Abstract
Viral symptoms are frequently observed in production fields of ranunculus (Ranunculus asiaticus L.) in Japan. Based on incidence of diseases caused by a large number of ranunculus-infective viruses, ranunculus mild mosaic virus (RanMMV), tomato spotted wilt virus (TSWV) and cucumber mosaic virus (CMV) infections were the focus of an epidemiological field survey in Japan. To efficiently investigate the incidence and distribution of the three viruses, we first developed a new multiplex reverse transcription-polymerase chain reaction method that enables simultaneous detection of RanMMV, TSWV, and CMV in ranunculus. A field survey of virus infections in ranunculus production fields in Tohoku and Kyushu regions revealed that the infection rate of RanMMV was much higher than that of the other viruses in all fields sampled. Interestingly, the infection rate of RanMMV showed an increasing trend in proportion to the number of vegetative propagation cycles of ranunculus, implying virus transmission by aphids. Taken together, this method was proven to be effective for simultaneous detection of RanMMV, TSWV and CMV in ranunculus plants, and RanMMV was recognized as one of the most prevalent plant viruses in ranunculus fields in Japan.
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Asano, S., Matsushita, Y., Hirayama, Y., & Naka, T. (2015). Simultaneous detection of tomato spotted wilt virus, dahlia mosaic virus and chrysanthemum stunt viroid by multiplex RT-PCR in dahlias and their distribution in Japanese dahlias. Letters in Applied Microbiology, 61, 113–120.
Bellardi, M. G., Bertaccini, A., & Marini, F. (1988). A PVY isolate infecting Ranunculus. Phytopathologia Mediterranea, 27, 157–162.
Ciuffo, M., Testa, M., Lenzi, R., & Turina, M. (2011). Ranunculus latent virus: A strain of Artichoke latent virus or a new macluravirus infecting artichoke? Archives of Virology, 156, 1053–1057.
Kamenetsky, R., Peterson, R. L., Melville, L. H., Machado, C. F., & Bewley, J. D. (2005). Seasonal adaptations of the tuberous roots of Ranunculus asiaticus to and resurrection by changes in cell structure and protein content. New Phytologist, 166, 193–204.
Kawano, A., & Kanno, Y. (2004). Survey of virus diseases on ranunculus (Ranunculus asiaticus L.) in Miyazaki prefecture and development of the serologic identification method. Plant Protection, 60, 668–672 (In Japanese).
Liu, S., He, X., Park, G., Josefsson, C., & Perry, K. L. (2002). A conserved capsid protein surface domain of Cucumber mosaic virus is essential for efficient aphid vector transmission. Journal of Virology, 76, 9756–9762.
Minutolo, M., Sorrentino, R., Masenga, V., & Alioto, D. (2016). First report of Broad bean wilt virus 2 and Ranunculus mild mosaic virus in Ranunculus asiaticus in southern Italy. Plant Disease, 100, 235.
Murakami, K., & Furuichi, T. (2001). Establishment of shoot apex culture methods and proliferation culture methods of ranunculus. Bulletin of the Kagawa Prefecture Agricultural Experiment Station, 54, 33–40 (In Japanese with English Summary).
Murakami, K., & Ishikawa, K. (2009). Detection of virus infected Ranunculus asiaticus using RT-PCR method. Journal of the Japanese Society for Horticultural Science, 8, 317 (In Japanese).
Nakamura, K., Nagatomo, Y., & Gunji, T. (2014). Effects of propagation temperature on root formation of cuttings and acceleration of subsequent growth and tuberization of Ranunculus asiaticus L. Horticultural Research (Japan), 13, 113–117 (In Japanese with English Abstract).
Nagatomo, Y., Nakamura, K., Honda, Y., & Gunji, S. (2013). Effects of different terms of seed cold storage on growth and flowering in Ranunculus asiaticus L. Horticultural Research (JAPAN), 12(Suppl. 2), 236 (In Japanese).
Ohshima, K., Yamaguchi, Y., Hirota, R., Hamamoto, T., Tomimura, K., Tan, Z., Sano, T., Azuhata, F., Walsh, J. A., Fletcher, J., Chen, J., Gera, A., & Gibbs, A. (2002). Molecular evolution of Turnip mosaic virus: Evidence of host adaptation, genetic recombination and geographical spread. Journal of General Virology, 83, 1511–1521.
Okuda, M., Sakai, J., & Hanada, K. (2001). Comparison of the nucleocapsid genes and the 3’ non-transcriptional regions of the S RNA among Tomato spotted wilt virus isolates from Kyushu. Kyushu Plant Protection Research, 47, 21–24 (In Japanese).
van Oosten, H. J. (1970). Herbaceous host plants for the sharka (plum pox) virus. Netherlands Journal of Plant Pathology, 76, 253–260.
Palukaitis, P., & García-Arenal, F. (2003). Cucumoviruses. Advances in Virus Research, 62, 241–323.
Parrella, G., Gongnalons, K., Gebre-Selassie, C., & Marchoux, G. (2003). An update of the host range of Tomato spotted wilt virus. Journal of Plant Pathology, 85, 227–264.
Sagae, T., Ono, K., Sato, H., Fukase, E., Yokokawa, S., & Oyamada, M. (1989). Cultivation methods using seed grown tuberous roots on Rununculus asiaticus L.. 1. Tuberous roots production. Tohoku Agric. Res., 42, 297–298 (In Japanese).
Song, A., You, Y., Chen, F., Li, P., Jiang, J., & Chen, S. (2012). A multiplex RT-PCR for rapid and simultaneous detection of viruses and viroids in chrysanthemum. Letters in Applied Microbiology, 56, 8–13.
Suzuki, M., Kuwata, S., Kataoka, J., Masuta, C., Nitta, N., & Takanami, Y. (1991). Functional analysis of deletion mutants of cucumber mosaic virus RNA3 using an in vitro transcription system. Virology, 183, 106–113.
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTALW: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight choice. Nucleic Acids Research, 22, 4673–4680.
Turina, M., Ciuffo, M., Lenzi, R., Rostagno, L., Mela, L., Derin, E., & Palmano, S. (2006). Characterization of four viral species belonging to the family Potyviridae isolated from Ranunculus asiaticus. Phytopathology, 96, 560–566.
Turina, M., Kormelink, R., & Resende, R. O. (2016). Resistance to tospoviruses in vegetable crops: Epidemiological and molecular aspects. Annual Review of Phytopathology, 54, 347–371.
Ushiyama, T., Hanada, K., Honda, Y., Aono, N., & Kameyama, M. (1989). Some viruses isolated from summer phlox, ranunculus and petunia plants. Bulletin of the Kanagawa Horticultural Experimental Station, 38, 43–49 (In Japanese with English Summary).
Vaira, A. M., Milne, R. G., Accotto, G. P., Luisoni, E., Masenga, V., & Lisa, V. (1997). Partial characterization of a new virus from ranunculus with a divided RNA genome and circular supercoiled thread-like particles. Archives of Virology, 142, 2131–2146.
Whitfield, A. E., Campbell, L. R., Sherwood, J. L., & Ullman, D. E. (2003). Tissue blot immunoassay for detection of Tomato spotted wilt virus in Ranunculus asiaticus and other ornamentals. Plant Disease, 87, 618–622.
Wilson, C. R. (1998). Incidence of weed reservoirs and vectors of tomato spotted wilt tospovirus on southern Tasmanian lettuce farms. Plant Pathology, 47, 171–176.
Acknowledgements
We thank Dr. K. Nakamura for critical reading of this manuscript, and Mr. Y. Yoshida, Ms. E. Kodama, Ms. T. Kitamura, and Ms. M. Nagatomo for preparing the experimental materials. This study was supported by a Grant-in-Aid for “Research and development projects for application in promoting new policy of agriculture, forestry and fisheries (25075c)” from the Ministry of Agriculture, Forestry, and Fisheries of Japan.
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Hayahi, S., Matsushita, Y., Kanno, Y. et al. Field survey of ranunculus mild mosaic virus, tomato spotted wilt virus and cucumber mosaic virus infections in Ranunculus asiaticus L. in Japan by newly developed multiplex RT-PCR. Eur J Plant Pathol 150, 205–212 (2018). https://doi.org/10.1007/s10658-017-1268-8
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DOI: https://doi.org/10.1007/s10658-017-1268-8