Bell pepper endornavirus: molecular and biological properties, and occurrence in the genus Free

Abstract

Bell peppers () harbour a large dsRNA virus. The linear genome (14.7 kbp) of two isolates from Japanese and USA bell pepper cultivars were completely sequenced and compared. They shared extensive sequence identity and contained a single, long ORF encoding a 4815 aa protein. This polyprotein contained conserved motifs of putative viral methyltransferase (MTR), helicase 1 (Hel-1), UDP-glycosyltransferase and RNA-dependent RNA polymerase. This unique arrangement of conserved domains has not been reported in any of the known endornaviruses. Hence this virus, for which the name Bell pepper endornavirus (BPEV) is proposed, is a distinct species in the genus (family ). The BPEV-encoded polyprotein contains a cysteine-rich region between the MTR and Hel-1 domains, with conserved CXCC motifs shared among several endornaviruses, suggesting an additional functional domain. In agreement with general endornavirus features, BPEV contains a nick in the positive-strand RNA molecule. The virus was detected in all bell pepper cultivars tested and transmitted through seed but not by graft inoculations. Analysis of dsRNA patterns and RT-PCR using degenerate primers revealed putative variants of BPEV, or closely related species, infecting other genotypes and three other species ( and ).

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.034686-0
2011-11-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/11/2664.html?itemId=/content/journal/jgv/10.1099/vir.0.034686-0&mimeType=html&fmt=ahah

References

  1. Coutts R. H. A. 2005; First report of an endornavirus in the Cucurbitaceae. . Virus Genes 31:361–362 [View Article][PubMed]
    [Google Scholar]
  2. DeWitt D., Bosland P. W. 1996 Peppers of the World Berkeley, CA: Ten Speed Press;
    [Google Scholar]
  3. Finn R. D., Mistry J., Tate J., Coggill P., Heger A., Pollington J. E., Gavin O. L., Gunasekaran P., Ceric G. et al. 2010; The Pfam protein families database. Nucleic Acids Res 38:Database issueD211–D222 [View Article][PubMed]
    [Google Scholar]
  4. Fukuhara T., Moriyama H., Nitta T. 1995; The unusual structure of a novel RNA replicon in rice. J Biol Chem 270:18147–18149 [View Article][PubMed]
    [Google Scholar]
  5. Fukuhara T., Koga R., Aoki N., Yuki C., Yamamoto N., Oyama N., Udagawa T., Horiuchi H., Miyazaki S. et al. 2006; The wide distribution of endornaviruses, large double-stranded RNA replicons with plasmid-like properties. Arch Virol 151:995–1002 [View Article][PubMed]
    [Google Scholar]
  6. Gibbs M. J., Koga R., Moriyama H., Pfeiffer P., Fukuhara T. 2000; Phylogenetic analysis of some large double-stranded RNA replicons from plants suggests they evolved from a defective single-stranded RNA virus. J Gen Virol 81:227–233[PubMed]
    [Google Scholar]
  7. Guindon S., Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 [View Article][PubMed]
    [Google Scholar]
  8. Hacker C. V., Brasier C. M., Buck K. W. 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 [View Article][PubMed]
    [Google Scholar]
  9. Huelsenbeck J. P., Ronquist F. 2001; mrbayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755 [View Article][PubMed]
    [Google Scholar]
  10. Ikeda K., Nakamura H., Matsumoto N. 2003; Hypovirulent strain of the violet root rot fungus Helicobasidium mompa . J Gen Plant Pathol 69:385–390 [View Article]
    [Google Scholar]
  11. Koonin E. V., Dolja V. V., Morris T. J. 1993; Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit Rev Biochem Mol Biol 28:375–430 [View Article][PubMed]
    [Google Scholar]
  12. Lambden P. R., Cooke S. J., Caul E. O., Clarke I. N. 1992; Cloning of noncultivatable human rotavirus by single primer amplification. J Virol 66:1817–1822[PubMed]
    [Google Scholar]
  13. Lütcke H. A., Chow K. C., Mickel F. S., Moss K. A., Kern H. F., Scheele G. A. 1987; Selection of AUG initiation codons differs in plants and animals. EMBO J 6:43–48[PubMed]
    [Google Scholar]
  14. Maddison W. P., Maddison D. R. 2010; Mesquite: a modular system for evolutionary analysis. Version 2.74 http://mesquiteproject.org
  15. Marchler-Bauer A., Anderson J. B., Derbyshire M. K., DeWeese-Scott C., Gonzales N. R., Gwadz M., Hao L., He S., Hurwitz D. I. et al. 2007; CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res 35:Database issueD237–D240 [View Article][PubMed]
    [Google Scholar]
  16. Márquez L. M., Redman R. S., Rodríguez R. J., Roossinck M. J. 2007; A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–515 [View Article][PubMed]
    [Google Scholar]
  17. McLeod M. J., Guttman S. I., Eshbaugh W. H. 1982; Early evolution of chili peppers (Capsicum). Econ Bot 36:361–368 [View Article]
    [Google Scholar]
  18. Moriyama H., Nitta T., Fukuhara T. 1995; Double-stranded RNA in rice: a novel RNA replicon in plants. Mol Gen Genet 248:364–369 [View Article][PubMed]
    [Google Scholar]
  19. Moriyama H., Horiuchi H., Koga R., Fukuhara T. 1999; Molecular characterization of two endogenous double-stranded RNAs in rice and their inheritance by interspecific hybrids. J Biol Chem 274:6882–6888 [View Article][PubMed]
    [Google Scholar]
  20. Morris T. J., Dodds J. A. 1979; Isolation and analysis of double-stranded RNA from virus-infected plant and fungal tissue. Phytopathology 69:854–858 [View Article]
    [Google Scholar]
  21. Moscone E. A., Scaldaferro M. A., Grabiele M, Cecchini N. M., Sánchez Garcia Y., Jarret R., Daviña J. R., Ducasse D. A., Barboza G. E., Eherendorfer F. 2007; The evolution of chili peppers (Capsicum – Solanaceae): a cytogenetic perspective. Acta Hortic 745:137–170
    [Google Scholar]
  22. Osaki H., Nakamura H., Sasaki A., Matsumoto N., Yoshida K. 2006; An endornavirus from a hypovirulent strain of the violet root rot fungus, Helicobasidium mompa. . Virus Res 118:143–149 [View Article][PubMed]
    [Google Scholar]
  23. Pfeiffer P. 1998; Nucleotide sequence, genetic organization and expression strategy of the double-stranded RNA associated with the ‘447’ cytoplasmic male sterility trait in Vicia faba. . J Gen Virol 79:2349–2358[PubMed]
    [Google Scholar]
  24. Pickersgill B. 1966; The variability and relationships of Capsicum chinense Jacq. PhD dissertation Bloomington, Indiana, USA: Indiana University;
    [Google Scholar]
  25. Pickersgill B. 1971; Relationships between weedy and cultivated forms in some species of chili peppers (genus Capsicum). Evolution 25:683–691 [View Article]
    [Google Scholar]
  26. Poch O., Sauvaget I., Delarue M., Tordo N. 1989; Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J 8:3867–3874[PubMed]
    [Google Scholar]
  27. Roossinck M. J., Sabanadzovic S., Okada R., Valverde R. A. 2011; The remarkable evolutionary history of endornaviruses. J Gen Virol 92:2674–2678 [CrossRef]
    [Google Scholar]
  28. Roossinck M. J., Saha P., Wiley G. B., Quan J., White J. D., Lai H., Chavarría F., Shen G., Roe B. A. 2010; Ecogenomics: using massively parallel pyrosequencing to understand virus ecology. Mol Ecol 19:Suppl. 181–88 [View Article][PubMed]
    [Google Scholar]
  29. Rozanov M. N., Koonin E. V., Gorbalenya A. E. 1992; Conservation of the putative methyltransferase domain: a hallmark of the ‘Sindbis-like’ supergroup of positive-strand RNA viruses. J Gen Virol 73:2129–2134 [View Article][PubMed]
    [Google Scholar]
  30. Sabanadzovic S., Valverde R. A. 2011; Properties and detection of two cryptoviruses from pepper (Capsicum annuum). Virus Genes 43:307–312 [View Article][PubMed]
    [Google Scholar]
  31. Stielow B., Klenk H.-P., Menzel W. 2011; Complete genome sequence of the first endornavirus from the ascocarp of the ectomycorrhizal fungus Tuber aestivum Vittad. Arch Virol 156:343–345 [View Article][PubMed]
    [Google Scholar]
  32. Swofford D. L. 2002; paup*: Phylogenetic analysis using parsimony (and other methods), version 4. Sunderland, MA: Sinauer Associates;
    [Google Scholar]
  33. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [View Article][PubMed]
    [Google Scholar]
  34. Tuomivirta T. T., Kaitera J., Hantula J. 2009; A novel putative virus of Gremmeniella abietina type B (Ascomycota: Helotiaceae) has a composite genome with endornavirus affinities. J Gen Virol 90:2299–2305 [View Article][PubMed]
    [Google Scholar]
  35. Valverde R. A., Fontenot J. F. 1991; Variation in double-stranded ribonucleic acid among pepper cultivars. J Am Soc Hortic Sci 116:903–905
    [Google Scholar]
  36. Valverde R. A., Gutierrez D. L. 2007; Transmission of a dsRNA in bell pepper and evidence that it consists of the genome of an endornavirus. Virus Genes 35:399–403 [View Article][PubMed]
    [Google Scholar]
  37. Valverde R. A., Gutierrez D. L. 2008; Molecular and biological properties of a putative partitivirus from Jalapeño pepper (Capsicum annuum L.). Rev Mex Fitopatol 26:1–6
    [Google Scholar]
  38. Valverde R. A., Nameth S. T., Jordan R. L. 1990a; Analysis of double-stranded RNA for plant virus diagnosis. Plant Dis 74:255–258 [CrossRef]
    [Google Scholar]
  39. Valverde R. A., Nameth S., Abdalla O., Al-Musa O., Desjardins P. R., Dodds J. A. 1990b; Indigenous double-stranded RNA from pepper (Capsicum annum). Plant Sci 67:195–201 [View Article]
    [Google Scholar]
  40. Wakarchuk D. A., Hamilton R. I. 1990; Partial nucleotide sequence from enigmatic dsRNAs in Phaseolus vulgaris. . Plant Mol Biol 14:637–639 [View Article][PubMed]
    [Google Scholar]
  41. Zabalgogeazcoa I. A., Gildow F. E. 1992; Double-stranded ribonucleic acid in ‘Barsoy’ Barley. Plant Sci 83:187–194 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.034686-0
Loading
/content/journal/jgv/10.1099/vir.0.034686-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed