A novel monopartite dsRNA virus isolated from the phytopathogenic fungus Ustilaginoidea virens and ancestrally related to a mitochondria-associated dsRNA in the green alga Bryopsis

Virology

Volumn 462-463, Issue 1, 2014, Pages 227-235

  Zhang, Tingting ^a   Jiang, Yinhui ^a   Dong, Wubei ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

BDRM; DsRNA; Frameshift translation; Horizontal gene transfer; Mycovirus; Picorna like viruses; Ustilaginoidea virens

Indexed keywords

DOUBLE STRANDED RNA; MITOCHONDRIAL RNA;

ARTICLE; ASCOMYCETES; BRYOPSIS; CALICIVIRUS; CONTROLLED STUDY; CRYPTIC (ERA); FUNGAL STRAIN; GREEN ALGA; MITOCHONDRION; MYCOVIRUS; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PARTITIVIRIDAE; PHYLOGENY; PICORNAVIRUS; PRIORITY JOURNAL; RIBOSOMAL FRAMESHIFTING; RNA VIRUS; SEQUENCE ANALYSIS; TAXONOMY; USTILAGINOIDEA VIRENS; VIRUS ISOLATION; VIRUS STRAIN; WICKERHAMOMYCES; WICKERHAMOMYCES CIFERRII;

BDRM; DSRNA; FRAMESHIFT TRANSLATION; HORIZONTAL GENE TRANSFER; MYCOVIRUS; PICORNA-LIKE VIRUSES; USTILAGINOIDEA VIRENS;

CHINA; CHLOROPHYTA; CLUSTER ANALYSIS; GENOME, VIRAL; HYPOCREALES; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHYLOGENY; RNA VIRUSES; RNA, DOUBLE-STRANDED; RNA, VIRAL; SACCHAROMYCETALES; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY;

EID: 84903794987     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.06.003     Document Type: Article

References (60)

1. Agranovsky A., Koonin E., Boyko V., Maiss E., Frötschl R., Lunina N., Atabekov J. Beet yellows closterovirus: complete genome structure and identification of a leader papain-like thiol protease. Virology 1994, 198:311-324.
2. Baranov P.V., Gesteland R.F., Atkins J.F. P-site tRNA is a crucial initiator of ribosomal frameshifting. RNA 2004, 10:221-230.
3. Baranov P.V., Henderson C.M., Anderson C.B., Gesteland R.F., Atkins J.F., Howard M.T. Programmed ribosomal frameshifting in decoding the SARS-CoV genome. Virology 2005, 332:498-510.
4. Bejarano E.R., Khashoggi A., Witty M., Lichtenstein C. Integration of multiple repeats of geminiviral DNA into the nuclear genome of tobacco during evolution. Proc. Natl. Acad. Sci. 1996, 93:759-764.
5. Bekaert M., Atkins J.F., Baranov P.V. ARFA: a program for annotating bacterial release factor genes, including prediction of programmed ribosomal frameshifting. Bioinformatics 2006, 22:2463-2465.
6. Bratke K.A., McLysaght A. Identification of multiple independent horizontal gene transfers into poxviruses using a comparative genomics approach. BMC Evol. Biol 2008, 8:1-13.
7. Brierley I., Jenner A.J., Inglis S.C. Mutational analysis of the "slippery-sequence" component of a coronavirus ribosomal frameshifting signal. J. Mol. Biol. 1992, 227:463-479.
8. Bruenn J.A. A closely related group of RNA-dependent RNA polymerases from double-stranded RNA viruses. Nucleic Acids Res. 1993, 21:5667-5669.
9. Chare E.R., Gould E.A., Holmes E.C. Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses. J. Gen. Virol. 2003, 84:2691-2703.
10. Filée J., Pouget N., Chandler M. Phylogenetic evidence for extensive lateral acquisition of cellular genes by nucleocytoplasmic large DNA viruses. BMC Evol. Biol. 2008, 8:1-13.
11. Firth A., Jagger B., Wise H., Nelson C., Parsawar K., Wills N., Napthine S., Taubenberger J., Digard P., Atkins J. Ribosomal frameshifting used in influenza A virus expression occurs within the sequence UCC_UUU_CGU and is in the+1 direction. Open Biol. 2012, 2:e120109.
12. Firth A.E., Brierley I. Non-canonical translation in RNA viruses. J. Gen. Virol 2012, 93:1385-1409.
13. Forterre P. Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. Proc. Natl. Acad. Sci. USA 2006, 103:3669-3674.
14. Frank A.C., Wolfe K.H. Evolutionary capture of viral and plasmid DNA by yeast nuclear chromosomes. Eukaryot. Cell 2009, 8:1521-1531.
15. Froussard P. rPCR: a powerful tool for random amplification of whole RNA sequences. Genom. Res. 1993, 2:185-190.
16. Geuking M.B., Weber J., Dewannieux M., Gorelik E., Heidmann T., Hengartner H., Zinkernagel R.M., Hangartner L. Recombination of retrotransposon and exogenous RNA virus results in nonretroviral cDNA integration. Science 2009, 323:393-396.
17. Ghabrial S.A., Suzuki N. Viruses of plant pathogenic fungi. Annu. Rev. Phytopathol. 2009, 47:353-384.
18. Goodman R.P., Freret T.S., Kula T., Geller A.M., Talkington M.W., Tang-Fernandez V., Suciu O., Demidenko A.A., Ghabrial S.A., Beach D.H. Clinical isolates of Trichomonas vaginalis concurrently infected by strains of up to four Trichomonasvirus species (Family Totiviridae). J. Virol. 2011, 85:4258-4270.
19. Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59:307-321.
20. Hon C.C., Lam T.T.-Y., Yip C.W., Wong R.T.Y., Shi M., Jiang J., Zeng F., Leung F.C.C. Phylogenetic evidence for homologous recombination within the family Birnaviridae. J. Gen. Virol. 2008, 89:3156-3164.
21. Horie M., Honda T., Suzuki Y., Kobayashi Y., Daito T., Oshida T., Ikuta K., Jern P., Gojobori T., Coffin J.M. Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 2010, 463:84-87.
22. Ivanov I.P., Atkins J.F. Ribosomal frameshifting in decoding antizyme mRNAs from yeast and protists to humans: close to 300 cases reveal remarkable diversity despite underlying conservation. Nucleic Acids Res. 2007, 35:1842-1858.
23. Jiang D., Ghabrial S.A. Molecular characterization of Penicillium chrysogenum virus: reconsideration of the taxonomy of the genus Chrysovirus. J. Gen. Virol. 2004, 85:2111-2121.
24. Jiang Y., Luo C., Jiang D., Li G., Huang J. The complete genomic sequence of a second novel partitivirus infecting Ustilaginoidea virens. Arch. Virol. 2014, 1-4.
25. Koga R., Fukuhara T., Nitta T. Molecular characterization of a single mitochondria-associated double-stranded RNA in the green alga Bryopsis. Plant Mol. Biol. 1998, 36:717-724.
26. Koonin E.V. Taming of the shrewd: novel eukaryotic genes from RNA viruses. BMC Biol. 2010, 8. (2-2).
27. Koonin E.V., Dolja V.V. Evolution of complexity in the viral world: the dawn of a new vision. Virus Res. 2006, 117:1-4.
28. Koonin E.V., Senkevich T.G., Dolja V.V. The ancient virus world and evolution of cells. Biol. Direct 2006, 1:29.
29. Koonin E.V., Wolf Y.I., Nagasaki K., Dolja V.V. The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat. Rev. Microbiol. 2008, 6:925-939.
30. Kunii M., Kanda M., Nagano H., Uyeda I., Kishima Y., Sano Y. Reconstruction of putative DNA virus from endogenous rice tungro bacilliform virus-like sequences in the rice genome: implications for integration and evolution. BMC Genomics 2004, 5:1-14.
31. Lesage P., Todeschini A. Happy together: the life and times of Ty retrotransposons and their hosts. Cytogenet. Genome Res. 2005, 110:70-90.
32. Li L., Wang A.L., Wang C.C. Structural analysis of the -1 ribosomal frameshift elements in giardiavirus mRNA. J. Virol. 2001, 75:10612-10622.
33. Lin Y.-H., Chiba S., Tani A., Kondo H., Sasaki A., Kanematsu S., Suzuki N. A novel quadripartite dsRNA virus isolated from a phytopathogenic filamentous fungus, Rosellinia necatrix. Virology 2012, 426:42-50.
34. Liu H., Fu Y., Jiang D., Li G., Xie J., Cheng J., Peng Y., Ghabrial S.A., Yi X. Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes. J. Virol. 2010, 84:11876-11887.
35. Liu H., Fu Y., Xie J., Cheng J., Ghabrial S., Li G., Peng Y., Yi X., Jiang D. Evolutionary genomics of mycovirus-related dsRNA viruses reveals cross-family horizontal gene transfer and evolution of diverse viral lineages. BMC Evol. Biol 2012, 12:1-15.
36. Liu H., Fu Y., Xie J., Cheng J., Ghabrial S.A., Li G., Yi X., Jiang D. Discovery of novel dsRNA viral sequences by in silico cloning and implications for viral diversity, host range and evolution. PloS One 2012, 7:e42147.
37. Maori E., Tanne E., Sela I. Reciprocal sequence exchange between non-retro viruses and hosts leading to the appearance of new host phenotypes. Virology 2007, 362:342-349.
38. Martin R., Zhou J., Tzanetakis I. Blueberry latent virus: an amalgam of the Partitiviridae and Totiviridae. Virus Res. 2011, 155:175-180.
39. Monier A., Pagarete A., de Vargas C., Allen M.J., Claverie J.M., Ogata H. Horizontal gene transfer of an entire metabolic pathway between a eukaryotic alga and its DNA virus. Genome Res. 2009, 19:1441-1449.
40. Moreira D., López-García P. Ten reasons to exclude viruses from the tree of life. Nat. Rev. Microbiol. 2009, 7:306-311.
41. Morris T., Dodds J. Isolation and analysis of double-stranded RNA from virus-infected plant and fungal tissue. Phytopathology 1979, 69:854-858.
42. Parker W.B. Metabolism and antiviral activity of ribavirin. Virus Res. 2005, 107:165-171.
43. Pearson M.N., Beever R.E., Boine B., Arthur K. Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol. Plant Pathol 2009, 10:115-128.
44. Polashock J.J., Hillman B.I. 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. Natl. Acad. Sci. 1994, 91:8680-8684.
45. Potgieter A.C., Page N.A., Liebenberg J., Wright I.M., Landt O., van Dijk A.A. Improved strategies for sequence-independent amplification and sequencing of viral double-stranded RNA genomes. J. Gen. Virol. 2009, 90:1423-1432.
46. Reuter J.S., Mathews D.H. RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinform. 2010, 11:1-9.
47. Shi M., Jagger B.W., Wise H.M., Digard P., Holmes E.C., Taubenberger J.K. Evolutionary conservation of the PA-X open reading frame in segment 3 of influenza A virus. J. Virol. 2012, 86:12411-12413.
48. Sun X., Kang S., Zhang Y., Tan X., Yu Y., He H., Zhang X., Liu Y., Wang S., Sun W. Genetic diversity and population structure of rice pathogen Ustilaginoidea virens in China. PloS One 2013, 8:e76879.
49. Tamm T., Suurväli J., Lucchesi J., Olspert A., Truve E. Stem-loop structure of Cocksfoot mottle virus RNA is indispensable for programmed -1 ribosomal frameshifting. Virus Res. 2009, 146:73-80.
50. Tanaka E., Ashizawa T., Sonoda R., Tanaka C. Villosiclava virens gen. nov., comb. nov., the teleomorph of Ustilaginoidea virens, the causal agent of rice false smut. Mycotaxon 2008, 106:491-501.
51. Tanne E., Sela I. Occurrence of a DNA sequence of a non-retro RNA virus in a host plant genome and its expression: evidence for recombination between viral and host RNAs. Virology 2005, 332:614-622.
52. Taylor D.J., Bruenn J. The evolution of novel fungal genes from non-retroviral RNA viruses. BMC Biol. 2009, 7:1-11.
53. Urayama S.-i., Sakoda H., Takai R., Katoh Y., Minh Le T., Fukuhara T., Arie T., Teraoka T., Moriyama H. A dsRNA mycovirus, Magnaporthe oryzae chrysovirus 1-B, suppresses vegetative growth and development of the rice blast fungus. Virology 2014, 448:265-273.
54. Vainio E.J., Hyder R., Aday G., Hansen E., Piri T., Doǧmuş-Lehtijärvi T., Lehtijärvi A., Korhonen K., Hantula J. Population structure of a novel putative mycovirus infecting the conifer root-rot fungus Heterobasidion annosum sensu lato. Virology 2012, 422:366-376.
55. Wu M., Zhang L., Li G., Jiang D., Ghabrial S.A. Genome characterization of a debilitation-associated mitovirus infecting the phytopathogenic fungus Botrytis cinerea. Virology 2010, 406:117-126.
56. Yewdell J.W., Ince W.L. Frameshifting to PA-X Influenza. Science 2012, 337:164-165.
57. Yu X., Li B., Fu Y., Jiang D., Ghabrial S.A., Li G., Peng Y., Xie J., Cheng J., Huang J. A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc. Natl. Acad. Sci. 2010, 107:8387-8392.
58. Zhang T., Jiang Y., Huang J., Dong W. Complete genome sequence of a putative novel victorivirus from Ustilaginoidea virens. Arch. Virol. 2013, 1-4.
59. Zhang T., Jiang Y., Huang J., Dong W. Genomic organization of a novel partitivirus from the phytopathogenic fungus Ustilaginoidea virens. Arch. Virol. 2013, 1-5.
60. Zimmer M., Sattelberger E., Inman R.B., Calendar R., Loessner M.J. Genome and proteome of Listeria monocytogenes phage PSA: an unusual case for programmed +1 translational frameshifting in structural protein synthesis. Mol. Microbiol. 2003, 50:303-317.