Abstract
In this study, we report the complete genome sequence of a novel toti-like virus, tentatively named "Rhizopus stolonifer double-stranded RNA virus 1" (RsDSV1), identified from a phytopathogenic fungal agent of apple fruit rot disease, Rhizopus stolonifer strain A2-1. RsDSV1 has a double-stranded RNA genome. The complete RsDSV1 genome is 5178 nucleotides (nt) in length and contains two open reading frames (ORFs) encoding a putative coat protein (CP) and an RNA-dependent RNA polymerase (RdRp). Phylogenetic analysis based on RdRp and CP amino acid sequences revealed that RsDSV1 is closely related to unclassified members of the family Totiviridae. In stress-inducing Vogel’s minimal and sodium dodecyl sulfate-containing media, hyphal growth of A2-1 was suppressed, but the accumulation of RsDSV1 RNA increased, indicating that stresses promote RsDSV1 replication. To our knowledge, this is the first report of a mycovirus found in R. stolonifer.
References
Ghabrial SA, Suzuki N (2009) Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47:353–384
Hollings M (1962) Viruses associated with a die-back disease of cultivated mushroom. Nature 196:962–965
Kotta-Loizou I (2021) Mycoviruses and their role in fungal pathogenesis. Curr Opin Microbiol 63:10–18
Hough B, Steenkamp E, Wingfield B, Read D (2023) Fungal Viruses Unveiled: A Comprehensive Review of Mycoviruses. Viruses 15
Marquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–515
Shah UA, Kotta-Loizou I, Fitt BDL, Coutts RHA (2018) Identification, molecular characterization, and biology of a novel Quadrivirus infecting the phytopathogenic fungus Leptosphaeria biglobosa. Viruses 11
Yu X, 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 U S A 107:8387–8392
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
Yu X, Li B, Fu Y, Xie J, Cheng J, Ghabrial SA, Li G, Yi X, Jiang D (2013) Extracellular transmission of a DNA mycovirus and its use as a natural fungicide. Proc Natl Acad Sci U S A 110:1452–1457
Anagnostakis SL (1982) Biological control of chestnut blight. Science 215:466–471
Bautista-Baños S, Bosquez-Molina E, Barrera-Necha LL (2014) Rhizopus stolonifer (Soft rot). In: Bautista-Baños S (ed) Postharvest decay. Academic Press, Cambridge, Massachusetts, pp 1–44
Baggio JS, Gonçalves FP, Lourenço SA, Tanaka FAO, Pascholati SF, Amorim L (2016) Direct penetration of Rhizopus stolonifer into stone fruits causing Rhizopus rot. Plant Pathol 65:633–642
Edmunds BA, Holmes GJ (2009) Evaluation of alternative decay control products for control of postharvest Rhizopus soft rot of sweet potatoes. Plant Health Progress 10
Kong J, Zhang Y, Ju J, Xie Y, Guo Y, Cheng Y, Qian H, Quek SY, Yao W (2019) Antifungal effects of thymol and salicylic acid on cell membrane and mitochondria of Rhizopus stolonifer and their application in postharvest preservation of tomatoes. Food Chem 285:380–388
Yang X, Jiang X (2015) Antifungal activity and mechanism of tea polyphenols against Rhizopus stolonifer. Biotechnol Lett 37:1463–1472
Li H, Bian R, Liu Q, Yang L, Pang T, Salaipeth L, Andika IB, Kondo H, Sun L (2019) Identification of a novel hypovirulence-inducing hypovirus from Alternaria alternata. Front Microbiol 10:1076
Eusebio-Cope A, Suzuki N (2015) Mycoreovirus genome rearrangements associated with RNA silencing deficiency. Nucleic Acids Res 43:3802–3813
Sun L, Nuss DL, Suzuki N (2006) Synergism between a mycoreovirus and a hypovirus mediated by the papain-like protease p29 of the prototypic hypovirus CHV1-EP713. J Gen Virol 87:3703–3714
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols. Academic Press, Cambridge, Massachusetts, pp 315–322
Lian Z, Das S, Luo J, Andika IB, Sun L (2021) Complete genome sequence of a novel ourmia-like mycovirus infecting the phytopathogenic fungus Botryosphaeria dothidea. Arch Virol 166:3461–3465
Wickner RB, Ghabrial SA, Nibert ML, Patterson JL, Wang CC (2012) Family Totiviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy: ninth report of the international committee on taxonomy of viruses. Elsevier, Amsterdam, Netherlands, pp 639–650
Goodman RP, Ghabrial SA, Fichorova RN, Nibert ML (2011) Trichomonasvirus: a new genus of protozoan viruses in the family Totiviridae. Arch Virol 156:171–179
Ghabrial SA, Caston JR, Jiang D, Nibert ML, Suzuki N (2015) 50-plus years of fungal viruses. Virology 479–480:356–368
Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol 38:3022–3027
Xiang CY, Gao F, Jakovlić I, Lei HP, Hu Y, Zhang H, Zou H, Wang GT, Zhang D (2023) Using PhyloSuite for molecular phylogeny and tree-based analyses. iMeta 2
Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE 9:e108277
Lerer V, Shlezinger N (2022) Inseparable companions: Fungal viruses as regulators of fungal fitness and host adaptation. Front Cell Infect Microbiol 12:1020608
Zheng D, Zhang S, Zhou X, Wang C, Xiang P, Zheng Q, Xu JR (2012) The FgHOG1 pathway regulates hyphal growth, stress responses, and plant infection in Fusarium graminearum. PLoS ONE 7:e49495
Acknowledgments
We thank the High-Performance Computing Center of Northwest A&F University for providing computing resources. This work was supported in part by the National Natural Science Foundation of China (31970163) and the Natural Science Foundation of Xinjiang Uygur Autonomous Region (2021D01D12) to LY. Sun and (31970159) to IB. Andika.
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Wang, H., Luo, J., Dai, R. et al. Complete genome sequence of a novel double-stranded RNA virus infecting the phytopathogenic fungus Rhizopus stolonifer. Arch Virol 168, 239 (2023). https://doi.org/10.1007/s00705-023-05869-5
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DOI: https://doi.org/10.1007/s00705-023-05869-5