The Ecology and Evolution of Fungal Viruses

Studies in Viral Ecology: Microbial and Botanical Host Systems

Volumn 1, Issue , 2011, Pages 217-253

  Milgroom, Michael G ^a   Hillman, Bradley I ^b  

^a Department of Obstetrics Gynecology   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Fungal virus ecology and evolution slow start, viruses not readily detectable, in fungal hosts in natural settings; Fungal virus transmission, and direct cell to cell contact no vectors or extracellular phase; Fungal virus, ecology and evolution fungal virus, biology and diversity

Indexed keywords

EID: 84886076085     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781118025666.ch9     Document Type: Chapter

References (202)

1. Ahn, I. P. and Lee, Y. H. (2001). A viral doublestranded RNA up regulates the fungal virulence of Nectria radicicola. Mol. Plant Microbe Interact. 14, 496-507.
2. Allemann, C., Hoegger, P., Heiniger, U., and Rigling, D. (1999). Genetic variation of Cryphonectria hypoviruses (CHV1) in Europe, assessed using RFLP markers. Mol. Ecol. 8, 843-854.
3. Anagnostakis, S. L. (1982). Biological control of chestnut blight. Science 215, 466-471.
4. Anagnostakis, S. L. (1983). Conversion to curative morphology in Endothia parasitica and its restriction by vegetative compatibility. Mycologia 75, 777-780.
5. Anagnostakis, S. L. (1987). Chestnut blight: the classical problem of an introduced pathogen. Mycologia 79, 23-37.
6. Anagnostakis, S. L., Chen, B., Geletka, L. M., and Nuss, D. L. (1998). Hypovirus transmission to ascospore progeny by field-released transgenic hypovirulent strains of Cryphonectria parasitica. Phytopathology 88, 598-604.
7. Anagnostakis, S. L., Hau, B., and Kranz, J. (1986). Diversity of vegetative compatibility groups of Cryphonectria parasitica in Connecticut and Europe. Plant Dis. 70, 536-538.
8. Baidyaroy, D., Glynn, J. M., and Bertrand, H. (2000). Dynamics of asexual transmission of a mitochondrial plasmid in Cryphonectria parasitica. Curr. Genet. 37, 257-267.
9. Bandy, B. R., and Tavantzis, S. M. (1990). Effect of hypovirulent Rhizoctonia solani on rhizoctonia disease, growth, and development of potato plants. Am. Potato J. 67, 189-199.
10. Beauregard, A., Curcio, M. J., and Belfort, M. (2008). The take and give between retrotransposable elements and their hosts. Annu. Rev. Genet. 42, 587-617.
11. Bertrand, H. (2000). Role of mitochondrial DNA in the senescence and hypovirulence of fungi and potential for plant disease control. Annu. Rev. Phytopathol. 38, 397-422.
12. Bharathan, N., and Tavantzis, S. M. (1990). Genetic diversity of double-stranded RNA from Rhizoctonia solani. Phytopathology 80, 631-635.
13. Biella, S., Smith, M. L., Aist, J. R., Cortesi, P., and Milgroom, M. G. (2002). Programmed cell death correlates with virus transmission in a filamentous fungus. Proc. R Soc. Lond. B 269, 2269-2276.
14. Bisiach,M.,DeMartino, A., Gobbi, E., Intropido, M., and Vegetti, G. (1988). Studies on chestnut blight: activity report. Riv. Patol. Veg. 24 (S. IV), 3-13.
15. Boeke, J. D., Eickbush, T., Sandmeyer, S., and Voytas, D. F. (2005). Pseudoviridae. In: Fauquet, C. M., Mayo, M. A., Maniloff, J., Desselberger, U.,and Ball, A. L. (eds), Virus Taxonomy: Eighth Report of the International Committee for the Taxonomy of Viruses. Elsevier/Academic Press, London, pp. 397-407.
16. Boone, C., Sdicu, A. M., Wagner, J., Degre, R., Sanchez, C., and Bussey, H. (1990). Integration of the yeast K1 killer toxin gene into the genome of marked wine yeasts and its effect on vinification. Am. J. Enol. Vitic. 41, 37-42.
17. Brasier, C.M. (1983).Acytoplasmically transmitted disease of Ceratocystis ulmi. Nature 305, 220-223.
18. Brasier, C. M. (1988). Rapid changes in genetic structure of epidemic populations of Ophiostoma ulmi. Nature 332, 538-541.
19. Brasier, C. M. (1990). The unexpected element: mycovirus involvement in the outcome of two recent pandemics, Dutch elm disease and chestnut blight. In: Burdon, J. J., and Leathers, S. R. (eds), Pests, Pathogen and Plant Communities. Blackwell Scientific Publications, Oxford, pp. 289-307.
20. Brewer, B. J., and Fangman, W. L. (1980). Preferential inclusion of extrachromosomal genetic elements in yeast meiotic spores. Proc. Natl. Acad. Sci. U. S. A. 77, 5380-5384.
21. Bruenn, J. A. (1980). Virus-like particles of yeast. Annu. Rev. Microbiol. 34, 49-68.
22. Buck, K.W. (1986). Fungal virology-an overview. In: Buck, K.W. (ed), Fungal Virology.CRCPress, Inc., Boca Raton, FL, pp. 1-84.
23. Buck, K.W. (1998). Molecular variability of viruses of fungi. In: Bridge, P. D., Couteaudier, Y., and Clarkson, J. M. (eds), Molecular Variability of Fungal Pathogens. CAB International, Wallingford, pp. 53-72.
24. Buck, K. W., Brasier, C. M., Paoletti, M., and Crawford, L. J. (2003). Virus transmission and gene flow between two species of Dutch elm disease fungi, Ophiostoma ulmi and O. novoulmi: deleterious viruses as selective agents for gene introgression. In: Hails, R. S., Beringer, J. E., and Godfray, H. C. J. (eds), Genes in the Environment. Blackwell Publishing, Oxford, pp. 26-45.
25. Bull, J. J. (1994). Virulence. Evolution 48, 1423-1437.
26. Bussey, H., Vernet, T., and Sdicu, A. M. (1988). Mutual antagonism among killer yeasts: competition between K1 and K2 killers and a novel cDNA-based K1-K2 killer strain of Saccharomyces cerevisiae. Can. J. Microbiol. 34, 38-44.
27. Cai, G., Myers, K., Hillman, B. I., and Fry, W. E. (2009). A novel virus of the late blight pathogen, Phytophthora infestans, with two RNA segments and a supergroup 1 RNA-dependent RNA polymerase. Virology 392, 52-61.
28. Cambareri, E. B., Jensen, B. C., Schabtach, E., and Selker, E. U. (1989). Repeat-induced G-C to A-T mutations in Neurospora. Science 244, 1571-1575.
29. Carbone, I., Liu, Y.-C., Hillman, B. I., and Milgroom, M. G. (2004). Recombination and migration of Cryphonectria hypovirus 1 as inferred from gene genealogies and the coalescent. Genetics 166, 1611-1629.
30. Castanho, B., and Butler, E. E. (1978). Rhizoctonia decline: degenerative disease of Rhizoctonia solani. Phytopathology 68, 1505-1510.
31. Castanho, B., Butler, E. E., and Shepherd, R. J. (1978). The association of double-stranded RNA with Rhizoctonia decline. Phytopathology 68, 1515-1519.
32. Caten, C. E. (1972). Vegetative incompatibility and cytoplasmic infection in fungi. J. Gen. Microbiol. 72, 221-229.
33. Charlton, N. D., Carbone, I., Tavantzis, S. M., and Cubeta, M. A. (2008). Phylogenetic relatedness of the M2 double-stranded RNA in Rhizoctonia fungi. Mycologia 100, 555-564.
34. Charlton, N. D., and Cubeta, M. A. (2007). Transmission of the M2 double-stranded RNA in Rhizoctonia solani anastomosis group 3 (AG-3). Mycologia 99, 859-867.
35. Chen, B. S., Chen, C. H., Bowman, B. H., and Nuss, D. L. (1996). Phenotypic changes associated with wild-type and mutant hypovirusRNAtransfection of plant pathogenic fungi phylogenetically related to Cryphonectria parasitica. Phytopathology 86, 301-310.
36. Chen, B. S., Choi, G. H., and Nuss, D. L. (1994a). Attenuation of fungal virulence by synthetic infectious hypovirus transcripts. Science 264, 1762-1764.
37. Chen, B. S., Craven, M. G., Choi, G. H., and Nuss, D. L. (1994b). cDNA-derived hypovirus RNA in transformed chestnut blight fungus is spliced and trimmed of vector nucleotides. Virology 202, 441-448.
38. Chen, B. S., and Nuss, D. L. (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, 985-992.
39. Choi, G. H., and Nuss, D. L. (1992). Hypovirulence of chestnut blight fungus conferred by an infectious viral cDNA. Science 257, 800-803.
40. Chun, S. J., and Lee, Y. H. (1997). Inheritance of dsRNAs in the rice blast fungus, Magnaporthe grisea. FEMS Microbiol. Lett. 148, 159-162.
41. Coenen, A., Kevei, F., and Hoekstra, R. F. (1997). Factors affecting the spread of double-stranded RNA viruses in Aspergillus nidulans. Genet. Res. 69, 1-10.
42. Cogoni, C., and Macino, G. (1999a). Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature 399, 166-169.
43. Cogoni, C., and Macino, G. (1999b). Posttranscriptional gene silencing in Neurospora by a RecQ DNA helicase. Science 286, 2342-2344.
44. Cogoni, C., and Macino, G. (1999c). Homologydependent gene silencing in plants and fungi: a number of variations on the same theme. Curr. Opin. Microbiol. 2, 657-662.
45. Cole, T. E., Muller, B. M., Hong, Y., Brasier, C. M., and Buck, K. W. (1998). Complexity of virus-like double-stranded RNA elements in a diseased isolate of the Dutch elm disease fungus, Ophiostoma novo-ulmi. J. Phytopathol. 146, 593-598.
46. Cortesi, P., McCulloch, C. E., Song, H., Lin, H., and Milgroom, M. G. (2001). Genetic control of horizontal virus transmission in the chestnut blight fungus, Cryphonectria parasitica. Genetics 159, 107-118.
47. Cortesi, P., and Milgroom, M. G. (1998). Genetics of vegetative incompatibility in Cryphonectria parasitica. Appl. Environ. Microbiol. 64, 2988-2994.
48. Csorba, T., Pantaleo, V., and Burgyan, J. (2009). RNA silencing: an antiviral mechanism. Adv. Virus Res. 75, 35-71.
49. Daboussi, M. J., and Capy, P. (2003). Transposable elements in filamentous fungi. Annu. Rev. Microbiol. 57, 275-299.
50. Dalzoto, P. R., Glienke-Blanco, C., Kava-Cordeiro, V., Ribeiro, J. Z., Kitajima, E. W., and Azevedo, J. L. (2006). Horizontal transfer and hypovirulence associated with double-stranded RNA in Beauveria bassiana. Mycol. Res. 110, 1475-1481.
51. Davelos, A. L., and Jarosz, A. M. (2004). Demography of American chestnut populations: effects of a pathogen and a hyperparasite. J. Ecol. 92, 675-685.
52. Day, P. R., and Dodds, J. A. (1979). Viruses of plant pathogenic fungi. In: Lemke, P. A. (ed), Viruses and Plasmids in Fungi. Marcel Dekker, New York, pp. 201-238.
53. Deng, F. Y., Allen, T. D., Hillman, B. I., and Nuss, D. L. (2007a). Comparative analysis of alterations in host phenotype and transcript accumulation following hypovirus and mycoreovirus infections of the chestnut blight fungus Cryphonectria parasitica. Eukaryot. Cell 6, 1286-1298.
54. Deng, F. Y., Allen, T. D., and Nuss, D. L. (2007b). Ste12 transcription factor homologue CpST12 is down-regulated by hypovirus infection and required for virulence and female fertility of the chestnut blight fungus Cryphonectria parasitica. Eukaryot. Cell 6, 235-244.
55. Deng, F., Xu, R., and Boland, G. J. (2003). Hypovirulence-associated double-stranded RNA from Sclerotinia homoeocarpa is conspecific with Ophiostoma novo-ulmi mitovirus 3a-Ld. Phytopathology 93, 1407-1414.
56. Deng, Q. C., Ye, Y., Miao, M., Fang, Q., Li, T., and Wang, K. (2009). The horizontal transmission of Cryphonectria hypovirus 1 (CHV1) is affected by virus strains. Chinese Sci. Bull. 54, 3053-3060.
57. Double, M. L. (1982). The ability of hypovirulent isolates and mixtures of hypovirulent isolates to control artificially established virulent cankers. In: Smith, H. C., and MacDonald W. L. (eds), USDA Forest Service American Chestnut Cooperators' Meeting. West Virginia University Books, Morgantown, WV, pp. 145-152.
58. Dutech, C., Rossi, J. P., Fabreguettes, O., and Robin, C. (2008). Geostatistical genetic analysis for inferring the dispersal pattern of a partially clonal species: example of the chestnut blight fungus. Mol. Ecol. 17, 4597-4607.
59. Eickbush, T., Boeke, J. D., Sandmeyer, S., and Voytas, D. F. (2005). Metaviridae. In: Fauquet, C. M., Mayo, M. A., Maniloff, J., Desselberger, U.,and Ball, A. L. (eds), Virus Taxonomy: Eighth Report of the International Committee for the Taxonomy of Viruses. Elsevier/Academic Press, London, pp. 409-420.
60. Elias, K. S., and Cotty, P. J. (1996). Incidence and stability of infection by double-stranded RNA genetic elements in Aspergillus section flavi and effects on aflatoxigenicity. Can. J. Bot. 74, 716-725.
61. Elliston, J. E. (1985). Preliminary evidence for two debilitating cytoplasmic agents in a strain of Endothia parasitica from western Michigan. Phytopathology 75, 170-173.
62. El-Sherbeni, M., and Bostian, K. A. (1987). Viruses in fungi: infection of yeast with the K1 and K2 killer viruses. Proc. Natl. Acad. Sci. U. S. A. 84, 4293-4297.
63. Enebak, S. A., MacDonald,W. L., and Hillman, B. I. (1994). Effect of dsRNA associated with isolates of Cryphonectria parasitica from the central Appalachians and their relatedness to other dsRNAs from North America and Europe. Phytopathology 84, 528-534.
64. Escande, A. R., and Echandi, E. (1991). Protection of potato from Rhizoctonia canker with binucleate Rhizoctonia fungi. Plant Pathol. 40, 197-202.
65. Esteban, R., and Fujimura, T. (2003). Launching the yeast 23S RNA Narnavirus shows 5' and 3' cisacting signals for replication. Proc. Natl. Acad. Sci. U. S. A. 100, 2568-2573.
66. Eusebio-Cope, A., Sun, L. Y., Hillman, B. I., and Suzuki, N. (2010). Mycoreovirus 1 S4-coded protein is dispensable for viral replication but necessary for efficient vertical transmission and normal symptom induction. Virology 397, 399-408.
67. Fauquet, C. M., Mayo, M. A., Maniloff, J., Desselberger, U., and Ball, L. A. (2005). Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, San Diego, CA.
68. Fletcher, J. T., White, P. F., and Gaze, R. H. (1989). Mushrooms: Pest and Disease Control. Intercept, Andover, UK.
69. Freitag, M., Williams, R. L., Kothe, G. O., and Selker, E.U. (2002).Acytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc. Natl. Acad. Sci. U. S. A. 99, 8802-8807.
70. Galagan, J. E., and Selker, E. U. (2004). RIP: the evolutionary cost of genome defense. Trends Genet. 20, 417-423.
71. Ghabrial, S. A. (1998). Origin, adaptation and evolutionary pathways of fungal viruses. Virus Genes 16, 119-131.
72. Ghabrial, S. A., Buck, K. W., Hillman, B. I., and Milne, R. G. (2005). Family Partitiviridae. In: Fauquet, C. M., Mayo, M. A., Maniloff, J., Desselberger, U., and Ball, A. L. (eds), Virus Taxonomy: Eighth Report of the International Committee for the Taxonomy of Viruses. Elsevier/Academic Press, London, pp. 581-590.
73. Ghabrial, S. A., and Suzuki, N. (2009). Viruses of plant pathogenic fungi. Annu. Rev. Phytopathol. 47, 353-384.
74. Ghedin, E., and Claverie, J. M. (2005). Mimivirus relatives in the Sargasso sea. Virol. J. 2, 62.
75. Glass, N. L., and Dementhon, K. (2006). Non-self recognition and programmed cell death infilamentous fungi. Curr. Opin. Microbiol. 9, 553-558.
76. Glass, N. L., and Kaneko, I. (2003). Fatal attraction: nonself recognition and heterokaryon incompatibility in filamentous fungi. Eukaryot. Cell 2, 1-8.
77. Glass, N. L., and Kuldau, G. A. (1992). Mating type and vegetative incompatibility in filamentous ascomycetes. Annu. Rev. Phytopathol. 30, 201-224.
78. Gobbin, D., Hoegger, P. J., Heiniger, U., and Rigling, D. (2003). Sequence variation and evolution of Cryphonectria hypovirus 1 (CHV-1) in Europe. Virus Res. 97, 39-46.
79. Goodin, M. M., Schlagnhaufer, B., and Romaine, C. P. (1992). Encapsidation of the La France disease-specific double-stranded RNAs in 36-nm isometric virus-like particles. Phytopathology 82, 285-290.
80. Grente, J., and Berthelay-Sauret, S. (1978). Biological control of chestnut blight in France. In: MacDonald, W. L., Cech, F. C., Luchok, J.,and Smith, C. (eds), Proceedings of the American Chestnut Symposium. West Virginia University Books, Morgantown, WV, pp. 30-34.
81. Heiniger, U., and Rigling, D. (1994). Biological control of chestnut blight in Europe. Annu. Rev. Phytopathol. 32, 581-599.
82. Herrero, N., Marquez, S. S., and Zabalgogeazcoa, I. (2009). Mycoviruses are common among different species of endophytic fungi of grasses. Arch. Virol. 154, 327-330.
83. Hillman, B. I., Supyani, S., Kondo, H., and Suzuki, N. (2004).Areovirus of the fungus Cryphonectria parasitica that is infectious as particles and related to the Coltivirus genus of animal pathogens. J. Virol. 78, 892-898.
84. Hillman, B. I., and Suzuki, N. (2004). Viruses of the chestnut blight fungus, Cryphonectria parasitica. Adv. Virus Res. 63, 423-472.
85. Hoekstra, R. F. (1996). Horizontal transmission in fungal populations. In: Bos, C. J. (ed), Fungal Genetics: Principles and Practice. Marcel Dekker, New York, pp. 337-348.
86. Hollings, M. (1962). Viruses associated with a dieback disease of cultivated mushroom. Nature 196, 962-965.
87. Hong, Y. G., 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.
88. Howitt, R. L. J., Beever, R. E., Pearson, M. N., and Forster, R. L. S. (2001). Genome characterization of Botrytis virus F, a flexuous rod-shaped mycovirus resembling plant 'potex-like' viruses. J. Gen. Virol. 82, 67-78.
89. Howitt, R. L., Beever, R. E., Pearson, M. N., and Forster, R. L. (2006). Genome characterization of a flexuous rod-shaped mycovirus, Botrytis virus X, reveals high amino acid identity to genes from plant 'potex-like' viruses. Arch. Virol. 151, 563-579.
90. Ihrmark, K., Johannesson, H., Strenstrom, E., and Stenlid, J. (2002). Transmission of double-stranded RNA in Heterobasidion annosum. Fungal Genet. Biol. 36, 147-154.
91. Ikeda, K., Nakamura, H., Arakawa, M., and Matsumoto, N. (2004). Diversity and vertical transmission of double-stranded RNA elements in root rot pathogens of trees, Helicobasidium mompa and Rosellinia necatrix. Mycol. Res. 108, 626-634.
92. Jian, J. H., Lakshman, D. K., and Tavantzis, S. M. (1997). Association of distinct double-stranded RNAs with enhanced or diminished virulence in Rhizoctonia solani infecting potato. Mol. Plant Microbe Interact. 10, 1002-1009.
93. Jian, J. H., Lakshman, D. K., and Tavantzis, S. M. (1998). A virulence-associated, 6.4-kb, doublestranded RNA from Rhizoctonia solani is phylogenetically related to plant bromoviruses and electron transport enzymes. Mol. Plant Microbe Interact. 11, 601-609.
94. Kanematsu, S., Arakawa, M., Oikawa, Y., Onoue, M., Osaki, H., Nakamura, H., Ikeda, K., Kuga-Uetake, Y., Nitta, H., Sasaki, A., Suzaki, K., Yoshida, K., and Matsumoto, N. (2004). A reovirus causes hypovirulence of Rosellinia necatrix. Phytopathology 94, 561-568.
95. Kapoor, A., Simmonds, P., Lipkin, W. I., Zaidi, S., and Delwart, E. (2010). Use of nucleotide composition analysis to infer hosts for three novel Picorna-like viruses. J. Virol. 84(19), 10322-10328.
96. Kim,Y. J., Kim, J.Y., Kim, J. H.,Yoon, S. M.,Yoo,Y. B., and Yie, S. W. (2008). The identification of a novel Pleurotus ostreatus dsRNA virus and determination of the distribution of viruses in mushroom spores. J. Microbiol. 46, 95-99.
97. Kobayashi, D. Y., and Hillman, B. I. (2005). Fungi, bacteria, and viruses as pathogens of the fungal community. In: Dighton, J., White, J. F., and Oudemans, P. V. (eds), The Fungal Community: Its Organization and Role in the Ecosystem. CRC Press, Boca Raton, FL, pp. 399-421.
98. Koltin, Y. (1988). The killer system of Ustilago maydis: secreted polypeptides encoded by viruses. In: Koltin, Y., and Leibowitz, M. J. (eds), Viruses of Fungi and Simple Eukaryotes. Marcel Dekker, New York, pp. 209-242.
99. Koonin, E. V., Choi, G. H., Nuss, D. L., Shapira, R., and Carrington, J. C. (1991). Evidence for common ancestry of a chestnut blight hypovirulenceassociated double-stranded RNA and a group of positive-strand RNA plant viruses. Proc. Natl. Acad. Sci. U. S. A. 88, 10647-10651.
100. Kretschmer, M., Leroch, M., Mosbach, A., Walker, A. S., Fillinger, S., Mernke, D., Schoonbeek, H. J., Pradier, J. M., Leroux, P., De Waard, M. A., and Hahn, M. (2009). Fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PLoS Pathog. 5, e1000696.
101. Lecoq, H., Boissonnet-Menes, M., and Delhotal, P. (1979). Infectivity and transmission of fungal viruses. In: Molitoris, H. P., Hollings, M.,and Wood, H. A. (eds), Fungal Viruses. Springer-Verlag, Berlin, pp. 34-47.
102. Leslie, J. F. (1993). Fungal vegetative compatibility. Annu. Rev. Phytopathol. 31, 127-150.
103. Levin, B. R. (1996). The evolution and maintenance of virulence in microparasites. Emerg. Infect. Dis. 2, 93-102.
104. Liang, P., and Chen, K. (1987). Virus transmission through interspecies protoplast fusion in Aspergillus. Trans. Br. Mycol. Soc. 89, 73-81.
105. Liang, P., Chen, K., Zhou, S., Quan, Y., and Liu, H. (1992). Isolation and conversion of dsRNA from hypovirulent strains of Endothia parasitica in China. Acta Microbiol. Sin. 32, 253-261.
106. Lim,W. S., Jeong, J. H., Jeong, R. D.,Yoo,Y. B.,Yie, S. W., and Kim, K. H. (2005). Complete nucleotide sequence and genome organization of a dsRNA partitivirus infecting Pleurotus ostreatus. Virus Res. 108, 111-119.
107. 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.
108. Lipsitch, M., and Moxon, E. R. (1997).Virulence and transmissibility of pathogens: what is the relationship? Trends Microbiol. 5, 31-37.
109. Liu, Y.-C., Durrett, R., and Milgroom, M. G. (2000). A spatially-structured stochastic model to simulate heterogeneous transmission of viruses in fungal populations. Ecol. Model. 127, 291-308.
110. Liu, Y.-C., Dynek, J. N., Hillman, B. I., and Milgroom, M. G. (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, 433-442.
111. Liu, H., Fu, Y., Jiang, D., Li, G., Xie, J., Peng, Y., Yi, X., and Ghabrial, S. A. (2009). A novel mycovirus that is related to the human pathogen hepatitis E virus and rubi-like viruses. J. Virol. 83, 1981-1991.
112. Liu,Y.-C., Hillman, B. I., Linder-Basso, D., Kaneko, S., and Milgroom, M. G. (2003). Evidence for interspecies transmission of viruses in natural populations of filamentous fungi in the genus Cryphonectria. Mol. Ecol. 12, 1619-1628.
113. Liu, Y.-C., and Milgroom, M. G. (1996). Correlation between hypovirus transmission and the number of vegetative incompatibility (vic) genes different among isolates from a natural population of Cryphonectria parasitica. Phytopathology 86, 79-86.
114. Liu, Y.-C., and Milgroom, M. G. (2007). High diversity of vegetative compatibility types in Cryphonectria parasitica in Japan and China. Mycologia 99, 279-284.
115. Lopez, V., Gil, R., Vicente Carbonell, J., and Navarro, A. (2002). Occurrence of 20S RNA and 23S RNA replicons in industrial yeast strains and their variation under nutritional stress conditions. Yeast 19, 545-552.
116. Lu, R., Folimonov, A., Shintaku, M., Li,W. X., Falk, B. W., Dawson, W. O., and Ding, S. W. (2004). Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc. Natl. Acad. Sci. U. S. A. 101, 15742-15747.
117. MacDonald, W. L., and Fulbright, D. W. (1991). Biological control of chestnut blight: use and limitations of transmissible hypovirulence. Plant Dis. 75, 656-661.
118. Maqueda, M., Zamora, E., Rodriguez-Cousino, N., and Ramirez, M. (2010). Wine yeast molecular typing using a simplified method for simultaneously extracting mtDNA, nuclear DNA and virus dsRNA. Food Microbiol. 27, 205-209.
119. Marquez, L. M., Redman, R. S., Rodriguez, R. J., and Roossinck, M. J. (2007). A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315, 513-515.
120. Marquina, D., Santos, A., and Peinado, J. M. (2002). Biology of killer yeasts. Int. Microbiol. 5, 65-71.
121. Martinez-Espinoza, A. D., Garcia-Pedrajas, M. D., and Gold, S. E. (2002). The Ustilaginales as plant pests and model systems. Fungal Genet. Biol. 35, 1-20.
122. McBride, R., Greig, D., and Travisano, M. (2008). Fungal viral mutualism moderated by ploidy. Evolution 62, 2372-2380.
123. McCabe, P. M., Pfeiffer, P., and Van Alfen, N. K. (1999). The influence of dsRNA viruses on the biology of plant pathogenic fungi. Trends Microbiol. 7, 377-381.
124. Melzer, M. J., and Bidochka, M. J. (1998). Diversity of double-stranded RNA viruses within populations of entomopathogenic fungi and potential implications for fungal growth and virulence. Mycologia 90, 586-594.
125. Melzer, M. S., and Boland, G. J. (1996). Transmissible hypovirulence in Sclerotinia minor. Can. J. Plant Pathol. 18, 19-28.
126. Melzer,M. S., Ikeda, S. S., and Boland, G. J. (2002). Interspecific transmission of double-stranded RNA and hypovirulence from Sclerotinia sclerotiorum to S. minor. Phytopathology 92, 780-784.
127. Milgroom, M. G. (1999). Viruses in fungal populations. In: Worrall, J. J. (ed), Structure and Dynamics of Fungal Populations. Kluwer Academic Publishers, Dordrecht, pp. 283-305.
128. Milgroom, M. G., and Cortesi, P. (1999). Analysis of population structure of the chestnut blight fungus based on vegetative incompatibility genotypes. Proc. Natl. Acad. Sci. U. S. A. 96, 10518-10523.
129. Milgroom, M. G., and Cortesi, P. (2004). Biological control of chestnut blight with hypovirulence: a critical analysis. Annu. Rev. Phytopathol. 42, 311-338.
130. Milgroom, M. G., MacDonald, W. L., and Double, M. L. (1991). Spatial analysis of vegetative compatibility groups in the chestnut blight fungus, Cryphonectria parasitica. Can. J. Bot. 69, 1407-1413.
131. Milgroom, M. G., Sotirovski, K., Spica, D., Davis, J. E., Brewer, M. T., Milev, M., and Cortesi, P. (2008). Clonal population structure of the chestnut blight fungus in expanding ranges in southeastern Europe. Mol. Ecol. 17, 4446-4458.
132. Milgroom, M. G., Wang, K., Zhou, Y., Lipari, S. E., and Kaneko, S. (1996). Intercontinental population structure of the chestnut blight fungus, Cryphonectria parasitica. Mycologia 88, 179-190.
133. Nagasaki, K. (2008). Dinoflagellates, diatoms, and their viruses. J. Microbiol. 46, 235-243.
134. Nakayashiki, T., Kurtzman, C. P., Edskes, H. K., and Wickner, R. B. (2005). Yeast prions [URE3] and [PSI{Thorn}] are diseases. Proc. Natl. Acad. Sci. U. S. A. 102, 10575-10580.
135. Nishimura, M., Hayashi, N., Jwa, N. S., Lau, G.W., Hamer, J. E., and Hasebe, A. (2000). Insertion of the LINE retrotransposon MGL causes a conidiophore pattern mutation in Magnaporthe grisea. Mol. Plant Microbe Interact. 13, 892-894.
136. Nuss, D. L. (1992). Biological control of chestnut blight: an example of virus-mediated attenuation of fungal pathogenesis. Microbiol. Rev. 56, 561-576.
137. Nuss, D. L. (2005). Hypovirulence: mycoviruses at the fungal-plant interface. Nat. Rev. Microbiol. 3, 632-642.
138. Nuss, D. L. (2010). Mycoviruses. In: Borkovich, K. A., and Ebbole, D. J. (eds), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC.
139. Paoletti, M., and Saupe, S. J. (2009). Fungal incompatibility: evolutionary origin in pathogen defense? Bioessays 31, 1201-1210.
140. Papazova-Anakieva, I., Sotirovski, K., Cortesi, P., and Milgroom, M. G. (2008). Horizontal transmission of hypoviruses between vegetative compatibility types of Cryphonectria parasitica in Macedonia. Eur. J. Plant Pathol. 120, 35-42.
141. Park, C. M., Berry, J. O., and Bruenn, J. A. (1996). High-level secretion of a virally encoded antifungal toxin in transgenic tobacco plants. Plant Mol. Biol. 30, 359-366.
142. Park, Y. J., Chen, X. B., and Punja, Z. K. (2006). Diversity, complexity and transmission of doublestranded RNA elements in Chalara elegans (synanam. Thielaviopsis basicola). Mycol. Res. 110, 697-704.
143. Park, S. M., Kim, J. M., Chung, H. J., Lim, J. Y., Kwon, B. R., Lim, J. G., Kim, J. A., Kim, M. J., Cha, B. J., Lee, S. H., Kim, K. H., Lee,Y. S.,Yang, M. S., and Kim, D. H. (2008). Occurrence of diverse dsRNA in a Korean population of the chestnut blight fungus, Cryphonectria parasitica. Mycol. Res. 112, 1220-1226.
144. Pearson, M. N., Beever, R. E., Boine, B., and Arthur, K. (2009). Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol. Plant Pathol. 10, 115-128.
145. Peever, T. L., Liu, Y.-C., Cortesi, P., and Milgroom, M. G. (2000). Variation in tolerance and virulence in the chestnut blight fungus-hypovirus interaction. Appl. Environ. Microbiol. 66, 4863-4869.
146. Peever, T. L., Liu, Y.-C., and Milgroom, M. G. (1997). Diversity of hypoviruses and other double-stranded RNAs in Cryphonectria parasitica in North America. Phytopathology 87, 1026-1033.
147. Peever, T. L., Liu, Y.-C., Wang, K., Hillman, B. I., Foglia, R., and Milgroom, M. G. (1998). Incidence and diversity of double-stranded RNAs infecting the chestnut blight fungus, Cryphonectria parasitica, in China and Japan. Phytopathology 88, 811-817.
148. Pfeiffer, I., Kucsera, J., Varga, J., Parducz, A., and Ferenczy, L. (1996).Variability and inheritance of double-stranded RNAviruses in Phaffia rhodozyma. Curr. Genet. 30, 294-297.
149. Polashock, J. J., Bedker, P. J., and Hillman, B. I. (1997). Movement of a small mitochondrial double-stranded RNA element of Cryphonectria parasitica: ascospore inheritance and implications for mitochondrial recombination. Mol. Gen. Genet. 256, 566-571.
150. 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. U. S. A. 91, 8680-8684.
151. Rao, J. R., Nelson, D.W. A., and McClean, S. (2007). The enigma of double-stranded RNA (dsRNA) associated with mushroom virus X (MVX). Curr. Issues Mol. Biol. 9, 103-121.
152. Redman, R. S., Sheehan, K. B., Stout, R. G., Rodriguez, R. J., and Henson, J. M. (2002). Thermotolerance generated by plant/fungal symbiosis. Science 298, 1581-1581.
153. Robin, C., Anziani, C., and Cortesi, P. (2000). Relationship between biological control, incidence of hypovirulence, and diversity of vegetative compatibility types of Cryphonectria parasitica in France. Phytopathology 90, 730-737.
154. Robin, C., and Heiniger,U. (2001). Chestnut blight in Europe: diversity of Cryphonectria parasitica, hypovirulence and biocontrol. For. Snow Lands. Res. 76, 361-367.
155. Rodriguez, R. J., White, J. F., Arnold, A. E., and Redman, R. S. (2009). Fungal endophytes: diversity and functional roles. New Phytol. 182, 314-330.
156. Rogers, H. J., Buck, K.W., and Brasier,C.M. (1986). Transmission of double-stranded RNA and a disease factor in Ophiostoma ulmi. Plant Pathol. 35, 277-287.
157. Romaine, C. P., and Schlagnhaufer, B. (1989). Prevalence of double-strandedRNAs in healthy and La France disease-affected basidiocarps of Agaricus bisporus. Mycologia 81, 822-825.
158. Romaine, C. P., and Schlagnhaufer, B. (1995). PCR analysis of the viral complex associated with La France disease of Agaricus bisporus. Appl. Environ. Microbiol. 61, 2322-2325.
159. Romaine, C. P., Ulhrich, P., and Schlagnhaufer, B. (1993). Transmission of La France isometric virus during basidiosporogenesis in Agaricus bisporus. Mycologia 85, 175-179.
160. Root, C., Balbalian, C., Bierman, R., Geletka, L. M., Anagnostakis, S., Double, M., MacDonald, W., and Nuss, D. L. (2005). Multi-seasonal field release and spermatization trials of transgenic hypovirulent strains of Cryphonectria parasitica containing cDNA copies of hypovirus CHV1-EP713. For. Pathol. 35, 277-297.
161. Russin, J. S., and Shain, L. (1985). Disseminative fitness of Endothia parasitica containing different agents for cytoplasmic hypovirulence. Can. J. Bot. 65, 54-57.
162. Sasaki, A., Onoue, M., Kanematsu, S., Suzaki, K., Miyanishi, M., Suzuki, N., Nuss, D. L., and Yoshida, K. (2002). Extending chestnut blight hypovirus host range within diaporthales by biolistic delivery of viral cDNA. Mol. Plant Microbe Interact. 15, 780-789.
163. Schisler, L. C., Sinden, J. W., and Sigel, E. M. (1967). Etiology, symptomatology, and epidemiology of a virus disease of cultivated mushrooms. Phytopathology 57, 519-526.
164. Schmitt, M. J., and Breinig, F. (2002). The viral killer system in yeast: from molecular biology to application. FEMS Microbiol. Rev. 26, 257-276.
165. Schmitt, M. J., and Breinig, F. (2006). Yeast viral killer toxins: lethality and self-protection. Nat. Rev. Microbiol. 4, 212-221.
166. Schmitt, M. J., and Schernikau, G. (1997). Construction of a cDNA-based K1/K2/K28 triple killer strain of Saccharomyces cerevisiae. Food Technol. Biotechnol. 35, 281-285.
167. Segers, G. C., van Wezel, R., Zhang, X., Hong, Y., and Nuss, D. L. (2006). Hypovirus papain-like protease p29 suppresses RNA silencing in the natural fungal host and in a heterologous plant system. Eukaryot. Cell 5, 896-904.
168. Segers, G. C., Zhang, X., Deng, F., Sun, Q., and Nuss, D. L. (2007). Evidence that RNA silencing functions as an antiviral defense mechanism in fungi. Proc. Natl. Acad. Sci. U. S. A. 104, 12902-12906.
169. Sonnenberg, A. S. M., Van Kempen, I. P. J., and Van Griensven, L. J. L. D. (1995). Detection of Agaricus bisporus viral dsRNAs in pure cultures, spawn and spawn-run compost by RT-PCR. In: Elliott, T. J. (ed), Proceedings of the 14th International Congress of Science and Cultivation of Edible Fungi. Balkema, Rotterdam, pp. 587-594.
170. Sotirovski, K., Rigling, D., Heiniger, U., and Milgroom, M. G. (2011). Variation in virulence of Cryphonectria hypovirus 1 (CHV-1) in Macedonia. For. Pathol. 41, 59-65, DOI: 10.1111/j.1439-0329.2009.00637.x.
171. Spanu, P. D., Abbott, J. C., Amselem, J., Burgis, T. A., Soanes, D. M., Stüber, K., van Themaat, E. V. L., Brown, J. K. M., Butcher, S. A., Gurr, S. J., Lebrun, M.-H., Ridout, C. J., Schulze-Lefert, P., Talbot,N. J., Ahmadinejad, N.,Ametz, C., Barton, G. R., Benjdia, M., Bidzinski, P., Bindschedler, L. V., Both, M., Brewer, M. T., Cadle-Davidson, L., Cadle-Davidson, M. M., Collemare, J., Cramer, R., Frenkel, O., Godfrey, D., Harriman, J., Hoede, C., King, B. C., Klages, S., Kleemann, J., Knoll, D., Koti, P. S., Kreplak, J., López-Ruiz, F. J., Lu, X., Maekawa, T., Mahanil, S., Micali, C., Milgroom, M. G., Montana, G., Noir, S., O'Connell, R. J., Oberhaensli, S., Parlange, F., Pedersen, C., Quesneville, H., Reinhardt, R., Rott, M., Sacristán, S., Schmidt, S. M., Schön, M., Skamnioti, P., Sommer, H., Stephens,A., Takahara,H., Thordal-Christensen, H., Vigouroux, M., Weβling, R., Wicker, T., Panstruga, R., 2010. Genome expansion and gene loss in powdery mildew fungi reveal functional tradeoffs in extreme parasitism. Science 330, 1543-1546.
172. Spear, A., Sisterson, M. S., Yokomi, R., and Stenger, D. C. (2010). Plant-feeding insects harbor doublestranded RNA viruses encoding a novel proline-alanine rich protein and a polymerase distantly related to that of fungal viruses. Virology 404, 304-311.
173. Starmer,W. T., Ganter, P. F., Aberdeen,V., Lachance, M. A., and Phaff, H. J. (1987). The ecological role of killer yeasts in natural communities of yeasts. Can. J. Microbiol. 33, 783-796.
174. Sun, L., Nuss, D. L., and Suzuki, N. (2006). Synergism between a mycoreovirus and a hypovirus mediated by the papain-like protease p29 of the prototypic hypovirus CHV1-EP713. J. Gen. Virol. 87, 3703-3714.
175. Sutherland, M. L., and Brasier, C. M. (1997). A comparison of thirteen d-factors as potential biological control agents of Ophiostoma novo-ulmi. Plant Pathol. 46, 680-693.
176. Suzuki, Y., Gojobori, T., and Nakagomi, O. (1998). Intragenic recombinations in rotaviruses. FEBS Lett. 427, 183-187.
177. Suzaki, K., Ikeda, K., Sasaki, A., Kanematsu, S., Matsumoto, N., and Yoshida, K. (2005). Horizontal transmission and host-virulence attenuation of totivirus in violet root rot fungus Helicobasidium mompa. J. Gen. Plant Pathol. 71, 161-168.
178. Tavantzis, S. M. (1994). Double-stranded RNAassociated cytoplasmic hypovirulence in Rhizoctonia solani: prospects for developing a reliable, target-specific biocontrol system. In: Zehnder, G.W. Powelson, M. L., Jansson, R. K., and Raman, K. V. (eds), Advances in Potato Pest Biology and Management. American Phytopathological Society Press, St. Paul, MN, pp. 565-579.
179. Tiago, P. V., Fungaro, M. H. P., Faria, M. R., and Furlaneto, M. C. (2004). Effects of double-stranded RNA in Metarhizium anisopliae var. acridum and Paecilomyces fumosoroseus on protease activities, conidia production, and virulence. Can. J. Microbiol. 50, 335-339.
180. Tooley, P.W., Hewings, A. D., and Falkenstein, K. F. (1989). Detection of double-stranded RNA in Phytophthora infestans. Phytopathology 79, 470-474.
181. Van Alfen, N. K. (1982). Biology and potential for disease control of hypovirulence of Endothia parasitica. Annu. Rev. Phytopathol. 20, 349-362.
182. van de Sande, W. W. J., Lo-Ten-Foe, J. R., van Belkum, A., Netea, M. G., Kullberg, B. J., and Vonk,A.G. (2010). Mycoviruses: future therapeutic agents of invasive fungal infections in humans? Eur. J. Clin. Microbiol. Infect. Dis. 29, 755-763.
183. van Diepeningen, A. D., Debets, A. J. M., and Hoekstra, R. F. (1997). Heterokaryon incompatibility blocks virus transfer among natural isolates of black Aspergilli. Curr. Genet. 32, 209-217.
184. van Diepeningen, A. D., Debets, A. J. M., and Hoekstra, R. F. (1998). Intra-and interspecific virus transfer in Aspergilli via protoplast fusion. Fungal Genet. Biol. 25, 171-180.
185. van Diepeningen, A. D., Debets, A. J. M., and Hoekstra, R. F. (2006). Dynamics of dsRNA mycoviruses in black Aspergillus populations. Fungal Genet. Biol. 43, 446-452.
186. Van Etten, J. L., Graves, M. V., Muller, D. G., Boland, W., and Delaroque, N. (2002). Phycodnaviridae-large DNA algal viruses. Arch. Virol. 147, 1479-1516.
187. van Heerden, S. W., Geletka, L. M., Preisig, O., Nuss, D. L.,Wingfield, B. D., andWingfield, M. J. (2001). Characterization of South African Cryphonectria cubensis isolates infected with a C. parasitica hypovirus. Phytopathology 91, 628-632.
188. van Zaayen, A. (1979). Mushroom viruses. In: Lemke, P. A. (ed), Viruses and Plasmids in Fungi. Marcel Dekker, Inc., New York, pp. 239-324.
189. Varga, J., Rinyu, E., Kevei, E., Toth, B., and Kozakiewicz, Z. (1998). Double-stranded RNA mycoviruses in species of Aspergillus sections Circumdati and Fumigati. Can. J. Microbiol. 44, 569-574.
190. Villarreal, L. P. (2007). Virus-host symbiosis mediated by persistence. Symbiosis 44, 1-9.
191. Voth, P. D., Mairura, L., Lockhart, B. E., and May,G. (2006). Phylogeography of Ustilago maydis virus H1 in the USA and Mexico. J. Gen. Virol. 87, 3433-3441.
192. Wang, M. B., and Metzlaff, M. (2005). RNA silencing and antiviral defense in plants. Curr. Opin. Plant Biol. 8, 216-222.
193. Wang, K., Shao, J., and Lu, J. (1991). On vegetative compatibility of Cryphonectria parasitica in Jiangsu and Anhui. J. Nanjing Agric. Univ. 14, 44-48.
194. Weaver, S. C., and Reisen,W. K. (2010). Present and future arboviral threats. Antiviral Res. 85, 328-345.
195. Webber, J. F. (1987). Influence of the d2 factor on survival and infection by the Dutch elm disease pathogen Ophiostoma ulmi. Plant Pathol. 36, 531-538.
196. Wickner, R. B. (1996). Double-stranded RNA viruses of yeast. Microbiol. Rev. 60, 250-265.
197. Wickner, R. B. (2001). Viruses of yeasts, fungi, and parasitic microorganisms. In: Knipe, D. M., and Howley, P. M. (eds), Fundamental Virology. LippincottWilliams&Wilkins, Philadelphia, PA, pp. 473-528.
198. Wu, M. D., Zhang, L., Li, G. Q., Jiang, D. H., and Ghabrial, S. A. (2010). Genome characterization of a debilitation-associated mitovirus infecting the phytopathogenic fungus Botrytis cinerea. Virology 406(1), 117-126.
199. Wu, M. D., Zhang, L., Li, G. Q., Jiang, D. H., Hou, M. S., and Huang, H.-C. (2007). Hypovirulence and double-stranded RNA in Botrytis cinerea. Phytopathology 97, 1590-1599.
200. Yu, X., Li, B., Fu, Y., Jiang, D., Ghabrial, S. A., Li, G., Peng, Y., Xie, J., Cheng, J., Huang, J., and Yi, X. (2010). A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc. Natl. Acad. Sci. U. S. A. 107, 8387-8392.
201. Yu, H. J., Lim, D., and Lee, H. S. (2003). Characterization of a novel single-stranded RNAmycovirus in Pleurotus ostreatus. Virology 314, 9-15.
202. Zhou, T., and Boland, G. J. (1998). Suppression of dollar spot by hypovirulent isolates of Sclerotinia homoeocarpa. Phytopathology 88, 788-794.