Abstract
Three novel viruses were detected from Japanese persimmon ‘Reigyoku’ (Diospyros kaki), which grows poorly when top-grafted onto some interstocks. The genomic characterization and the phylogenetic analysis of these viruses indicated that they are likely new members of the genera Ampelovirus, Polerovirus, and Waikavirus, tentatively named Persimmon ampelovirus (PAmpV), Persimmon polerovirus (PPolV), and Persimmon waikavirus (PWaiV). The alignment of two PAmpV variants with Plum bark necrosis stem pitting–associated virus isolates had 72.5%–79.0% amino acid sequence identities with RNA-dependent RNA polymerase, 71.6%–79.2% with a heat shock protein 70 homolog, and 66.2%–69.8% with coat protein, respectively. Two PPolV variants showed the highest amino acid sequence identities (46.6%) with the P1–P2 fusion protein of Brassica yellows virus. PWaiV had the highest amino acid sequence identity (41.9%) with the conserved domain between proteinase and polymerase of Rice tungro spherical virus. Reverse-transcription and polymerase chain reaction detected Persimmon virus A, Apple crinkle fruit viroid, and Citrus viroid VI from the mother clone with good growth, and PAmpV, PPolV, and Persimmon latent viroid (PLVd) additionally from 20 trees with poor growth. PAmpV, PPolV, and PLVd were detected from four, 10, and 10 of 14 trees with good growth, respectively, and the grafting of budwood harboring these three pathogens caused significant stunt in mother clones.
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Afouda, L., Kone, D., Zinsou, V., Dossou, L., Kenyon, L., Winter, S., & Knierim, D. (2017). Virus surveys of Capsicum spp. in the Republic of Benin reveal the prevalence of pepper vein yellows virus and the identification of a previously uncharacterised polerovirus species. Archives of Virology, 162, 1599–1607.
Al Rwahnih, M., Uyemoto, J. K., Falk, B. W., & Rowhani, A. (2007). Molecular characterization and detection of plum bark necrosis stem pitting-associated virus. Archives of Virology, 152, 2197–2206.
Boscia, D., Myrta, A., & Uyemoto, J. K. (2011). Plum bark necrosis stem pitting-associated virus. In A. Hadidi, M. Barba, T. Candresse, & W. Jelkmann (Eds.), Virus and virus-like diseases of pome and stone fruits (pp. 177–179). St. Paul, MN: The American Phytopathological Society.
Cserzo, M., Wallin, E., Simon, I., von Heijne, G., & Elofsson, A. (1997). Prediction of transmembrane α-helices in procaryotic membrane proteins: The dense alignment surface method. Protein Engineering, 10, 673–676.
Domier, L. L. (2012). Family Luteoviridae. In A. M. Q. King, M. J. Adams, E. B. Carstens, & E. J. Lefkowitz (Eds.), Virus taxonomy, ninth report of the international committee on taxonomy of viruses (pp. 1045–1053). San Diego, CA: Academic Press.
El-Gebali, S., Mistry, J., Bateman, A., Eddy, S. R., Luciani, A., Potter, S. C., Qureshi, M., Richardson, L. J., Salazar, G. A., Smart, A., Sonnhammer, E. L. L., Hirsh, L., Paladin, L., Piovesan, D., Tosatto, S. C. E., & Finn, R. D. (2019). The Pfam protein families database in 2019. Nucleic Acids Research, 47, D427–D432.
Imada, J. (2000). Fruit apex disorder, a graft-transmissible of Japanese persimmon. Japanese Journal of Phytopathology, 66, 148 (Abstract in Japanese).
Ito, T., Suzaki, K., & Nakano, M. (2013a). Genetic characterization of novel putative rhabdovirus and dsRNA virus from Japanese persimmon. Journal of General Virology, 94, 1917–1921.
Ito, T., Suzaki, K., Nakano, M., & Sato, A. (2013b). Characterization of a new apscaviroid from American persimmon. Archives of Virology, 158, 2629–2631.
Ito, T., Sato, A., & Suzaki, K. (2015). An assemblage of divergent variants of a novel putative closterovirus from American persimmon. Virus Genes, 51, 105–111.
Janssen, S., & Giegerich, R. (2015). The RNA shapes studio. Bioinformatics, 31, 423–425.
Kanzaki, S. (2016). The origin and cultivar development of Japanese persimmon (Diospyros kaki Thunb.). Nippon Shokuhin Kagaku Kogaku Kaishi, 63, 328–330 (in Japanese with English abstract).
King, A. M. Q., Lefkowitz, E. J., Mushegian, A. R., Adams, M. J., Dutilh, B. E., Gorbalenya, A. E., Harrach, B., Harrison, R. L., Junglen, S., Knowles, N. J., Kropinski, A. M., Krupovic, M., Kuhn, J. H., Nibert, M. L., Rubino, L., Sabanadzovic, S., Sanfaçon, H., Siddell, S. G., Simmonds, P., Varsani, A., Zerbini, F. M., & Davison, A. J. (2018). Changes to taxonomy and the international code of virus classification and nomenclature ratified by the international committee on taxonomy of viruses (2018). Archives of Virology, 163, 2601–2631.
Kusano, N., & Shimomura, K. (1994). Occurrence of a graft-transmissible disease of persimmon. Annals of the Phytopathological Society of Japan, 60, 739 (Abstract in Japanese).
Marais, A., Faure, C., Couture, C., Bergey, B., Gentit, P., & Candresse, T. (2014). Characterization by deep sequencing of divergent Plum bark necrosis stem pitting-associated virus (PBNSPaV) isolates and development of a broad-spectrum PBNSPaV detection assay. Phytopathology, 104, 660–666.
Martelli, G. P., Abou Ghanem-Sabanadzovic, N., Agranovsky, A. A., Al Rwahnih, M., Dolja, V. V., Dovas, C. I., Fuchs, M., Gugerli, P., Hu, J. S., Jelkmann, W., Katis, N. I., Maliogka, V. I., Melzer, M. J., Menzel, W., Minafra, A., Rott, M. E., Rowhani, A., Sabanadzovic, S., & Saldarelli, P. (2012). Taxonomic revision of the family Closteroviridae with special reference to the grapevine leafroll-associated members of the genus Ampelovirus and the putative species unassigned to the family. Journal of Plant Pathology, 94, 7–19.
Morelli, M., Chiumenti, M., La Notte, P., Minafra, A., & Martelli, G. P. (2014). First report of persimmon virus A in Italy. Journal of Plant Pathology, 96, 610.
Morelli, M., Chiumenti, M., De Stradis, A., La Notte, P., & Minafra, A. (2015). Discovery and molecular characterization of a new cryptovirus dsRNA genome from Japanese persimmon through conventional cloning and high-throughput sequencing. Virus Genes, 50, 160–164.
Nakaune, R., & Nakano, M. (2006). Efficient methods for sample processing and cDNA synthesis by RT-PCR for the detection of grapevine viruses and viroids. Journal of Virological Methods, 134, 244–249.
Nakaune, R., & Nakano, M. (2008). Identification of a new Apscaviroid from Japanese persimmon. Archives of Virology, 153, 969–972.
Owens, R. A., Flores, R., Di Serio, F., Li, S.-F., Pallás, V., Randles, J. W., Sano, T., & Vidalakis, G. (2012). Viroids. In A. M. Q. King, M. J. Adams, E. B. Carstens, & E. J. Lefkowitz (Eds.), Virus taxonomy, ninth report of the international committee on taxonomy of viruses (pp. 1221–1234). San Diego, CA: Academic Press.
Qu, L., Cui, H., Wu, G., Zhou, J., Su, J., Wang, G., & Hong, N. (2014). Genetic diversity and molecular evolution of Plum bark necrosis stem pitting-associated virus from China. PLoS One, 9, e105443.
Sato, A., & Yamada, M. (2016). Persimmon breeding in Japan for pollination-constant non-astringent (PCNA) type with marker-assisted selection. Breeding Science, 66, 60–68.
Sato, A., Yamada, M., Kono, A., Mitani, N., Ban, Y., Ueno, T., Shiraishi, M., Onoue, N., Iwanami, H., & Yoshioka, M. (2019). New persimmon cultivar ‘Reigyoku’. Bulletin of the NARO, Fruit Tree and Tea Science, 3, 75–89 (in Japanese with English abstract).
Scott, S. W., & Payne, J. A. (1988). Decline of oriental persimmon. Phytopathology, 78, 1568.
Shimizu, S., Ito, T., Miyoshi, T., Tachibana, Y., & Ito, T. (2011). A broad spectrum, one-step RT-PCR to detect Satsuma dwarf virus variants using universal primers targeting both segmented RNAs 1 and 2. Journal of General Plant Pathology, 77, 326–330.
Theis, C., Reeder, J., & Giegerich, R. (2008). KnotInFrame: Prediction of −1 ribosomal frameshift events. Nucleic Acids Research, 36, 6013–6020.
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.
Thompson, J. R., Dasgupta, I., Fuchs, M., Iwanami, T., Karasev, A. V., Petrzik, K., Sanfaçon, H., Tzanetakis, I., van der Vlugt, R., Wetzel, T., Yoshikawa, N., & ICTV Report Consortium. (2017). ICTV virus taxonomy profile: Secoviridae. Journal of General Virology, 98, 529–531.
Xiang, H.-Y., Dong, S.-W., Shang, Q.-X., Zhou, C.-J., Li, D.-W., Yu, J.-L., & Han, C.-G. (2011). Molecular characterization of two genotypes of a new polerovirus infecting brassicas in China. Archives of Virology, 156, 2251–2255.
Yanase, H., Umemoto, S., Kume, Y., & Saigusa, M. (1992). Occurrence of a new graft-transmissible disease of kaki, kaki dwarf. Annals of the Phytopathological Society of Japan, 58, 618–619 (abstract in Japanese).
Acknowledgements
We acknowledge A. Kono, N. Onoue, and M. Nishimura in NARO for the genotyping of persimmon seedlings and useful advices. We also acknowledge all researchers that provided us with ‘Reigyoku’ samples and evaluated tree growth. This study was funded by NARO.
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Both authors contributed to the study conception and design and preparation of the materials. Data collection and analysis were performed by Takao Ito. The first draft of the manuscript was written by Takao Ito and Akihiko Sato commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Both authors belong to NARO. The authors declare that they have no conflict of interest.
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Ito, T., Sato, A. Three novel viruses detected from Japanese persimmon ‘Reigyoku’ associated with graft-transmissible stunt. Eur J Plant Pathol 158, 163–175 (2020). https://doi.org/10.1007/s10658-020-02063-0
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DOI: https://doi.org/10.1007/s10658-020-02063-0