Expanding Viral Diversity in Rice Fields by Next-Generation Sequencing
Received date: 2024-08-18
Accepted date: 2024-12-05
Online published: 2024-12-10
In rice fields, rice plants usually grow alongside wild weeds and are attacked by various invertebrate species. Viruses are abundant in plants and invertebrates, playing crucial ecological roles in controlling microbial abundance and maintaining community structures. To date, only 16 rice viruses have been documented in rice-growing regions. These viruses pose serious threats to rice production and have traditionally been identified only from rice plants and insect vectors by isolation techniques. Advances in next-generation sequencing (NGS) have made it feasible to discover viruses on a global scale. Recently, numerous viruses have been identified in plants and invertebrates using NGS technologies. In this review, we discuss viral studies in rice plants, invertebrate species, and weeds in rice fields. Many novel viruses have been discovered in rice ecosystems through NGS technologies, with some also detected using metatranscriptomic and small RNA sequencing. These analyses greatly expand our understanding of viruses in rice fields and provide valuable insights for developing efficient strategies to manage insect pests and virus-mediated rice diseases.
Wang Haoran, Chen Guoqing, Feng Guozhong . Expanding Viral Diversity in Rice Fields by Next-Generation Sequencing[J]. Rice Science, 2025 , 32(1) : 44 -51 . DOI: 10.1016/j.rsci.2024.12.004
| [1] | Aguiar E R G R, Olmo R P, Paro S, et al. 2015. Sequence- independent characterization of viruses based on the pattern of viral small RNAs produced by the host. Nucleic Acids Res, 43(13): 6191-6206. |
| [2] | Bernardo P, Charles-Dominique T, Barakat M, et al. 2018. Geometagenomics illuminates the impact of agriculture on the distribution and prevalence of plant viruses at the ecosystem scale. ISME J, 12(1): 173-184. |
| [3] | Bexfield N, Kellam P. 2011. Metagenomics and the molecular identification of novel viruses. Vet J, 190(2): 191-198. |
| [4] | Bonning B C, Miller W A. 2010. Dicistroviruses. Annu Rev Entomol, 55: 129-150. |
| [5] | Cadenas-Castrejón E, Verleyen J, Boukadida C, et al. 2023. Evaluation of tools for taxonomic classification of viruses. Brief Funct Genomics, 22(1): 31-41. |
| [6] | Cantalupo P G, Pipas J M. 2019. Detecting viral sequences in NGS data. Curr Opin Virol, 39: 41-48. |
| [7] | Chao S F, Wang H R, Yan Q, et al. 2021. Metatranscriptomic sequencing suggests the presence of novel RNA viruses in rice transmitted by brown planthopper. Viruses, 13(12): 2464. |
| [8] | Chao S F, Wang H R, Zhang S, et al. 2022. Novel RNA viruses discovered in weeds in rice fields. Viruses, 14(11): 2489. |
| [9] | Datta S, Budhauliya R, Das B, et al. 2015. Next-generation sequencing in clinical virology: Discovery of new viruses. World J Virol, 4(3): 265-276. |
| [10] | Elena S F, Fraile A, García-Arenal F. 2014. Evolution and emergence of plant viruses. Adv Virus Res, 88: 161-191. |
| [11] | Gilmer D, Ratti C, Consortium I R. 2017. ICTV virus taxonomy profile: Benyviridae. J Gen Virol, 98(7): 1571-1572. |
| [12] | Hamilton A J, Baulcombe D C. 1999. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science, 286: 950-952. |
| [13] | Hasiów-Jaroszewska B, Boezen D, Zwart M P. 2021. Metagenomic studies of viruses in weeds and wild plants: A powerful approach to characterise variable virus communities. Viruses, 13(10): 1939. |
| [14] | Hibino H. 1978. Association of two types of virus particles with penyakit habang (tungro disease) of rice in Indonesia. Phytopathology, 68(10): 1412. |
| [15] | Hibino H. 1996. Biology and epidemiology of rice viruses. Annu Rev Phytopathol, 34: 249-274. |
| [16] | Horiuchi H, Moriyama H, Fukuhara T. 2003. Inheritance of Oryza sativa endornavirus in F1 and F2 hybrids between japonica and indica rice. Genes Genet Syst, 78(3): 229-234. |
| [17] | Hubert J G, Pinel-Galzi A, Dibwe D, et al. 2013. First report of rice yellow mottle virus on rice in the Democratic Republic of Congo. Plant Dis, 97(12): 1664. |
| [18] | Inoue-Nagata A K, Jordan R, Kreuze J, et al. 2022. ICTV virus taxonomy profile: Potyviridae 2022. J Gen Virol, 103(5): 001738. |
| [19] | Jia D S, Luo G Z, Shi W, et al. 2022. Rice gall dwarf virus promotes the propagation and transmission of rice stripe mosaic virus by co-infected insect vectors. Front Microbiol, 13: 834712. |
| [20] | Li C X, Shi M, Tian J H, et al. 2015. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife, 4: e05378. |
| [21] | Li D, Duan W J, Liu Q E, et al. 2024. Gapless genome assembly of ZH8015 and preliminary multi-omics analysis to investigate ZH8015’s responses against brown planthopper infestation. Rice Sci, 31(3): 317-327. |
| [22] | Liu S J, Vijayendran D, Bonning B C. 2011. Next generation sequencing technologies for insect virus discovery. Viruses, 3(10): 1849-1869. |
| [23] | Liu S J, Chen Y T, Bonning B C. 2015. RNA virus discovery in insects. Curr Opin Insect Sci, 8: 54-61. |
| [24] | Ma Y X, Marais A, Lefebvre M, et al. 2020. Metagenomic analysis of virome cross-talk between cultivated and wild. Virology, 540: 38-44. |
| [25] | Matthijnssens J, Attoui H, Bányai K, et al. 2022a. ICTV virus taxonomy profile: Sedoreoviridae 2022. J Gen Virol, 103(10): 001782. |
| [26] | Matthijnssens J, Attoui H, Bányai K, et al. 2022b. ICTV virus taxonomy profile: Spinareoviridae 2022. J Gen Virol, 103(11): 001781. |
| [27] | Moubset O, François S, Maclot F, et al. 2022. Virion-associated nucleic acid-based metagenomics: A decade of advances in molecular characterization of plant viruses. Phytopathology, 112(11): 2253-2272. |
| [28] | Murakami R, Suetsugu Y, Kobayashi T, et al. 2013. The genome sequence and transmission of an iflavirus from the brown planthopper, Nilaparvata lugens. Virus Res, 176(1/2): 179-187. |
| [29] | Murakami R, Suetsugu Y, Nakashima N. 2014. Complete genome sequences of two iflaviruses from the brown planthopper, Nilaparvata lugens. Arch Virol, 159(3): 585-588. |
| [30] | Nouri S, Salem N, Nigg J C, et al. 2016. Diverse array of new viral sequences identified in worldwide populations of the Asian Citrus psyllid (Diaphorina citri) using viral metagenomics. J Virol, 90(5): 2434-2445. |
| [31] | Oludare A, Sow M, Afolabi O, et al. 2015. First report of rice stripe necrosis virus infecting rice in Benin. Plant Dis, 99(5): 735. |
| [32] | Power A G, Mitchell C E. 2004. Pathogen spillover in disease epidemics. Am Nat, 164: S79-S89. |
| [33] | Power A G, Borer E T, Hosseini P, et al. 2011. The community ecology of barley/cereal yellow dwarf viruses in Western US grasslands. Virus Res, 159(2): 95-100. |
| [34] | Prendeville H R, Ye X H, Morris T J, et al. 2012. Virus infections in wild plant populations are both frequent and often unapparent. Am J Bot, 99(6): 1033-1042. |
| [35] | Qin P, Lu H W, Du H L, et al. 2021. Pan-genome analysis of 33 genetically diverse rice accessions reveals hidden genomic variations. Cell, 184(13): 3542-3558.e16. |
| [36] | Roossinck M J. 2017. Deep sequencing for discovery and evolutionary analysis of plant viruses. Virus Res, 239: 82-86. |
| [37] | Roossinck M J, García-Arenal F. 2015. Ecosystem simplification, biodiversity loss and plant virus emergence. Curr Opin Virol, 10: 56-62. |
| [38] | Sasaya T, Palacios G, Briese T, et al. 2023. ICTV virus taxonomy profile: Phenuiviridae 2023. J Gen Virol, 104(9). 001893. |
| [39] | Schoelz J E, Stewart L R. 2018. The role of viruses in the phytobiome. Annu Rev Virol, 5(1): 93-111. |
| [40] | Schopman N C T, Willemsen M, Liu Y P, et al. 2012. Deep sequencing of virus-infected cells reveals HIV-encoded small RNAs. Nucleic Acids Res, 40(1): 414-427. |
| [41] | Shi M, Lin X D, Tian J H, et al. 2016. Redefining the invertebrate RNA virosphere. Nature, 540: 539-543. |
| [42] | Shi M, Neville P, Nicholson J, et al. 2017. High-resolution metatran- scriptomics reveals the ecological dynamics of mosquito- associated RNA viruses in western Australia. J Virol, 91(17): e00680-17. |
| [43] | Simmons H E, Dunham J P, Stack J C, et al. 2012. Deep sequencing reveals persistence of intra- and inter-host genetic diversity in natural and greenhouse populations of zucchini yellow mosaic virus. J Gen Virol, 93: 1831-1840. |
| [44] | Sõmera M, Fargette D, Hébrard E, et al. 2021. ICTV virus taxonomy profile: Solemoviridae 2021. J Gen Virol, 102(12): 001707. |
| [45] | Sparks M E, Gundersen-Rindal D E, Harrison R L. 2013. Complete genome sequence of a novel iflavirus from the transcriptome of Halyomorpha halys, the brown marmorated stink bug. Genome Announc, 1(6): e00910-13. |
| [46] | Teycheney P Y, Geering A D W, Dasgupta I, et al. 2020. ICTV virus taxonomy profile: Caulimoviridae. J Gen Virol, 101(10): 1025-1026. |
| [47] | Uehara-Ichiki T, Shiba T, Matsukura K, et al. 2013. Detection and diagnosis of rice-infecting viruses. Front Microbiol, 4: 289. |
| [48] | Vainio E J, Jurvansuu J, Streng J, et al. 2015. Diagnosis and discovery of fungal viruses using deep sequencing of small RNAs. J Gen Virol, 96: 714-725. |
| [49] | Valles S M, Chen Y, Firth A E, et al. 2017. ICTV virus taxonomy profile: Iflaviridae. J Gen Virol, 98(4): 527-528. |
| [50] | Walker P J, Freitas-Astúa J, Bejerman N, et al. 2022. ICTV virus taxonomy profile: Rhabdoviridae 2022. J Gen Virol, 103(6): 001689. |
| [51] | Wang D, Fu S, Wu H Y, et al. 2022. Discovery and genomic function of a novel rice dwarf-associated bunya-like virus. Viruses, 14(6): 1183. |
| [52] | Wang H R, Chao S F, Yan Q, et al. 2024. Genetic diversity of RNA viruses infecting invertebrate pests of rice. Sci China Life Sci, 67(1): 175-187. |
| [53] | Wang P Y, Liu J J, Lyu Y J, et al. 2022. A review of vector-borne rice viruses. Viruses, 14(10): 2258. |
| [54] | Wang W S, Mauleon R, Hu Z Q, et al. 2018. Genomic variation in 3, 010 diverse accessions of Asian cultivated rice. Nature, 557: 43-49. |
| [55] | Wang Y X, Piao J, Cheng Z B, et al. 2020. Risk assessment of gramineae weeds for rice stripe virus epidemic in the field. J Weed Sci, 38. |
| [56] | Webster C L, Waldron F M, Robertson S, et al. 2015. The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster. PLoS Biol, 13(7): e1002210. |
| [57] | Wei T Y, Li Y. 2016. Rice reoviruses in insect vectors. Annu Rev Phytopathol, 54: 99-120. |
| [58] | Wu N, Zhang L, Ren Y D, et al. 2020. Rice black-streaked dwarf virus: From multiparty interactions among plant-virus-vector to intermittent epidemics. Mol Plant Pathol, 21(8): 1007-1019. |
| [59] | Wu Q F, Wang Y, Cao M J, et al. 2012. Homology-independent discovery of replicating pathogenic circular RNAs by deep sequencing and a new computational algorithm. Proc Natl Acad Sci USA, 109(10): 3938-3943. |
| [60] | Wu Q F, Ding S W, Zhang Y J, et al. 2015. Identification of viruses and viroids by next-generation sequencing and homology-dependent and homology-independent algorithms. Annu Rev Phytopathol, 53: 425-444. |
| [61] | Yan W K, Zhu Y, Liu W C, et al. 2023. Discovery of aphid- transmitted rice tiller inhibition virus from native plants through metagenomic sequencing. PLoS Pathog, 19(3): e1011238. |
| [62] | Zhang T Z, Li C Y, Cao M J, et al. 2021. A novel rice curl dwarf- associated picornavirus encodes a 3C serine protease recognizing uncommon EPT/S cleavage sites. Front Microbiol, 12: 757451. |
| [63] | Zhang Y Z, Shi M, Holmes E C. 2018. Using metagenomics to characterize an expanding virosphere. Cell, 172(6): 1168-1172. |
| [64] | Zhao F M, Baek D, Igori D, et al. 2017. Complete genome sequence of rice virus A, a new member of the family Tombusviridae. Arch Virol, 162(10): 3247-3250. |
| [65] | Zhao M, Liu X X, Wan J, et al. 2024. Host-induced gene silencing of effector AGLIP1 enhanced resistance of rice to Rhizoctonia solani AG1-IA. Rice Sci, 31(4): 463-474. |
| [66] | Zheng Y, Gao S, Padmanabhan C, et al. 2017. VirusDetect: An automated pipeline for efficient virus discovery using deep sequencing of small RNAs. Virology, 500: 130-138. |
| [67] | Zhou G H, Xu D L, Xu D G, et al. 2013. Southern rice black- streaked dwarf virus: A white-backed planthopper-transmitted fijivirus threatening rice production in Asia. Front Microbiol, 4: 270. |
/
| 〈 |
|
〉 |