Abstract
Ophiostoma bicolor is a pathogenic fungus associated with bark beetles that can cause serious damage to host plants. In this study, a novel fungal virus, “Ophiostoma bicolor endornavirus 1” (ObEV1), was obtained from O. bicolor, and its complete genome sequence was determined. ObEV1 has a single-stranded positive-sense (+ ss) RNA genome of 10,119 nucleotides. Sequence annotation and comparison showed that the viral genome has a single large open reading frame (ORF) encoding a polyprotein of 362.48 kDa. The polyprotein contains seven conserved domains: RNA-dependent RNA polymerase (RdRp), viral RNA helicase 1 (VHel1), viral methyltransferase (VMet), DEAD-like helicase (DEXDc), gliding-GltJ (G1), large tegument protein UL36 (PHA), and YlqF-related-GTPase (Y). Sequence comparisons and phylogenetic analysis showed that ObEV1 is a novel mycovirus belonging to the genus Betaendornavirus of the family Endornaviridae. This is the first report of a mycovirus in the ophiostomatoid fungus O. bicolor.
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References
Davidson RW (2018) Wood-staining fungi associated with bark beetles in Engelmann spruce in colorado. Mycologia 47:58–67
Kirisits T (2004) Fungal associates of European bark beetles with special emphasis on the ophiostomatoid fungi. In: Lieutier F, Day KR, Battisti A (eds) Bark and wood boring insects in living trees in Europe, a synthesis:185–223
Chang R, Duong TA, Taerum SJ, Wingfield MJ, Zhou X, de Beer ZW (2020) Ophiostomatoid fungi associated with mites phoretic on bark beetles in Qinghai, China. IMA Fungus 11:15
Zipfel RD, de Beer ZW, Jacobs K, Wingfield BD, Wingfield MJ (2006) Multi-gene phylogenies define Ceratocystiopsis and Grosmannia distinct from Ophiostoma. Stud Mycol 55:75–97
Jankowiak R, Strzałka B, Bilański P, Kacprzyk M, Wieczorek P, Linnakoski R (2019) Ophiostomatoid fungi associated with hardwood-infesting bark and ambrosia beetles in Poland: Taxonomic diversity and vector specificity. Fungal Ecol 39:152–167
Six DL, Wingfield MJ (2011) The role of phytopathogenicity in bark beetle-fungus symbioses: a challenge to the classic paradigm. Annu Rev Entomol 56:255–272
Hofstetter R, Moser JC, Blomquist SR (2013) Mites associated with bark beetles and their hyperphoretic ophiostomatoid fungi. Biodivers Ser 12:165–176
Solheim H (1988) Pathogenicity of some Ips typographus-associated blue-stain fungi to Norway spruce. Medd Nor Inst Skoforsk 40:1–11
Linnakoski R, de Beer ZW, Ahtiainen J, Sidorov E, Niemela P, Pappinen A, Wingfield MJ (2010) Ophiostoma spp. associated with pine- and spruce-infesting bark beetles in Finland and Russia. Persoonia 25:72–93
Wang Z, Zhou Q, Zheng G, Fang J, Han F, Zhang X, Lu Q (2021) Abundance and diversity of Ophiostomatoid fungi associated with the great spruce bark beetle (Dendroctonus micans) in the Northeastern Qinghai-Tibet Plateau. Front Microbiol 12:721395
Kirisits T (2010) Fungi isolated from Picea abies in fested by the bark beetle Ips typographus in the Białowieża forest in north-eastern Poland. Forest Pathol 40:100–110
Viiri H, Lieutier F (2004) Ophiostomatoid fungi associated with the spruce bark beetle, Ips typographus, in three areas in France. Ann For Sci 61:215–219
Song LW, Zhang QH, Chen YQ, Zuo TT, Ren BZ (2011) Field responses of the Asian larch bark beetle, Ips subelongatus, to potential aggregation pheromone components: disparity between two populations in northeastern China. Insect Sci 18:311–319
Paciura D, de Beer ZW, Jacobs K, Zhou XD, Ye H, Wingfield MJ (2010) Eight new Leptographium species associated with tree-infesting bark beetles in China. Persoonia 25:94–108
Yamaoka Y, Wingfield M, Takahashi J, Solheim I H (1997) Ophiostomatoid fungi associated with the spruce bark beetle Ips typographus f. aponicus in Japan. Mycol Res 101(10):1215–1227
Jankowiak R (2005) Fungi associated with Ips typographus on picea abies in southern poland and their succession into the phloem and sapwood of beetle-infested trees and logs. Forest Pathology 35(1):37–55
Jankowiak R, Hilszczanski J (2005) Ophiostomatoid fungi associated with Ips typographus (L.) on Picea abies [(L.) H. Karst.] and Pinus sylvestris L. in North-Eastern Poland. Acta Soc Bot Pol 74:4
Chang R, Duong TA, Taerum SJ, Wingfield MJ, Zhou X, Yin M, de Beer ZW (2019) Ophiostomatoid fungi associated with the spruce bark beetle Ips typographus, including 11 new species from China. Persoonia 42:50–74
Hýsek Å, Löwe R, Turčáni M (2021) What happens to wood after a tree is attacked by a bark beetle? Forests 12(9):1163
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
Ghabrial SA, Caston JR, Jiang D, Nibert ML, Suzuki N (2015) 50-plus years of fungal viruses. Virology 479–480:356–368
Donaire L, Pagan I, Ayllon MA (2016) Characterization of Botrytis cinerea negative-stranded RNA virus 1, a new mycovirus related to plant viruses, and a reconstruction of host pattern evolution in negative-sense ssRNA viruses. Virology 499:212–218
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 USA 107:8387–8392
Howitt RLJ, Beever RE, Pearson MN, Forster RLS (2001) Genome characterization of Botrytis virus F, a flexuous rod-shaped mycovirus resembling plant 'potex-like’ viruses. J Gen Virol 82:67–78
Ayllon MA, Turina M, Xie J, Nerva L, Marzano SL, Donaire L, Jiang D, Consortium IR (2020) ICTV Virus Taxonomy Profile: Botourmiaviridae. J Gen Virol 101:454–455
Hacker CV, Brasier CM, Buck KW (2005) A double-stranded RNA from a Phytophthora species is related to the plant endornaviruses and contains a putative UDP glycosyltransferase gene. J Gen Virol 86:1561–1570
Yaegashi H, Kanematsu S, Ito T (2012) Molecular characterization of a new hypovirus infecting a phytopathogenic fungus, Valsa ceratosperma. Virus Res 165:143–150
Ghabrial SA, Suzuki N (2009) Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47:353–384
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
Wu M, Jin F, Zhang J, Yang L, Jiang D, Li G (2012) Characterization of a novel bipartite double-stranded RNA mycovirus conferring hypovirulence in the phytopathogenic fungus Botrytis porri. J Virol 86:6605–6619
Krupovic M, Ghabrial SA, Jiang D, Varsani A (2016) Genomoviridae: a new family of widespread single-stranded DNA viruses. Arch Virol 161:2633–2643
Okada R, Yong CK, Valverde RA, Sabanadzovic S, Aoki N, Hotate S, Kiyota E, Moriyama H, Fukuhara T (2013) Molecular characterization of two evolutionarily distinct endornaviruses co-infecting common bean (Phaseolus vulgaris). J Gen Virol 94:220–229
Khalifa ME, Pearson MN (2014) Molecular characterisation of an endornavirus infecting the phytopathogen Sclerotinia sclerotiorum. Virus Res 189:303–309
Yang D, Wu M, Zhang J, Chen W, Li G, Yang L (2018) Sclerotinia minor endornavirus 1, a novel pathogenicity debilitation-associated mycovirus with a wide spectrum of horizontal transmissibility. Viruses 10(11):589
Lambden PR, Cooke SJ, Caul EO, Clarke IN (1992) Cloning of noncul-tivatable human rotavirus by single primer amplification. J Virol 66(3):1817–1822
Liu W, Hai D, Mu F, Yu X, Zhao Y, He B, Xie J, Jiang D, Liu H (2020) Molecular characterization of a novel fusarivirus infecting the plant-pathogenic fungus Botryosphaeria dothidea. Arch Virol 165:1033–1037
Lee JS, Goh CJ, Park D, Hahn Y (2019) Identification of a novel plant RNA virus species of the genus Amalgavirus in the family Amalgaviridae from chia (Salvia hispanica). Genes & genomics 41(5):507–514
Bejerman N, Roumagnac P, Nemchinov LG (2020) High-throughput sequencing for deciphering the virome of alfalfa (Medicago sativa L.). Front Microbiol 11:553109
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477
Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22(13):1658–1659
Acknowledgements
The authors are grateful to Dr. Huanting Liu (University of St. Andrews) and Wenyi Liu (Zhejiang A&F University, China) for help in improvement of the manuscript.
Funding
This research was supported by the National Key R&D Program of China (2017YFD0600102-7) and the Agricultural Science and Technology Fund of Shandong Province of China (Innovation Project of Forestry Science and Technology) Project (2019LY003-4).
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Zhu, Y., Lu, A., Wang, Z. et al. Molecular characterization of a novel endornavirus isolated from Ophiostoma bicolor associated with bark beetles. Arch Virol 167, 2839–2843 (2022). https://doi.org/10.1007/s00705-022-05613-5
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DOI: https://doi.org/10.1007/s00705-022-05613-5