Abstract
Cucurbit viruses have been associated with important economic losses in Xinjiang of China. Therefore, a comprehensive survey and sample collection was performed during the 2013 and 2014 growing seasons from the major melon-growing locations in Xinjiang which is the largest area for melon production in China. Samples were analyzed using reverse transcription-polymerase chain reaction (RT-PCR) to detect Watermelon mosaic virus (WMV), Zucchini yellow mosaic virus (ZYMV), Cucumber mosaic virus (CMV), Papaya ringspot virus (PRSV), Squash mosaic virus (SqMV), Tomato ringspot virus (ToRSV), Moroccan watermelon mosaic virus (MWMV), Tomato spotted wilt virus (TSWV), Watermelon silver mottle virus (WSMoV), Cucumber green mottle mosaic virus (CGMMV), and Zucchini yellow fleck virus (ZYFV). We collected 492 melon samples with virus-like symptoms. Out of these, 94.5 % of the samples were infected by at least one of these viruses. WMV was the most prevalent virus detected. WMV, CMV, and ZYMV were detected in 77.0 %, 60.0 %, and 41.1 % of infected samples, respectively, and the infection rate of these three viruses changed significantly among melon cultivars. Other viruses analysed were not detected in any sample tested. The number of multiple infections was high (average 57.2 %), with the most common double infection WMV + CMV (17.8 %), closely followed by WMV + ZYMV (14.4 %). Statistical analysis of the potential association among viruses showed that there was a strong association between several viruses for multiple infections. An analysis of WMV genetic diversity suggested that all isolates obtained in this study clustered into group A and that purifying selection was restricting variability in the population.
Similar content being viewed by others
References
Ali, A., Natsuaki, T., & Okuda, S. (2004). Identification and molecular characterization of viruses infecting cucurbits in Pakistan. Journal of Phytopathology, 152, 677–682.
Ali, A., Mohammad, O., & Khattab, A. (2012). Distribution of viruses infecting cucurbit crops and isolation of potential new virus-like sequences from weeds in Oklahoma. Plant Disease, 96, 243–248.
Atreya, C. D., Raccah, B., & Pirone, T. P. (1990). A point mutation in the coat protein abolishes aphid transmissibility of a potyvirus. Virology, 178, 161–165.
Bananej, K., & Vahdat, A. (2008). Identification, distribution and incidence of viruses in field-grown cucurbit crops of Iran. Phytopathologia Meditterranea, 47, 247–257.
Chu, F. H., Chao, C. H., Chung, M. H., Chen, C. C., & Yeh, S. D. (2001). Completion of the genome sequence of Watermelon silver mottle virus and utilization of degenerate primers for detecting tospoviruses in five serogroups. Phytopathology, 91, 361–367.
Desbiez, C., & Lecoq, H. (2008). Evidence for multiple intraspecific recombinants in natural populations of Watermelon mosaic virus (WMV, Potyvirus). Archives of Virology, 153, 1749–1754.
Desbiez, C., Costa, C., Wipf-Scheibel, C., Girard, M., & Lecoq, H. (2007). Serological and molecular variability of Watermelon mosaic virus (genus Potyvirus). Archives of Virology, 152, 775–781.
Desbiez, C., Joannon, B., Wipf-Scheibel, C., Chandeysson, C., & Lecoq, H. (2009). Emergence of new strains of Watermelon mosaic virus in Southeastern France: evidence for limited spread but rapid local population shift. Virus Research, 141, 201–208.
FAOSTAT (2014) Food and Agriculture Organization of the United Nations. Statistics Division. http://faostat3.fao.org. Accessed XX July 2016.
Garcia-Arenal, F., Fraile, A., & Malpica, J. M. (2001). Variability and genetic structure of plant virus populations. Annual Review of Phytopathology, 39, 157–186.
Gomez, P., Sempere, R. N., Amari, K., Gomez-Aix, C., & Aranda, M. A. (2010). Epidemics of Tomato torrado virus, Pepino mosaic virus and Tomato chlorosis virus in tomato crops: do mixed infections contribute to torrado disease epidemiology? Annals of Applied Biology, 156, 401–410.
Griesbach, J. A. (1995). Detection of tomato ringspot virus by polymerase chain reaction. Plant Disease, 79, 1054–1056.
Jain, R. K., Sharma, J., Sivakumar, A. S., Sharma, P. K., Byadgi, A. S., Verma, A. K., et al. (2004). Variability in the coat protein gene of Papaya ringspot virus isolates from multiple locations in India. Archives of Virology, 149, 2435–2442.
Juarez, M., Legua, P., Mengual, C. M., Kassem, M. A., Sempere, R. N., Gómez, P., Truniger, V., & Aranda, M. A. (2013). Relative incidence, spatial distribution and genetic diversity of cucurbit viruses in eastern Spain. Annals of Applied Biology, 162, 362–370.
Kassem, M. A., Sempere, R. N., Juarez, M., Aranda, M. A., & Truniger, V. (2007). Cucurbit aphid-borne yellows virus is prevalent in field-grown cucurbit crops of southeastern Spain. Plant Disease, 91, 232–238.
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., & McWilliam, H. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947–2948.
Lecoq, H., & Desbiez, C. (2012). Viruses of cucurbit crops in theMediterranean region: an ever-changing picture. Advances in Virus Research, 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 Disease, 87, 955–959.
Lecoq, H., Justafré, I., Wipf-Scheibel, C., & Desbiez, C. (2008). Moroccan watermelon mosaic virus newly reported on zucchini squash in France. Plant Pathology, 57, 766.
Lecoq, H., Wipf-Schibel, C., Chandeysson, C., Le Van, A., Fabre, F., & Desbiez, C. (2009). Molecular epidemiology of Zucchini yellow mosaic virus in France: An historical overview. Virus Research, 141, 190–200.
Li, W. H. (1993). Unbiased estimation of the rates of synonymous and nonsynonymous substitution. Journal of Molecular Evolution, 36, 96–99.
Liu, W. R., & Xiang, B. C. (2008). Nucleotide sequence analysis of coat protein gene of Watermelon mosaic virus 2 Xinjiang Changji isolates. Acta phytopathologica sinica, 38, 576–581 (In Chinese).
Luis-Arteaga, M., Alvarez, J. M., Alonso-Prados, J. L., Bernal, J. J., García-Arenal, F., Laviña, A., et al. (1998). Occurrence, distribution, and relative incidence of mosaic viruses infecting field-grown melon in Spain. Plant Disease, 82, 979–982.
Mascarell-Creus, A., Cañizares, J., Vilarrasa-Blasi, J., Mora-García, S., Blanca, J., Gonzalez-Ibeas, D., et al. (2009). An oligo-based microarray offers novel transcriptomic approaches for the analysis of pathogen resistance and fruit quality traits in melon (Cucumis melo L.). BMC Genomics, 10, 467.
Massumi, H., Samei, A., Hosseini Pour, A., Shaabanian, M., & Rahimian, H. (2007). Occurrence, distribution, and relative incidence of seven viruses infecting greenhouse-grown cucurbits in Iran. Plant Disease, 91, 159–163.
Masuta, C., Seshimo, Y., Mukohara, M., Jung, H. J., Udea, S., Ryu, K. H., & Choi, J. K. (2002). Evolutionary characterization of two lily isolates of Cucumber mosaic virus isolated in Japan and Korea. Journal of General Plant Pathology, 68, 163–168.
Miras, M., Sempere, R. N., Kraft, J. J., Miller, W. A., Aranda, M. A., & Truniger, V. (2014). Interfamilial recombination between viruses led to acquisition of a novel translation-enhancing RNA element that allows resistance breaking. New Phytologist, 202, 233–246.
Moreno, I. M., Malpica, J. M., Díaz-Pendón, J. A., Moriones, E., Fraile, A., & García-Arenal, F. (2004). Variability and genetic structure of the population of Watermelon mosaic virus infecting melon in Spain. Virology, 318, 451–460.
Pamilo, P., & Bianchi, N. O. (1993). Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Molecular Biology and Evolution, 10, 271–281.
Perotto, M. C., Celli, M. G., Pozzi, E. A., Luciani, C. E., & Conci, V. C. (2016). Occurrence and characterization of a severe isolate of Watermelon mosaic virus from Argentina. European Journal of Plant Pathology. doi:10.1007/s10658-016-0904-z.
Pfosser, M. F., & Baumann, H. (2002). Phylogeny and geographical differentiation of Zucchini yellow mosaic virus isolates (Potyviridae) based on molecular analysis of the coat protein and part of the cytoplasmic inclusion protein genes. Archives of Virology, 147, 1599–1609.
Romay, G., Lecoq, H., Geraud-Pouey, F., Chirinos, D. T., & Desbiez, C. (2014). Current status of cucurbit viruses in Venezuela and characterization of Venezuelan isolates of Zucchini yellow mosaic virus. Plant Pathology, 63, 78–87.
Romay, G., Lecoq, H., & Desbiez, C. (2015). Melon chlorotic mosaic virus and associated alphasatellite from Venezuela: genetic variation and sap transmission of a begomovirus–satellite complex. Plant Pathology, 64, 1224–1234.
Rui, Z. Y., Goldfarb, R. J., Qiu, Y. M., Zhou, T. H., Chen, R. Y., Pirajno, F., & Yun, G. (2002). Paleozoic–early Mesozoic gold deposits of the Xinjiang Autonomous Region, northwestern China. Mineralium Deposita, 37, 393–418.
Sharifi, M., Massumi, H., Heydarnejad, J., Hosseini Pour, A., Shaabanian, M., & Rahimian, H. (2008). Analysis of the biological and molecular variability of Watermelon mosaic virus isolates from Iran. Virus Genes, 37, 304–313.
Stanković, I., Bulajić, A., Vučurović, A., Ristić, D., Milojević, K., Berenji, J., & Krstić, B. (2011). Status of tobacco viruses in Serbia and molecular characterization of Tomato spotted wilt virus isolates. Acta Virologica, 55, 337–347.
Svoboda, J., & Leisova-Svobodova, L. (2011). First report of Squash mosaic virus in ornamental pumpkin in the Czech Republic. Plant Disease, 95(10), 1321.
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. Molecular Biology and Evolution, 28, 2731–2739.
Tomassoli, L., Tiberini, A., & Meneghini, M. (2010). Zucchini yellow fleck virus is an emergent virus on melon in Sicily (Italy). Journal of Phytopathology, 158, 314–316.
Vučurović, A., Bulajić, A., Stanković, I., Ristić, D., Berenji, J., Jović, J., et al. (2012). Non-persistently aphid-borne viruses infecting pumpkin and squash in Serbia and partial characterization of Zucchini yellow mosaic virus isolates. European Journal of Plant Pathology, 133, 935–947.
Wang, Y., Gaba, V., Yang, J., Palukaitis, P., & Gal-On, A. (2002). Characterizations of synergy between cucumber mosaic virus and potyviruses in cucurbit hosts. Phytopathology, 147, 2301–2312.
Webb, R. E., & Scott, H. A. (1965). Isolation and identification of Watermelon mosaic virus 1 and 2. Phytopathology, 55, 895–900.
Wei, N. S., Zhang, M. L., Wu, Y. F., & Wei, Y. L. (1991). Identification and control of muskmelon virus diseases in Xinjiang and Gansu province of China. Acta Phytophylacica Sinica, 18, 81–85 (In Chinese).
Wu, E. N. S., Li, W. Q., & Peng, J. M. (1980). Studies on the pathogens of Hami melon mosaic disease in Sinkiang, China. Acta Biochimica et Biophysica Sinica, 12(3), 237–241 (In Chinese).
Xie, H., Yang, X. R., & Dong, P. (1994). Crop virus diseases. Urumqi: Xinjiang People’s Publishing House (In Chinese).
Xinjiang Statistical Yearbook (2015) Statistic Bureau of Xinjiang Uygur Autonomous Region. http://www.xjtj.gov.cn/sjcx/tjnj_3415/. Accessed XX July 2016.
Xu, D. Y. (1989). Geographic zoning of agro-climatic resources in Xinjiang. Beijing: China Meteorological Press (In Chinese).
Yin, Y. Q., Cui, X. M., Quan, J. R., Liu, Y., & Liang, X. S. (1982). Isolation and identification of viruses infecting saccharine melon in Xinjiang. Acta phytophylacica sinica, 9, 157–163 (In Chinese).
Zeng, R., Liao, Q., Feng, J. D., Li, J. D., & Chen, J. (2007). Synergy between Cucumber mosaic virus and Zucchini yellow mosaic virus on Cucurbitaceae hosts tested by real-time reverse transcription-polymerase chain reaction. Acta Biochimica et Biophysica Sinica, 39, 431–437.
Zhao, M. F., Chen, J., Zheng, H. Y., Adams, M. J., & Chen, J. P. (2003). Molecular analysis of Zucchini yellow mosaic virus isolates from Hangzhou, China. Journal of Phytopathology, 151, 307–311.
Zheng, G. Y., & Dong, T. (1989). Occurrence of Zucchini yellow mosaic virus in Xinjiang. Acta Phytopathologica Sinica, 21, 72 (In Chinese).
Acknowledgments
This work was supported by the National Natural Science Funding of China (31060148, 31260258), the Innovative Project of Xinjiang University, China (XJUBSCX-2012025). We thank Zi-Qiang Zhang and Hao Lu (College of Life Science and Technology, Xinjiang University, China) for help with the sample collection.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
This study was funded by the National Natural Science Funding of China (31060148, 31260258), the Innovative Project of Xinjiang University, China (XJUBSCX-2012025).
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Table 1
List of the representative Watermelon mosaic virus isolates from GenBank used for phylogenetic analysis of the complete coat protein sequences (DOCX 15 kb)
Supplementary Fig. 1
Virus-like symptoms observed in different melon-growing locations in Xinjiang of China. (a) mild mosaic, (b) moderate mosaic, (c) severe mosaic, (d) local necrosis, (e) obvious malformation of leaves, (f) severe blistering and mosaic without deformation of leaves and (g) severe blistering and mosaic with obvious deformation of leaves (JPG 3192 kb)
Supplementary Fig. 2
One weed species Sophora alopecuroides with virus-like symptoms. (a) The naturally infected plant showing virus-like symptoms and (b) healthy plant (JPG 1616 kb)
Rights and permissions
About this article
Cite this article
Wang, D., Li, G. & Du, S.S. Occurrence of viruses infecting melon in Xinjiang of China and molecular characterization of Watermelon mosaic virus isolates. Eur J Plant Pathol 147, 919–931 (2017). https://doi.org/10.1007/s10658-016-1060-1
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-016-1060-1