acujff Artvin Çoruh Üniversitesi Orman Fakültesi Dergisi 2146-1880 2146-698X Artvin Çoruh University 10.17474/artvinofd.836419 Agricultural, Veterinary and Food Sciences Ziraat, Veterinerlik ve Gıda Bilimleri Mikovirüslerin Rhizoctonia solani Kühn ve diğer bazı bitki patojenlerinde kullanım olanakları The usage of mycoviruses in Rhizoctonia solani Kühn and some plant pathogens https://orcid.org/0000-0001-5308-9414 Avan Meltem ANKARA UNIVERSITY, FACULTY OF AGRICULTURE 05 12 2021 22 1 134 147 12 05 2020 01 05 2021 Copyright © 2000, Artvin Coruh University Journal of Forestry Faculty 2000 Artvin Coruh University Journal of Forestry Faculty

Bitki patojeni fungusların da yer aldığı birçok organizmada yaygın olarak bulunan mikovirüsler, biyolojik mücadelede alternatif bir kullanım olanağı sağlayan obligat parazitlerdir. Çoğunluğu biyolojik ajan olarak mikoviral dsRNA genomuna sahip olmakla birlikte, DNA genomlarına sahip olanları da bulunmaktadır. Mikovirüsler, fungus hücrelerinde hücre birleşmesi yoluyla, hücre bölünmesi ve eşeyli, eşeysiz spor formları ile yayılış göstermektedir. Enfekte ettikleri funguslarda bazı morfolojik ve fizyolojik farklılıklara sebebiyet vermekte, virülensi artırma ve azaltma yönünde etkide bulunmaktadırlar. Bu derlemede mikovirüslerin Rhizoctonia solani ve diğer bazı funguslara karşı etkileri ve virülensi azaltma etkisinden yola çıkarak, bitki hastalıklarıyla biyolojik mücadelede kullanım olanakları araştırılmıştır.

Mycoviruses, which are commonly found in many organisms including plant pathogenic fungi, are obligate parasites that provide an alternative use in biological control. Although the majority have mycoviral dsRNA genome as biological agent, there are also those with DNA genomes. Mycoviruses are spread in fungus cells through cell fusion, cell division and sexual and asexual spore forms. In fungi infected by mycoviruses, they cause some morphological and physiological differences and have an effect on increasing and decreasing virulence. In this review, it was aimed to give information on the effects of mycoviruses against some fungi, including Rhizoctonia solani, and their use in biological control against plant diseases, based on the effect of reducing virulence.

 Mikovirüsler dsRNA Hipovirulenslik Biyolojik kontrol Rhizoctonia solani Mycovirus dsRNA Hypovirulence Biological control Rhizoctonia solani Abbas A (2016) A review paper on mycoviruses. Journal of Plant Pathology and Microbiology, 7: 12. Abdoulaye AH, Foda MF, Kotta-Loizou I (2019) Viruses infecting the plant pathogenic fungus Rhizoctonia solani. Viruses, 11(12): 1113. Ahn IP, Lee YH (2001) A viral double-stranded RNA up regulates the fungal virulence of Nectria radicicola. Molecular Plant-Microbe Interactions, 14: 496-507. Agrios GN (2005) Plant Pathology, 5th ed.; Department of Plant Pathology, University of Florida: Gainesville, FL, USA. Akıllı S, Ulubaş-Serçe Ç, Katırcıoğlu YZ, Maden S, Rigling D (2012) Characterization ofhypovirulent isolates of the chestnut blight fungus, Cryphonectria parasitica from the Marmara and Black Sea regions of Turkey. European Journal of Plant Pathology, 135(2): 323-334. Anagnostakis SL (1987) Chestnut Blight: The Classical problem of an Introduced Pathogen. Mycologia, 79: 23-37. Anagnostakis SL, Day PR (1979) Hypovirulence conversion in Endothia parasitica. Phytopathology, 69: 1226-1229. Andika IB, Wei S, Cao C, Salaipeth L, Kondo H, Sun L (2017). Phytopathogenic fungus hosts a plant virus: A naturally occurring cross-kingdom viral infection. Proceedings of The National Academy Of Sciences USA, 114: 12267–12272. Arakawa M, Nakamura H, Uetake Y, Matsumoto N (2002) Presence and distribution of double- stranded RNA elements in the white root rot fungus Rosellinia necatrix. Mycoscience, 43: 21–26. Bartholomäus A, Wibberg D, Winkler A, Pühler A, Schlüter A, Varrelmann M (2016) Deep sequencing analysis reveals the mycoviral diversity of the virome of an avirulent isolate of Rhizoctonia solani AG-2-2 IV. 11, e0165965. Bharathan N, Saso Gudipati HL, Bharathan S, Whited K (2005) Plant Pathology, 54: 196. Boland GJ (1992) Hypovirulence and double-stranded RNA in Sclerotinia sclerotiorum. Canadian Journal of Plant Pathology, 14: 10-17. Bruenn JA (1993) Nucleic Acids Res 21, 5667±5669. Brusini J, Robin C (2013) Mycovirus transmission revisited by in situ pairings of vegetatively incompatible isolates of Cryphonectria parasitica. Journal of Virological Methods, 187: 435–442. Boland GJ (1992) Hypovirulence and double stranded RNA in Sclerotinia sclerotiorum. Canadian Journal of Plant Pathology, 14: 10–17. Boland GJ, Hall R (1994) Index of plant hosts of Sclerotinia sclerotiorum. Canadian Journal of Plant Pathology, 16(2): 93-108. Bolton M, Thomma BP, Nelson BD (2006) Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Molecular Plant Pathology, 7(1): 1-16. Bottacin AM, Levesque CA, Punja ZK (1994) Characterization of dsRNA in Chalara elegans and effects on growth and virulence. Phytopathology, 84: 303-312. Buck KW (1986) Fungal virology: An overview. In: Fungal Virology (Ed.: K.W. Buck), CRC Press, Boca Raton, FL, 1-85. Büchen-Osmond A (2004) ICTVdb Index of viruses. Available from URL: http://www.ncbi.nlm.nih.gov/ICTVdb/Ictv/index.htm [Ulaşım: 20 Nisan 2006]. Chen Y, Gai XT, Chen RX, Li CX, Zhao GK, Xia, Z. Y., Zou, C. M., & Zhong, J. (2019). Characterization of three novel betapartitiviruses co-infecting the phytopathogenic fungus Rhizoctonia solani. Virus Research, 270: 197649. Chiba S, Salaipeth L, Lin YH, Sasaki A, Kanematsu S, Suzuki NA (2009) Novel bipartite double-stranded RNA mycovirus from the white root rot fungus Rosellinia necatrix: Molecular and biological characterization, taxonomic considerations, and potential for biological control. Journal of Virology, 83: 12801–12812. 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. Journal of Virology, 87: 2330- 2341. 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. Journal of Virology, 87: 6727-6738. Cho WK, Lee KM, Yu J, Son M, Kim KH (2013) Insight into mycoviruses infecting Fusarium species. Advances in Virus Research, 86: 273-288. Chu YM, Jeon JJ, Yea SJ, Kim YH, Yun SH, Lee YW, et al. (2002) Double-stranded RNA mycovirus from Fusarium graminearum. Applied and Environmental Microbiology, 68: 2529–2534. Chu YM, Lim WS, Yea SJ, Cho JD, Lee YW, Kim KH (2004) Complexity of dsRNA mycovirus isolated from Fusarium graminearum. Virus Genes, 28: 135–143. Chun SJ, Lee YH (1997) Inheritance of dsRNAs in the rice blast fungus, Magnaporthe grisea. FEMS microbiology letters, 148(2): 159-162. Compel P, Papp I, Bibo M, Fekete C, Hornok L (1999) Genetic interrelationships and genome organization of double-stranded RNA elements of Fusarium poae. Virus Genes, 18: 49–56. Darissa O, Willingmann P, Schafer W, Adam G (2011) A novel double-stranded RNA mycovirus from Fusarium graminearum: nucleic acid sequence and genomic structure. Archives of Virology, 156: 647–658. Darissa O, Adam G, Schäfer W (2012) A dsRNA mycovirus causes hypovirulence of Fusarium graminearum to wheat and maize. European Journal of Plant Pathology, 134(1): 181-189. Davison AJ (2017) Journal of General Virology–Introduction to ‘ICTV Virus Taxonomy Profiles’. Journal of General Virology, 98: 1. Dawe AL, Nuss DL (2013) Hypovirus molecular biology: from Koch's postulates to host self- recognition genes that restrict virus transmission. Advances in Virus Research, 86: 109– 147. Deng F, Allen TD, Hillman BI, Nuss DL (2007) Comparative analysis of alterations in host phenotype and transcript accumulation following hypovirus and mycoreovirus infections of the chestnut blight fungus Cryphonectria parasitica. Eukaryotic Cell, 6(8): 1286-1298. Erincik Ö, Mersin E, Açıkgöz S (2018) Cryphonectria parasitica’nın hipovirülent strainlerinin fenol ve kloroform içermeyen dsRNA analiz yöntemi ile belirlenmesi ve Cryphonectria hypovirus 1’in RT-PCR İle Tanılanması. Adnan Menderes Üniversitesi Ziraat Fakültesi Dergisi, 15(2): 25-32. Eguchi N, Kondo K, Yamagishi N (2009) Bait twig method for soil detection of Rosellinia necatrix, causal agent of white root rot of Japanese pear and apple, at an early stage of tree infection. Journal of General Plant Pathology, 75: 325–330. Feau N, Dutech C, Brusini J, Rigling D, Robin C (2014) Multiple introductions and recombination in Cryphonectria hypovirus 1: Perspective for a sustainable biological control of chestnut blight. Evolutionary Applications, 7: 580–596. García-Pedrajas MD, Cañizares MC, Sarmiento-Villamil JL, Jacquat AG, Dambolena JS (2019). Mycoviruses in biological control: From basic research to field implementation. Phytopathology, 109(11): 1828-1839. Ghabrial SA (1998) Origin, adaptation and evolutionary of fungal viruses. Virus Genes, 16: 119-131. Ghabrial SA (2001) Fungal viruses. In: Maloy, O. & Murray, T., (Eds.), Encyclopedia of plant pathology. John Wiley & Sons, New York, pp. 478-483. Ghabrial SA (2009) Suzuki N. Viruses of plant pathogenic fungi. The Annual Review of Phytopathology, 47: 353-384. Go SJ, Cha DY, Wessels JGH (1992) Symptoms of virus infected oyster mushroom, Pleurotus florida. The Korean Journal of Mycology, 20: 229-233. Göker M, Scheuner C, Klenk HP, Stielow JB, Menzel W (2011) Codivergence of mycoviruses with their hosts. PLoS One, 6(7), e22252. Griffin GJ, Robbins N, Hogan EP, Farias‐Santopietro G (2004) Nucleotide sequence identification of Cryphonectria hypovirus 1 infecting Cryphonectria parasitica on grafted American chestnut trees 12–18 years after inoculation with a hypovirulent strain mixture. Forest Pathology, 34(1): 33-46. Guerin L, Froidefond G, Xu M (2001) Seasonal patterns of dispersal of ascospores of Cryphonectria parasitica (Chestnut blight). Plant Pathology, 50: 717-724. Hamid M, Xie J, Wu S, Maria S, Zheng D, Assane HA, Wang Q, Cheng J, Fu Y, Jiang DA (2018) Novel Deltaflexivirus that Infects the Plant Fungal Pathogen, Sclerotinia sclerotiorum, Can Be Transmitted Among Host Vegetative Incompatible Strains. Viruses, 10: 295. Hansen DR, van Alfen NK, Gillies K, Powell WA (1985) Naked dsRNA associated with hypovirulence of Endothia parasitica is packaged in fungal vesicles. Journal of General Virology, 66: 2605-2614. Hillman BI, Suzuki N (2004a) Viruses of the chestnut blight fungus, Cryphonectria parasitica. Advances in Virus Research, 63: 423-472. Hillman BI, Supyrani S, Kondo H, Suzuki N (2004b) A reovirus of the fungus Cryphonectria parasitica that is infectious as particles and related to the Coltivirus genus of animal pathogens, Journal of Virology,78: 892-898. Hollings M (1982) Mycoviruses and plant pathology. Plant Disease, 66: 1106-1112. Hong Y, Cole TE, Brasier CM, Buck KW (1998) Evolutionary relationships among putative RNAdependent RNA polymerases encoded by a mitochondrial virus-like RNA in the Dutch elm disease fungus, Ophiostoma novo-ulmi, by other viruses and virus-like RNAs and by the Arabidopsis mitochondrial genome. Virology, 246: 158- 169. Howitt RL, Beever RE, Pearson MN, Forster RL (2006). Genome characterization of a flexuous rod-shaped mycovirus, Botrytis virus X, reveals high amino acid identity to genes from plant 'potex-like’viruses. Archives of Virology, 151: 563-79. Huang X, Zhang N, Yong X, Yang X, Shen Q (2012) Biocontrol of Rhizoctonia solani damping-off disease in cucumber with Bacillus pumilus SQR-N43. Microbiological Research, 167: 135–143. Ihrmark K, Stenström E, Stenlid J (2004) Double-stranded RNA transmission through basidiospores of Heterobasidion annosum. Mycological Research, 108: 149–153. Ikeda K, Nakamura H, Arakawa M, Matsumoto N (2004) Diversity and vertical transmission of double-stranded RNA elements in root rot pathogens of trees, Helicobasidium mompa and Rosellinia necatrix. Mycological Research, 108: 626-634. Jian J, Lakshman DK, Tavantzis SM (1997) Association of distinct double-stranded RNAs with enhanced or diminished virulence in Rhizoctonia solani infecting potato. Mol. Plant-Microbe Interact 1997, 10, 1002–1009., J.; Lakshman, D.K.; Tavantzis, S.M. Association of distinct double-stranded RNAs with enhanced or diminished virulence in Rhizoctonia solani infecting potato. Molecular Plant-Microbe Interactions, 10: 1002–1009. Jiang D, Li G, Fu Y, Yi X, Wang D (1998) Transmissible hypovirulent element in isolate Ep- 1PN of Sclerotinia sclerotiorum. Chinese Science Bulletin, 43: 779–781. Jiang D, Fu Y, Ghabrial SA (2013) Mycoviruses: Chapter eight—viruses of the plant pathogenic fungus Sclerotinia sclerotiorum. Advances in Virus Research, 86: 215– 248. Kanadani G, Date H, Nasu H (1998) Effect of Fluazinam soildrench on white root rot of grapevine. Annals of the Phytopathological Society of Japan, 64: 139–141. Kanematsu S, Arakawa M, Oikawa Y, Onoue M, Osaki H, Nakamura H, Ikeda K, KugaUetake Y, Nitta H, Sasaki A, Suzaki K, Yoshida K, Matsumoto N (2004) A reovirus cases hypovirulence of Rosellinia necatrix. Phytopathology, 94: 561-568. Kotta-Loizou I, Coutts RH (2017) Mycoviruses in Aspergillius: A comprehensive review.Frontiers in Microbiology, 8: 1699. Kouzai Y, Kimura M, Watanabe M, Kusunoki K, Osaka D, Suzuki T, Matsui H, Yamamoto M, Ichinose Y, Toyoda K (2018). Salicylic acid-dependent immunity contributes to resistance against Rhizoctonia solani, a necrotrophic fungal agent of sheath blight, in rice and Brachypodium distachyon. New Phytologist, 217: 771–783. Kwon SJ, Cho SY, Lee KM, Yu J, Son M, Kim KH (2009) Proteomic analysis of fungal host factors differentially expressed by Fusarium graminearum infected with Fusarium graminearum virus-DK21. Virus Research, 144(1-2): 96-106. Lakshman DK, Jian J, Tavantzis SM (1998) A doublestranded RNA element from a hypovirulent strain of Rhizoctonia solani occurs in DNA from and is genetically related to the pentafunctional AROM protein of the shikimate pathway. Proceedings of the National Academy of Sciences of the USA, 95: 6425-6429. Lemke PA, Molitoris HP, Hollings M, Wood HA (1979) Fungal Viruses. Springer- Verlag, Berlin, pp. 2±7. Lemus-Minor CG, Canizares MC, Garcia-Pedrajas MD, Perez-Artes E (2015) Complete genome sequence of a novel dsRNA mycovirus isolated from the phytopathogenic fungus Fusarium oxysporum f. sp. dianthi. Archives of Virolog, 160: 2375–2379. Lemus-Minor CG, Cañizares-Nolasco C, Mdd GP, Pérez-Artés E (2018) Fusarium oxysporum f. sp. dianthi virus 1 accumulation is correlated with changes in virulence and other phenotypic traits of its fungal host. Phytopathology, 108: 957–963. Li G, Wang D, Huang HC Zhou Q (1996) Polymorphisms of Sclerotinia sclerotiorum isolated from eggplant in Jiamusi, Heilongjiang Province. Zhi Wu Bing Li Xue Bao, 26: 237–242. Li G, Jiang D, Wang D, Zhu B, Rimmer R (1999b) Doublestranded RNAs associated with the hypovirulence of Sclerotinia sclerotiorum strain Ep-1PN. Progress in Natural Science, 9: 836–841. Li P, Zhang H, Chen X, Qiu D, Guo L (2015) Molecular characterization of a novel hypovirus from the plant pathogenic fungus Fusarium graminearum. Virology, 481: 151–160. Li Z, Chen L, Meiling Z, Mei Y, Erxun Z (2018) Diversity of dsRNA viruses infecting rice sheath blight fungus Rhizoctonia solani AG-1 IA. Rice Science, 25: 57–60. Li W, Xia Y, Zhang H, Zhang X, Chen H (2019) A Victorivirus from Fusarium asiaticum, the pathogen of Fusarium head blight in China. Archives of Virolog, 164: 313–316. Lin YH, Chiba S, Tani A, Kondo H, Sasaki A, Kanematsu S, Suzuki N (2012) A novel quadripartite dsRNA virus isolated from a phytopathogenic filamentous fungus, Rosellinia necatrix. Virology, 426: 42–50. Lin YH, Fujita M, Chiba S, Hyodo K, Andika IB, Suzuki N, Kondo H (2019) Two novel fungal negative-strand RNA viruses related to mymonaviruses and phenuiviruses in the shiitake mushroom (Lentinula edodes). Virology, 533: 125–136. Liu YC, Milgroom MG (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. Liu C, Lakeshman DK, Tavantzis SM (2003) Quinic acid induces hypovirulence and expression of a hypovirulence-associated double-strand RNA in Rhizoctonia solani. Current Genetics, 43: 103–111. Liu H, Fu Y, Jiang D, Li G, Xie J, Cheng J, Peng Y, Ghabrial SA, Yi X (2010) Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes J. Virology, 84(22): 11876-11887. Liu C, Zeng M, Zhang M, Shu C, Zhou E (2018) Complete nucleotide sequence of a partitivirus from Rhizoctonia solani AG-1 IA strain C24. Viruses, 10: 703. Lyu R, Zhang Y, Tang Q, Li Y, Cheng J, Fu Y, Chen T, Jiang D, Xie J (2018) Two alphapartitiviruses co-infecting a single isolate of the plant pathogenic fungus Rhizoctonia solani. Archives of Virolog, 163: 515–520. Magliani W, Conti S, Gerloni M, Bertolotti D, Polonelli L (1997) Yeast killer systems. Clinical Microbiology Reviews, 10: 369-400. Marvelli RA, Hobbs HA, Li S, McCoppin NK, Domier LL, Hartman GL, Eastburn DM (2014) Identification of novel double-stranded RNA mycoviruses of Fusarium virguliforme and evidence of their effects on virulence. Archives of Virology, 159(2): 349-352. McCabe PM, Pfeiffer P, Van Alfen NK (1999)VThe influence of dsRNA viruses on the biology of plant pathogenic fungi. Trends Microbiology, 7: 377–81. Melzer MS, Boland GJ (1996) Transmissible hypovirulence in Sclerotinia minor. Canadian Journal of Plant Pathology, 18: 19–28. Milgroom MG, Cortesi P (2004) Biological control of chestnut blight with hypovirulence: A critical analysis. Annual Review of Phytopathology, 42: 311-338. Moleleki N, van Heerden SW, Wingfield MJ, Wingfield BD, Preisig O (2003) Transfection of Diaporthe perjuncta with Diaporthe RNA virus. Applied and Environmental Microbiology, 69: 3952–3956. Muñoz-Adalia EJ, Fernández MM, Diez JJ (2016) The use of mycoviruses in the control of forest diseases. Biocontrol Science and Technology, 26 (5): 577-604. Nerva L, Forgia M, Ciuffo M, Chitarra W, Chiapello M, Vallino M, Varese G, Turina M (2019) The mycovirome of a fungal collection from the sea cucumber Holothuria polii. Virus Research, 273: 197737. Newhouse JR, Hoch HC, MacDonald WL (1983) The ultra structure of Endothia parasitica comparison of a virulent with a hypovirulent isolate. Canadian Journal of Botany, 61: 389-399. Nogawa M, Kageyama T, Nakatani AG, Shimosaka M, Okazaki M (1996) Cloning and characterization of mycovirus double-stranded RNA from the plant pathogenic fungus, Fusarium solani f. sp. robiniae. Bioscience, Biotechnology, and Biochemistry, 60: 784–788. Nuss DL (2005) Hypovirulence: mycoviruses at the fungal–plant interface. Nature Reviews Microbiology, 3(8): 632-642. Nuss DL (2011) Mycoviruses, RNA silencing, and viral RNA recombination. Advances in Virus Research, 80: 25-48. Osaki H, Sasaki A, Nomiyama K, Sekiguchi H, Tomioka K, Takehara T (2015) Isolation and characterization of two mitoviruses and a putative alphapartitivirus from Fusarium spp. Virus Genes, 50: 466–473. Pearson MN, Beever RE, Boine B, Arthur K (2009) Mycoviruses of filamentous fungi and their relevance to plant pathology. Molecular Plant Pathology, 10: 115–128. Peever TL, Liu YC, Cortesi P, Milgroom MG (2000) Variation in tolerance and virulence in the chestnut blight fungus-hypovirus interaction. Applied and Environmental Microbiology, 66(11): 4863-4869. Picarelli MAS, Forgia M, Rivas EB, Nerva L, Chiapello M, Turina M, Colariccio A (2019) Extreme diversity of mycoviruses present in isolates of Rhizoctonia solani AG2-2 LP from Zoysia japonica from Brazil. Frontiers in Cellular and Infection Microbiology, 9: 244. Rigling D, van Alfen NK (1993) Extra- and intracellular laccase of the chestnut blight fungus, Cryphonectria parasitica. Applied and Environmental Microbiology, 59: 3634-3639. Robin C, Heiniger U (2001) Chestnut blight in Europe: Diversity of Cryphonectria parasitica, hypovirulence and biocontrol. Forest Snow and Land scape Research, 76: 361–367. Rogers HJ, Buck KW, Brasier CM (1987) A mitochondrial target for double-stranded RNA in diseased isolates of the fungus that causes Dutch elm disease. Nature, 329 (6139): 558. Sasaki A, Miyanishi M, Ozaki K, Onoue M, Yoshida K (2005) Molecular characterization of a partitivirus from the plant pathogenic ascomycete Rosellinia necatrix. Archives of Virology, 150: 1069–1083. Sasaki A, Kanematsu S, Onoue M, Oyama Y, Yoshida K (2006) Infection of Rosellinia necatrix with purified viral particles of a member of Partitiviridae (RnPV1-W8). Archives of Virology, 151: 697-707. 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. The EMBO Journal, 10(4): 731-739. Sharma M, Guleria S, Singh K, Chauhan A, Kulshrestha S (2018) Mycovirus associated hypovirulence, a potential method for biological control of Fusarium species. Virus disease, 29: 134–140. Smart CD, Yuan W, Foglia R, Nuss DL, Fulbright DW, Hillman BI (1999) Cryphonectria hypovirus 3, a virus species in the family Hypoviridae with a single open reading frame. Virology, 265(1): 66-73. Son M, Yu J, Kim KH (2015) Five questions about mycoviruses. PLOS Pathogens, 11: e1005172. Sonnenberg ASM, Van Griensven LJLD (1991) Evidence for transmission of La France disease in Agaricus bisporus by dsRNA. In: Genetics and breeding of Agaricus: proceedings of the first international seminar on mushroom science, Mushroom Experimental Station, Horst, the Netherlands. Ed. by Van Griensven, L. J.L.D. Pudoc. Wageningen, the Netherlands. pp. 109-113. Sonnenberg ASM, van Kempen IPJ, van Griensven LJDL (1995) Detection of Agaricus bisporus viral dsRNAs in pure cultures, spawn and spawn-run compost by RT-PCR. In: Mushroom Science, 14 (Eds.: T.J. Elliott. A.A. Balkema), Rotterdam, the Netherlands, 587-594. Sutherland ML, Brasier CM (1995) Effect of d-factors on in vitro cerato-ulmin production by the Dutch elm disease pathogen Ophiostoma novo-ulmi. Mycological Research, 99(10): 1211-1217. Van Regenmortel MH, Fauquet CM, Bishop DHL, Carstens EB, Estes MK, Lemon SM, Aniloff J, Mayo MA, Mcgeoch DJ, Pringle CR, Wickner RB (2000) Virus taxonomy, classification and nomenclature of viruses. Seventh Report of the International Committee on Taxonomy of Viruses, Academic Press, San Diego, USA, 1162 pp. Velasco L, Arjona-Girona I, Cretazzo E, López-Herrera C (2019) Viromes in Xylariaceae fungi infecting avocado in Spain. Virology, 532: 11–21. Xie J, Jiang D (2014) New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annual Review of Phytopathology, 52: 45-68. Yaegashi H, Nakamura H, Sawahata T, Sasaki A, Iwanami Y, Ito T, Kanematsu S (2012) Appearance of mycovirus-like double-stranded RNAs in the white root rot fungus, Rosellinia necatrix, in an apple orchard. FEMS Microbiology Ecology, 83(1): 49-62. Yu J, Kwon SJ, Lee KM, Son M, Kim KH (2009) Complete nucleotide sequence of double- stranded RNA viruses from Fusarium graminearum strain DK3. Archives of Virology, 154: 1855–1858. Yu X, Li B, Fu Y, Jiang D, Ghabrial SA, Li G, Peng Y, Xie J, Cheng J, Huang J, Yi X (2010) A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proceedings of the National Academy of Sciences, 107(18): 8387-8392. Yu JS, Lee KM, Son MI, Kim KH (2011) Molecular characterization of Fusarium graminearum virus 2 Isolated from Fusarium graminearum strain 98-8-60. Plant Pathology, 27: 285–290. Yu X, Li B, Fu Y, Xie J, Cheng J, Ghabrial SA, Li G, Yi X, Jiang D (2013) Extracellular transmission of a DNA mycovirus and its use as a natural fungicide. Proceedings of the National Academy of Sciences, 110(4): 1452-1457. 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 Research, 174 (1-2): 69-77. Wang L, Zhang J, Zhang H, Qiu D, Guo L (2016a) Two novel relative double-stranded RNA mycoviruses infecting Fusarium poae strain SX63. International Journal of Molecular Sciences, 17: E641. Wang S, Ongena M, Qiu D, Guo L (2017) Fungal viruses: Promising fundamental research and biological control agents of fungi. SM Virology, 2(1): 1011. Wei CZ, Osaki H, Iwanami T, Matsumoto N, 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. Journal of General Virology, 84: 2431-2437. Wei CZ, Osaki H, Iwanami T, Matsumoto N, Ohtsu Y (2004) Complete nucleotide sequences of genome segments 1 and 3 of Rosellinia anti-rot virus in the family Reoviridae. Archives of Virology, 149: 773–777. Zhang L, Fu Y, Xie J, Jiang D, Li G, Yi X (2009) A novel virus that infecting hypovirulent strain XG36-1 of plant fungal pathogen Sclerotinia sclerotiorum. Virology, 6: 96. Zhang X, Gao F, Zhang F, Xie Y, Zhou L, Yuan H, et al. (2018) The complete genomic sequence of a novel megabirnavirus from Fusarium pseudograminearum, the causal agent of wheat crown rot. Archives of Virology, 163: 3173–3175. Zhang M, Zheng L, Liu C, Shu C, Zhou E (2018) Characterization of a novel dsRNA mycovirus isolated from strain A105 of Rhizoctonia solani AG-1 IA. Archives of Virology, 163: 427–430. Zhang X, Xie Y, Zhang F, Sun H, Zhai Y, Zhang S, et al. (2019) Complete genome sequence of an alternavirus from the phytopathogenic fungus Fusarium incarnatum. Archives of Virology, 164: 923–925. 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. Archives of Virology, 158: 1609–1612. Zheng L, Zhang M, Chen Q, Zhu M, Zhou EA (2014) Novel mycovirus closely related to viruses in the genus Alphapartitivirus confers hypovirulence in the phytopathogenic fungus Rhizoctonia solani. Virology, 456: 220–226. Zheng, L., Shu, C., Zhang, M., Yang, M., & Zhou, E. (2019). Molecular Characterization of a Novel Endornavirus Conferring Hypovirulence in Rice Sheath Blight Fungus Rhizoctonia solani AG-1 IA Strain GD-2. Viruses, 11, 178. Zhong, J., Chen, C. Y., & Gao, B. D. (2015). Genome sequence of a novel mycovirus of Rhizoctonia solani, a plant pathogenic fungus. Virus Genes, 51, 167–170. Zhou, T. & Boland, G. J. (1997). Hypovirulence and double stranded RNAs in Sclerotinia homoecocarpa. Phytopathology, 87, 147–153.