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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)
Publication Information
Molecules and Cells / v.23, no.3, 2007 , pp. 304-315 More about this Journal
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
dsRNA Mycovirus; F. graminearum; Genome Organization; Hypovirulence;
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1 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   DOI   ScienceOn
2 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
3 Boland, G. J. (1992) Hypovirulence and double-stranded RNA in Sclerotinia sclerotiorum. Can. J. Plant Pathol. 14, 10-17   DOI
4 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   DOI   ScienceOn
5 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   DOI   ScienceOn
6 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   DOI   ScienceOn
7 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   DOI   ScienceOn
8 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
9 Koonin, E. V. (1991) The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 72, 2197-2206   DOI   ScienceOn
10 Kozak, M. (1999) Initiation of translation in prokaryotes and eukaryotes. Gene 234, 187-208   DOI   ScienceOn
11 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
12 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
13 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   DOI   ScienceOn
14 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
15 Mayo, M. A. (2002) A summary of taxonomic changes recently approved by ICTV. Arch. Virol. 147, 1655-1663   DOI   ScienceOn
16 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   DOI   ScienceOn
17 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   DOI   ScienceOn
18 Page, R. D. M. (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 22, 357-358
19 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   DOI
20 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   DOI   ScienceOn
21 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
22 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   DOI   ScienceOn
23 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   DOI   ScienceOn
24 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
25 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   DOI
26 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
27 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
28 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   DOI   ScienceOn
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 Maia, I. G., Seron, K., Haenni, A. L., and Bernardi, F. (1996) Gene expression from viral RNA genomes. Plant Mol. Biol. 32, 367-391   DOI
31 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
32 Wickner, R. B., Esteban, R., and Suzuki, N. (2000) Virus Taxonomy. Academic Press, San Diego, CA
33 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   DOI
34 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
35 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   DOI   ScienceOn
36 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   DOI   ScienceOn
37 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
38 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   DOI   ScienceOn
39 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   DOI   ScienceOn
40 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   DOI   ScienceOn
41 Ghabrial, S. A. (1998) Origin, adaptation and evolutionary pathways of fungal viruses. Virus Genes 16, 119-131   DOI   ScienceOn
42 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   DOI   ScienceOn
43 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   DOI   ScienceOn
44 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   DOI   ScienceOn
45 Hull, R. (2002) Matthews' Plant Virology. Academic Press, San Diego, CA
46 Moriyama, H., Nitta, T., and Fukuhara, T. (1995) Doublestranded RNA in rice: a novel RNA replicon in plants. Mol. Gen. Genet. 248, 364-369   DOI   ScienceOn
47 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
48 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   DOI   ScienceOn
49 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   DOI
50 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
51 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   DOI   ScienceOn
52 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
53 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
54 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   DOI   ScienceOn
55 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   DOI   ScienceOn
56 Ghabrial, S. A., Soldevila, A., and Haven, W. M. (2002) Molecular Biology of double-stranded RNA. CRC, Boca Raton, FL
57 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   DOI
58 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
59 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   DOI   ScienceOn
60 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   DOI
61 Gubler, U. and Hoffman, B. J. (1983) A simple and very efficient method for generating cDNA libraries. Gene 25, 163-269
62 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   DOI
63 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
64 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   DOI   ScienceOn
65 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