Advertisement

Archives of Virology

, Volume 159, Issue 8, pp 2157–2160 | Cite as

A unique mitovirus from Glomeromycota, the phylum of arbuscular mycorrhizal fungi

  • Ryoko Kitahara
  • Yoji Ikeda
  • Hanako Shimura
  • Chikara Masuta
  • Tatsuhiro EzawaEmail author
Annotated Sequence Record

Abstract

Arbuscular mycorrhizal (AM) fungi that belong to the phylum Glomeromycota associate with most land plants and supply mineral nutrients to the host plants. One of the four viral segments found by deep-sequencing of dsRNA in the AM fungus Rhizophagus clarus strain RF1 showed similarity to mitoviruses and is characterized in this report. The genome segment is 2,895 nucleotides in length, and the largest ORF was predicted by applying either the mold mitochondrial or the universal genetic code. The ORF encodes a polypeptide of 820 amino acids with a molecular mass of 91.2 kDa and conserves the domain of the mitovirus RdRp superfamily. Accordingly, the dsRNA was designated as R. clarus mitovirus 1 strain RF1 (RcMV1-RF1). Mitoviruses are localized exclusively in mitochondria and thus generally employ the mold mitochondrial genetic code. The distinct codon usage of RcMV1-RF1, however, suggests that the virus is potentially able to replicate not only in mitochondria but also in the cytoplasm. RcMV1-RF1 RdRp showed the highest similarity to the putative RdRp of a mitovirus-like ssRNA found in another AM fungus, followed by RdRp of a mitovirus in an ascomycotan ectomycorrhizal fungus. The three mitoviruses found in the three mycorrhizal fungi formed a deeply branching clade that is distinct from the two major clades in the genus Mitovirus.

Keywords

Arbuscular Mycorrhizal Mycorrhizal Fungus Tryptophan Residue Universal Genetic Code Hypovirulent Strain 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This study was partially supported by The Asahi Glass Foundation (CM and TE) and a Grant-in-Aid for Scientific Research (22380042) from Japan Society for the Promotion of Science (TE).

Supplementary material

705_2014_1999_MOESM1_ESM.pdf (2.5 mb)
Supplementary material 1 (PDF 2560 kb)

References

  1. 1.
    Ghabrial SA, Suzuki N (2009) Viruses of plant pathogenic fungi. Ann Rev Phytopathol 47:353–384CrossRefGoogle Scholar
  2. 2.
    Hijikata N, Murase M, Tani C, Ohtomo R, Osaki M, Ezawa T (2010) Polyphosphate has a central role in the rapid and massive accumulation of phosphorus in extraradical mycelium of an arbuscular mycorrhizal fungus. New Phytol 186:285–289PubMedCrossRefGoogle Scholar
  3. 3.
    Hillman BI, Cai G (2013) Chapter Six—The family narnaviridae: simplest of RNA viruses. In: Ghabrial SA (ed) Advances in virus research. Academic Press, New York, pp 149–176Google Scholar
  4. 4.
    Hintz WE, Carneiro JS, Kassatenko I, Varga A, James D (2013) Two novel mitoviruses from a Canadian isolate of the Dutch elm pathogen Ophiostoma novo-ulmi (93–1224). Virol J 10:252PubMedCentralPubMedCrossRefGoogle Scholar
  5. 5.
    Ikeda Y, Shimura H, Kitahara R, Masuta C, Ezawa T (2012) A novel virus-like double-stranded rna in an obligate biotroph arbuscular mycorrhizal fungus: a hidden player in mycorrhizal symbiosis. Mol Plant-Microbe Interact 25:1005–1012PubMedCrossRefGoogle Scholar
  6. 6.
    Lakshman DK, Jian J, Tavantzis SM (1998) A double-stranded RNA element from a hypovirulent strain of Rhizoctonia solani occurs in DNA form and is genetically related to the pentafunctional AROM protein of the shikimate pathway. Proc Nat Acad Sci USA 95:6425–6429PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–515PubMedCrossRefGoogle Scholar
  8. 8.
    Osaki H, Nakamura H, Nomura K, Matsumoto N, Yoshida K (2005) Nucleotide sequence of a mitochondrial RNA virus from the plant pathogenic fungus, Helicobasidium mompa Tanaka. Virus Res 107:39–46PubMedCrossRefGoogle Scholar
  9. 9.
    Poch O, Sauvaget I, Delarue M, Tordo N (1989) Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J 8:3867–3874PubMedCentralPubMedGoogle Scholar
  10. 10.
    Polashock JJ, Hillman BI (1994) A small mitochondrial double-stranded (ds) RNA element associated with a hypovirulent strain of the chestnut blight fungus and ancestrally related to yeast cytoplasmic T and W dsRNAs. Proc Nat Acad Sci USA 91:8680–8684PubMedCentralPubMedCrossRefGoogle Scholar
  11. 11.
    Rastgou M, Habibi MK, Izadpanah K, Masenga V, Milne RG, Wolf YI, Koonin EV, Turina M (2009) Molecular characterization of the plant virus genus Ourmiavirus and evidence of inter-kingdom reassortment of viral genome segments as its possible route of origin. J Gen Virol 90:2525–2535PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Rogers HJ, Buck KW, Brasier CM (1987) A mitochondrial target for double-stranded RNA in diseased isolates of the fungus that causes Dutch elm disease. Nature 329:558–560CrossRefGoogle Scholar
  13. 13.
    Shackelton LA, Holmes EC (2008) The role of alternative genetic codes in viral evolution and emergence. J Theoret Biol 254:128–134CrossRefGoogle Scholar
  14. 14.
    Simon L, Bousquet J, Levesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363:67–69CrossRefGoogle Scholar
  15. 15.
    Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New YorkGoogle Scholar
  16. 16.
    Stielow JB, Bratek Z, Klenk H-P, Winter S, Menzel W (2012) A novel mitovirus from the hypogeous ectomycorrhizal fungus Tuber excavatum. Arch Virol 157:787–790CrossRefGoogle Scholar
  17. 17.
    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    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 406:117–126PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  • Ryoko Kitahara
    • 1
  • Yoji Ikeda
    • 1
  • Hanako Shimura
    • 1
  • Chikara Masuta
    • 1
  • Tatsuhiro Ezawa
    • 1
    Email author
  1. 1.Graduate School of AgricultureHokkaido UniversitySapporoJapan

Personalised recommendations