High-Throughput Sequencing for Plant Virome Characterization: A Mini-Review

Abstract

Plant viruses and viroids cause extensive losses with reduction in crop productivity worldwide. The emergence of high-throughput sequencing technologies, commonly referred to as ‘Next-generation sequencing’ together with the metagenomics approach has led to a rapid increase in our understanding of plant viral communities. The utilization of high throughput NGS technologies has proven to be effective in the detection of previously unidentified disease-associated with new pathogens including viruses. Virome analysis using high-throughput sequencing technologies leads to the exploration of different viruses. These technologies, in combination with automation, artificial intelligence can allow for the efficient utilization of plant disease clinics in virome diagnostics. High-throughput sequencing methods have advantages of identification and genomic characterization of viruses and are important for diversity studies of plant viromes. Plant virome studies have the capability to carry out the detection of unknown viruses in mixed infection to reveal the presence of novel viruses. Further, the new machine learning/deep learning tools have enabled the detection of new viral sequences in already available host nucleotide sequences, enabling us to identify lysogenic viruses. In the era of metagenomics, plant-specific virome studies will help in checking the potential epiphytotic soon. Therefore, the present review highlights the successful utilization of high-throughput sequencing technologies in characterizing plant virome.

Keywords

metagenomics / next generation sequencing / viral communities / deep learning

References

[1] Ahmadian, A., Ehn, M. and Hober, S. (2006). Pyrosequencing: History, biochemistry and future. Clin. Chim. Acta 363: 83-94.

[2] Ambardar, S., Gupta, R., Trakroo, D., Lal, R. and Vakhlu, J. (2016). High Throughput Sequencing: An Overview of Sequencing Chemistry. Indian J. Microbiol. 56(4): 394-404.

[3] Bag, S., Al Rwahnih, M., Li, A., Gonzalez, A., Rowhani, A., Uyemoto, J. K. and Sudarshana, M. R. (2015). Detection of a new luteovirus in imported nectarine trees: A case study to propose adoption of metagenomics in post-entry quarantine. Phytopathology 105: 840-846.

[4] Barba, M., Czosnek, H. and Hadidi, A. (2014). Historical perspective, development and applications of next-generation sequencing in plant virology. Viruses 6(1): 106-136.

[5] Boonham, N., Glover, R., Tomlinson, J. and Mumford, R. (2008). Exploiting generic platform technologies for the detection and identification of plant pathogens. Eur. J. Plant Pathol. 121: 355-363.

[6] Boonham, N., Kreuze, J., Winter, S., Van der Vlugt, R., Bergervoet, J., Tomlinson, J. and Mumford, R. (2014). Methods in virus diagnostics from ELISA to next generation sequencing. Virus Res. 186: 20-31.

[7] 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.

[8] Chalupowicz, L., Dombrovsky, A., Gaba, V., Luria, N., Reuven, M., Beerman, A. and Manulis- Sasson, S. (2019). Diagnosis of plant diseases using the Nanopore sequencing platform. Plant Pathol. 68(2): 229-238.

[9] Cho, I., Kwon, S., Yoon, J., Chung, B., Hammond, J. and Lim, H. (2017). First report of apple necrotic mosaic virus infecting apple trees in korea. J. Plant Pathol. 99: 815.

[10] Costa, L. C., Atha III, B., Hu, X., Lamour, K., Yang, Y., O’Connell, M., McFarland, C., Foster, J. A. and Hurtado-Gonzales, O. P. (2022). High- throughput detection of a large set of viruses and viroids of pome and stone fruit trees by multiplex PCR-based amplicon sequencing. Front. Plant Sci. 13: 1072768. https://doi.org/10.3389/fpls.2022.1072768.

[11] Della Bartola, M., Byrne, S., Mullins, E. (2020). Characterization of potato virus Y isolates and assessment of nanopore sequencing to detect and genotype potato viruses. Viruses 12: 478.

[12] Dombrovsky, A., Glanz, E., Lachman, O., Sela, N., Doron-Faigenboim, A. and Antignus, Y. (2013). The complete genomic sequence of pepper yellow leaf curl virus (PYLCV) and its implications for our understanding of evolution dynamics in the genus Polerovirus. PLoS ONE 8(7): e70722.

[13] Dombrovsky, A., Sapkota, R., Lachman, O. and Antignus, Y. (2012). Eggplant mild leaf mottle virus (EMLMV), a new putative member of the genus Ipomovirus that harbors an HC-Pro gene. Virus Genes 44: 329-337.

[14] Donaire, L. and Aranda, M. A. (2023). Computational pipeline for the detection of plant RNA viruses using high throughput sequencing . In: Plant-Virus Interactions (pp. 1-20). New York: Springer.

[15] Fellers, J. P., Webb, C., Fellers, M. C., Shoup Rupp, J., De Wolf, E. (2019). Wheat virus identification within infected tissue using nanopore sequencing technology. Plant Dis. 103: 2199-2203.

[16] 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.

[17] Gaafar, Y. Z. A., Westenberg, M., Botermans, M., László K., De Jonghe, K., Foucart, Y., Kreuze, J., Muller, G., Vakirlis, N., Beris, D., Varveri, C. and Ziebell, H. (2021). Interlaboratory comparison study on ribodepleted total RNA high-throughput sequencing for plant virus diagnostics and bioinformatic competence. Pathogens 10: 1174. https://doi.org/10.3390/pathogens10091174.

[18] 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.

[19] Guo, J., Bolduc, B., Zayed, A. A., Varsani, A., Dominguez-Huerta, G., Delmont, T. O., Pratama, A. A., Gazitú M. C., Vik, D., Sullivan, M. B. and Roux, S. (2021). VirSorter2: A multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses. Microbiome 9: 1-13.

[20] Handelsman, J., Rondon, M. R., Brady, S. F., Clardy, J. and Goodman, R. M. (1998). Molecular biological access to the chemistry of unknown soil microbes: A new frontier for natural products. Chem. Biol. 5(10): 245-249.

[21] He, Y., Cai, L., Zhou, L., Yang, Z., Hong, N., Wang, G., Li, S. and Xu, W (2017). Deep sequencing reveals the first fabavirus infecting peach. Sci. Rep. 7:11329.

[22] Hess, M., Sczyrba, A., Egan, R., Kim, T, W., Chokhawala, H., Schroth, G. and Rubin, E. M. (2011). Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331: 463-467.

[23] Igori, D., Lim, S., Baek, D., Kim, S. Y., Seo, E., Cho, I. S., Choi, G.-S., Lim, H.-S. and Moon, J. S. (2017). Complete nucleotide sequence and genome organization of peach virus D, a putative new member of the genus. Marafivirus. Arch. Virol. 162, 1769-1772.

[24] 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 quasi species. BMC Genom. 18: 453.

[25] Jo, Y., Choi, H., Kyong Cho, J., Yoon, J. Y., Choi, S. K., Kyong Cho, W. (2015). In silico approach to reveal viral populations in grapevine cultivar Tannat using transcriptome data. Sci. Rep. 5:15841.

[26] Jo, Y., Choi, H., Lee, J. H., Moh, S. H. and Cho, W. K. (2022). Viromes of 15 pepper (Capsicum annuum L.) cultivars. Int. J. Mol. Sci. 23(18): 10507.

[27] Jones, S., Baizan-Edge, A., MacFarlane, S. and Torrance, L. (2017). Viral diagnostics in plants using next generation sequencing: Computational analysis in practice. Front. Plant Sci. 8: 1770.

[28] Kehoe, M. A., Coutts, B. A., Buirchell, B. J. and Jones, R. A. (2014). Plant virology and next generation sequencing: Experiences with a Potyvirus. PLoS ONE 9(8): e104580.

[29] Krehenwinkel, H., Pomerantz, A. and Prost, S. (2019). Genetic biomonitoring and biodiversity assessment using portable sequencing technologies: Current uses and future directions. Genes 10: 858.

[30] 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): 1-7.

[31] Krizbai, L., Kriston, E., Kreuze, J. and Melika, G. (2017). Identification of nectarine stem pitting-associated virus infecting prunus persica in Hungary. New Dis. Rep. 35: 18.

[32] Lane, D. J., Pace, B., Olsen, G. J., Stahl, D. A., Sogin, M. L. and Pace, N. R. (1985). Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc. Natl. Acad. Sci. USA 82(20): 6955-6959.

[33] Lavezzo, E., Barzon, L., Toppo, S. and Palu, G. (2016). Third generation sequencing technologies applied to diagnostic microbiology: Benefits and challenges in applications and data analysis. Expert Rev. Mol. Diag. 16: 1011-1023.

[34] Lee, H. J., Kim, S. M. and Jeong, R. D. (2023). Analysis of wheat virome in Korea using Illumina and oxford nanopore sequencing platforms. Plants 12: 2374.

[35] Li, K., Bihan, M., Yooseph, S. and Methe, B. A. (2012). Analyses of the microbial diversity across the human microbiome. PLoS ONE 7(6): e32118.

[36] Liefting, L. W., Waite, D. W. and Thompson, J. R. (2021). Application of oxford nanopore technology to plant virus detection. Viruses 13(8): 1424.

[37] Lu, H., Giordano, F. and Ning, Z. (2016). Oxford Nanopore MinION sequencing and genome assembly. Genom. Proteom. Bioinform. 14: 265-279.

[38] Maclot, F., Candresse, T., Filloux, D., Malmstrom, C. M., Roumagnac, P., Van der Vlugt, R. and Massart, S. (2020). Illuminating an ecological blackbox: Using high throughput sequencing to characterize the plant virome across scales. Front. Microbiol. 11: 578064.

[39] Maina, S., Zheng, L. and Rodoni, B. C. (2021). Targeted genome sequencing (TG-seq) approaches to detect plant viruses. Viruses 13: 15. https://doi.org/10.1038/158885a0.

[40] Malapi-Wight, M., Salgado-Salazar, C., Demers, J. E., Clement, D. L., Rane, K. K. and Crouch, J. A. (2016). Sarcococca blight: Use of whole- genome sequencing for fungal plant disease diagnosis. Plant Dis. 100(6): 1093-1100.

[41] Maliogka, V. I., Minafra, A., Saldarelli, P., Ruiz-García, 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.

[42] Matsumura, E., Coletta-Filho, H., Nouri, S., Falk, B., Nerva, L. and Oliveira, T. (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.

[43] 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(3): 412.

[44] Mushtaq, Z., Prasad, K. P. and Qayoom, U. (2020). Nanopore Sequencing for diagnosis and resistance profiling of pathogens. Biot. Res. Today 2: 908-911.

[45] Nabi, S. U., Yousuf, N., Yadav, M. K., Choudhary, D. K., Ahmad, D., Kirmani, S. N. and Ahmed, I. (2021). Recent insights in detection and diagnosis of plant viruses using next- generation sequencing technologies. Innov. Approaches Diagn. Manag. Crop Dis. 85: 100.

[46] 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(5): 675. https://doi.org/10.3390/plants11050675.

[47] Nakasu, E. Y. T., Silva, G., Montes, S. M. and Mello, A. F. S. (2022). Virome analysis of sweet potato in three Brazilian regions using high-throughput sequencing. Trop. Plant Pathol. 47: 800-806.

[48] Noda, H., Yamagishi, N., Yaegashi, H., Xing, F., Xie, J., Li, S., Zhou, T., Ito, T. and Yoshikawa, N. (2017). Apple necrotic mosaic virus, a novel ilarvirus from mosaic-diseased apple trees in Japan and China. J. Gen. Plant Pathol. 83: 83-90.

[49] Petersen, L. M., Martin, I., Moschetti, W. E., Kershaw, C. M. and Tsongalis, G. J. (2019). Third- generation sequencing in the clinical laboratory: Exploring the advantages and challenges of nanopore sequencing. J. Clin. Microbiol. 58: e01315-19.

[50] Poojari, S., Alabi, O. J., Fofanov, V. Y. and Naidu, R. A. (2013). A leafhopper-transmissible DNA virus with novel evolutionary lineage in the family geminiviridae implicated in grapevine red leaf disease by next generation sequencing. PLoS ONE 8(6): e64194.

[51] Prabha, K., Baranwal, V. K. and Jain, R. K. (2013). Applications of next generation high throughput sequencing technologies in characterization, discovery and molecular interaction of plant viruses. Indian J. Virol. 24: 157-165.

[52] Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C. and Wang, J. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.

[53] Reddy, N. V., Hiremath, S., Muttappagol, M., Vinay Kumar, H. D., Prasanna, S. K., Mohan Kumar, T. L. and Lakshminarayana Reddy, C. N. (2023). Virome analyses by next- generation sequencing (NGS) in chilli (Capsicum annuum L.) presented with diverse symptoms phenotype revealed the association of seven plant viruses. BioRxiv. https://doi.org/10.1101/2023.01.11.523546.

[54] Ren, J., Ahlgren, N. A., Lu, Y. Y., Fuhrman, J. A. and Sun, F. (2017). VirFinder: A novel kmer based tool for identifying viral sequences from assembled metagenomic data. Microbiome 5(1): 69.

[55] Ren, J., Song, K., Deng, C., Ahlgren, N. A., Fuhrman, J. A., Li, Y., Xie, X., Poplin, R. and Sun, F. (2020). Identifying viruses from metagenomic data using deep learning. Quant. Biol. 8: 64-77.

[56] Rivarez, M. P. S., Vučurović 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.

[57] Ronaghi, M., Uhlén, M. and Nyrén, P. (1998). A sequencing method based on real-time pyrophosphate. Science 281: 363-365.

[58] Rott, M., Xiang, Y., Boyes, I., Belton, M., Saeed, H., Kesanakurti, P. and Rast, H. (2017). Application of next generation sequencing for diagnostic testing of tree fruit viruses and viroids. Plant Dis. 101(8): 1489-1499.

[59] Samarfard, S., Taggart, A. R., Sharman, M., Bejerman, N. E. and Dietzgen, R. G. (2020). Viromes of ten alfalfa plants in Australia reveal diverse known viruses and a novel RNA virus. Pathogens 9(3): 214.

[60] Sanger, F., Air, G. M., Barrell, B. G., Brown, N. L., Coulson, A. R., Fiddes, J. C. and Smith, M. (1977). Nucleotide sequence of bacteriophage φX174 DNA. Nature 265: 687-695.

[61] Seguin, J., Rajeswaran, R., Malpica-López, N., Martin, R. R., Kasschau, K., Dolja, V. V. and Pooggin, M. M. (2014). De novo reconstruction of consensus master genomes of plant RNA and DNA viruses from siRNAs. PLoS ONE 9(2): e88513.

[62] Studholme, D. J., Glover, R. H. and Boonham, N. (2011). Application of high-throughput DNA sequencing in phytopathology. Annu. Rev. Phytopathol. 49: 87-105.

[63] Sukhorukov, G., Khalili, M., Gascuel, O., Candresse, T., Marais-Colombel, A. and Nikolski, M. (2022). VirHunter: A deep learning-based method for detection of novel RNA viruses in plant sequencing data. Front. Bioinform. 2: 867111.

[64] Valenzuela, S. L., Norambuena, T., Morgante, V., García, F., Jiménez, J. C., Núñez, C., Fuentes, I. and Pollak, B. (2022). Viroscope: Plant viral diagnosis from high-throughput sequencing data using biologically informed genome assembly coverage. Front. Microbiol. 13: 96702.

[65] Van Dijk, E. L., Jaszczyszyn, Y., Naquin, D. and Thermes, C. (2018). The third revolution in sequencing technology. Trends Genet. 34: 666-681.

[66] Verbeek, M., Dullemans, A. M., van Raaij, H. M., Verhoeven, J. T. J. and van der Vlugt, R. A. (2014). Lettuce necrotic leaf curl virus, a new plant virus infecting lettuce and a proposed member of the genus Torradovirus. Arch. Virol. 159: 801-805.

[67] 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(5): 716-725.

[68] Villamor, D. E. V., Mekuria, T. A., Pillai, S. S. and Eastwell, K. (2016). High throughput sequencing identifies novel viruses in nectarine: Insights to the etiology of stem pitting disease. Phytopathology 106: 519-527.

[69] Vives, M. C., Velázquez, K., Pina, J. A., Moreno, P., Guerri, J. and Navarro, L. (2013). Identification of a new Enamovirus associated with citrus vein enation disease by deep sequencing of small RNAs. Phytopathology 103(10):1077-1086.

[70] Wang, Z., Gerstein, M. and Snyder, M. (2009). RNA-Seq: A revolutionary tool for transcriptomics. Nat. Rev. Genet. 10(1): 57-63.

[71] Wu, Q., Luo, Y., Lu, R., Lau, N., Lai, E. C., Li, W. X. and Ding, S. W. (2010). Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs. Proc. Natl. Acad. Sci. USA 107: 1606-1611.

[72] Wu, L.-P., Liu, H.-W., Bateman, M., Liu, Z. and Li, R. (2017). Molecular characterization of a novel luteovirus from peach identified by high throughput sequencing. Arch. Virol. 162: 2903-2905.

[73] Yan, F., Zhang, H., Adams, M. J., Yang, J., Peng, J., Antoniw, J. F. and Chen, J. (2010). Characterization of siRNAs derived from rice stripe virus in infected rice plants by deep sequencing. Arch. Virol. 155: 935-940.

[74] Zhang, Y., Singh, K., Kaur, R. and Qiu, W. (2011). Association of a novel DNA virus with the grapevine vein-clearing and vine decline syndrome. Phytopathology 101: 1081-1090.

[75] Zhang, Z., Qi, S., Tang, N., Zhang, X., Chen, S., Zhu, P. and Wu, Q. (2014). Discovery of replicating circular RNAs by RNAseq and computational algorithms. PLoS Pathog. 10(12): e1004553.