New insights into mycoviruses and exploration for the biological control of crop fungal diseases

Annual Review of Phytopathology

Volumn 52, Issue , 2014, Pages 45-68

  Xie, Jiatao ^a   Jiang, Daohong ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Biological control; Crop fungal diseases; Fungal plant pathogen; Hypovirulence; Mycovirus

Indexed keywords

BIOLOGICAL PEST CONTROL; CROP; FUNGUS; MICROBIOLOGY; MYCOSES; VIROLOGY;

CROPS, AGRICULTURAL; FUNGI; MYCOSES; PEST CONTROL, BIOLOGICAL;

EID: 84905502065     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-phyto-102313-050222     Document Type: Article

References (136)

1. Anagnostakis SL. 1982. Anagnostakis biological control of chestnut blight. Science 215:466-71
2. Bidard F, Clave C, Saupe SJ. 2013. The transcriptional response to nonself in the fungus Podospora anserina. G3 (Bethesda) 3(6):1015-30
3. Biella S, Smith ML, Aist JR, Cortesi P, Milgroom MG. 2002. Programmed cell death correlates with virus transmission in a filamentous fungus. Proc. Biol. Sci. 269:2269-76
4. Biraghi A. 1953. Possible active resistance to Endothia parasitica in Castanea sativa. Rep.Congr. Int.Union For. Res. Org., 11th, Rome
5. Boine B, Kingston RL, Pearson MN. 2012. Recombinant expression of the coat protein of Botrytis virus X and development of an immunofluorescence detection method to study its intracellular distribution in Botrytis cinerea. J. Gen. Virol. 93:2502-11
6. Boland GJ. 1992. Hypovirulence and double-stranded RNA in Sclerotinia sclerotiorum. Can. J. Plant Pathol. 14:10-17
7. Bolton M, Thomma BPHJ, Nelson B. 2006. Sclerotinia sclerotiorum (Lib.) de Bary: biology andmolecular traits of a cosmopolitan pathogen. Mol. Plant. Pathol. 7:1-16
8. Brusini J, Robin C. 2013. Mycovirus transmission revisited by in situ pairings of vegetatively incompatible isolates of Cryphonectria parasitica. J. Virol. Methods 187(2):435-42
9. Bryner SF, Rigling D. 2012. Virulence not only costs but also benefits the transmission of a fungal virus. Evolution 66(8):2540-50
10. Cai G, Hillman BI. 2013. Phytophthora viruses. Adv. Virus Res. 86:327-50
11. Caston JR, Luque D, Trus BL, Rivas G, Alfonso C, et al. 2006. Three-dimensional structure and stoichiometry of Helmintosporium victoriae 190S totivirus. Virology 347:323-32
12. Castro M, Kramer K, Valdivia L, Ortiz S, Castillo A. 2003. A double-stranded RNA mycovirus confers hypovirulence-associated traits to Botrytis cinerea. FEMS Microbiol. Lett. 228(1):87-91
13. Chen B, Choi GH, Nuss DL. 1994. Attenuation of fungal virulence by synthetic infectious hypovirus transcripts. Science 264:1762-64
14. Chen B, Nuss DL. 1999. Infectious cDNA clone of hypovirus CHV1-Euro7: a comparative virology approach to investigate virus-mediated hypovirulence of the chestnut blight fungus Cryphonectria parasitica. J. Virol. 73:985-92
15. Chiba S, Kondo H, Tani A, Saisho D, Sakamoto W, et al. 2011. Widespread endogenization of genome sequences of non-retroviral RNA viruses into plant genomes. PLoS Pathog. 7(7):e1002146
16. Chiba S, Lin YH, Kondo H, Kanematsu S, Suzuki N. 2013. Effects of defective interfering RNA on symptom induction by, and replication of, a novel partitivirus from a phytopathogenic fungus, Rosellinia necatrix. J. Virol. 87(4):2330-41
17. Chiba S, Lin YH, Kondo H, Kanematsu S, Suzuki N. 2013. A novel Victorivirus from a phytopathogenic fungus, Rosellinia necatrix, is infectious as particles and targeted by RNA silencing. J. Virol. 87(12):6727-38
18. Chiba S, Salaipeth L, Lin YH, Sasaki A, Kanematsu S, et al. 2009. A novel bipartite double-strandedRNA mycovirus from the white root rot fungus Rosellinia necatrix: molecular and biological characterization, taxonomic considerations, and potential for biological control. J. Virol. 83(24):12801-12
19. Cho WK, Lee KM, Yu J, Son M, Kim KH. 2013. Insight into mycoviruses infecting Fusarium species. Adv. Virus Res. 86:273-88
20. Cho WK, Yu J, Lee KM, Son M, Min K, et al. 2012. Genome-wide expression profiling shows transcriptional reprogramming in Fusarium graminearum by Fusarium graminearum virus 1-DK21 infection. BMC Genomics 13:173
21. Choi GH, Dawe AL, Churbanov A, Smith ML, Milgroom MG, et al. 2012. Molecular characterization of vegetative incompatibility genes that restrict hypovirus transmission in the chestnut blight fungus Cryphonectria parasitica. Genetics 190(1):113-27
22. Choi GH, Nuss DL. 1992. A viral gene confers hypovirulence associated traits to the chestnut blight fungus. EMBO J. 11:473-77
23. Choi GH, Nuss DL. 1992. Hypovirulence of chestnut blight fungus conferred by an infectious viral cDNA. Science 257:800-3
24. Chun SJ, Lee YH. 1997. Inheritance of dsRNAs in the rice blast fungus, Magnaporthe grisea. FEMS Microbiol. Lett. 148(2):159-62
25. Dawe AL, Nuss DL. 2001. Hypoviruses and chestnut blight: exploiting viruses to understand and modulate fungal pathogenesis. Annu. Rev. Genet. 35:1-29
26. Dawe AL, Nuss DL. 2013. Hypovirus molecular biology: fromKoch's postulates to host self-recognition genes that restrict virus transmission. Adv. Virus Res. 86:109-47
27. Dayaram A, Jaschke A, Hadfield J, Baschiera M, Dobson RC, et al. 2012. Molecular characterisation of a novel cassava associated circular ssDNA virus. Virus Res. 166:130-35
28. Deng F, Boland GJ. 2003. Hypovirulence-associated double-stranded RNA from Sclerotinia homoeocarpa is conspecific with Ophiostoma novo-ulmi mitovirus 3a-Ld. Phytopathology 93(11):1407-14
29. Deng Q, Ye Y, Miao M, Fang Q, Li T, et al. 2010. The horizontal transmission of Cryphonectria hypovirus 1 (CHV1) is affected by virus strains. Chinese Sci. Bull. 54(17):3053-60
30. de Sa PB, Havens WM, Ghabrial SA. 2010. Characterization of a novel broad-spectrum antifungal protein from virus-infected Helminthosporium (Cochliobolus) victoriae. Phytopathology 100(9):880-89
31. Ding SW. 2010. RNA-based antiviral immunity. Nat. Rev. Immunol. 10:632-44
32. Dunn SE, Li H, Cardone G, Nibert ML, Ghabrial SA, et al. 2013. Three-dimensional structure of victorivirus HvV190S suggests coat proteins in most totiviruses share a conserved core. PLoS Pathog. 9(3):e1003225
33. Fedorova ND, Badger JH, Robson GD, Wortman JR, Nierman WC. 2005. Comparative analysis of programmed cell death pathways in filamentous fungi. BMC Genomics 6:177
34. Fulbright DW. 1984. Effect of eliminating dsRNA in hypovirulent Endothia parasitica. Phytopathology 74:722-72
35. Ghabrial SA. 1998. Origin, adaptation and evolutionary pathways of fungal viruses. VirusGenes 16(1):119-31
36. Ghabrial SA, Dunn SE, Li H, Xie J, Baker TS. 2013. Viruses of Helminthosporium (Cochlioblus) victoriae. Adv. Virus Res. 86:289-325
37. Ghabrial SA, Havens WM. 1992. The Helminthosporium victoriae 190S mycovirus has two forms distinguishable by capsid protein composition and phosphorylation state. Virology 188:657-65
38. Ghabrial SA, Soldevila AI, Havens WM. 2002. Molecular genetics of the viruses infecting the plant pathogenic fungus Helminthosporium victoriae. In Molecular Biology of Double-Stranded RNA: Concepts and Applications in Agriculture, Forestry and Medicine, ed. S Tavantzis, pp. 213-36. Boca Raton, FL: CRC Press
39. Ghabrial SA, Suzuki N. 2009. Viruses of plant pathogenic fungi. Annu. Rev. Phytopathol. 47:353-84
40. Grasse W, Zipper R, Totska M, Spring O. 2013. Plasmopara halstedii virus causes hypovirulence in Plasmopara halstedii, the downy mildew pathogen of the sunflower. Fungal Genet. Biol. 57:42-47
41. Heiniger U, Rigling D. 1994. Biological control of chestnut blight in Europe. Annu. Rev. Phytopathol. 32:581-99
42. Heller-Dohmen M, Gopfert JC, Pfannstiel J, Spring O. 2011. The nucleotide sequence and genome organization of Plasmopara halstedii virus. Virol. J. 8:123
43. Hillman BI, Fulbright DW, Nuss DL, Van Alfen NK. 1995. Hypoviridae. In Virus Taxonomy, ed. FA Murphy, pp. 261-64. New York: Springer Verlag
44. Hillman BI, Halpern BT, Brown MP. 1994. A viral dsRNA element of the chestnut blight fungus with a distinct genetic organization. Virology 201:241-50
45. Hillman BI, Shapira R, Nuss DL. 1990. Hypovirulence-associated suppression of host functions in Cryphonectria parasitica can be partially relieved by high light intensity. Phytopathology 80:950-56
46. Hillman BI, Supyani S, Kondo H, Suzuki N. 2004. A reovirus of the fungus Cryphonectria parasitica that is infectious as particles and related to the Coltivirus genus of animal pathogens. J. Virol. 78:892-98
47. Hillman BI, Suzuki N. 2004. Viruses of the chestnut blight fungus, Cryphonectria parasitica. Adv. Virus Res. 63:423-72
48. Hillman BI, Tian Y, Bedker PJ, Brown MP. 1992. ANorth American hypovirulent isolate of the chestnut blight fungus with European isolate-related dsRNA. J. Gen. Virol. 73:681-86
49. Howitt R, Beever RE, Pearson MN, Forster RL. 1995. Presence of double-stranded RNA and virus like particles in Botrytis cinerea. Mycol. Res. 99:1472-78
50. Hutchison E, Brown S, Tian C, Glass NL. 2005. Transcriptional profiling and functional analysis of heterokaryon incompatibility in Neurospora crassa reveals that reactive oxygen species, but not metacaspases, are associated with programmed cell death. Microbiology 155:3957-70
51. Ikeda K, Inoue K, Kida C, Uwamori T, Sasaki A, et al. 2013. Potentiation of mycovirus transmission by zinc compounds via attenuation of heterogenic incompatibility in Rosellinia necatrix. Appl. Environ. Microbiol. 79(12):3684-91
52. Jian JH, Lakshman DK, Tavantzis SM. 1998. A virulence-associated, 6.4-kb, double-strandedRNAfrom Rhizoctonia solani is phylogenetically related to plant bromoviruses and electron transport enzymes. Mol. Plant-Microbe Interact. 11(7):601-9
53. Jiang D, Fu Y, Li G, Ghabrial SA. 2013. Viruses of the plant pathogenic fungus Sclerotinia sclerotiorum. Adv. Virus Res. 86:215-48
54. Kanematsu S, Sasaki A, Onoue M, Oikawa Y, Ito T. 2010. Extending the fungal host range of a partitivirus and a mycoreovirus from Rosellinia necatrix by inoculation of protoplasts with virus particles. Phytopathology 100(9):922-30
55. Khalifa ME, Pearson MN. 2013. Molecular characterization of three mitoviruses co-infecting a hypovirulent isolate of Sclerotinia sclerotiorum fungus. Virology 441(1):22-30
56. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, eds. 2012. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Amsterdam, The Neth.: Elsevier Acad.
57. Kondo H, Chiba S, Toyoda K, Suzuki N. 2013. Evidence for negative-strand RNA virus infection in fungi. Virology 435(2):201-9
58. Kondo H, Kanematsu S, Suzuki N. 2013. Viruses of the white root rot fungus, Rosellinia necatrix. Adv. Virus Res. 86:177-214
59. Koonin EV, Choi GH, Nuss DL, Shapira R, Carrington JC. 1991. Evidence for common ancestry of a chestnut blight hypovirulence associated double-stranded RNA and a group of positive-strand RNA plant viruses. Proc. Natl. Acad. Sci. USA 88:10647-51
60. Kraberger S, Stainton D, Dayaram A, Zawar-Reza P, Gomez C, et al. 2013. Discovery of Sclerotinia sclerotiorum hypovirulence-associated virus-1 in urban river sediments of Heathcote and Styx Rivers in Christchurch city, New Zealand. Genome Announc. 1(4):e559-613
61. Krupovic M. 2013. Networks of evolutionary interactions underlying the polyphyletic origin of ssDNA viruses. Curr. Opin. Virol. 3(5):578-86
62. Kwon SJ, Cho SY, Lee KM, Yu J, Son M, et al. 2009. Proteomic analysis of fungal host factors differentially expressed by Fusarium graminearum infected with Fusarium graminearum virus-DK21. Virus Res. 144(1-2):96-106
63. Kwon SJ, Lim WS, Park SH, Park MR, Kim KH. 2007. 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. Mol. Cells 23(3):304-15
64. 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. Natl. Acad. Sci. USA 195(11):6425-29
65. Lee KM, Yu J, Son M, Lee YW, Kim KH. 2012. Transmission of Fusarium boothii mycovirus via protoplast fusion causes hypovirulence in other phytopathogenic fungi. PLoS ONE 6:e21629
66. Li G, Wang D, Jiang D, Huang HC. 2000. First report of Sclerotinia nivalis on lettuce in central China. Mycol. Res. 104(2):232-37
67. Li H, Fu Y, Jiang D, Li G, Ghabrial SA, et al. 2008. Down-regulation of Sclerotinia sclerotiorum gene expression in response to infectionwith Sclerotinia sclerotiorum debilitation-associatedRNAvirus. Virus Res. 135(1):95-106
68. Li H, Havens WM, Nibert ML, Ghabrial SA. 2011. RNA sequence determinants of a coupled termination-reinitiation strategy for downstream open reading frame translation in Helminthosporium victoriae virus 190S and other victoriviruses (Family Totiviridae). J. Virol. 85(14):7343-52
69. Lin YH, Chiba S, Tani A, Kondo H, Sasaki A, et al. 2012. A novel quadripartite dsRNA virus isolated from a phytopathogenic filamentous fungus, Rosellinia necatrix. Virology 2426(1):42-50
70. Lin YH, Hisano S, Yaegashi H, Kanematsu S, Suzuki N. 2013. A second quadrivirus strain from the phytopathogenic filamentous fungus Rosellinia necatrix. Arch. Virol. 158(5):1093-98
71. Linder-Basso D, Dynek JN, Hillman BI. 2005. Genome analysis of Cryphonectria hypovirus 4, the most common hypovirus species in North America. Virology 337:192-203
72. Liu H, Fu Y, Jiang D, Li G, Xie J, et al. 2009. A novel mycovirus that is related to the human pathogen hepatitis E virus and rubi-like viruses. J. Virol. 83(4):1981-91
73. Liu H, Fu Y, Jiang D, LiG, Xie J, et al. 2010. Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes. J. Virol. 84(22):11876-87
74. Liu H, Fu Y, Xie J, Cheng J, Ghabrial SA, et al. 2012. Discovery of novel dsRNA viral sequences by in silico cloning and implications for viral diversity, host range and evolution. PLoS ONE 7(7):e42147
75. Liu H, Fu Y, Xie J, Cheng J, Ghabrial SA, et al. 2012. Evolutionary genomics of mycovirus-related dsRNA viruses reveals cross-family horizontal gene transfer and evolution of diverse viral lineages. BMC Evol. Biol. 12:91
76. Liu YC, Dynek JN, Hillman BI, Milgroom MG. 2007. Diversity of viruses in Cryphonectria parasitica and C. nitschkei in Japan and China, and partial characterization of a new chrysovirus species. Mycol. Res. 111:433-43
77. Liu YC, Linder-Basso D, Hillman BI, Kaneko S, Milgroom MG. 2003. Evidence for interspecies transmission of viruses in natural populations of filamentous fungi in the genus Cryphonectria. Mol. Ecol. 12(6):1619-28
78. Maejima K, Himeno M, Komatsu K, Kakizawa S, Yamaji Y, et al. 2008. Complete nucleotide sequence of a new double-strandedRNAvirus from the rice blast fungus, Magnaporthe oryzae. Arch. Virol. 153(2):389-91
79. Marvelli RA, Hobbs HA, Li S, McCoppin NK, Domier LL, et al. 2014. Identification of novel doublestranded RNA mycoviruses of Fusarium virguliforme and evidence of their effects on virulence. Arch. Virol. 159(2):349-52
80. McCabe PM, Pfeiffer P, Van Alfen NK. 1999. The influence of dsRNA viruses on the biology of plant pathogenic fungi. Trends Microbiol. 7:377-81
81. McFadden JJP, Buck KW, Rawlinson CJ. 1983. Infrequent transmission of double-stranded RNA virus particles but absence ofDNA proviruses in single ascospore cultures of Gaeumannomyces graminis. J. Gen. Virol. 64:927-37
82. Melzer MS, Ikeda SS, Boland GJ. 2002. Interspecific transmission of double-stranded RNA and hypovirulence from Sclerotinia sclerotiorum to S. minor. Phytopathology 92(7):780-84
83. Milgroom MG, Cortesi P. 2004. Biological control of chestnut blight with hypovirulence: a critical analysis. Annu. Rev. Phytopathol. 42:311-38
84. Milgroom MG, Wang K, Zhou Y, Lipari SE, Kaneko S. 1996. Intercontinental population structure of the chestnut blight fungus, Cryphonectria parasitica. Mycologia 88:179-90
85. Moleleki N, Wingfield MJ, Wingfield BD, Preisig O. 2011. Effect of Diaporthe RNA virus 1 (DRV1) on growth and pathogenicity of different Diaporthe species. Eur. J. Plant. Pathol. 131(2):261-68
86. Ng TF, Willner DL, Lim YW, Schmieder R, Chau B, et al. 2011. Broad surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLoS ONE 6:e20579
87. Nuss DL. 1992. Biological control of chestnut blight: an example of virus-mediated attenuation of fungal pathogenesis. Microbiol. Rev. 56:561-76
88. Nuss DL. 1996. Using hypoviruses to probe and perturb signal transduction processes underlying fungal pathogenesis. Plant Cell 8:1846-53
89. Nuss DL. 2000. Hypovirulence and chestnut blight: from the field to the laboratory and back. In Fungal Pathology, ed. JW Kronstad, pp. 149-70. The Hague, The Neth.: Kluwer Acad.
90. Nuss DL. 2005. Hypovirulence: mycoviruses at the fungal-plant interface. Nat. Rev. Microbiol. 3:632-42
91. Nuss DL. 2011. Mycoviruses, RNA silencing, and viral RNA recombination. Adv. Virus Res. 80:25-48
92. Nuss DL, Koltin Y. 1990. Significance of dsRNA genetic elements in plant pathogenic fungi. Annu. Rev. Phytopathol. 28:37-58
93. Pearson MN, Beever RE, Boine B, Arthur K. 2009. Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol. Plant Pathol. 10(1):115-28
94. Phan TG, Kapusinszky B, Wang C, Rose RK, Lipton HL, et al. 2011. The fecal viral flora of wild rodents. PLoS Pathog. 7(9):e1002218
95. 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 andWdsRNAs. Proc. Natl. Acad. Sci. USA 91:8680-84
96. Preisig O, Moleleki N, Smit WA, Wingfield BD, Wingfield MJ. 2000. A novel RNA mycovirus in a hypovirulent isolate of the plant pathogen Diaporthe ambigua. J. Gen. Virol. 81(12):3107-14
97. Rodrguez-Garca C, Medina V, Alonso A, Ayllon MA. 2013. Mycoviruses of Botrytis cinerea isolates from different hosts. Ann. Appl. Biol. 164:46-61
98. Roossinck MJ. 2011. The good viruses: viral mutualistic symbioses. Nat. Rev. Microbiol. 9(2):99-108
99. Rosario K, Dayaram A, Marinov M, Ware J, Kraberger S, et al. 2012. Diverse circular ssDNA viruses discovered in dragonflies (Odonata: Epiprocta). J. Gen. Virol. 93(12):2668-81
100. Saccardo F, Cettul E, Palmano S, Noris E, Firrao G. 2011. On the alleged origin of geminiviruses from extrachromosomal DNAs of phytoplasmas. BMC Evol. Biol. 11:185
101. Salaipeth L, Chiba S, Eusebio-Cope A, Kanematsu S, Suzuki N. 2013. Biological properties and expression strategy of Rosellinia necatrix megabirnavirus 1 analyzed in an experimental host, Cryphonectria parasitica. J. Gen. Virol. 95 (Pt. 3):740-50
102. Sasaki A, Kanematsu S, Onoue M, Oikawa Y, Nakamura H, et al. 2007. Artificial infection of Rosellinia necatrix with purified viral particles of a member of the genus mycoreovirus reveals its uneven distribution in single colonies. Phytopathology 97:278-86
103. Sasaki A, Onoue M, Kanematsu S, Suzaki K, Miyanishi M, et al. 2002. Extending chestnut blight hypovirus host range within diaporthales by biolistic delivery of viral cDNA. Mol. Plant-Microbe Interact. 15(8):780-89
104. Shang J, Wu X, Lan X, Fan Y, Dong H, et al. 2008. Large-scale expressed sequence tag analysis for the chestnut blight fungus Cryphonectria parasitica. Fungal Genet. Biol. 45(3):319-27
105. Shapira R, Choi GH, Nuss DL. 1991. Virus-like genetic organization and expression strategy for a double-stranded RNA genetic element associated with biological control of chestnut blight. EMBO J. 10(4):731-39
106. Sikorskia A, Massaro M, Kraberger S, Young LM, Smalley D, et al. 2013. Novel myco-like DNA viruses discovered in the faecal matter of various animals. Virus Res. 177(2):209-16
107. Smart CD, Yuan W, Foglia R, Nuss DL, Fulbright DW, et al. 1999. Cryphonectria hypovirus 3, a virus species in the family Hypoviridae with a single open reading frame. Virology 265:66-73
108. Son M, Lee KM, Yu J, Kang M, Park JM, et al. 2013. The HEX1 gene of Fusarium graminearum is required for fungal asexual reproduction and pathogenesis and for efficient viral RNA accumulation of Fusarium graminearum virus 1. J. Virol. 87(18):10356-67
109. Strauss EE, Lakshman DK, Tavantzis SM. 2000. Molecular characterization of the genome of a partitivirus from the basidiomycete Rhizoctonia solani. J. Gen. Virol. 81(2):549-55
110. Tuomivirta TT, Kaitera T, Hantula J. 2009. A novel putative virus of Gremmeniella abietina type B (Ascomycota: Helotiaceae) has a composite genome with endornavirus affinities. J. Gen. Virol. 90:2299-305
111. Urayama S, Kato S, Suzuki Y, Aoki N, Le TM, et al. 2010. Mycoviruses related to chrysovirus affect vegetative growth in the rice blast fungus Magnaporthe oryzae. J. Gen. Virol. 91:3085-94
112. Vainio EJ, Korhonen K, Tuomivirta TT, Hantula J. 2010.Anovel putative partitivirus of the saprotrophic fungus Heterobasidion ecrustosum infects pathogenic species of the Heterobasidion annosum complex. Fungal Biol. 114:955-65
113. Vainio EJ, Piri T, Hantula J. 2013. Virus community dynamics in the conifer pathogenic fungus Heterobasidion parviporum following an artificial introduction of a partitivirus. Microb. Ecol. 65:28-38
114. van den Brand JM, van Leeuwen M, Schapendonk CM, Simon JH, Haagmans BL, et al. 2012. Metagenomic analysis of the viral flora of pine marten and European badger feces. J. Virol. 86:2360-65
115. Vilches S, Castillo A. 1997. A double-stranded RNA mycovirus in Botrytis cinerea. FEMS Microbiol. Lett. 155:125-30
116. Wang S, Kondo H, Liu L, Guo L, Qiu D. 2013. A novel virus in the family Hypoviridae from the plant pathogenic fungus Fusarium graminearum. Virus Res. 174(1-2):69-77
117. Whon TW, Kim MS, Roh SW, Shin NR, Lee HW, et al. 2012. Metagenomic characterization of airborne viral DNA diversity in the near-surface atmosphere. J. Virol. 86(15):8221-31
118. Wu M, Jin F, Zhang J, Yang L, Jiang D, et al. 2012. Characterization of a novel bipartite double-stranded RNA mycovirus conferring hypovirulence in the pathogenic fungus Botrytis porri. J. Virol. 86:6605-19
119. Wu M, Zhang L, LiG, Jiang D, Ghabrial SA. 2010. Genome characterization of a debilitation-associated mitovirus infecting the phytopathogenic fungus Botrytis cinerea. Virology 406(1):117-26
120. Wu M, Zhang L, Li G, Jiang D, Hou M, et al. 2007. Hypovirulence and double-stranded RNA in Botrytis cinerea. Phytopathology 97(12):1590-99
121. Xie J, Ghabrial SA. 2012. Molecular characterization of two mitoviruses co-infecting a hypovirulent isolate of the plant pathogenic fungus Sclerotinia sclerotiorum. Virology 428(2):77-85
122. Xie J, Wei D, Jiang D, Fu Y, Li G, et al. 2006. Characterization of debilitation-associated mycovirus infecting the plant-pathogenic fungus Sclerotinia sclerotiorum. J. Gen. Virol. 87(1):241-49
123. Xie J, Xiao X, Fu Y, Liu H, Cheng J, et al. 2011. A novel mycovirus closely related to hypoviruses that infects the plant pathogenic fungus Sclerotinia sclerotiorum. Virology 418(1):49-56
124. Yaegashi H, Kanematsu S, Ito T. 2012. Molecular characterization of a new hypovirus infecting a phytopathogenic fungus, Valsa ceratosperma. Virus Res. 165(2):143-50
125. Yaegashi H, Nakamura H, Sawahata T, Sasaki A, Iwanami Y, et al. 2013. Appearance of mycoviruslike double-stranded RNAs in the white root rot fungus, Rosellinia necatrix, in an apple orchard. FEMS Microbiol. Ecol. 83(1):40-62
126. Yaegashi H, Yoshikawa N, Ito T, Kanematsu S. 2013. A mycoreovirus suppresses RNA silencing in the white root rot fungus, Rosellinia necatrix. Virology 444(1-2):409-16
127. Yokoi T, Takemoto Y, Suzuki M, Yamashita S, Hibi T. 1999. The nucleotide sequence and genome organization of Sclerophthora macrospora virus B. Virology 264(2):344-49
128. Yokoi T, Yamashita S, Hibi T. 2003. The nucleotide sequence and genome organization of Sclerophthora macrospora virus A. Virology 311(2):394-99
129. Yokoi T, Yamashita S, Hibi T. 2007. The nucleotide sequence and genome organization ofMagnaporthe oryzae virus 1. Arch. Virol. 152(12):2265-69
130. Yu X, Li B, Fu Y, Jiang D, Ghabrial SA, et al. 2010. A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc. Natl. Acad. Sci. USA 107:8387-92
131. Yu X, Li B, Fu Y, Xie J, Cheng J, et al. 2013. Extracellular transmission of a DNA mycovirus and its use as a natural fungicide. Proc. Natl. Acad. Sci. USA 110(4):1452-57
132. Zhang L, Fu Y, Xie J, Jiang D, Li G, et al. 2009. A novel virus that infecting hypovirulent strain XG36-1 of plant fungal pathogen Sclerotinia sclerotiorum. Virol. J. 6:96
133. Zhang T, Jiang Y, Huang J, Dong W. 2013. Complete genome sequence of a putative novel victorivirus from Ustilaginoidea virens. Arch. Virol. 158(6):1403-6
134. Zhang T, Jiang Y, Huang J, Dong W. 2013. Genomic organization of a novel partitivirus from the phytopathogenic fungus Ustilaginoidea virens. Arch. Virol. 158(11):2415-19
135. Zheng L, Liu H, Zhang M, Cao X, Zhou E. 2013. The complete genomic sequence of a novel mycovirus from Rhizoctonia solani AG-1 IA strain B275. Arch. Virol. 158(7):1609-12
136. Zhu W, Wei W, Fu Y, Cheng J, Xie J, et al. 2013. A secretory protein of necrotrophic fungus Sclerotinia sclerotiorum that suppresses host resistance. PLoS ONE 8(1):e53901