Abstract
Fusarium oxysporum is a cosmopolitan plant pathogen that causes fusarium wilt and fusarium root rot in many economically important crops. There is still limited information about mycoviruses that infect F. oxysporum. Here, a novel mitovirus tentatively named "Fusarium oxysporum mitovirus 1" (FoMV1) was identified in F. oxysporum strain B2-10. The genome of FoMV1 is 2,453 nt in length with a predicted AU content of 71.6% and contains one large open reading frame (ORF) using the fungal mitochondrial genetic code. The ORF putatively encodes an RNA-dependent RNA polymerase (RdRp) of 723 aa with a molecular mass of 84.98 kDa. The RdRp domain of FoMV1 shares 29.01% to 68.43% sequence identity with the members of the family Mitoviridae. Phylogenetic analysis further suggested that FoMV1 is a new member of a distinct species in the genus Mitovirus.
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References
Michielse CB, Rep M (2009) Pathogen profile update: Fusarium oxysporum. Mol Plant Pathol 10:311–324. https://doi.org/10.1111/j.1364-3703.2009.00538.x
Pietro AD, Madrid MP, Caracuel Z, Delgado-Jarana J, Roncero MIG (2003) Fusarium oxysporum: exploring the molecular arsenal of a vascular wilt fungus. Mol Plant Pathol 4:315–325. https://doi.org/10.1046/j.1364-3703.2003.00180.x
Armstrong GM, Armstrong JK (1968) Formae specials and races of Fusarium oxysporum causing a tracheomycosis in the syndrome diseases. Phytopathology 58:1242–1246. https://doi.org/10.1094/phyto-68-19
Chehri K, Salleh B, Zakaria L (2015) Morphological and phylogenetic analysis of Fusarium solani species complex in Malaysia. Microbial Ecol 69:457–471. https://doi.org/10.1007/s00248-014-0494-2
Yang M, Cao JD, Zheng YX, Zhou HF, He MD, Duan J, Tong WJ, Deng XP, Chen XL (2020) First report of fusarium root rot of tobacco caused by Fusarium solani in Lincang, China. Plant Dis 104:1541. https://doi.org/10.1094/PDIS-08-19-1711-PDN
LaMondia JA (2015) Fusarium wilt of tobacco. Crop Protec 73:73–77. https://doi.org/10.1016/j.cropro.2015.03.003
Snow D, Lucas GB (1966) Diseases of Tobacco. J Appl Ecol 3:409. https://doi.org/10.2307/2401265
Ghabrial S, Suzuki N (2009) Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47:353–384. https://doi.org/10.1146/annurev-phyto-080508-081932
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. https://doi.org/10.1371/journal.ppat.1006183
Son M, Yu J, Kim KH (2015) Five questions about mycoviruses. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1005172
Herrero N, Dueñas E, Quesada-Moraga E, Zabalgogeazcoa I (2012) Prevalence and diversity of viruses in the entomopathogenic fungus Beauveria bassiana. Appl Environ Microbiol 78:8523–8530. https://doi.org/10.1128/AEM.01954-12
Ghabrial SA, Caston JR, Jiang D, Nibert ML, Suzuki N (2015) 50-plus years of fungal viruses. Virology 479:356–368. https://doi.org/10.1016/j.virol.2015.02.034
Deng F, Xu R, Boland GJ (2003) Hypovirulence-associated double-stranded RNA from Sclerotinia homoeocarpa is conspecific with Ophiostoma novo-ulmi mitovirus 3a-Ld. Phytopathology 93:1407–1414. https://doi.org/10.1094/PHYTO.2003.93.11.1407
Xie J, Jiang D (2014) New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annu Rev Phytopathol 52:45–68. https://doi.org/10.1146/annurev-phyto-102313-050222
Hillman BI, Suzuki N (2004) Viruses of the chestnut blight fungus, Cryphonectria parasitica. Adv Virus Res 63:423–472. https://doi.org/10.1016/S0065-3527(04)63007-7
Xiao Y, Li B, Fu Y, Jiang D, Ghabrial SA, Li G, Peng Y, Xie J, Cheng J, Huang J, Yi X (2010) A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci USA 107:8387–8392. https://doi.org/10.1016/S0065-3527(04)63007-7
Xiao Y, Li B, Fu Y, Xie J, Cheng J, Ghabrial SA et al (2013) Extracellular transmission of a DNA mycovirus and its use as a natural fungicide. Proc Natl Acad Sci USA 110(4):1452–1457. https://doi.org/10.1073/pnas.1213755110
Chiba S, Salaipeth L, Lin YH, Sasaki A, Kanematsu S, Suzuki N (2009) A novel bipartite double-stranded RNA mycovirus from the white root rot fungus Rosellinia necatrix: molecular and biological characterization, taxonomic considerations, and potential for biological control. J Virol 83:12801–12812. https://doi.org/10.1128/JVI.01830-09
Salaipeth L, Eusebio-Cope A, Chiba S, Kanematsu S, Suzuki N (2014) Biological properties and expression strategy of Rosellinia necatrix megabirnavirus 1 in an experimental host Cryphonectria parasitica. J Virol 95:740–750. https://doi.org/10.1099/vir.0.058164-0
Kilic O, Griffin GJ (1998) Effect of dsRNA-containing and dsRNA-free hypovirulent isolates of Fusarium oxysporum on severity of fusarium seedling disease of soybean in naturally infested soil. Plant Soil 201:125–135. https://doi.org/10.1023/A:1004319614390
Lemus-Minor CG, Carmen CM, García-Pedrajas MD, Pérez-Artés E (2019) Horizontal and vertical transmission of the hypovirulence-associated mycovirus Fusarium oxysporum f. sp. dianthi virus 1. Eur J Plant Pathol 153:645–650. https://doi.org/10.1007/s10658-018-1554-0
Zhao Y, Zhang Y, Wan X, She Y, Li M, Xi H, Xie J, Wen C (2020) A Novel Ourmia-Like Mycovirus Confers Hypovirulence-Associated Traits on Fusarium oxysporum. Front Microbiol. https://doi.org/10.3389/fmicb.2020.569869
Torres-Trenas A, Cañizares MC, García-Pedrajas MD, Pérez-Artés E (2020) Molecular and biological characterization of the first hypovirus identified in fusarium oxysporum. Front Microbiol 10:3131–3143. https://doi.org/10.3389/fmicb.2019.03131
Torres-Trenas A, Pérez-Artés E (2020) Characterization and Incidence of the First Member of the Genus Mitovirus Identified in the Phytopathogenic Species Fusarium oxysporum. Viruses 12:279–293. https://doi.org/10.3390/v12030279
Sato Y, Shamsi W, Jamal A, Bhatti MF, Suzuki N (2020) Hadaka virus 1: a capsidless eleven-segmented positive-sense single-stranded rna virus from a phytopathogenic fungus Fusarium oxysporum. mBio 11:20–38. https://doi.org/10.1128/mBio.00450-20
Mishra PK, Fox RT, Culham A (2003) Development of a PCR-based assay for rapid and reliable identification of pathogenic Fusaria. FEMS Microbiol Lett 218:329–332. https://doi.org/10.1016/S0378-1097(02)01174-6
O’Donnell K, Sutton DA, Rinaldi MG, Sarver BA, Balajee SA, Schroers HJ et al (2010) Internet-accessible DNA sequence database for identifying fusaria from human and animal infections. J Clin Microbiol 48:3708–3718
Wang J, Ni Y, Liu X, Zhao H, Xiao Y, Xiao X, Li S, Liu H (2020) Divergent RNA Viruses In Macrophomina phaseolina exhibit potential as virocontrol agents. Virus Evolution. https://doi.org/10.1093/ve/veaa095
Yao Z, Zou C, Peng N, Zhu Y, Bao Y, Zhou Q, Wu Q, Chen B, Zhang M (2020) Virome Identification and Characterization of Fusarium sacchari and F. andiyazi: Causative Agents of Pokkah Boeng Disease in Sugarcane. Front Microbiol 11:240. https://doi.org/10.3389/fmicb.2020.00240
Paquin B, Laforest MJ, Forget L, Roewer I, Wang Z, Longcore J, Lang BF (1997) The fungal mitochondrial genome project: Evolution of fungal mitochondrial genomes and their gene expression. Curr Genet 31:380–395. https://doi.org/10.1248/yakushi.126.1179
Nibert ML (2017) Mitovirus UGA (Trp) codon usage parallels that of host mitochondria. Virology 507:96–100. https://doi.org/10.1016/j.virol.2017.04.010
Hong Y, Dover SL, Cole TE, Brasier CM, Buck KW (1999) Multiple mitochondrial viruses in an isolate of the Dutch elm disease fungus Ophiostoma novo-ulmi. Virology 258:118–127. https://doi.org/10.1006/viro.1999.9691
Hillman BI, Cai G (2013) The family Narnaviridae: simplest of RNA viruses. Adv Virus Res 86:149–176. https://doi.org/10.1016/B978-0-12-394315-6.00006-4
Wu M, Zhang L, Li G, Jiang D, Ghabrial SA (2010) Genome characterization of a debilitation-associated mitovirus infecting the phytopathogenic fungus botrytis cinerea. Virology 406(1):117–126. https://doi.org/10.1016/j.virol.2010.07.010
Huang S, Ghabrial SA (1996) Organization and expression of the double-stranded RNA genome of Helminthosporium victoriae 190S virus, a totivirus infecting a plant pathogenic filamentous fungus. Proc Natl Acad Sci U S A 93:12541–12546. https://doi.org/10.2307/40654
Wang J, Xiao Y, Liu X, Ni Y, Zhao H, Zhao X, Liu H, Xiao X (2020) Complete genome sequence of a novel victorivirus isolated from the sesame charcoal rot fungus Macrophomina phaseolina. Arch Virol 165(2):509–514. https://doi.org/10.1007/s00705-019-04497-2
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This research work was supported by the Science and Technology Project of Henan Provincial Tobacco Company (2020410000270012). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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J.W. and S.J.L. conceived and designed the experiments; J.W. performed the experiments; R.Q., C.J.L., X.J.L., J.Z., J.K.B., and Y.G.C. collected the samples; J.W. wrote the paper; and S.J.L. and R.Q. revised the paper.
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Wang, J., Li, C., Qiu, R. et al. Complete genome sequence of a novel mitovirus from the phytopathogenic fungus Fusarium oxysporum. Arch Virol 166, 3211–3216 (2021). https://doi.org/10.1007/s00705-021-05210-y
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DOI: https://doi.org/10.1007/s00705-021-05210-y