Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지

Molecular Characterization of a dsRNA Mycovirus, Fusarium graminearum Virus-DK21, which Is Phylogenetically Related to Hypoviruses but Has a Genome Organization and Gene Expression Strategy Resembling Those of Plant Potex-like Viruses

  • Kwon, Sun-Jung (Research Institute for Agriculture and Life Sciences, Seoul National University) ;
  • Lim, Won-Seok (Department of Agricultural Biotechnology and Center for Plant Molecular Genetics and Breeding Research, Seoul National University) ;
  • Park, Sang-Ho (Department of Agricultural Biotechnology and Center for Plant Molecular Genetics and Breeding Research, Seoul National University) ;
  • Park, Mi-Ri (Department of Agricultural Biotechnology and Center for Plant Molecular Genetics and Breeding Research, Seoul National University) ;
  • Kim, Kook-Hyung (Research Institute for Agriculture and Life Sciences, Seoul National University)
  • Received : 2007.01.06
  • Accepted : 2007.02.23
  • Published : 2007.06.30
⟨ Previous Next ⟩

Abstract

Fusarium graminearum causes a serious scab disease of small grains in Korea. The nucleotide sequence of the genomic RNA of a double-stranded RNA (dsRNA) virus, Fusarium graminearum virus-DK21 (FgV-DK21), from F. graminearum strain DK21, which is associated with hypovirulence in F. graminearum, was determined and compared to the genome sequences of other mycoviruses, including Cryponectria hypoviruses. The FgV-DK21 dsRNA consists of 6,624 nucleotides, excluding the 3'-terminal poly(A) tail. The viral genome has 53- and 46-nucleotide 5' and 3' untranslated regions (UTRs), respectively, and five putative open reading frames. A phylogenetic analysis of the deduced amino acid sequence of ORF1, which encodes a putative RNA-dependent RNA polymerase, and those of other mycoviruses revealed that this organism forms a distinct virus clade with other hypoviruses, and is more distantly related to other mycoviruses (3.8 to 24.0% identity). However, pairwise sequence comparisons of the nucleotide and deduced amino acid sequences of ORFs 2 through 5 revealed no close relationships to other protein sequences currently available in GenBank. Analyses of RNA accumulation by Northern blot and primer extension indicated that these putative gene products are expressed from at least two different subgenomic RNAs (sgRNAs), in contrast to the cases in other hypoviruses. This study suggests the existence of a new, as yet unassigned, genus of mycoviruses that exhibits a potex-like genome organization and sgRNA accumulation.

Keywords

Acknowledgement

Supported by : Korea Research Foundation

References

  1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 https://doi.org/10.1093/nar/25.17.3389
  2. Attoui, H., Billoir, F., Cantaloube, J. F., Biagini, P., de Micco, P., et al. (2000) Strategies for the sequence determination of viral dsRNA genomes. J. Virol. Methods 89, 147-158 https://doi.org/10.1016/S0166-0934(00)00212-3
  3. Ausubel, F. M., Brent, R., Kingstone, R. E., Moore, D. D., Seidman, J. G., et al. (1989) Current protocols in molecular biology. John Wiley & Sons, New York, NY
  4. Beardall, J. M. and Miller, J. D. (1994) Diseases in humans with mycotoxins as possible causes; in Mycotoxins in Grain-Compounds Other than Aflatoxin, Miller, J. D. and Trenbolm, H. L. (eds.), pp. 487-539, Eagan Press, St Paul, MN
  5. Boland, G. J. (1992) Hypovirulence and double-stranded RNA in Sclerotinia sclerotiorum. Can. J. Plant Pathol. 14, 10-17 https://doi.org/10.1080/07060669209500900
  6. Castro, M., Kramer, K., Valdivia, L., Ortiz, S., and Castillo, A. (2003) A double-stranded RNA mycovirus confers hypovirulence- associated traits to Botrytis cinerea. FEMS Microbiol. Lett. 228, 87-91 https://doi.org/10.1016/S0378-1097(03)00755-9
  7. Charmley, L. L., Rosenberg, A., and Trenholm, H. L. (1994) Factors responsible for economic losses due to Fusarium mycotoxin contamination of grains, foods and feedstuffs; in Mycotoxins in Grain-Compounds Other that Aflatoxin, Miller, J. D. and Trenbolm, H. L. (eds.), pp. 471-486, Eagan Press, St Paul, MN
  8. Choi, G. H., Shapira, R., and Nuss, D. L. (1991) Co-translational autoproteolysis involved in gene expression from a doublestranded RNA genetic element associated with hypovirulence of the chestnut blight fungus. Proc. Natl. Acad. Sci. USA 88, 1167-1171
  9. Chu, Y.-M., Jeon, J.-J., Yea, S.-J., Kim, Y.-H., Yun, S.-H., et al. (2002) Double-stranded RNA mycovirus from Fusarium graminearum. Appl. Environ. Microbiol. 68, 2529-2534 https://doi.org/10.1128/AEM.68.5.2529-2534.2002
  10. Chu, Y.-M., Lim, W.-S., Yea, S.-J., Cho, J.-D., Lee, Y.-W., et al. (2004) Complexity of dsRNA mycovirus isolated from Fusarium graminearum. Virus Genes 28, 131-139
  11. Compel, P., Papp, I., Bibo, M., Fekete, C., and Hornok, L. (1999) Genetic interrelationships and genome organization of double-stranded RNA elements of Fusarium poae. Virus Genes 18, 49-56 https://doi.org/10.1023/A:1008069318838
  12. Cook, R. J. (1981) Fusarium diseases of wheat and other small grains in North America; in Fusarium Diseases, Biology, and Taxonomy, Nelson, P. E., Toussoun, T. A., and Cook, R. J. (eds.), pp. 39-52, The Pennsylvania State University Press, University Park, PA
  13. Dawe, A. L. and Nuss, D. L. (2001) Hypoviruses and chestnut blight: exploiting viruses to understand and modulate fungal pathogenesis. Annu. Rev. Genet. 35, 1-29 https://doi.org/10.1146/annurev.genet.35.102401.085929
  14. Dodds, J. A. (1980) Association of type 1 viral-like dsRNA with club-shaped particles in hypovirulent strains of Endothia parasitica. Virology 107, 1-12 https://doi.org/10.1016/0042-6822(80)90267-6
  15. Drugeon, G., Urcuqui-Inchima, S., Milner, M., Kadare, G., Valle, R. P. C., et al. (1999) The strategies of plant virus gene expression: models of economy. Plant Sci. 148, 77-88 https://doi.org/10.1016/S0168-9452(99)00123-5
  16. Fekete, C., Giczey, G., Papp, I., Szabo, L., and Hornok, L. (1995) High-frequency occurrence of virus-like particles with double-stranded RNA genome in Fusarium poae. FEMS Microbiol. Lett. 131, 295-299 https://doi.org/10.1111/j.1574-6968.1995.tb07790.x
  17. Ghabrial, S. A. (1998) Origin, adaptation and evolutionary pathways of fungal viruses. Virus Genes 16, 119-131 https://doi.org/10.1023/A:1007966229595
  18. Ghabrial, S. A., Bozarth, R. F., Buck, K. W., Martelli, G. P., and Milne, R. G. (2000) Partitiviridae; in Virus taxonomy: Seventh Report of the International Committee on Taxonomy of Viruses, van Regenmortel, M. H. V., Fauquet, C. M., Bishop, D. H. L., Carstens, E. B., Estes, M. K., et al. (eds.), pp. 503-513, Academic Press, San Diego, CA
  19. Ghabrial, S. A., Soldevila, A., and Haven, W. M. (2002) Molecular Biology of double-stranded RNA. CRC, Boca Raton, FL
  20. Gorbalenya, A. E., Koonin, E. V., Donchenko, A. P., and Blinov, V. M. (1988) A novel superfamily of nucleoside triphosphatebinding motif-containing proteins which are probably involved in duplex unwinding in DNA and RNA replication and recombination. FEBS Lett. 239, 16-24
  21. Gorbalenya, A. E., Koonin, E. V., Donchenko, A. P., and Blinov, V. M. (1989) Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res. 17, 4713-4730 https://doi.org/10.1093/nar/17.12.4713
  22. Gubler, U. and Hoffman, B. J. (1983) A simple and very efficient method for generating cDNA libraries. Gene 25, 163-269
  23. Hacker, C. V., Brasier, C. M., and Buck, K. W. (2005) A doublestranded RNA from a Phytophthora species is related to the plant endornaviruses and contains a putative UDP glycosyltransferase gene. J. Gen. Virol. 86, 1561-1570 https://doi.org/10.1099/vir.0.80808-0
  24. Hansen, D. R., Van Alfen, N. K., Gillies, K., and Powell, W. A. (1985) Naked dsRNA associated with hypovirulence of Endothia parasitica is packaged in fungal vesicles. J. Gen. Virol. 66, 2605-2614 https://doi.org/10.1099/0022-1317-66-12-2605
  25. Hillman, B. I., Tian, Y., Bedker, P. J., and Brown, M. P. (1992) A North American hypovirulent isolate of the chestnut blight fungus with European isolate-related dsRNA. J. Gen. Virol. 73, 681-686 https://doi.org/10.1099/0022-1317-73-3-681
  26. Hong, Y., Dover, S. L., Cole, T. E., Brasier, C. M., and Buck, K. W. (1999) Multiple mitochondrial viruses in an isolate of the Dutch Elm disease fungus Ophiostoma novo-ulmi. Virology 258, 118-127 https://doi.org/10.1006/viro.1999.9691
  27. Huang, S. and Ghabrial, S. A. (1996) Organization and expression of the double-stranded RNA genome of Helminthosporium victoriae 190S virus, a totivirus infecting a plant pathogenic filamentous fungus. Proc. Natl. Acad. Sci. USA 93, 12541-12546
  28. Hull, R. (2002) Matthews' Plant Virology. Academic Press, San Diego, CA
  29. Icho, T. and Wickner, R. B. (1989) The double-stranded RNA genome of yeast virus L-A encodes its own putative RNA polymerase by fusing two open reading frames. J. Biol. Chem. 264, 6716-6723
  30. Kang, J., Wu, J., Bruenn, J. A., and Park. C. (2001) The H1 double-stranded RNA genome of Ustilago maydis virus-H1 encodes a polyprotein that contains structural motifs for capsid polypeptide, papain-like protease, and RNA-depen-dent RNA polymerase. Virus Res. 76, 183-189 https://doi.org/10.1016/S0168-1702(01)00250-7
  31. Kim, K.-H. and Hemenway, C. L. (1996) The 5′ nontranslated region of potato virus X RNA affects both genomic and subgenomic RNA synthesis. J. Virol. 70, 5533-5540
  32. Kim, K.-H. and Hemenway, C. L. (1997) Mutations that alter a conserved element upstream of the potato virus X triple block and coat protein genes affect subgenomic RNA accumulation. Virology 232, 187-197 https://doi.org/10.1006/viro.1997.8565
  33. Kommedahl, T. and Windels, C. E. (1981) Root-, stalk-, and earinfecting Fusarium species on corn in the USA; in Fusarium Diseases, Biology, and Taxonomy, Nelson, P. E., Toussoun, T. A., and Cook, R. J. (eds.), pp. 94-103, The Pennsylvania State University Press, University Park, PA
  34. Koonin, E. V. (1991) The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 72, 2197-2206 https://doi.org/10.1099/0022-1317-72-9-2197
  35. Koonin, E. V., Choi, G. H., Nuss, D. L., Shapira, R., and Carrington, J. C. (1991) Evidence for common ancestry of a chestnut blight hypovirulence-associated double-stranded RNA and a group of positive-strand RNA viruses. Proc. Natl. Acad. Sci. USA 88, 10647-10651
  36. Kozak, M. (1999) Initiation of translation in prokaryotes and eukaryotes. Gene 234, 187-208 https://doi.org/10.1016/S0378-1119(99)00210-3
  37. Kwon, S.-J. and Kim, K.-H. (2006) The SL1 stem-loop structure at the 5′-end of Potato virus X RNA is required for efficient binding to host proteins and for viral infectivity. Mol. Cells 21, 63-75
  38. Lakshman, D. K., Jian, J., and Tavantzis, S. M. (1998) A doublestranded 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. Natl. Acad. Sci. USA 95, 6425-6429
  39. Linder-Basso, D., Dynek, J. N., and Hillman, B. I. (2005) Genome analysis of Cryphonectria hypovirus 4, the most common hypovirus species in North America. Virology 337, 192-203 https://doi.org/10.1016/j.virol.2005.03.038
  40. Maia, I. G., Seron, K., Haenni, A. L., and Bernardi, F. (1996) Gene expression from viral RNA genomes. Plant Mol. Biol. 32, 367-391 https://doi.org/10.1007/BF00039391
  41. Marasas, W. F. O., Nelson, P. E., and Toussoun, T. A. (1984) Toxigenic Fusarium species: identity and mycotoxicology. The Pennsylvania State University Press, University Park, PA
  42. Mayo, M. A. (2002) A summary of taxonomic changes recently approved by ICTV. Arch. Virol. 147, 1655-1663 https://doi.org/10.1007/s007050200039
  43. Moriyama, H., Nitta, T., and Fukuhara, T. (1995) Doublestranded RNA in rice: a novel RNA replicon in plants. Mol. Gen. Genet. 248, 364-369 https://doi.org/10.1007/BF02191603
  44. Nogawa, M., Kageyama, S. T., and Okazaki, M. (1993) A double-stranded RNA mycovirus from the plant pathogenic fungus, Fusarium solani f. sp. robiniae. FEMS Microbiol. Lett. 110, 153-158 https://doi.org/10.1111/j.1574-6968.1993.tb06312.x
  45. Nogawa, M., Kageyama, T., Nakatani, A., Taguchi, G., Shimosaka, M., et al. (1996) Cloning and characterization of mycovirus double-stranded RNA from the plant pathogenic fungus, Fusarium solani f. sp. robiniae. Biosci. Biotechnol. Biochem. 60, 784-788 https://doi.org/10.1271/bbb.60.784
  46. Osaki, H., Nakamura, H., Sasaki, A., Matsumoto, N., and Yoshida, K. (2006) An endornavirus from a hypovirulent strain of the violet root rot fungus, Helicobasidium mompa. Virus Res. 118, 143-149 https://doi.org/10.1016/j.virusres.2005.12.004
  47. Page, R. D. M. (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 22, 357-358
  48. Pfeiffer, P. (1998) Nucleotide sequence, genetic organization and expression strategy of the double-stranded RNA associated with the '447' cytoplasmic male steility trait in Vicia fava. J. Gen. Virol. 79, 2349-2358 https://doi.org/10.1099/0022-1317-79-10-2349
  49. Polashock, J. J. and Hillman, B. I. (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. Natl. Acad. Sci. USA 91, 8680-8684
  50. Preisig, O., Wingfield, B. D., and Wingfield, M. J. (1998) Coinfection of a fungal pathogen by two distinct double-stranded RNA viruses. Virology 252, 399-406 https://doi.org/10.1006/viro.1998.9480
  51. Preisig, O., Moleleki, N., Smit, W. A., Wingfield, B. D., and Wingfield, M. J. (2000) A novel RNA mycovirus in a hypovirulent isolate of the plant pathogen Diaporthe ambigua. J. Gen. Virol. 81, 3107-3114 https://doi.org/10.1099/0022-1317-81-12-3107
  52. Rae, B. P., Hillman, B. I., Tartaglia, J., and Nuss, D. L. (1989) Characterization of double-stranded RNA genetic elements associated with biological control of chestnut blight: organization of terminal domains and identification of gene products. EMBO J. 8, 657-663
  53. Rong, R., Rao, S., Scott, S. W., Carner, G. R., and Tainter, F. H. (2002) Complete sequence of the genome of two dsRNA viruses from Discula destructiva. Virus Res. 90, 217-224 https://doi.org/10.1016/S0168-1702(02)00178-8
  54. Seo, J. K., Lim, W. S., Jeong, J. H., Yoo, Y. B., Yie, S. W., et al. (2004) Characterization and RT-PCR detection of dsRNA mycoviruses from the oyster mushroom, Pleurotus ostreatus. Plant Pathol. J. 20, 200-205 https://doi.org/10.5423/PPJ.2004.20.3.200
  55. Smart, C. D., Yuan, W., Foglia, R., Nuss, D. L., Fulbright, D. W., et al. (1999) Cryphonectria hypovirus 3, a virus species in the family hypoviridae with a single open reading frame. Virology 265, 66-73 https://doi.org/10.1006/viro.1999.0039
  56. Soldevila, A. I. and Ghabrial, S. A. (2000) Expression of the Totivirus Helminthosporium victoriae 190S virus RNAdependent RNA polymerase from its downstream open reading frame in dicistronic constructs. J. Virol. 74, 997- 1003 https://doi.org/10.1128/JVI.74.2.997-1003.2000
  57. Strauss, E. E., Lakshman, D. K., and Tavantzis, S. M. (2000) Molecular characterization of the genome of a partitivirus from the basidiomycete Rhizoctonia solani. J. Gen. Virol. 81, 549-555 https://doi.org/10.1099/0022-1317-81-2-549
  58. Suzuki, N., Supyani, S., Maruyama, K., and Hillman, B. I. (2004) Complete genome sequence of Mycoreovirus-1/Cp9B21, a member of a novel genus within the family Reoviridae, isolated from the chestnut blight fungus Cryphonectria parasitica. J. Gen. Virol. 85, 3437-3448 https://doi.org/10.1099/vir.0.80293-0
  59. Varga, J., Toth, B., Szencz, S., Molnar, J., Fekete, C. S., et al. (2001) Double-stranded rna elements and virus-like particles in Aspergilli. Acta. Biol. Hung. 52, 355-363 https://doi.org/10.1556/ABiol.52.2001.2-3.20
  60. Varga, J., Rigo, K., Molnar, J., Toth, B., Szencz, S., et al. (2003) Mycotoxin production and evolutionary relationships among species of Aspergillus section Clavati. Antonie Van Leeuwenhoek 83, 191-200 https://doi.org/10.1023/A:1023355707646
  61. Wang, A. L., Yang, H. M., Shen, K. A., and Wang, C. C. (1993) Giardiavirus double-stranded RNA genome encodes a capsid polypeptide and a gag-pol-like fusion protein by a translation frameshift. Proc. Natl. Acad. Sci. USA 90, 8595-8599
  62. Wei, C. Z., Osaki, H., Iwanami, T., Matsumoto, N., and Ohtsu, Y. (2003) Molecular characterization of dsRNA segments 2 and 5 and electron microscopy of a novel reovirus from a hypovirulent isolate, W370, of the plant pathogen Rosellinia necatrix. J. Gen. Virol. 84, 2431-2437 https://doi.org/10.1099/vir.0.19098-0
  63. Wickner, R. B., Esteban, R., and Suzuki, N. (2000) Virus Taxonomy. Academic Press, San Diego, CA
  64. Wickner, R. B., Ghabrial, S. A., Bruenn, J., Buck, K. W., Patterson, J. K., et al. (2000) Tortiviridae; in Virus Taxonomy: Seventh Report of the International Committee on Taxonomy of Viruses, Regenmortel, M. H. V., Fauquet, C. M., Bishop, D. H. L., Carstens, E. B., Estes, M. K., et al. (eds.), pp. 491-501, Academic Press, San Diego, CA
  65. Windels, C. E. (2000) Economic and social impacts of Fusarium headblight changing farms and rural communities in the Northern Great Plains. Phytopathology 90, 17-21 https://doi.org/10.1094/PHYTO.2000.90.1.17