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http://dx.doi.org/10.5423/PPJ.OA.03.2022.0047

Metatranscriptomic Analysis of Plant Viruses in Imported Pear and Kiwifruit Pollen  

Lee, Hyo-Jeong (Department of Applied Biology, Institute of Environmentally Friendly Agriculture, Chonnam National University)
Jeong, Rae-Dong (Department of Applied Biology, Institute of Environmentally Friendly Agriculture, Chonnam National University)
Publication Information
The Plant Pathology Journal / v.38, no.3, 2022 , pp. 220-228 More about this Journal
Abstract
Pollen is a vector for viral transmission. Pollenmediated viruses cause serious economic losses in the fruit industry. Despite the commercial importance of pollen-associated viruses, the diversity of such viruses is yet to be fully explored. In this study, we performed metatranscriptomic analyses using RNA sequencing to investigate the viral diversity in imported apple and kiwifruit pollen. We identified 665 virus-associated contigs, which corresponded to four different virus species. We identified one virus, the apple stem grooving virus, from pear pollen and three viruses, including citrus leaf blotch virus, cucumber mosaic virus, and lychnis mottle virus in kiwifruit pollen. The assembled viral genome sequences were analyzed to determine phylogenetic relationships. These findings will expand our knowledge of the virosphere in fruit pollen and lead to appropriate management of international pollen trade. However, the pathogenic mechanisms of pollen-associated viruses in fruit trees should be further investigated.
Keywords
kiwifruit; pear; pollen; RNA sequencing;
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1 Adams, I. P., Glover, R. H., Monger, W. A., Mumford, R., Jackeviciene, E., Navalinskiene, M., Samuitiene, M. and Boonham, N. 2009. Next-generation sequencing and metagenomic analysis: a universal diagnostic tool in plant virology. Mol. Plant Pathol. 10:537-545.   DOI
2 Al Rwahnih, M., Daubert, S., Urbez-Torres, J. R., Cordero, F. and Rowhani, A. 2011. Deep sequencing evidence from single grapevine plants reveals a virome dominated by mycoviruses. Arch. Virol. 156:397-403.   DOI
3 Card, S. D., Pearson, M. N. and Clover, G. R. G. 2007. Plant pathogens transmitted by pollen. Australas. Plant Pathol. 36:455-461.   DOI
4 Czotter, N., Molnar, J., Szabo, E., Demian, E., Kontra, L., Baksa, I., Szittya, G., Kocsis, L., Deak, T., Bisztray, G., Tusnady, G. E., Burgyan, J. and Varallyay, E. 2018. NGS of virus-derived small RNAs as a diagnostic method used to determine viromes of Hungarian vineyards. Front. Microbiol. 9:122.   DOI
5 Grisoni, M., Marais, A., Filloux, D., Saison, A., Faure, C., Julian, C., Theil, S., Contreras, S., Teycheney, P.-Y., Roumagnac, P. and Candresse, T. 2017. Two novel alphaflexiviridae members revealed by deep sequencing of the vanilla (Orchidaceae) virome. Arch. Virol. 162:3855-3861.   DOI
6 Hadidi, A., Flores, R., Candresse, T. and Barba, M. 2016. Next-generation sequencing and genome editing in plant virology. Front. Microbiol. 7:1325.   DOI
7 Hull, R. 2002. Transmission 2: Mechanical, seed, pollen and epidemiology. In: Mathew's plant virology, ed. by R. Hull, pp. 533-581. Academic Press, New York, USA.
8 Jakovljevic, V., Otten, P., Berwarth, C. and Jelkmann, W. 2017. Analysis of the apple rubbery wood disease by next generation sequencing of total RNA. Eur. J. Plant Pathol. 148:637-646.   DOI
9 Jo, Y. and Cho, W. K. 2018. RNA viromes of the oriental hybrid lily cultivar "Sorbonne". BMC Genomics 19:748.   DOI
10 Jo, Y., Choi, H., Kim, S.-M., Kim, S.-L., Lee, B. C. and Cho, W. K. 2017. The pepper virome: natural co-infection of diverse viruses and their quasispecies. BMC Genomics 18:453.   DOI
11 Hull, R., 2013. Plant virology. Academic Press, San Diego, CA, USA. 1118 pp.
12 Kim, N.-Y., Lee, H-.J., Kim, H.-S., Lee, S.-H., Moon, J.-S. and Jeong, R.-D. 2021. Identification of plant viruses infecting pear using RNA sequencing. Plant Pathol. J. 37:258-267.   DOI
13 Akinyemi, I. A., Wang, F., Zhou, B., Qi, S. and Wu, Q. 2016. Ecogenomic survey of plant viruses infecting tobacco by next generation sequencing. Virol. J. 13:181.   DOI
14 Isogai, M., Shimoda, R., Nishimura, H. and Yaegashi, H. 2022. Pollen grains infected with apple stem grooving virus serve as a vector for horizontal transmission of the virus. J. Gen. Plant Pathol. 88:81-87.   DOI
15 Al Rwahnih, M., Daubert, S., Golino, D. and Rowhani, A. 2009. Deep sequencing analysis of RNAs from a grapevine showing Syrah decline symptoms reveals a multiple virus infection that includes a novel virus. Virology 387:395-401.   DOI
16 Blouin, A. G., Pearson, M. N., Chavan, R. R., Woo, E. N. Y., Lebas, B. S. M., Veerakone, S., Ratti, C., Biccheri, R., Mac-Diarmid, R. M. and Cohen, D. 2013. Viruses of kiwifruit (Actinidia species). J. Plant Pathol. 95:221-235.
17 Desvignes, J. C. 1985. Peach latent mosaic and its relation to peach mosaic and peach yellow mosaic virus diseases. Acta Hortic. 193:51-58.   DOI
18 Hernandez, C. and Flores, R. 1992. Plus and minus RNAs of peach latent mosaic viroid self-cleave in vitro via hammerhead structures. Proc. Natl. Acad. Sci. U. S. A. 89:3711-3715.   DOI
19 Osman, F., Hodzic, E., Kwon, S.-J., Wang, J. and Vidalakis, G. 2015. Development and validation of a multiplex reverse transcription quantitative PCR (RT-qPCR) assay for the rapid detection of citrus tristeza virus, citrus psorosis virus, and citrus leaf blotch virus. J. Virol. Methods 220:64-75.   DOI
20 Massart, S., Olmos, A., Jijakli, H. and Candresse, T. 2014. Current impact and future directions of high throughput sequencing in plant virus diagnostics. Virus Res. 188:90-96.   DOI
21 Jonghe, K. D., Haegeman, A., Foucart, Y. and Maes, M. 2018. The use of high-throughput sequencing for the study and diagnosis of plant viruses and viroids in pollen. Methods Mol. Biol. 17446:131-149.
22 Jo, Y., Bae, J.-Y., Kim, S.-M., Choi, H., Lee, B. C. and Cho, W. K. 2018a. Barley RNA viromes in six different geographical regions in Korea. Sci. Rep. 81:13237.
23 Jo, Y., Choi, H., Lian, S., Cho, J. K., Chu, H. and Cho, W. K. 2020. Identification of viruses infecting six plum cultivars in Korea by RNA-sequencing. PeerJ 8:e9588.   DOI
24 Jo, Y., Song, M.-K., Choi, H., Park, J.-S., Lee, J.-W., Cho, W. K. and Kim, K.-H. 2018c. In silico identification of viruses and viroids infecting grapevine cultivar cabernet sauvignon using a grapevine transcriptome. J. Plant Pathol. 100:91-96.   DOI
25 Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. and Drummond, A. 2012. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647-1649.   DOI
26 Kim, M.-K., Kwak, H.-R., Lee, S.-H., Kim, J.-S., Kim, K.-H., Cha, B. and Choi, H.-S. 2011. Characteristics of cucumber mosaic virus isolated from Zea mays in Korea. Plant Pathol J. 27:372-377.   DOI
27 Kim, N.-K., Lee, H.-J., Kim, S.-M. and Jeong, R.-D. 2022. Identification of viruses infecting oats in Korea by metatranscriptomics. Plants 11:256.   DOI
28 Kreuze, J. F., Perez, A., Untiveros, M., Quispe, D., Fuentes, S., Barker, I. and Simon, R. 2009. Complete viral genome sequence and discovery of novel viruses by deep sequencing of small RNAs: a generic method for diagnosis, discovery and sequencing of viruses. Virology 388:1-7.   DOI
29 Martin, R. R., Constable, F. and Tzanetakis, I. E. 2016. Quarantine regulations and the impact of modern detection methods. Annu. Rev. Phytopathol. 54:189-205.   DOI
30 Maliogka, V. I., Minafra, A., Saldarelli, P., Ruiz-Garcia, A. B., Glasa, M., Katis, N. and Olmos, A. 2018. Recent advances on detection and characterization of fruit tree viruses using high-throughput sequencing technologies. Viruses 10:436.   DOI
31 Malandraki, I., Beris, D., Isaioglou, I., Olmos, A., Varveri, C. and Vassilakos, N. 2017. Simultaneous detection of three Pome fruit tree viruses by one-step multiplex quantitative RT-PCR. PLoS ONE 12:e0180877.   DOI
32 Li, Y., Jia, A., Qiao, Y., Xiang, J., Zhang, Y. and Wang, W. 2018. Virome analysis of lily plants reveals a new potyvirus. Arch. Virol. 163:1079-1082.   DOI
33 Lopez, M. M., Bertolini, E., Olmos, A., Caruso, P., Gorris, M. T., Llop, P., Penyalver, R. and Cambra, M. 2003. Innovative tools for detection of plant pathogenic viruses and bacteria. Int. Microbiol. 64:233-243.
34 Lu, Y., Yao, B., Wang, G. and Hong, N. 2018. The detection of ACLSV and ASPV in pear plants by RT-LAMP assays. J. Virol. Methods 252:80-85.   DOI
35 Osaki, H., Yamaguchi, M., Sato, Y., Tomita, Y., Kawai, Y., Miyamoto, Y. and Ohtsu, Y. 1999. Peach latent mosaic viroid isolated from stone fruits in Japan. Ann. Phytopathol. Soc. Jpn. 65:3-8.   DOI
36 Matsumura, E. E., Coletta-Filho, H. D., Nouri, S., Falk, B. W., Nerva, L., Oliveira, T. S., Dorta, S. O. and Machado, M. A. 2017. Deep sequencing analysis of RNAs from citrus plants grown in a citrus sudden death-affected area reveals diverse known and putative novel viruses. Viruses 9:92.   DOI
37 Huang, B., Jennison, A., Whiley, D., McMahon, J., Hewitson, G., Graham, R., De Jong, A. and Warrilow, D. 2019. Illumina sequencing of clinical samples for virus detection in a public health laboratory. Sci. Rep. 9:5409.   DOI
38 Morgulis, A., Coulouris, G., Raytselis, Y., Madden, T. L., Agarwala, R. and Schaffer, A. A. 2008. Database indexing for production MegaBLAST searches. Bioinformatics 24:1757-1764.   DOI
39 Massart, S., Candresse, T., Gil, J., Lacomme, C., Predajna, L., Ravnikar, M., Reynard, J.-S., Rumbou, A., Saldarelli, P., Skoric, D., Vainio, E. J., Valkonen, J. P. T., Vanderschuren, H., Varveri, C. and Wetzel, T. 2017. A framework for the evaluation of biosecurity, commercial, regulatory, and scientific impacts of plant viruses and viroids identified by NGS technologies. Front. Microbiol. 8:45.
40 Mink, G. I. 1993. Pollen and seed-transmitted viruses and viroids. Annu. Rev. Phytopathol. 31:375-402.   DOI
41 Radford, A. D., Chapman, D., Dixon, L., Chantrey, J., Darby, A. C. and Hall, N. 2012. Application of next-generation sequencing technologies in virology. J. Gen. Virol. 93:1853-1868.   DOI
42 Roossinck, M. J., Martin, D. P. and Roumagnac, P. 2015. Plant virus metagenomics: advances in virus discovery. Phytopathology 105:716-727.   DOI
43 Nabi, S. U., Baranwal, V. K., Rao, G. P., Mansoor, S., Vladulescu, C., Raja, W. H., Jan, B. L. and Alansi, S. 2022. High-throughput RNA sequencing of mosaic infected and non-infected apple (Malus × domestica Borkh.) cultivars: from detection to the reconstruction of whole genome of viruses and viroid. Plants 11:675.   DOI
44 Qian, Y., Xu, Y., Zhou, Q. and Zhou, X. 2014. Application of next-generation sequencing technology for plant virus identification. Sci. Sin. Vitae 44:351-363.   DOI
45 Rivarez, M. P. S., Vucurovic, A., Mehle, N., Ravnikar, M. and Kutnjak, D. 2021. Global advances in tomato virome research: current status and the impact of high-throughput sequencing. Front. Microbiol. 12:671925.   DOI
46 Shamloul, A. M., Minafra, A., Hadidi, A., Waterworth, H. E., Giunchedi, L. and Allam, E. K. 1994. Peach latent mosaic viroid: nucleotide sequence of an Italian isolate, sensitive detection using RT-PCR and geographic distribution. Acta Hortic. 386:522-530.   DOI
47 Shim, H., Min, Y., Hong, S., Kwon, M., Kim, D., Kim, H., Choi, Y., Lee, S. and Yang, J. 2004. Nucleotide sequences of a Korean isolate of apple stem grooving virus associated with black necrotic leaf spot disease on pear (Pyrus pyrifolia). Mol. Cells 18:192-199.
48 Thompson, J. D., Gibson, T. J. and Higgins, D. G. 2003. Multiple sequence alignment using ClustalW and ClustalX. Curr. Protoc. Bioinformatics 2:2.3.1-2.3.22.
49 Torrance, L. and Jones, R. A. C. 1981. Recent developments in serological methods suited for use in routine testing for plant viruses. Plant Pathol. 30:1-24.   DOI
50 Shaffer, C., Gress, J. C. and Tzanetakis, I. E. 2019. First report of cycas necrotic stunt virus and lychnis mottle virus in peony in the United States. Plant Dis. 103:1048.
51 Wright, A. A., Cross, A. R. and Harper, S. J. 2020. A bushel of viruses: identification of seventeen novel putative viruses by RNA-seq in six apple trees. PLoS ONE 15:e0227669.   DOI
52 Wylie, S. J., Li, H., Saqib, M. and Jones, M. G. K. 2014. The global trade in fresh produce and the vagility of plant viruses: a case study in garlic. PLoS ONE 98:e105044.
53 Zhang, P., Liu, Y., Liu, W., Cao, M., Massart, S. and Wang, X. 2017. Identification, characterization and full-length sequence analysis of a novel polerovirus associated with wheat leaf yellowing disease. Front. Microbiol. 8:1689.   DOI
54 Jo, Y., Lian, S., Chu, H., Cho, J. K., Yoo, S.-H., Choi, H., Yoon, J.-Y., Choi, S.-K., Lee, B. C. and Cho, W. K. 2018b. Peach RNA viromes in six different peach cultivars. Sci. Rep. 8:1844.   DOI
55 Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.   DOI
56 Villamor, D. E. V., Ho, T., Al Rwahnih, M., Martin, R. R. and Tzanetakis, I. E. 2019. High throughput sequencing for plant virus detection and discovery. Phytopathology 109:716-725.   DOI
57 Yoo, R. H., Zhao, F., Lim, S., Igori, D., Lee, S.-H. and Moon, J. S. 2015. The complete nucleotide sequence and genome organization of lychnis mottle virus. Arch. Virol. 160:2891-2894.   DOI