Abstract
A unique capsidless virus with a positive-sense, single-stranded RNA genome (hadakavirus 1, HadV1), a member of the extended picorna-like supergroup, was isolated previously from the phytopathogenic fungus Fusarium oxysporum. Here, we describe the molecular and biological characterisation of a second hadakavirus strain from Fusarium nygamai, which has not been investigated in detail previously as a virus host. This virus, hadakavirus 1 strain 1NL (HadV1-1NL), has features similar to the first hadakavirus, HadV1-7n, despite having a different number of segments (10 for HadV1-1NL vs. 11 for HadV1-7n). The 10 genomic RNA segments of HadV1-1NL range in size from 0.9 kb to 2.5 kb. All HadV1-1NL segments show 67% to 86% local nucleotide sequence identity to their HadV1-7n counterparts, whereas HadV1-1NL has no homolog of HadV1-7n RNA8, which encodes a zinc-finger motif. Another interesting feature is the possible coding incapability of HadV1-1NL RNA10. HadV1-1NL was predicted to be capsidless based on the RNase A susceptibility of its replicative form dsRNA. Phenotypic comparison of multiple virus-infected and virus-free single-spore isolates indicated asymptomatic infection by HadV1-1NL. Less-efficient vertical transmission via spores was observed as the infected fungal colonies from which the spores were derived became older, as was observed for HadV1-7n. This study shows a second example of a hadakavirus that appears to have unusual features.
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References
Alastruey-Izquierdo A, Cuenca-Estrella M, Monzon A, Mellado E, Rodriguez-Tudela JL (2008) Antifungal susceptibility profile of clinical Fusarium spp. isolates identified by molecular methods. J Antimicrob Chemother 61:805–809
Appel DJ, Gordon TR (1996) Relationships among pathogenic and nonpathogenic isolates of Fusarium oxysporum based on the partial sequence of the intergenic spacer region of the ribosomal DNA. Mol Plant-Microbe Interact MPMI 9:125–138
Bormann J, Heinze C, Blum C, Mentges M, Brockmann A, Alder A, Landt SK, Josephson B, Indenbirken D, Spohn M, Plitzko B, Loesgen S, Freitag M, Schafer W (2018) Expression of a structural protein of the mycovirus FgV-ch9 negatively affects the transcript level of a novel symptom alleviation factor and causes virus-infection like symptoms in Fusarium graminearum. J Virol 92:e00326-e1318
Chiapello M, Rodriguez-Romero J, Ayllon MA, Turina M (2020) Analysis of the virome associated to grapevine downy mildew lesions reveals new mycovirus lineages. Virus Evol 6:veaa058
Chiba Y, Oiki S, Yaguchi T, Urayama SI, Hagiwara D (2021) Discovery of divided RdRp sequences and a hitherto unknown genomic complexity in fungal viruses. Virus Evol 7:veaa101
Cho WK, Lee KM, Yu J, Son M, Kim KH (2013) Insight into mycoviruses infecting Fusarium species. Adv Virus Res 86:273–288
Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430
Donnell K, Kistler HC, Tacke BK, Casper HH (2000) Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum the fungus causing wheat scab. Proc Natl Acad Sci 97:7905
Eusebio-Cope A, Suzuki N (2015) Mycoreovirus genome rearrangements associated with RNA silencing deficiency. Nucleic Acids Res 43:3802–3813
Heun Hong J, Gross KC (1998) Surface sterilization of whole tomato fruit with sodium hypochlorite influences subsequent postharvest behavior of fresh-cut slices. Postharvest Biol Technol 13:51–58
Hillman BI, Fulbright DW, Nuss DL, Van Alfen NK (1995) Family Hypoviridae. In: Murphy FA, Fauquet CM, Bishop DHL, Ghabrial SA, Jarvis AW, Martelli GP, Mayo MA, Summers MD (eds) Virus taxonomy: sixth report of the international committee on taxonomy of viruses. Springer, New York, pp 261–264
Hisano S, Zhang R, Faruk MI, Kondo H, Suzuki N (2018) A neo-virus lifestyle exhibited by a (+)ssRNA virus hosted in an unrelated dsRNA virus: taxonomic and evolutionary considerations. Virus Res 244:75–83
Jamal A, Sato Y, Shahi S, Shamsi W, Kondo H, Suzuki N (2019) Novel victorivirus from a Pakistani isolate of Alternaria alternata lacking a typical translational stop/restart sequence signature. Viruses 11:577
Jia H, Dong K, Zhou L, Wang G, Hong N, Jiang D, Xu W (2017) A dsRNA virus with filamentous viral particles. Nat Commun 8:168
Kanhayuwa L, Kotta-Loizou I, Ozkan S, Gunning AP, Coutts RH (2015) A novel mycovirus from Aspergillus fumigatus contains four unique dsRNAs as its genome and is infectious as dsRNA. Proc Natl Acad Sci USA 112:9100–9105
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166
Koonin EV, Wolf YI, Nagasaki K, Dolja VV (2008) The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat Rev Microbiol 6:925–939
Koonin EV, Dolja VV (2014) Virus world as an evolutionary network of viruses and capsidless selfish elements. Microbiol Mol Biol Rev 78:278–303
Koonin EV, Dolja VV, Krupovic M, Varsani A, Wolf YI, Yutin N, Zerbini FM, Kuhn JH (2020) Global organization and proposed megataxonomy of the virus world. Microbiol Mol Biol Rev 84:e00061-e119
Kotta-Loizou I, Coutts RHA (2017) Studies on the virome of the entomopathogenic fungus Beauveria bassiana reveal novel dsRNA elements and mild hypervirulence. PLoS Pathog 13:e1006183
Kotta-Loizou I, Caston JR, Coutts RHA, Hillman BI, Jiang D, Kim DH, Moriyama H, Suzuki N, ICTV Report C (2020) ICTV virus taxonomy profile: Chrysoviridae. J Gen Virol 99:19–20
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Li P, Bhattacharjee P, Wang S, Zhang L, Ahmed I, Guo L (2019) Mycoviruses in Fusarium species: an update. Front Cell Infect Microbiol 9:257. https://doi.org/10.3389/fcimb.2019.00257
Li PF, Wang SC, Zhang LH, Qiu DW, Zhou XP, Guo LH (2020) A tripartite ssDNA mycovirus from a plant pathogenic fungus is infectious as cloned DNA and purified virions. Sci Adv 6:eaay9634. https://doi.org/10.1126/sciadv.aay9634
Mizutani Y, Abraham A, Uesaka K, Kondo H, Suga H, Suzuki N, Chiba S (2018) Novel mitoviruses and a unique tymo-like virus in hypovirulent and virulent strains of the Fusarium head bight fungus, Fusarium boothii. Viruses 10:E584
Nalim FA, Elmer WH, McGovern RJ, Geiser DM (2009) Multilocus phylogenetic diversity of Fusarium avenaceum pathogenic on lisianthus. Phytopathology 99:462–468
Nerva L, Forgia M, Ciuffo M, Chitarra W, Chiapello M, Vallino M, Varese GC, Turina M (2019) The mycovirome of a fungal collection from the sea cucumber Holothuria polii. Virus Res 273:197737
O’Donnell K, Cigelnik E, Nirenberg HI (1998) Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90:465–493
O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC (1998) Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc Natl Acad Sci 95:2044
O’Donnell K, Gueidan C, Sink S, Johnston PR, Crous PW, Glenn A, Riley R, Zitomer NC, Colyer P, Waalwijk C, Tvd L, Moretti A, Kang S, Kim H-S, Geiser DM, Juba JH, Baayen RP, Cromey MG, Bithell S, Sutton DA, Skovgaard K, Ploetz R, Corby Kistler H, Elliott M, Davis M, Sarver BAJ (2009) A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genet Biol 46:936–948
Sato Y, Jamal A, Kondo H, Suzuki N (2020) Molecular characterization of a novel polymycovirus from Penicillium janthinellum with a focus on its genome-associated PASrp. Front Microbiol 11:592789
Sato Y, Shamsi W, Jamal A, Bhatti MF, Kondo H, Suzuki N (2020) Hadaka virus 1: a capsidless eleven-segmented positive-sense single-stranded RNA virus from a phytopathogenic fungus, Fusarium oxysporum. MBio 11:e00450-20.
Shamsi W, Sato Y, Jamal A, Shahi S, Kondo H, Suzuki N, Bhatti MF (2019) Molecular and biological characterization of a novel botybirnavirus identified from a Pakistani isolate of Alternaria alternata. Virus Res 263:119–128
Son M, Lee KM, Yu J, Kang M, Park JM, Kwon SJ, Kim KH (2013) The HEX1 gene of Fusarium graminearum is required for fungal asexual reproduction and pathogenesis and for efficient viral RNA accumulation of Fusarium graminearum virus 1. J Virol 87:10356–10367
Sun L, Suzuki N (2008) Intragenic rearrangements of a mycoreovirus induced by the multifunctional protein p29 encoded by the prototypic hypovirus CHV1-EP713. RNA 14:2557–2571
Sutela S, Forgia M, Vainio EJ, Chiapello M, Daghino S, Vallino M, Martino E, Girlanda M, Perotto S, Turina M (2020) The virome from a collection of endomycorrhizal fungi reveals new viral taxa with unprecedented genome organization. Virus Evol 6:veaa076
Suzuki N, Watanabe Y, Kusano T, Kitagawa Y (1990) Sequence analysis of rice dwarf phytoreovirus genome segments S4, S5, and S6: comparison with the equivalent wound tumor virus segments. Virology 179:446–454
Suzuki N, Maruyama K, Moriyama M, Nuss DL (2003) Hypovirus papain-like protease p29 functions in trans to enhance viral double-stranded RNA accumulation and vertical transmission. J Virol 77:11697–11707
Suzuki N, Supyani S, Maruyama K, Hillman BI (2004) Complete genome sequence of Mycoreovirus-1/Cp9B21, a member of a novel genus within the family Reoviridae, isolated from the chestnut blight fungus Cryphonectria parasitica. J Gen Virol 85:3437–3448
Suzuki N, Ghabrial SA, Kim KH, Pearson M, Marzano SL, Yaegashi H, Xie J, Guo L, Kondo H, Koloniuk I, Hillman BI, ICTV Report C (2018) ICTV virus taxonomy profile: Hypoviridae. J Gen Virol 99:615–616
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577
Urayama S, Katoh Y, Fukuhara T, Arie T, Moriyama H, Teraoka T (2015) Rapid detection of Magnaporthe oryzae chrysovirus 1-A from fungal colonies on agar plates and lesions of rice blast. J Gen Plant Pathol 81:97–102
Valverde RA, Khalifa ME, Okada R, Fukuhara T, Sabanadzovic S, Ictv Report C (2019) ICTV virus taxonomy profile: Endornaviridae. J Gen Virol 100:1204–1205
Walker PJ, Siddell SG, Lefkowitz EJ, Mushegian AR, Adriaenssens EM, Dempsey DM, Dutilh BE, Harrach B, Harrison RL, Hendrickson RC, Junglen S, Knowles NJ, Kropinski AM, Krupovic M, Kuhn JH, Nibert M, Orton RJ, Rubino L, Sabanadzovic S, Simmonds P, Smith DB, Varsani A, Zerbini FM, Davison AJ (2020) Changes to virus taxonomy and the statutes ratified by the International Committee on Taxonomy of Viruses (2020). Arch Virol 165:2737–2748
Wei CZ, Osaki H, Iwanami T, Matsumoto N, Ohtsu Y (2004) Complete nucleotide sequences of genome segments 1 and 3 of Rosellinia anti-rot virus in the family Reoviridae. Arch Virol 149:773–777
White T, Bruns T, Lee S, Taylor J, Innis M, Gelfand D, Sninsky J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc Guide Methods Appl. 18:315–322
Wickner RB, Fujimura T, Esteban R (2013) Viruses and prions of Saccharomyces cerevisiae. Adv Virus Res 86:1–36
Wolf YI, Kazlauskas D, Iranzo J, Lucia-Sanz A, Kuhn JH, Krupovic M, Dolja VV, Koonin EV (2018) Origins and evolution of the global RNA virome. MBio 9: e02329-18
Yu J, Lee KM, Cho WK, Park JY, Kim KH (2018) Differential contribution of RNA interference components in response to distinct Fusarium graminearum virus infections. J Virol 92:e01756-01717
Zhai L, Xiang J, Zhang M, Fu M, Yang Z, Hong N, Wang G (2016) Characterization of a novel double-stranded RNA mycovirus conferring hypovirulence from the phytopathogenic fungus Botryosphaeria dothidea. Virology 493:75–85
Zhang R, Hisano S, Tani A, Kondo H, Kanematsu S, Suzuki N (2016) A capsidless ssRNA virus hosted by an unrelated dsRNA virus. Nat Microbiol 1:15001.
Acknowledgements
The authors are grateful to Dr. Sabitree Shahi and Ms. Sakae Hisano for technical assistance. HAK is thankful to the Higher Education Commission (HEC) of Pakistan for a fellowship under the International Research Support Initiative Program (IRSIP). YS is a JSPS (Japan Society for the Promotion of Science) fellow.
Funding
This study was supported in part by Yomogi Inc., the Ohara Foundation for Agriculture Research (to NS), Grants-in-Aid for Scientific Research on Innovative Areas from the Japanese Ministry of Education, Culture, Sports, Science and Technology (KAKENHI 17H01463, 16H06436, 16H06429 and 16K21723 to N.S. and H.K.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Conceptualization, NS; investigation, HAK, YS, AJ, HK, and NS; supervision, AJ and MFB; writing—original draft, HAK, YS, and NS; writing—reviewing and editing, AJ, MFB, and HK; funding acquisition, NS.
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The complete genomic nucleotide sequence of HadV1-1NL was deposited in the GenBank/ENA/DDBJ database under accession numbers LC592214 to LC592223.
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Khan, H.A., Sato, Y., Kondo, H. et al. A second capsidless hadakavirus strain with 10 positive-sense single-stranded RNA genomic segments from Fusarium nygamai. Arch Virol 166, 2711–2722 (2021). https://doi.org/10.1007/s00705-021-05176-x
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DOI: https://doi.org/10.1007/s00705-021-05176-x