Abstract
In the past two decades, viruses in the genera Crinivirus and Begomovirus, transmitted by whiteflies, have emerged as threatening diseases to cucurbit cultivation. The criniviruses Cucurbit chlorotic yellows virus (CCYV) and Cucurbit yellow stunting disorder virus (CYSDV) occur in mixed infection at high rates in cucumber greenhouses in Lebanon. The begomovirus Squash leaf curl virus (SLCV) is also present in the country infecting cucumber but at a lower incidence. The effect of single, dual or triple virus infections on cucumber was studied. Single infection by SLCV did not lead to any symptoms or yield reduction. CYSDV or CCYV infections led to development of characteristic yellowing symptoms. In single infections, CYSDV caused the greatest reductions in height and yield that ranged from 25 to 62 % and 52 to 63 %, respectively, depending on season and variety. CCYV induced less severe reduction in height, 10 to 33 %, and in fruit number, 10 to 12 %. Yellowing symptoms induced by dual infections in any combination were similar to those of singly-infected plants. Triple infections resulted in substantial reductions in plant height and yield as compared to single or dual infections. This is the first report that characterizes a significant increase in disease severity upon co-infection between cucurbit-infecting criniviruses and begomoviruses. The implications of these observations on integrated disease management strategies are discussed.
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Abou-Jawdah, Y., Sobh, H., Fayyad, A., Lecoq, H., Delecolle, B., & Trad-ferre, J. (2000). Cucurbit yellow stunting disorder virus- a new threat to cucurbits in Lebanon. Journal of Plant Pathology, 82(1), 55–60.
Abrahamian, P. E., & Abou-Jawdah, Y. (2013). Detection and quantitation of the new world Squash leaf curl virus by TaqMan real-time PCR. Journal of Virological Methods, 191(1), 76–81.
Abrahamian, P. E., & Abou-Jawdah, Y. (2014). Whitefly-transmitted criniviruses of cucurbits: current status and future prospects. Indian Journal of Virology, 25(1), 26–38.
Abrahamian, P. E., Sobh, H., & Abou-Jawdah, Y. (2012). First Report of Cucurbit chlorotic yellows virus on cucumber in Lebanon. Plant Disease, 96(11), 1704.
Abrahamian, P. E., Seblani, R., Sobh, H., & Abou-Jawdah, Y. (2013). Detection and quantitation of two cucurbit criniviruses in mixed infection by real-time RT-PCR. Journal of Virological Methods, 193(2), 320–326.
Accerbi, M., Schmidt, S., Paoli, E., Park, S., Jeong, D.-H., & Green, P. (2010). Methods for isolation of total RNA to recover miRNAs and other small RNAs from diverse species. In B. C. Meyers, & P. J. Green (Eds.), Methods in Molecular Biology: Plant MicroRNAs (pp. 31–50,), Humana Press.
Al-Musa, A., Anfoka, G., Misbeh, S., Abhary, M., & Ahmad, F. H. (2008). Detection and molecular characterization of Squash leaf curl virus (SLCV) in Jordan. Journal of Phytopathology, 156(5), 311–316.
Alves-Júnior, M., Alfenas-Zerbini, P., Andrade, E. C., Esposito, D. A., Silva, F. N., da Cruz, A. C. F., et al. (2009). Synergism and negative interference during co-infection of tomato and Nicotiana benthamiana with two bipartite begomoviruses. Virology, 387(2), 257–266.
Bananej, K., & Vahdat, A. (2008). Identification, distribution and incidence of viruses in field-grown cucurbit crops of Iran. Phytopathologia Mediterranea, 47(3), 247–257.
Bananej, K., Menzel, W., Kianfar, N., Vahdat, A., & Winter, S. (2013). First report of cucurbit chlorotic yellows virus infecting cucumber, melon, and squash in Iran. Plant Disease, 97(7), 1005.
Fletcher, J. D., Wallace, A. R., & Rogers, B. T. (2000). Potyviruses in New Zealand buttercup squash (Cucurbits maxima duch.): yield and quality effects of ZYMV and WMV 2 virus infections. New Zealand Journal of Crop and Horticultural Science, 28(1), 17–26.
Flock, R. A., & Mayhew, D. E. (1981). Squash leaf curl, a new disease of cucurbits in California. Plant Disease, 65, 75–76.
FAO Statistics (2012) http://faostat.fao.org/. Accessed May 2014.
Gil-Salas, F. M., Peters, J., Boonham, N., Cuadrado, I. M., & Janssen, D. (2011). Yellowing disease in zucchini squash produced by mixed infections of Cucurbit yellow stunting disorder virus and Cucumber vein yellowing virus. Phytopathology, 101(11), 1365–1372.
Gil-Salas, F. M., Peters, J., Boonham, N., Cuadrado, I. M., & Janssen, D. (2012). Co-infection with Cucumber vein yellowing virus and Cucurbit yellow stunting disorder virus leading to synergism in cucumber. Plant Pathology, 61(3), 468–478.
Gu, Q. S., Liu, Y. H., Wang, Y. H., Huangfu, W. G., Gu, H. F., Xu, L., Song, F. M., & Brown, J. K. (2011). First report of cucurbit chlorotic yellows virus in cucumber, melon, and watermelon in China. Plant Disease, 95(1), 73.
Idris, A. M., Abdel-Salam, A., & Brown, J. K. (2006). Introduction of the New world squash leaf curl virus to squash (Cucurbita pepo) in Egypt: a potential threat to important food crops. Plant Disease, 90(9), 1262.
Kassem, M. A., Sempere, R. N., Juárez, 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(3), 232–238.
Keshavarz, T., Shams‐Bakhsh, M., Izadpanah, K., & Malboobi, M. A. (2014). Occurrence and genome analysis of cucurbit chlorotic yellows virus in Iran. Journal of Phytopathology, 162, 523–526.
Lecoq, H., & Desbiez, C. (2012). Viruses of cucurbit crops in the mediterranean region: an ever-changing picture. In G. Loebenstein & H. Lecoq (Eds.), Advances in virus research (pp. 67–126). Academic Press: London.
Massumi, H., Samei, A., Pour, A. H., Shaabanian, M., & Rahimian, H. (2007). Occurrence, distribution, and relative incidence of seven viruses infecting greenhouse-grown cucurbits in Iran. Plant Disease, 91(2), 159–163.
Navas-Castillo, J., Fiallo-Olivé, E., & Sánchez-Campos, S. (2011). Emerging virus diseases transmitted by whiteflies. Annual Review of Phytopathology, 49(1), 219–248.
Orfanidou, C., Maliogka, V. I., & Katis, N. (2014). First report of Cucurbit chlorotic yellows virus in cucumber, melon, and watermelon in Greece. Plant Disease, 98(10), 1446
Rubio, L., Abou-Jawdah, Y., Lin, H.-X., & Falk, B. W. (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(4), 929–933.
Sobh, H., Samsatly, J., Jawhari, M., Najjar, C., Haidar, A., & Abou-Jawdah, Y. (2012). First report of squash leaf curl virus in cucurbits in Lebanon. Plant Disease, 96(8), 1231.
Sufrin-Ringwald, T., & Lapidot, M. (2011). Characterization of a synergistic interaction between two cucurbit-infecting begomoviruses: Squash leaf curl virus and Watermelon chlorotic stunt virus. Phytopathology, 101(2), 281–289.
Syller, J. (2012). Facilitative and antagonistic interactions between plant viruses in mixed infections. Molecular Plant Pathology, 13(2), 204–216.
Tatineni, S., Graybosch, R. A., Hein, G. L., Wegulo, S. N., & French, R. (2010). Wheat cultivar-specific disease synergism and alteration of virus accumulation during co-infection with Wheat streak mosaic virus and Triticum mosaic virus. Phytopathology, 100(3), 230–238.
Tzanetakis, I. E., Martin, R. R., & Wintermantel, W. M. (2013). Epidemiology of criniviruses, an emerging problem in world agriculture. Frontiers in Microbiology, 4, 119.
Wang, Y., Gaba, V., Yang, J., Palukaitis, P., & Gal-On, A. (2002). Characterization of synergy between Cucumber mosaic virus and potyviruses in cucurbit hosts. Phytopathology, 92(1), 51–58.
Wang, J., Turina, M., Medina, V., & Falk, B. W. (2009). Synergistic interaction between the Potyvirus, Turnip mosaic virus and the Crinivirus, Lettuce infectious yellows virus in plants and protoplasts. Virus Research, 144(1–2), 163–170.
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(12), 1340–1345.
Zhang, Y.-P., Uyemoto, J. K., & Kirkpatrick, B. C. (1998). A small-scale procedure for extracting nucleic acids from woody plants infected with various phytopathogens for PCR assay. Journal of Virological Methods, 71(1), 45–50.
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This study was partially funded by a USAID-ME grant.
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Abrahamian, P., Sobh, H., Seblani, R. et al. Co-infection of two criniviruses and a begomovirus enhances the disease severity in cucumber. Eur J Plant Pathol 142, 521–530 (2015). https://doi.org/10.1007/s10658-015-0630-y
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DOI: https://doi.org/10.1007/s10658-015-0630-y