Abstract
The chrysanthemum stunt viroid (CSVd) causes severe stunting and significant reduction in flower yield and quality of commercial chrysanthemum (Chrysanthemum morifolium). The pattern of inheritance and the detailed mechanism underlying CSVd resistance remains unclear. Chrysanthemum morifolium shows unstable and variable chromosome numbers that form a hexaploid complex with aneuploidy. To overcome the issue of complex hybridity and polyploidy, a diploid wild chrysanthemum, C. seticuspe f. boreale was used here as an alternative model to C. morifolium. We screened 20 C. seticuspe accessions for resistance to CSVd and identified one resistant accession “AET-19” showing resistance. Tissue print hybridization analysis showed that CSVd concentration decreased in the uppermost leaves of the AET-19 after the scions were cut from the infected rootstocks, suggesting the resistance seems to be ‘CSVd-disappearance type’. In situ hybridization experiments revealed that CSVd does not invade the shoot tip of AET-19 plants after graft-inoculation onto infected rootstocks. Taken together, the results highlight the usefulness of C. setiscupe as a model for analyzing the mechanism of CSVd resistance and its pattern of inheritance.
Similar content being viewed by others
Change history
15 May 2019
Co author name misspelt and should read as Masaaki Osaka.
References
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.
Bouwen, I., & van Zaayen, A. (2004). Chrysanthemum stunt viroid. In A. Hadidi, J. Flores, W. Randles, & J. S. Semancik (Eds.), The Viroids (pp. 218–223). Melbourne: CSIRO.
Cho, W. K., Jo, Y., Jo, K.-M., & Kim, K.-H. (2013). A current overview of two viroids that infect chrysanthemums: Chrysanthemum stunt viroid and Chrysanthemum chlorotic mottle viroid. Viruses, 5, 1099–1113.
Chung, B. N., & Pak, H. S. (2008). Seed transmission of Chrysanthemum stunt viroid in chrysanthemum (Dendranthema grandiflorum) in Korea. Plant Pathology Journal, 24, 31–35.
Di Serio, F., Martínez de Alba, A. E., Navarro, B., Gisel, A., & Flores, R. (2010). RNA-dependent RNA polymerase 6 delays accumulation and precludes meristem invasion of a viroid that replicates in the nucleus. Journal of Virology, 84, 2477–2489.
Di Serio, F., Li, S. F., Pallás, V., Owens, R. A., Randles, J. W., Sano, T., Verhoeven, J. T. T., Vidalakis, G., & Flores, R. (2017). Viroid taxonomy. In A. Hadidi, R. Flores, P. Palukaitis, & J. Randles (Eds.), Viroids and satellites (pp. 135–146). London: Academic Press.
Diener, T. O., & Lawson, R. H. (1973). Chrysanthemum stunt: A viroid disease. Virology, 51, 94–101.
Dimock, A.W. (1947). Chrysanthemum stunt. NY State Flower Growers 313 Bulletin, 26, 2.
Ding, B., Kwon, M. O., Hammond, R., & Owens, R. (1997). Cell-to-cell movement of potato spindle tuber viroid. Plant Journal, 12, 931–936.
Doi, M., & Kato, K. (2004). Nucleotide sequence of Chrysanthemum stunt viroid (CSVd) occurred in Shizuoka prefecture and symptoms of chrysanthemum cultivar. Annual Report of The Kansai Plant Protection Society, 46, 11–14 In Japanese, with English abstract.
Flores, R., Gas, M. E. G., Molina-Serrano, D., Nohales, M. A., Carbonell, A., & Gago, S. (2009). Viroid replication: Rolling circles, enzymes and ribozymes. Viruses, 1, 317–334.
Higuchi, Y., Narumi, T., Oda, A., Nakano, Y., Sumitomo, K., Fukai, S., & Hisamatsu, T. (2013). The gated induction system of a systemic floral inhibitor, antiflorigen, determines obligate short-day flowering in chrysanthemums. Proceedings of the National Academy of Sciences, 110, 17137–17142.
Hollings, M., & Stone, O. M. (1973). Some properties of chrysanthemum stunt, a virus with the characteristics of an uncoated ribonucleic acid. Annals of Applied Biology, 74, 333–348.
Horst, R. K. (1977). Effects of chrysanthemum stunt, chlorotic mottle, aspermy and mosaic on flowering and rotting of chrysanthemums. Phytopathology, 67, 9–14.
Hosokawa, M. (2008). Leaf primordia-free shoot apical meristem culture: A new method for production of viroid-free plants. Journal of the Japanese Society for Horticultural Science, 77, 341–349.
Hosokawa, M., Matsushita, Y., Uchida, H., & Yazawa, S. (2005). Direct RT-PCR method for detecting two chrysanthemum viroids using minimal amounts of plant tissue. Journal of Virological Methods, 131, 28–33.
Hua, J. (2013). Modulation of plant immunity by light, circadian rhythm, and temperature. Current Opinion in Plant Biology, 16, 406–413.
Klie, M., Schie, S., Linde, M., & Debener, T. (2014). The type of ploidy of chrysanthemum is not black or white: A comparison of a molecular approach to published cytological methods. Frontiers in Plant Science, 5, 1–8.
Marais, A., Faure, C., Deogratias, J. M., & Candresse, T. (2011). First report of Chrysanthemum stunt viroid in various cultivars of Argyranthemum frutescens in France. Plant Disease, 5, 1196.
Matsushita, Y. (2013). Chrysanthemum stunt viroid. Japan Agricultural Research Quarterly, 47, 237–247.
Matsushita, Y., & Kumar, P. K. R. (2009). In vitro transcribed Chrysanthemum stunt viroid (CSVd) RNA is infectious to chrysanthemum and other plants. Phytopathology, 99, 58–66.
Matsushita, Y., & Shima, Y. (2015). Effect of low temperature on the distribution of Chrysanthemum stunt viroid in Chrysanthemum morifolium. Phytoparasitica, 43, 609–614.
Matsushita, Y., & Tsuda, S. (2014). Distribution of Potato spindle tuber viroid in reproductive organs of petunia during its developmental stages. Phytopathology, 104, 964–969.
Matsushita, Y., Tsukiboshi, T., Ito, & Chikuo, Y. (2007). Nucleotide sequences and distribution of Chrysanthemum stunt viroid in Japan. Journal of the Japanese Society for Horticultural Science, 76, 333–337.
Matsushita, Y., Usugi, T., & Tsuda, S. (2011). Distribution of tomato chlorotic dwarf viroid in floral organs of tomato. European Journal of Plant Pathology, 130, 441–447.
Matsushita, Y., Aoki, K. S., & Umitomo, K. (2012). Selection and inheritance of resistance to Chrysanthemum stunt viroid. Crop Protection, 35, 1–4.
Nabeshima, T., Hosokawa, M., Yano, S., Ohishi, K., & Doi, M. (2012). Screening of chrysanthemum cultivars with resistance to chrysanthemum stunt viroid. Journal of the Japanese Society for Horticultural Science, 81, 285–294.
Nabeshima, T., Hosokawa, M., Yano, S., Ohishi, K., & Doi, M. (2014). Evaluation of chrysanthemum stunt viroid (CSVd) infection in newly-expanded leaves from CSVd-inoculated shoot apical meristems as a method of screening for CSVd-resistant chrysanthemum cultivars. The Journal of Horticultural Science and Biotechnology, 89, 29–34.
Nabeshima, T., Doi, M., & Hosokawa, M. (2017). Comparative analysis of Chrysanthemum stunt viroid accumulation and movement in two chrysanthemum (Chrysanthemum morifolium) cultivars with differential susceptibility to the viroid infection. Frontiers in Plant Science, 8, 1940. https://doi.org/10.3389/fpls.2017.01940.
Nakano, Y., Higuchi, Y., Sumitomo, K., & Hisamatsu, T. (2013). Flowering retardation by high temperature in chrysanthemums: Involvement of FLOWERING LOCUS T-like 3 gene repression. Journal of Experimental Botany, 64, 909–920.
Nakashima, A., Hosokawa, M., Maeda, S., & Yazawa, S. (2007). Natural infection of Chrysanthemum stunt viroid in dahlia plants. Journal of General Plant Pathology, 73, 225–227.
Nie, X. Z., Singh, R. P., & Bostan, H. (2005). Molecular cloning, secondary structure, and phylogeny of three pospiviroids from ornamental plants. Canadian Journal of Plant Pathology, 27, 592–602.
Oda, A., Narumi, T., Li, T., Kando, T., Higuchi, Y., Sumitomo, K., Fukai, S., & Hisamatsu, T. (2012). CsFTL3, a chrysanthemum FLOWERING LOCUS T-like gene, is a key regulator of photoperiodic flowering in chrysanthemums. Journal of Experimental Botany, 63, 1461–1477.
Omori, H., Hosokawa, M., Shiba, H., Shitsukawa, N., Murai, K., & Yazawa, S. (2009). Screening of chrysanthemum plants with strong resistance to Chrysanthemum stunt viroid. Journal of the Japanese Society for Horticultural Science, 78, 350–355.
Palukaitis, P. (2017). Chrysanthemum stunt viroid. In A. Hadidi, R. Flores, P. Palukaitis, & J. Randles (Eds.), Viroids and satellites (pp. 181–190). London: Academic Press.
Palukaitis, P., & Symons, R. H. (1980). Purification and characterization of the circular and linear forms of Chrysanthemum stunt viroid. Journal of General Virology, 46, 477–489.
Sainte-Marie, G. (1962). A paraffin embedding technique for studies employing immunofluorescence. Journal of Histochemistry & Cytochemistry, 10, 250–256.
Stark-Lorenzen, P., Guitton, M. C., Werner, R., & Mühlbach, H. P. (1997). Detection and tissue distribution of potato spindle tuber viroid in infected tomato plants by tissue print hybridization. Archives of Virology, 142, 1289–1296.
Teixeira da Silva, J. A., Shinoyama, H., Aida, R., Matsushita, Y., Raj, S. K., Chen, F. D., & Chen, F. (2013). Chrysanthemum biotechnology: Quo vadis? Critical Reviews in Plant Sciences, 32, 21–52.
Verhoeven, J. T. J., Arts, M. S. J., Owens, R. A., & Roenhurst, J. W. (1998). Natural infection of petunia by Chrysanthemum stunt viroid. European Journal of Plant Pathology, 104, 383–386.
Verhoeven, J. T. J., Jansen, C. C. C., & Roenhurst, J. W. (2006). First report of potato virus M and Chrysanthemum stunt viroid in Solanum jasminoides. Plant Disease, 90, 1359–1359.
Zhu, Y., Green, L., Woo, Y. M., Owens, R. A., & Ding, B. (2001). Cellular basis of potato spindle tuber viroid systemic movement. Virology, 279, 69–77.
Acknowledgements
We are grateful to M. Nakano (Hiroshima University, Japan) for helpful comments and discussion. We thank NBRP Chrysanthemum (http://shigen.nig.ac.jp/chrysanthemum/) for providing chrysanthemum accessions.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
There are no potential conflicts of interest, and this research did not involve human participants and/or animals.
Rights and permissions
About this article
Cite this article
Matsushita, Y., Osaka, M. Screening of Chrysanthemum seticuspe accessions reveals different degrees of resistance to chrysanthemum stunt viroid. Eur J Plant Pathol 154, 1059–1066 (2019). https://doi.org/10.1007/s10658-019-01726-x
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-019-01726-x