potyvirus, family Potyviridae) is responsible for serious cucurbit yield losses worldwide. Different WMV genetic groups have been characterized so far. Among these, the “classical” (CL) group has been present in the Mediterranean basin for 40 years, whereas the “emergent” (EM) group includes isolates that are associated with more-severe symptoms observed since 2000. Information on the spatial and temporal evolution of WMV isolates in Italy is currently sparse. In this study, 39 WMV isolates samples collected in different regions over the last two decades were analysed at two different genomic regions that are known to be highly variable and contain recombination breakpoints. Most of the isolates collected between 2002 and 2009 were found to belong to the CL group, whereas the isolates from 2012 onwards were classified as EM, indicating that EM isolates have progressively displaced the CL population in Italy. Although genetic variability was observed within both CL and EM groups and recombinant isolates were detected, no positive selection or haplotype geographic structure were inferred. This suggest that the shift from CL to EM populations was likely due to multiple introductions of EM isolates in different regions of Italy rather than from genetic differentiation of local populations. The progressive increase in prevalence of the highly virulent EM populations is a serious concern because of their symptom severity, and the presence of multiple EM variants that include recombinants necessitates new efforts to develop durable control strategies.
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References
Lovisolo O, Lisa V (1983) Virosi e micoplasmosi delle cucurbitacee. In: Reda (ed) Le virosi delle piante ortive. Edizioni per l’agricoltura, pp 58–72
Lecoq H, Wisler G, Pitrat M (1998) Cucurbit viruses: the classics and the emerging. In: McCreight JD (ed) Cucurbitaceae '98: evaluation and enhancement of cucurbit germplasm. Pacific Grove, California, pp 126–142
Crescenzi A, Fanigliulo A, Comes S, Masenga V, Pacella R, Piazzolla P (2001) Necrosis of watermelon caused by watermelon mosaic virus. J Plant Pathol 83:227
Finetti-Sialer MM, Mascia T, Cillo F, Vovlas C, Gallitelli D (2012) Biological and molecular characterization of a recombinant isolate of Watermelon mosaic virus associated with a watermelon necrotic disease in Italy. Eur J Plant Pathol 132:317–322
Desbiez C, Costa C, Wipf-Scheibel C, Girard M, Lecoq H (2007) Serological and molecular variability of watermelon mosaic virus (genus Potyvirus). Arch Virol 152:775–781
Moreno IM, Malpica JM, Diaz-Pendon JA, Moriones E, Fraile A, Garcia-Arenal F (2004) Variability and genetic structure of the population of Watermelon mosaic virus infecting melon in Spain. Virology 318:451–460
Desbiez C, Lecoq H (2008) Evidence for multiple intraspecific recombinants in natural populations of Watermelon mosaic virus (WMV, Potyvirus). Arch Virol 153:1749–1754
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 141:201–208
Desbiez C, Joannon B, Wipf-Scheibel C, Chandeysson C, Lecoq H (2011) Recombination in natural populations of watermelon mosaic virus: new agronomic threat or damp squib? J Gen Virol 92:1939–1948
Joannon B, Lavigne C, Lecoq H, Desbiez C (2010) Barriers to gene flow between emerging populations of Watermelon mosaic virus in Southeastern France. Phytopathology 100:1373–1379
Juarez M, Legua P, Mengual CM, Kassem MA, Sempere RN, Gómez P, Truniger V, Aranda MA (2013) Relative incidence, spatial distribution and genetic diversity of cucurbit viruses in eastern Spain. Ann Appl Biol 162:362–370
Lecoq H, Fabre F, Joannon B, Wipf-Scheibel C, Chandeysson C, Schoeny A, Desbiez C (2011) Search for factors involved in the rapid shift in Watermelon mosaic virus (WMV) populations in South-eastern France. Virus Res 159:115–123
Fabre F, Chadoeuf J, Costa C, Lecoq H, Desbiez C (2010) Asymmetrical over-infection as a process of plant virus emergence. J Theor Biol 265:377–388
Kamberoglu MA, Desbiez C, Caliskan AF (2015) Characterization of an emerging isolate of Watermelon Mosaic Virus in Turkey. Int J Agric Biol 17:211–215
Trikulja 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. Disease Notes 98(12):1749
Desbiez C, Verdin E, Moury B, Lecoq H, Millot P, Wipf-Scheibel C, Mirzayeva S, Sultanova N, Balakishiyeva G, Mammadov A, Kheyr-Pour A, Huseynova I (2019) Prevalence and molecular diversity of the main viruses infecting cucurbit and solanaceous crops in Azerbaijan. Eur J Plant Pathol 153(2):359–369
Perotto MC, Zicca S, Manglli A, Celli MG, Conci VC, Tomassoli L (2013) Intraspecific variability of the coat protein of Watermelon mosaic virus. 46° Congresso Brasileiro de Fitopatologia Ouro Preto (Brasil), 20–25 October 2013
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol 1:vev003
Pamilo P, Bianchi NO (1993) Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. J Mol Evol 10:271–281
Weaver S, Shank SD, Spielman SJ, Li M, Muse SV, Kosakovsky Pond SL (2018) Datamonkey 2.0: a modern web application for characterizing selective and other evolutionary processes. Mol Biol Evol 35(3):773–777
Paradis E (2018) Analysis of haplotype networks: the randomized minimum spanning tree method. Methods Ecol Evol 9:1308–1317
Zhao L, Feng C, Hao X, Sou M, Zhang J, Wang Q, Wu Y (2014) Complete genomic sequence analyses of Watermelon Mosaic Virus isolates from China. J Plant Pathol 96(3):585–588
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 146:213–218
Lecoq H, Desbiez C (2012) Viruses 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 84: 67–126
Lecoq H, Desbiez C, Wipf-Scheibel C, Girard M (2003) Potential involvement of melon fruit in the long distance dissemination of cucurbit potyviruses. Plant Dis 87:955–959
Hajizadeh M, Bahrampour H, Abdollahzadeh J (2017) Genetic diversity and population structure of Watermelon mosaic virus. J Plant Dis Prot 124:601–610
García-Arenal F, Fraile A, Malpica JM (2001) Variability and genetic structure of plant virus populations. Annu Rev Phytopathol 39(1):157–186
Laney AG, Avanzato MV, Tzanetakis IE (2012) High incidence of seed transmission of Papaya ringspot virus and Watermelon mosaic virus, two viruses newly identified in Robinia pseudoacacia. Eur J Plant Pathol 134:227–230
Acknowledgements
The authors are grateful to Prof. Fernando García-Arenal (Centro de Biotecnología y Genómica de Plantas UPM-INIA, Campus de Montegancedo, Universidad Politécnica de Madrid, Spain) for his kind suggestions on sequence analysis. This work was supported by the project “EMERAMB, Emergent Viruses and Virus Vectors in Mediterranean Basin Crops”, which is funded through the ARIMNet2 2015 Call. ARIMNet2 (2014—2017) is an ERA-NET coordinated by INRA (France); it has received funding from the European Union’s Seventh Framework Programme for Research, Technological Development and Demonstration under Grant Agreement No. 618127.
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705_2020_4584_MOESM1_ESM.pdf
Fig. S1 Maximum-parsimony (MP) tree obtained using an 813-nt NIb/CP fragment of WMV isolates from Italy (in bold) and GenBank, for a total of 65 sequences. A sequence of the NIb/CP region of SMV was used as the outgroup. The bootstrap consensus tree inferred from 1000 replicates is represented, and the branches corresponding to partitions reproduced in less than 50% of the bootstrap replicates are collapsed. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test is shown next to the branches. (PDF 66 kb)
705_2020_4584_MOESM2_ESM.pdf
Fig. S2 Maximum-parsimony (MP) tree obtained using a 1371-nt HC-Pro fragment of 39 WMV isolates from Italy. A sequence of the HC-Pro region of SMV was used as the outgroup. The bootstrap consensus tree inferred from 1000 replicates is represented, and the branches corresponding to partitions reproduced in less than 50% of the bootstrap replicates are collapsed. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test is shown next to the branches. (PDF 48 kb)
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Fig. S3 A randomised minimum spanning tree (RMST) combined with multidimensional scaling (MDS) analysis (a), showing the relationships among WMV haplotype groups (1 to 7) and their geographic affiliations, visualized using a maximum-parsimony network (b) (PDF 110 kb)
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Bertin, S., Manglli, A., McLeish, M. et al. Genetic variability of watermelon mosaic virus isolates infecting cucurbit crops in Italy. Arch Virol 165, 937–946 (2020). https://doi.org/10.1007/s00705-020-04584-9
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DOI: https://doi.org/10.1007/s00705-020-04584-9