Browse > Article
http://dx.doi.org/10.5423/PPJ.OA.06.2022.0084

Nanopore Metagenomics Sequencing for Rapid Diagnosis and Characterization of Lily Viruses  

Lee, Hyo-Jeong (Department of Applied Biology, Institute of Environmentally Friendly Agriculture, Chonnam National University)
Cho, In-Sook (Horticultural and Herbal Crop Environment Division, National Institute of Horticultural and Herbal Science, Rural Development Administration)
Jeong, Rae-Dong (Department of Applied Biology, Institute of Environmentally Friendly Agriculture, Chonnam National University)
Publication Information
The Plant Pathology Journal / v.38, no.5, 2022 , pp. 503-512 More about this Journal
Abstract
Lilies (Lilium spp.) are one of the most important ornamental flower crops grown in Korea. Most viral diseases in lilies are transmitted by infected bulbs, which cause serious economic losses due to reduced yields. Various diagnostic techniques and high-throughput sequencing methods have been used to detect lily viruses. According to Oxford Nanopore Technologies (ONT), MinION is a compact and portable sequencing device. In this study, three plant viruses, lily mottle, lily symptomless, and plantago asiatica mosaic virus, were detected in lily samples using the ONT platform. As a result of genome assembly of reads obtained through ONT, 100% coverage and 90.3-93.4% identity were obtained. Thus, we show that the ONT platform is a promising tool for the diagnosis and characterization of viruses that infect crops.
Keywords
diagnosis; lily; nanopore sequencing; viruses;
Citations & Related Records
Times Cited By KSCI : 6  (Citation Analysis)
연도 인용수 순위
1 Kwon, J. Y., Ryu, K. H. and Choi, S. H. 2013. Reverse transcription polymerase chain reaction-based system for simultaneous detection of multiple lily-infecting viruse. Plant Pathol. J. 29:338-343.   DOI
2 Komatsu, K., Yamaji, Y., Ozeki, J., Hashimoto, M., Kagiwada, S., Takahashi, S. and Namba, S. 2008. Nucleotide sequence analysis of seven Japanese isolates of Plantago asiatica mosaic virus (PlAMV): a unique potexvirus with significantly high genomic and biological variability within the species. Arch. Virol. 153:193-198.   DOI
3 Lewandowski, K., Xu, Y., Pullan, S. T., Lumley, S. F., Foster, D., Sanderson, N., Vaughan, A., Morgan, M., Bright, N., Kavanagh, J., Vipond, R., Carroll, M., Marriott, A. C., Gooch, K. E., Andersson, M., Jeffery, K., Peto, T., Crook, D. W., Walker, A. S. and Matthews, P. C. 2019. Metagenomic nanopore sequencing of influenza virus direct from clinical respiratory samples. J. Clin. Microbiol. 58:e00963-e00919.
4 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
5 Liefting, L. W., Waite, D. W. and Thompson, J. R. 2021. Application of oxford nanopore technology to plant virus detection. Viruses 13:1424.
6 Lim, M. S., Kim, S. M. and Choi, S. H. 2016. Simultaneous detection of three lily-infecting viruses using a multiplex Luminex bead array. J. Virol. Methods 231:34-37.   DOI
7 Maestri, S., Cosentino, E., Paterno, M., Freitag, H., Garces, J. M., Marcolungo, L., Alfano, M., Njunjic, I., Schilthuizen, M., Slik, F., Menegon, M., Rossato, M. and Delledonne, M. 2019. A rapid and accurate MinION-based workflow for tracking species biodiversity in the field. Genes 10:468.
8 Cao, Y., Li, J., Chu, X., Liu, H., Liu, W. and Liu, D. 2019. Nanopore sequencing: a rapid solution for infectious disease epidemics. Sci. China Life Sci. 62:1101-1103.   DOI
9 Chang, J. J. M., Ip, Y. C. A., Bauman, A. G. and Huang, D. 2020. MinION-in-ARMS: nanopore sequencing to expedite barcoding of specimen-rich macrofaunal samples from autonomous reef monitoring structures. Front. Mar. Sci. 7:448.
10 Choi, S. A. and Ryu, K. H. 2003. The complete nucleotide sequence of the genome RNA of Lily symptomless virus and its comparison with that of other carlaviruses. Arch. Virol. 148:1943-1955.   DOI
11 Della Bartola, M., Byrne, S. and Mullins, E. 2020. Characterization of potato virus y isolates and assessment of nanopore sequencing to detect and genotype potato viruses. Viruses 12:478.
12 Fellers, J. P., Webb, C., Fellers, M. C., Shoup Rupp, J. and De Wolf, E. 2019. Wheat virus identification within infected tissue using nanopore sequencing technolog. Plant Dis. 103:2199-2203.   DOI
13 He, X., Xue, F., Xu, S. and Wang, W. 2016. Rapid and sensitive detection of Lily symptomless virus by reverse transcription loop-mediated isothermal amplification. J. Virol. Methods 238:38-41.   DOI
14 Kim, J. H., Yoo, H. N., Bae, E. H. and Jung, Y.-T. 2012. Development of an indirect ELISA and immunocapture rt-PCR for lily virus detection. J. Microbiol. Biotechnol. 22:1776-1781.   DOI
15 Eid, J., Fehr, A., Gray, J., Luong, K., Lyle, J., Otto, G., Peluso, P., Rank, D., Baybayan, P., Bettman, B., Bibillo, A., Bjornson, K., Chaudhuri, B., Christians, F., Cicero, R., Clark, S., Dalal, R., Dewinter, A., Dixon, J., Foquet, M., Gaertner, A., Hardenbol, P., Heiner, C., Hester, K., Holden, D., Kearns, G., Kong, X., Kuse, R., Lacroix, Y., Lin, S., Lundquist, P., Ma, C., Marks, P., Maxham, M., Murphy, D., Park, I., Pham,T., Phillips, M., Roy, J., Sebra, R., Shen, G., Sorenson, J., Tomaney, A., Travers, K., Trulson, M., Vieceli, J., Wegener, J., Wu, D., Yang, A., Zaccarin, D., Zhao, P., Zhong, F., Korlach, J. and Turner, S. 2009. Real-time DNA sequencing from single polymerase molecules. Science 323:133-138.
16 Javaran, V. J., Moffett, P., Lemoyne, P., Xu, D., Adkar-Purushothama, C. R. and Fall, M. L. 2021. Grapevine virology in the third-generation sequencing era: from virus detection to viral epitranscriptomics. Plants 10:2355.
17 Jo, Y. and Cho, W. K. 2018. RNA viromes of the oriental hybrid lily cultivar "Sorbonne". BMC Genomics 19:748.
18 Amoia, S. S., Minafra, A., Nicoloso, V., Loconsole, G. and Chiumenti, M. A. 2022. A new jasmine virus C isolate identified by nanopore sequencing is associated to yellow mosaic symptoms of Jasminum officinale in Italy. Plants 11:309.
19 Faria, N. R., Quick, J., Claro, I. M., Theze, J., de Jesus, J. G., Giovanetti, M., Kraemer, M., Hill, S. C., Black, A., da Costa, A. C., Franco, L. C., Silva, S. P., Wu, C. H., Raghwani, J., Cauchemez, S., du Plessis, L., Verotti, M. P., de Oliveira, W. K., Carmo, E. H., Coelho, G. E., Santelli, A. C. F. S., Vinhal, L. C., Henriques, C. M., Simpson, J. T., Loose, M., Andersen, K. G., Grubaugh, N. D., Somasekar, S., Chiu, C. Y., Munoz-Medina, J. E., Gonzalez-Bonilla, C. R., Arias, C. F., Lewis-Ximenez, L. L., Baylis, S. A., Chieppe, A. O., Aguiar, S. F., Fernandes, C. A., Lemos, P. S., Nascimento, B. L. S., Monteiro, H. A. O., Siqueira, I. C., de Queiroz, M. G., de Souza, T. R., Bezerra, J. F., Lemos, M. R., Pereira, G. F., Loudal, D., Moura, L. C., Dhalia, R., Franca, R. F., Magalhaes, T., Marques, E. T. Jr, Jaenisch, T., Wallau, G. L., de Lima, M. C., Nascimento, V., de Cerqueira, E. M., de Lima, M. M., Mascarenhas, D. L., Neto, J. P. M., Levin, A. S., Tozetto-Mendoza, T. R., Fonseca, S. N., Mendes-Correa, M. C., Milagres, F. P., Segurado, A., Holmes, E. C., Rambaut, A., Bedford, T., Nunes, M. R. T., Sabino, E. C., Alcantara, L. C. J., Loman, N. J. and Pybus, O. G. 2017. Establishment and cryptic transmission of Zika virus in Brazil and the Americas. Nature 546:406-410.
20 Jain, M., Fiddes, I. T., Miga, K. H., Olsen, H. E., Paten, B. and Akeson, M. 2015. Improved data analysis for the MinION nanopore sequencer. Nat. Methods 12:351-356.   DOI
21 Asjes, C. J. 2000. Control of aphid-borne Lily symptomless virus and Lily mottle virus in Lilium in the Netherlands. Virus Res. 71:23-32.   DOI
22 Barzon, L., Lavezzo, E., Militello, V., Toppo, S. and Palu, G. 2011. Applications of next-generation sequencing technologies to diagnostic virology. Int. J. Mol. Sci. 12:7861-7884.   DOI
23 Deamer, D., Akeson, M. and Branton, D. 2016. Three decades of nanopore sequencing. Nat. Biotechnol. 34:518-524.   DOI
24 Batovska, J., Lynch, S. E., Rodoni, B. C., Sawbridge, T. I. and Cogan, N. O. 2017. Metagenomic arbovirus detection using MinION nanopore sequencing. J. Virol. Methods 249:79-84.   DOI
25 Ben Chehida, S., Filloux, D., Fernandez, E., Moubset, O., Hoareau, M., Julian, C., Blondin, L., Lett, J.-M., Roumagnac, P. and Lefeuvre, P. 2021. Nanopore sequencing is a credible alternative to recover complete genomes of geminiviruses. Microorganisms 9:903.
26 Boykin, L. M., Ghalab, A., De Marchi, B. R., Savill, A., Wainaina, J. M., Kinene, T., Lamb, S., Rodrigues, M., Kehoe, M., Ndunguru, J., Tairo, F., Sseruwagi, P., Kayuki, C., Mark, D., Erasto, J., Bachwenkizi, H., Alicai, T., Okao-Okuja, G., Abidrabo, P., Osingada, J. F., Akono, J., Ateka, E., Muga, B. and Kiarie, S. 2018. Real time portable genome sequencing for global food security. bioRxiv preprint at https://doi.org/10.1101/314526.   DOI
27 Bronzato Badial, A., Sherman, D., Stone, A., Gopakumar, A., Wilson, V., Schneider, W. and King, J. 2018. Nanopore sequencing as a surveillance tool for plant pathogens in plant and insect tissues. Plant Dis. 102:1648-1652.   DOI
28 Aboul-Ata, A. A., Mazyad, H., El-Attar, A. K., Soliman, A. M., Anfoka, G., Zeidan, M., Gorovits, R., Sobol, I. and Czosnek, H. 2011. Diagnosis and control of cereal viruses in the Middle East. Adv. Virus Res. 81:33-61.   DOI
29 Boykin, L. M., Sseruwagi, P., Alicai, T., Ateka, E., Mohammed, I. U., Stanton, J. L., Kayuki, C., Mark, D., Fute, T., Erasto, J., Bachwenkizi, H., Muga, B., Mumo, N., Mwangi, J., Abidrabo, P., Okao-Okuja, G., Omuut, G., Akol, J., Apio, H. B., Osingada, F., Kehoe, M. A., Eccles, D., Savill, A., Lamb, S., Kinene, T., Rawle, C. B., Muralidhar, A., Mayall, K., Tairo, F. and Ndunguru, J. 2019. Tree lab: portable genomics for early detection of plant viruses and pests in sub-saharan africa. Genes 10:632.
30 Chalupowicz, L., Dombrovsky, A., Gaba, V., Luria, N., Reuven, M., Beerman, A., Lachman, O., Dror, O., Nissan, G. and Manulis-Sasson, S. 2019. Diagnosis of plant diseases using the Nanopore sequencing platform. Plant Pathol. 68:229-238.   DOI
31 Fang, Y. and Ramasamy, R. P. 2015. Current and prospective methods for plant disease detection. Biosensors 5:537-561.   DOI
32 Filloux, D., Fernandez, E., Loire, E., Claude, L., Galzi, S., Candresse, T., Winter, S., Jeeva, M. L., Makeshkumar, T., Martin, D. P. and Roumagnac, P. 2018. Nanopore-based detection and characterization of yam viruses. Sci. Rep. 8:17879.
33 Jang, H. and Kim, S. 2016. Analysis of the economic value of the production of lily bulbs in Korea. Korean J. Agric. Sci. 43:481-495 (in Korean).
34 Kang, Y.-I., Joung, H. Y., Goo, D. H., Choi, Y. J., Choi, M. P., An, H. R., Ko, J.-Y., Choi, K.-J., Lee, K. H. and Hong, K. W. 2013. A survey on cut flower cultivar trends and horticultural status of lilies (Lilium hybrids) in South Korea. HortTechnology 23:629-634.   DOI
35 Kumar, S., Stecher, G., Li, M., Knyaz, C. and Tamura, K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35:1547-1549.   DOI
36 Vazquez-Iglesias, I., McGreig, S., Pufal, H., Robinson, R., Clover, G. R. G., Fox, A., Boonham, N. and Adams, I. P. 2022. A novel high-throughput sequencing approach reveals the presence of a new virus infecting Rosa: rosa ilarvirus-1 (RIV-1). J. Virol. Methods 300:114417.
37 Quick, J., Loman, N. J., Duraffour, S., Simpson, J. T., Severi, E., Cowley, L., Bore, J. A., Koundouno, R., Dudas, G., Mikhail, A., Ouedraogo, N., Afrough, B., Bah, A., Baum, J. H., Becker-Ziaja, B., Boettcher, J. P., Cabeza-Cabrerizo, M., Camino-Sanchez, A., Carter, L. L., Doerrbecker, J., Enkirch, T., Dorival, I. G. G., Hetzelt, N., Hinzmann, J., Holm, T., Kafetzopoulou, L. E., Koropogui, M., Kosgey, A., Kuisma, E., Logue, C. H., Mazzarelli, A., Meisel, S., Mertens, M., Michel, J., Ngabo, D., Nitzsche, K., Pallash, E., Patrono, L. V., Portmann, J., Repits, J. G., Rickett, N. Y., Sachse, A., Singethan, K., Vitoriano, I., Yemanaberhan, R. L., Zekeng, E. G., Trina, R., Bello, A., Sall, A. A., Faye, O., Faye, O., Magassouba, N., Williams, C. V., Amburgey, V., Winona, L., Davis, E., Gerlach, J., Washington, F., Monteil, V., Jourdain, M., Bererd, M., Camara, A., Somlare, H., Camara, A., Gerard, M., Bado, G., Baillet, B., Delaune, D., Nebie, K. Y., Diarra, A., Savane, Y., Pallawo, R. B., Gutierrez, G. J., Milhano, N., Roger, I., Williams, C. J., Yattara, F., Lewandowski, K., Taylor, J., Rachwal, P., Turner, D., Pollakis, G., Hiscox, J. A., Matthews, D. A., O'Shea, M. K., Johnston, A. M., Wilson, D., Hutley, E., Smit, E., Di Caro, A., Woelfel, R., Stoecker, K., Fleischmann, E., Gabriel, M., Weller, S. A., Koivogui, L., Diallo, B., Keita, S., Rambaut, A., Formenty, P., Gunther, S. and Carroll, M. W. 2016. Real-time, portable genome sequencing for Ebola surveillance. Nature 530:228-232.
38 Marcolungo, L., Passera, A., Maestri, S., Segala, E., Alfano, M., Gaffuri, F., Marturano, G., Casati, P., Bianco, P. A. and Delledonne, M. 2022. Real-time on-site diagnosis of quarantine pathogens in plant tissues by nanopore-based sequencing. Pathogens 11:199.
39 Theuns, S., Vanmechelen, B., Bernaert, Q., Deboutte, W., Vandenhole, M., Beller, L., Matthijnssens, J., Maes, P. and Nauwynck, H. J. 2018. Nanopore sequencing as a revolutionary diagnostic tool for porcine viral enteric disease complexes identifies porcine kobuvirus as an important enteric virus. Sci. Rep. 8:9830.
40 van der Want, J. P. and Dijkstra, J. 2006. A history of plant virology. Arch. Virol. 151:1467-1498.   DOI
41 Zhang, Y., Wang, Y., Xie, Z., Yang, G., Guo, Z. and Wang, L. 2017. Simultaneous detection of three lily viruses using triplex IC-RT-PCR. J. Virol. Methods 249:69-75.   DOI
42 Zhang, Y., Wang, Y., Yang, W., Xie, Z., Wang, R., Kutcher, H. R. and Guo, Z. 2015b. A rapid immunochromatographic test to detect the lily mottle virus. J. Virol. Methods 220:43-48.   DOI
43 Zhang, Y., Xie, Z., Wang, Y., Wang, R., Guo, Z., Qiu, Y. and He, Y. 2022. Development of immunocapture reverse transcription loop-mediated isothermal amplification assays to detect both lily symptomless virus and cucumber mosaic virus. Ann. Appl. Biol. 180:132-139.   DOI
44 Zhu, X., Yan, S., Yuan, F. and Wan, S. 2020. The applications of nanopore sequencing technology in pathogenic microorganism detection. Can. J. Infect. Dis. Med. Microbiol. 2020:6675206.
45 Tamura, K., Nei, M. and Kumar, S. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. U. S. A. 101:11030-11035.   DOI
46 Mehetre, G. T., Leo, V. V., Singh, G., Sorokan, A., Maksimov, I., Yadav, M. K., Upadhyaya, K., Hashem, A., Alsaleh, A. N., Dawoud, T. M., Almaary, K. S. and Singh, B. P. 2021. Current developments and challenges in plant viral diagnostics: a systematic review. Viruses 13:412.
47 Naito, F., Melo, F. L., Fonseca, M., Santos, C., Chanes, C. R., Ribeiro, B. M., Gilbertson, R. L., Boiteux, L. S. and de Cassia Pereira-Carvalho, R. 2019. Nanopore sequencing of a novel bipartite New World begomovirus infecting cowpea. Arch. Virol. 164:1907-1910.   DOI
48 Phannareth, T., Nunziata, S. O., Stulberg, M. J., Galvez, M. E. and Rivera, Y. 2020. Comparison of nanopore sequencing protocols and real-time analysis for phytopathogen diagnostics. Plant Health Prog. 22:31-36.
49 Zhao, B., Yang, D., Zhang, Y., Xu, Y., Zhao, X., Liang, J., Fan, X., Du, Y., Zhu, Z., Shi, B., Zhang, Q., Zhang, X., Cai, Y. and Zhao, K. 2018. Rapid visual detection of lily mottle virus using a loop-mediated isothermal amplification method. Arch. Virol. 163:545-548.   DOI
50 Niimi, Y., Han, D.-S., Mori, S. and Kobayashi, H. 2003. Detection of cucumber mosaic virus, lily symptomless virus and lily mottle virus in Lilium species by RT-PCR technique. Sci. Hortic. 97:57-63.   DOI
51 Ryu, K. H., Park, H. W. and Park, J. K. 2002. Characterization and sequence analysis of a lily isolate of Cucumber mosaic virus from Lithium tsingtauense. Plant Pathol J. 18:85-92.   DOI
52 Sharma, A., Mahinghara, B. K., Singh, A. K., Kulshrestha, S., Raikhy, G., Singh, L., Verma, N., Hallan, V., Ram, R. and Zaidi, A. A. 2005. Identification, detection and frequency of lily viruses in Northern India. Sci. Hortic. 106:213-227.   DOI
53 Wang, M., Fu, A., Hu, B., Tong, Y., Liu, R., Liu, Z., Gu, J., Xiang, B., Liu, J., Jiang, W., Shen, G., Zhao, W., Men, D., Deng, Z., Yu, L., Wei, W., Li, Y. and Liu, T. 2020. Nanopore targeted sequencing for the accurate and comprehensive detection of SARS-CoV-2 and other respiratory viruses. Small 16:e2002169.
54 Wang, R., Wang, G., Zhao, Q., Zhu, Y., Zhan, J., Xie, Z., An, L. and Wang, Y. 2010. Molecular and cytopathologic evidences for a mixed infection of multiple viruses on Lanzhou lily (Lilium davidii var. unicolor) in Northwestern China. J. Plant Dis. Prot. 117:145-149.   DOI
55 Zhang, Y., Wang, Y., Meng, J., Xie, Z., Wang, R., Kutcher, H. R. and Guo, Z. 2015a. Development of an immunochromatographic strip test for rapid detection of lily symptomless virus. J. Virol. Methods 220:13-17.   DOI
56 Temmam, S., Davoust, B., Berenger, J. M., Raoult, D. and Desnues, C. 2014. Viral metagenomics on animals as a tool for the detection of zoonoses prior to human infection? Int. J. Mol. Sci. 15:10377-10397.   DOI
57 Zhang, Y., Wang, Y., Xie, Z., Wang, R., Guo, Z. and He, Y. 2020. Rapid detection of Lily mottle virus and Arabis mosaic virus infecting lily (Lilium spp.) using reverse transcription loopmediated isothermal amplification. Plant Pathol. J. 36:170-178.   DOI
58 Tarquini, G., Martini, M., Maestri, S., Firrao, G. and Ermacora, P. 2022. The virome of 'Lamon Bean': application of MinION sequencing to investigate the virus population associated with symptomatic beans in the Lamon Area, Italy. Plants 11:779.