Abstract
The complete genome sequence of a new member of the family Mitoviridae was obtained from walking iris (Trimezia northiana (Schneev.) Ravenna by high-throughput sequencing. This is the first putative mitovirus identified in a monocotyledonous plant. The new mitovirus was tentatively named “walking iris virus 1” (WIV1). The complete genome of WIV1 is 2,858 nt in length with a single ORF encoding a viral replicase (RdRp). The highest level of amino acid sequence identity was 45% to Beta vulgaris mitovirus 1. In the viral replicase, a conserved protein domain for mitovirus RNA-dependent RNA polymerase and six highly conserved motifs were detected, consistent with other members of the family Mitoviridae. Phylogenetic inferences placed WIV1 among members of the genus Duamitovirus (family Mitoviridae) in a monophyletic clade with other plant mitoviruses. Sequence comparison and phylogenetic analysis support the classification of WIV1 as a new member of the genus Duamitovirus (family Mitoviridae).
Similar content being viewed by others
References
Begeman A, Babaian A, Lewis SC (2023) Metatranscriptomic analysis uncovers prevalent viral ORFs compatible with mitochondrial translation. mSystems 8:e01002–01022
Botella L, Manny A, Nibert ML, Vainio E (2021) Create 100 new species and four new genera (Cryppavirales: Mitoviridae). ICTV (https://ictv.global/ictv/proposals/2021.003F.R.Mitoviridae_100nsp_4ngen.zip)
BRUNT AA (1977) Some hosts and properties of narcissus latent virus, a carlavirus commonly infecting narcissus and bulbous iris. Ann Appl Biol 87:355–364
Chandel V, Kulshrestha S, Hallan V, Zaidi AA (2006) Natural infection of Ornithogalum mosaic virus on Iris from India. Plant Pathol 55:284–284
Chen J, Shi YH, Li MY, Adams MJ, Chen JP (2008) A new potyvirus from butterfly flower (Iris japonica Thunb.) in Zhejiang, China. Arch Virol 153:567–569
Chen Z, Chen L, Anane RF, Wang Z, Gao L, Li S, Wen G, Yu D, Zhao M (2022) Complete genome sequence of a novel mitovirus detected in Paris polyphylla var. yunnanensis. Arch Virol 167:645–650
Choi HI, Lim HR, Song YS, Kim MJ, Choi SH, Song YS, Bae SC, Ryu KH (2010) The complete genome sequence of freesia mosaic virus and its relationship to other potyviruses. Arch Virol 155:1183–1185
Cole TE, Hong Y, Brasier CM, Buck KW (2000) Detection of an RNA-dependent RNA polymerase in mitochondria from a mitovirus-infected isolate of the Dutch Elm disease fungus, Ophiostoma novo-ulmi. Virology 268:239–243
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
Derks AFLM, Vink-van den Abeele JL, Muller PJ (1980) BEAN YELLOW MOSAIC VIRUS IN SOME IRIDACEOUS PLANTS. International Society for Horticultural Science (ISHS), Leuven, Belgium, pp 31–38
Di Silvestre D, Passignani G, Rossi R, Ciuffo M, Turina M, Vigani G, Mauri PL (2022) Presence of a Mitovirus Is Associated with Alteration of the Mitochondrial Proteome, as Revealed by Protein-Protein Interaction (PPI) and Co-Expression Network Models in Chenopodium quinoa Plants. Biology (Basel) 11
Fonseca P, Ferreira F, da Silva F, Oliveira LS, Marques JT, Goes-Neto A, Aguiar E, Gruber A (2020) Characterization of a Novel Mitovirus of the Sand Fly Lutzomyia longipalpis Using Genomic and Virus-Host Interaction Signatures. Viruses 13
Forgia M, Navarro B, Daghino S, Cervera A, Gisel A, Perotto S, Aghayeva DN, Akinyuwa MF, Gobbi E, Zheludev IN, Edgar RC, Chikhi R, Turina M, Babaian A, Di Serio F, de la Pena M (2023) Hybrids of RNA viruses and viroid-like elements replicate in fungi. Nat Commun 14:2591
Golblatt P (2003) Iridaceae. In: Flora of North America. In: Flora of North America Editorial Committee, eds. 1993+. Flora of North America North of Mexico [Online]. 22 + vols. New York and Oxford. Vol. 26. http://floranorthamerica.org/Iridaceae. Accessed December 13th 2022
Hillman BI, Cai G (2013) Chapter Six - The Family Narnaviridae: Simplest of RNA Viruses. In: Ghabrial SA (ed) Advances in Virus Research. Academic Press, pp 149–176
Hong Y, Cole TE, Brasier CM, Buck KW (1998) Evolutionary relationships among putative RNA-dependent RNA polymerases encoded by a mitochondrial virus-like RNA in the Dutch elm disease fungus, Ophiostoma novo-ulmi, by other viruses and virus-like RNAs and by the Arabidopsis mitochondrial genome. Virology 246:158–169
Hong Y, Dover SL, Cole TE, Brasier CM, Buck KW (1999) Multiple Mitochondrial Viruses in an Isolate of the Dutch Elm Disease FungusOphiostoma novo-ulmi. Virology 258:118–127
Jacquat AG, Ulla SB, Debat HJ, Munoz-Adalia EJ, Theumer MG, Pedrajas MDG, Dambolena JS (2022) An in silico analysis revealed a novel evolutionary lineage of putative mitoviruses. Environ Microbiol 24:6463–6475
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066
Li Y, Deng C, Shang Q, Zhao X, Liu X, Zhou Q (2016) The first complete genome sequence of iris severe mosaic virus. Arch Virol 161:1069–1072
Mifsud JCO, Gallagher RV, Holmes EC, Geoghegan JL (2022) Transcriptome Mining Expands Knowledge of RNA Viruses across the Plant Kingdom. J Virol 96:e0026022
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 Blight Fungus, Fusarium boothii. Viruses 10:584
Moradi Z, Mehrvar M (2022) First report of Narcissus latent virus infecting iris in Iran. New Disease Reports 46
Nerva L, Vigani G, Di Silvestre D, Ciuffo M, Forgia M, Chitarra W, Turina M (2019) Biological and Molecular Characterization of Chenopodium quinoa Mitovirus 1 Reveals a Distinct Small RNA Response Compared to Those of Cytoplasmic RNA Viruses. J Virol 93
Neupane A, Feng C, Feng J, Kafle A, Bücking H, Lee Marzano S-Y (2018) Metatranscriptomic Analysis and In Silico Approach Identified Mycoviruses in the Arbuscular Mycorrhizal Fungus Rhizophagus spp. Viruses 10
Nibert ML, Vong M, Fugate KK, Debat HJ (2018) Evidence for contemporary plant mitoviruses. Virology 518:14–24
Parizad S, Dizadji A, Habibi MK, Winter S, Kalantari S, García-Arenal F, Ayllón MA (2017) Prevanlence of saffron latent virus (SaLV), a new potyvirus species, in saffron fields of Iran. J Plant Pathol 99:802–802
POWO (2022) Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Published on the Internet; http://www.plantsoftheworldonline.org/ Accessed December 13th 2022
Shamsi W, Kondo H, Ulrich S, Rigling D, Prospero S (2022) Novel RNA viruses from the native range of Hymenoscyphus fraxineus, the causal fungal agent of ash dieback. Virus Res 320:198901
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 Evolution 6
Takemoto Y, Kanehira T, Shinohara M, Yamashita S, Hibi T (2000) The nucleotide sequence and genome organization of Japanese iris necrotic ring virus, a new species in the genus Carmovirus. Arch Virol 145:651–657
Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44:W232–W235
Vaira AM, Hansen MA, Murphy C, Reinsel MD, Hammond J (2009) First Report of Freesia sneak virus in Freesia sp. in Virginia. Plant Dis 93:965–965
Walker PJ, Siddell SG, Lefkowitz EJ, Mushegian AR, Adriaenssens EM, Alfenas-Zerbini P, Dempsey DM, Dutilh BE, García ML, Curtis Hendrickson R, Junglen S, Krupovic M, Kuhn JH, Lambert AJ, Łobocka M, Oksanen HM, Orton RJ, Robertson DL, Rubino L, Sabanadzovic S, Simmonds P, Smith DB, Suzuki N, Van Doorslaer K, Vandamme A-M, Varsani A, Zerbini FM (2022) Recent changes to virus taxonomy ratified by the International Committee on Taxonomy of Viruses (2022). Archives of Virology 167:2429–2440
Wylie SJ, Luo H, Li H, Jones MG (2012) Multiple polyadenylated RNA viruses detected in pooled cultivated and wild plant samples. Arch Virol 157:271–284
Xie J, Ghabrial SA (2012) Molecular characterizations of two mitoviruses co-infecting a hyovirulent isolate of the plant pathogenic fungus Sclerotinia sclerotiorum. Virology 428:77–85
Funding
This study was partially supported by USDA-ARS project number 8042-22000-280-00D.
Author information
Authors and Affiliations
Contributions
Conceptualization: Dimitre Mollov. Formal analysis: Robert A. Alvarez-Quinto, Samuel Grinstead, Richard Jones. Investigation: Robert A. Alvarez-Quinto, Samuel Grinstead, Richard Jones, Dimitre Mollov. Methodology: Samuel Grinstead, Richard Jones, Dimitre Mollov. Supervision: Dimitre Mollov. Writing – original draft: Robert A. Alvarez-Quinto, Dimitre Mollov. Writing – review & editing: Robert A. Alvarez-Quinto, Samuel Grinstead, Richard Jones, Dimitre Mollov
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Research involving human participants and/or animals
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by Stephen John Wylie
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Alvarez-Quinto, R., Grinstead, S., Jones, R. et al. Complete genome sequence of a new mitovirus associated with walking iris (Trimezia northiana). Arch Virol 168, 273 (2023). https://doi.org/10.1007/s00705-023-05901-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00705-023-05901-8