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Abstract

RNA interference (RNAi) is a conserved eukaryotic mechanism that uses small RNA molecules to suppress gene expression through sequence-specific messenger RNA degradation, translational repression, or transcriptional inhibition. In filamentous fungi, the protective function of RNAi in the maintenance of genome integrity is well known. However, knowledge of the regulatory role of RNAi in fungi has had to wait until the recent identification of different endogenous small RNA classes, which are generated by distinct RNAi pathways. In addition, RNAi research on new fungal models has uncovered the role of small RNAs and RNAi pathways in the regulation of diverse biological functions. In this review, we give an up-to-date overview of the different classes of small RNAs and RNAi pathways in fungi and their roles in the defense of genome integrity and regulation of fungal physiology and development, as well as in the interaction of fungi with biotic and abiotic environments.

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2017-09-08
2024-04-23
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Literature Cited

  1. Alexander WG, Raju NB, Xiao H, Hammond TM, Perdue TD. 1.  et al. 2008. DCL-1 colocalizes with other components of the MSUD machinery and is required for silencing. Fungal Genet. Biol. 45:719–27 [Google Scholar]
  2. Åsman AK, Fogelqvist J, Vetukuri RR, Dixwlius C. 2.  2016. Phytophthora infectans Argonaute 1 binds microRNA and small RNAs from effector genes and transposable elements. New Phytol 211:993–1007 [Google Scholar]
  3. Bai Y, Lan F, Yang W, Zhang F, Yang K. 3.  et al. 2015. sRNA profiling in Aspergillus flavus reveals differentially expressed miRNA-like RNAs response to water activity and temperature. Fungal Genet. Biol. 81:113–19 [Google Scholar]
  4. Bhatnagar-Mathur P, Sunkara S, Bhatnagar-Panwar M, Waliyar F, Sharma KK. 4.  2015. Biotechnological advances for combating Aspergillus flavus and aflatoxin contamination in crops. Plant Sci 234:119–32 [Google Scholar]
  5. Billmyre RB, Calo S, Feretzaki M, Wang X, Heitman J. 5.  2013. RNAi function, diversity, and loss in the fungal kingdom. Chromosome Res 21:561–72 [Google Scholar]
  6. Calo S, Nicolás FE, Lee SC, Vila A, Cervantes M. 6.  et al. 2017. A non-canonical RNA degradation pathway suppresses RNAi-dependent epimutations in the human fungal pathogen Mucor circinelloides. PLOS Genet. 13:e1006686 [Google Scholar]
  7. Calo S, Nicolás FE, Vila A, Torres-Martínez S, Ruiz-Vázquez RM. 7.  2012. Two distinct RNA-dependent RNA polymerases are required for initiation and amplification of RNA silencing in the basal fungus Mucor circinelloides. Mol. Microbiol. 83:379–94 [Google Scholar]
  8. Calo S, Shertz-Wall C, Lee SC, Bastidas RJ, Nicolás FE. 8.  et al. 2014. Antifungal drug resistance evoked via RNAi-dependent epimutations. Nature 513:555–58 [Google Scholar]
  9. Campo S, Gilbert KB, Carrington JC. 9.  2016. Small RNA-based antiviral defense in the phytopathogenic fungus Colletotrichum higginsianum. PLOS Pathog. 12:e1005640 [Google Scholar]
  10. Carreras-Villaseñor N, Esquivel-Naranjo EU, Villalobos-Escobedo JM, Abreu-Goodger C, Herrera-Estrella A. 10.  2013. The RNAi machinery regulates growth and development in the filamentous fungus Trichoderma atroviride. Mol. Microbiol. 89:96–112 [Google Scholar]
  11. Castanera R, López-Varas L, Borgognone A, LaButti K, Lapidus A. 11.  et al. 2016. Transposable elements versus the fungal genome: impact on whole-genome architecture and transcriptional profiles. PLOS Genet 12:e1006108 [Google Scholar]
  12. Catalanotto C, Azzalin G, Macino G, Cogoni C. 12.  2000. Gene silencing in worms and fungi. Nature 404:245 [Google Scholar]
  13. Catalanotto C, Azzalin G, Macino G, Cogoni C. 13.  2002. Involvement of small RNAs and role of the qde genes in the gene silencing pathway in Neurospora. Genes Dev. 16:790–95 [Google Scholar]
  14. Catalanotto C, Pallotta M, ReFalo P, Sachs MS, Vayssie L. 14.  et al. 2004. Redundancy of the two dicer genes in transgene-induced posttranscriptional gene silencing in Neurospora crassa. Mol. Cell. Biol. 24:2536–45 [Google Scholar]
  15. Cecere G, Cogoni C. 15.  2009. Quelling targets the rDNA locus and functions in rDNA copy number control. BMC Microbiol 9:44 [Google Scholar]
  16. Cervantes M, Vila A, Nicolás FE, Moxon S, de Haro JP. 16.  et al. 2013. A single argonaute gene participates in exogenous and endogenous RNAi and controls cellular functions in the basal fungus Mucor circinelloides. PLOS ONE 8:e69283 [Google Scholar]
  17. Chang SS, Zhang Z, Liu Y. 17.  2012. RNA interference pathways in fungi: mechanisms and functions. Annu. Rev. Microbiol. 66:305–23 [Google Scholar]
  18. Chen R, Jiang N, Jiang Q, Sun X, Wang Y. 18.  et al. 2014. Exploring microRNA-like small RNAs in the filamentous fungus Fusarium oxysporum. PLOS ONE 9:e104956 [Google Scholar]
  19. Chen Y, Gao Q, Huang M, Liu Y, Liu Z. 19.  et al. 2015. Characterization of RNA silencing components in the plant pathogenic fungus Fusarium graminearum. Sci. Rep. 5:12500 [Google Scholar]
  20. Choi J, Kim KT, Jeon J, Wu J, Song H. 20.  et al. 2014. funRNA: a fungi-centered genomics platform for genes encoding key components of RNAi. BMC Genom 15:Suppl. 9S14 [Google Scholar]
  21. Cogoni C, Macino G. 21.  1999. Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature 399:166–69 [Google Scholar]
  22. Cogoni C, Macino G. 22.  1999. Posttranscriptional gene silencing in Neurospora by a RecQ DNA helicase. Science 286:2342–44 [Google Scholar]
  23. Cullen BR. 23.  2014. Viruses and RNA interference: issues and controversies. J. Virol. 88:12934–36 [Google Scholar]
  24. Dahlmann TA, Kück U. 24.  2015. Dicer-dependent biogenesis of small RNAs and evidence for microRNA-like RNAs in the penicillin producing fungus Penicillium chrysogenum. PLOS ONE 10:e0125989 [Google Scholar]
  25. Dang Y, Cheng J, Sun X, Zhou Z, Liu Y. 25.  2016. Antisense transcription licenses nascent transcripts to mediate transcriptional gene silencing. Genes Dev 30:2417–32 [Google Scholar]
  26. Dang Y, Li L, Guo W, Xue Z, Liu Y. 26.  2013. Convergent transcription induces dynamic DNA methylation at disiRNA loci. PLOS Genet 9:e1003761 [Google Scholar]
  27. Dang Y, Zhang Z, Liu Y. 27.  2014. Small RNA-mediated gene silencing in Neurospora. See Ref. 100 269–89
  28. de Haro JP, Calo S, Cervantes M, Nicolás FE, Torres-Martínez S, Ruiz-Vázquez RM. 28.  2009. A single dicer gene is required for efficient gene silencing associated with two classes of small antisense RNAs in Mucor circinelloides. Eukaryot. Cell 8:1486–97 [Google Scholar]
  29. Decker LM, Boone EC, Xiao H, Shanker BS, Boone SF. 29.  et al. 2015. Complex formation of RNA silencing proteins in the perinuclear region of Neurospora crassa. Genetics 199:1017–21 [Google Scholar]
  30. Donaldson ME, Saville BJ. 30.  2012. Natural antisense transcripts in fungi. Mol. Microbiol. 85:405–17 [Google Scholar]
  31. Donaldson ME, Saville BJ. 31.  2013. Ustilago maydis natural antisense transcript expression alters mRNA stability and pathogenesis. Mol. Microbiol. 89:29–51 [Google Scholar]
  32. Drinnenberg IA, Fink GR, Bartel DP. 32.  2011. Compatibility with killer explains the rise of RNAi-deficient fungi. Science 333:1592 [Google Scholar]
  33. Dumesic PA, Natarajan P, Chen CB, Drinnenberg IA, Schiller BJ. 33.  et al. 2013. Stalled spliceosomes are a signal for RNAi-mediated genome defense. Cell 152:957–96 [Google Scholar]
  34. Ellendorff U, Fradin EF, de Jonge R, Thomma BP. 34.  2009. RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J. Exp. Bot. 60:591–602 [Google Scholar]
  35. Faghihi MA, Wahlestedt C. 35.  2009. Regulatory roles of natural antisense transcripts. Nat. Rev. Mol. Cell Biol. 10:637–43 [Google Scholar]
  36. Fahlgren N, Bollmann SR, Kasschau KD, Cuperus JT, Press CM. 36.  et al. 2013. Phytophthora have distinct endogenous small RNA populations that include short interfering and microRNAs. PLOS ONE 8:e77181 [Google Scholar]
  37. Feretzaki M, Billmyre RB, Clancey SA, Wang X, Heitman J. 37.  2016. Gene network polymorphism illuminates loss and retention of novel RNAi silencing components in the Cryptococcus pathogenic species complex. PLOS Genet 12:e1005868 [Google Scholar]
  38. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. 38.  1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–11 [Google Scholar]
  39. Francia S, Michelini F, Saxena A, Tang D, de Hoon M. 39.  et al. 2012. Site-specific DICER and DROSHA RNA products control the DNA damage response. Nature 488:231–35 [Google Scholar]
  40. Garre V, Nicolás FE, Torres-Martínez S, Ruiz-Vázquez RM. 40.  2014. The RNAi machinery in Mucorales: the emerging role of endogenous small RNAs. See Ref. 100 291–313
  41. Gazzani S, Lawrenson T, Woodward C, Headon D, Sablowski R. 41.  2004. A link between mRNA turnover and RNA interference in Arabidopsis. Science 306:1046–48 [Google Scholar]
  42. Ghildiyal M, Zamore PD. 42.  2009. Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10:94–108 [Google Scholar]
  43. Goes T, Bailão EFLC, Correa CR, Bozzi A, Santos LI. 43.  et al. 2014. New developments of RNAi in Paracoccidioides brasiliensis: prospects for high-throughput, genome-wide, functional genomics. PLOS Negl. Trop. Dis. 8:e3173 [Google Scholar]
  44. Grandaubert J, Lowe RG, Soyer JL, Schoch CL, Van de Wouw AP. 44.  et al. 2014. Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens. BMC Genom. 15:891 [Google Scholar]
  45. Hammond TM, Andrewski MD, Roossinck MJ, Keller NP. 45.  2008. Aspergillus mycoviruses are targets and suppressors of RNA silencing. Eukaryot. Cell 7:350–57 [Google Scholar]
  46. Hammond TM, Bok JW, Andrewski MD, Reyes-Domínguez Y, Scazzocchio C, Keller NP. 46.  2008. RNA silencing gene truncation in the filamentous fungus Aspergillus nidulans. Eukaryot. Cell 7:339–49 [Google Scholar]
  47. Hammond TM, Keller NP. 47.  2005. RNA silencing in Aspergillus nidulans is independent of RNA-dependent RNA polymerases. Genetics 169:607–17 [Google Scholar]
  48. Hammond TM, Spollen WG, Decker LM, Blake SM, Springer GK. 48.  et al. 2013. Identification of small RNAs associated with meiotic silencing by unpaired DNA. Genetics 194:279–84 [Google Scholar]
  49. Hammond TM, Xiao H, Boone EC, Decker LM, Lee SA. 49.  et al. 2013. Novel proteins required for meiotic silencing by unpaired DNA and siRNA generation in Neurospora crassa. Genetics 194:91–100 [Google Scholar]
  50. Hammond TM, Xiao H, Boone EC, Perdue TD, Pukkila PJ, Shiu PK. 50.  2011. SAD-3, a putative helicase required for meiotic silencing by unpaired DNA, interacts with other components of the silencing machinery. G3 5:369–76 [Google Scholar]
  51. Janbon G, Maeng S, Yang DH, Ko YJ, Jung KW. 51.  et al. 2010. Characterizing the role of RNA silencing components in Cryptococcus neoformans. Fungal Genet. Biol. 47:1070–80 [Google Scholar]
  52. Jiang N, Yang Y, Janbon G, Pan J, Zhu X. 52.  2012. Identification and functional demonstration of miRNAs in the fungus Cryptococcus neoformans. PLOS ONE 7:e52734 [Google Scholar]
  53. Kadotani N, Nakayashiki H, Tosa Y, Mayama S. 53.  2003. RNA silencing in the phytopathogenic fungus Magnaporthe oryzae. Mol. Plant Microbe Interact. 16:769–76 [Google Scholar]
  54. Kadotani N, Nakayashiki H, Tosa Y, Mayama S. 54.  2004. One of the two Dicer-like proteins in the filamentous fungi Magnaporthe oryzae genome is responsible for hairpin RNA-triggered RNA silencing and related small interfering RNA accumulation. J. Biol. Chem. 279:44467–74 [Google Scholar]
  55. Kang K, Zhong J, Jiang L, Liu G, Gou CY. 55.  et al. 2013. Identification of microRNA-like RNAs in the filamentous fungus Trichoderma reesei by Solexa sequencing. PLOS ONE 8:e76288 [Google Scholar]
  56. Koch A, Biedenkopf D, Furch A, Weber L, Rossbach O. 56.  et al. 2016. An RNAi-based control of Fusarium graminearum infections through spraying of long dsRNAs involves a plant passage and is controlled by the fungal silencing machinery. PLOS Pathog 12:e1005901 [Google Scholar]
  57. Koch A, Kogel KH. 57.  2014. New wind in the sails: improving the agronomic value of crop plants through RNAi-mediated gene silencing. Plant Biotechnol. J. 12:821–31 [Google Scholar]
  58. Kramer C, Loros JJ, Dunlap JC, Crosthwaite SK. 58.  2003. Role for antisense RNA in regulating circadian clock function in Neurospora crassa. Nature 421:948–52 [Google Scholar]
  59. Kronholm I, Johannesson H, Ketola T. 59.  2016. Epigenetic control of phenotypic plasticity in the filamentous fungus Neurospora crassa. G3 6:4009–22 [Google Scholar]
  60. Kuan T, Zhai Y, Ma W. 60.  2016. Small RNAs regulate plant responses to filamentous pathogens. Semin. Cell Dev. Biol. 56:190–200 [Google Scholar]
  61. Lange H, Zuber H, Sement FM, Chicher J, Kuhn L. 61.  et al. 2014. The RNA helicases AtMTR4 and HEN2 target specific subsets of nuclear transcripts for degradation by the nuclear exosome in Arabidopsis thaliana. PLOS Genet. 10:e1004564 [Google Scholar]
  62. Lau SK, Chow WN, Wong AY, Yeung JM, Bao J. 62.  et al. 2013. Identification of microRNA-like RNAs in mycelial and yeast phases of the thermal dimorphic fungus Penicillium marneffei. PLOS Negl. Trop. Dis. 7:e2398 [Google Scholar]
  63. Laurie JD, Linning R, Bakkeren G. 63.  2008. Hallmarks of RNA silencing are found in the smut fungus Ustilago hordei but not in its close relative Ustilago maydis. Curr. Genet. 53:49–58 [Google Scholar]
  64. Lee DW, Pratt RJ, McLaughlin M, Aramayo R. 64.  2003. An Argonaute-like protein is required for meiotic silencing. Genetics 164:821–28 [Google Scholar]
  65. Lee HC, Aalto AP, Yang Q, Chang SS, Huang G. 65.  et al. 2010. The DNA/RNA-dependent RNA polymerase QDE-1 generates aberrant RNA and dsRNA for RNAi in a process requiring replication protein A and a DNA helicase. PLOS Biol 8:e1000496 [Google Scholar]
  66. Lee HC, Chang SS, Choudhary S, Aalto AP, Maiti M. 66.  et al. 2009. qiRNA is a new type of small interfering RNA induced by DNA damage. Nature 459:274–77 [Google Scholar]
  67. Lee HC, Li L, Gu W, Xue Z, Crosthwaite SK. 67.  et al. 2010. Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. Mol. Cell 38:803–14 [Google Scholar]
  68. Li N, Joska TM, Ruesch CE, Coster SJ, Belden WJ. 68.  2015. The frequency natural antisense transcript first promotes, then represses, frequency gene expression via facultative heterochromatin. PNAS 112:4357–62 [Google Scholar]
  69. Lin R, He L, He J, Qin P, Wang Y. 69.  et al. 2016. Comprehensive analysis of microRNA-Seq and target mRNAs of rice sheath blight pathogen provides new insights into pathogenic regulatory mechanisms. DNA Res 23:415–25 [Google Scholar]
  70. Lin YL, Ma LT, Lee YR, Lin SS, Wang S-Y. 70.  et al. 2015. microRNA-like small RNAs prediction in the development of Antrodia cinnamomea. PLOS ONE 10:e0123245 [Google Scholar]
  71. Liu T, Hu J, Zuo Y, Jin Y, Hou J. 71.  2016. Identification of microRNA-like RNAs from Curvularia lunata associated with maize leaf spot by bioinformation analysis and deep sequencing. Mol. Genet. Genom. 291:587–96 [Google Scholar]
  72. Luo Z, Chen Z. 72.  2007. Improperly terminated, unpolyadenylated mRNA of sense transgenes is targeted by RDR6-mediated RNA silencing in Arabidopsis. Plant Cell 19:943–58 [Google Scholar]
  73. Maiti M, Lee HC, Liu Y. 73.  2007. QIP, a putative exonuclease, interacts with the Neurospora Argonaute protein and facilitates conversion of duplex siRNA into single strands. Genes Dev 21:590–600 [Google Scholar]
  74. Martinez F, Dubos B, Fermaud M. 74.  2005. The role of saprotrophy and virulence in the population dynamics of Botrytis cinerea in vineyards. Phytopathology 95:692–700 [Google Scholar]
  75. Mueth NA, Ramachandran SR, Hulbert SH. 75.  2015. Small RNAs from the wheat stripe rust fungus (Puccinia striiformis f. sp. tritici). BMC Genom. 16:718 [Google Scholar]
  76. Murata T, Kadotani N, Yamaguchi M, Tosa Y, Mayama S, Nakayashiki H. 76.  2007. siRNA-dependent and -independent post-transcriptional cosuppression of the LTR-retrotransposon MAGGY in the phytopathogenic fungus Magnaporthe oryzae. Nucleic Acids Res. 35:5987–94 [Google Scholar]
  77. Nakayashiki H, Hanada S, Nguyen BQ, Kadotani N, Tosa Y, Mayama S. 77.  2005. RNA silencing as a tool for exploring gene function in ascomycete fungi. Fungal Genet. Biol. 42:275–83 [Google Scholar]
  78. Nakayashiki H, Nguyen QB. 78.  2008. RNA interference: roles in fungal biology. Curr. Opin. Microbiol. 11:494–502 [Google Scholar]
  79. Napoli C, Lemieux C, Jorgensen R. 79.  1990. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279–89 [Google Scholar]
  80. Nguyen QB, Kadotani N, Kasahara S, Tosa Y, Mayama S, Nakayashiki H. 80.  2008. Systematic functional analysis of calcium-signalling proteins in the genome of the rice-blast fungus, Magnaporthe oryzae, using a high-throughput RNA silencing system. Mol. Microbiol. 68:1348–65 [Google Scholar]
  81. Nicolás FE, de Haro JP, Torres-Martínez S, Ruiz-Vázquez RM. 81.  2007. Mutants defective in a Mucor circinelloides dicer-like gene are not compromised in siRNA silencing but display developmental defects. Fungal Genet. Biol. 44:504–16 [Google Scholar]
  82. Nicolás FE, Moxon S, de Haro J, Calo S, Grigoriev IV. 82.  et al. 2010. Endogenous short RNAs generated by Dicer 2 and RNA-dependent RNA polymerase 1 regulate mRNAs in the basal fungus Mucor circinelloides. Nucleic Acids Res. 38:5535–41 [Google Scholar]
  83. Nicolás FE, Ruiz-Vázquez RM. 83.  2013. Functional diversity of RNAi-associated sRNAs in fungi. Int. J. Mol. Sci. 14:15348–60 [Google Scholar]
  84. Nicolás FE, Torres-Martínez S, Ruiz-Vázquez RM. 84.  2003. Two classes of small antisense RNAs in fungal RNA silencing triggered by non-integrative transgenes. EMBO J 22:3983–91 [Google Scholar]
  85. Nicolás FE, Torres-Martínez S, Ruiz-Vázquez RM. 85.  2013. Loss and retention of RNA interference in fungi and parasites. PLOS Pathog 9:e1003089 [Google Scholar]
  86. Nicolás FE, Vila A, Moxon S, Cascales MD, Torres-Martínez S. 86.  et al. 2015. The RNAi machinery controls distinct responses to environmental signals in the basal fungus Mucor circinelloides. BMC Genom. 16:237 [Google Scholar]
  87. Nolan T, Braccini L, Azzalin G, De Toni A, Macino G, Cogoni C. 87.  2005. The post-transcriptional gene silencing machinery functions independently of DNA methylation to repress a LINE1-like retrotransposon in Neurospora crassa. Nucleic Acids Res. 33:1564–73 [Google Scholar]
  88. Nunes CC, Dean RA. 88.  2012. Host-induced gene silencing: a tool for understanding fungal host interaction and for developing novel disease control strategies. Mol. Plant Pathol. 13:519–29 [Google Scholar]
  89. Nunes CC, Gowda M, Sailsbery J, Xue M, Chen F. 89.  et al. 2011. Diverse and tissue-enriched small RNAs in the plant pathogenic fungus Magnaporthe oryzae. BMC Genom. 12:288 [Google Scholar]
  90. Qiao Y, Liu L, Xiong Q, Flores C, Wong J. 90.  et al. 2013. Oomycete pathogens encode RNA silencing suppressors. Nat. Genet. 45:330–33 [Google Scholar]
  91. Qiao Y, Shi J, Zhai Y, Hou Y, Ma W. 91.  2015. Phytophthora effector targets a novel component of small RNA pathway in plants to promote infection. PNAS 112:5850–55 [Google Scholar]
  92. Qutob D, Chapman BP, Gijzen M. 92.  2013. Transgenerational gene silencing causes gain of virulence in a plant pathogen. Nat. Commun. 4:1349 [Google Scholar]
  93. Raman V, Simon SA, Romag A, Demirci F, Mathioni SM. 93.  et al. 2013. Physiological stressors and invasive plant infections alter the small RNA transcriptome of the rice blast fungus. Magnaporthe oryzae. BMC Genom. 14:326 [Google Scholar]
  94. Roche B, Arcangioli B, Martienssen RA. 94.  2016. RNA interference is essential for cellular quiescence. Science 354:aah5651 [Google Scholar]
  95. Romano N, Macino G. 95.  1992. Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol. Microbiol. 6:3343–53 [Google Scholar]
  96. Ruiz-Vázquez RM, Nicolás FE, Torres-Martínez S, Garre V. 96.  2015. Distinct RNAi pathways in the regulation of physiology and development in the fungus Mucor circinelloides. Adv. Genet. 91:55–102 [Google Scholar]
  97. Salame TM, Ziv C, Hadar Y, Yarden O. 97.  2011. RNAi as a potential tool for biotechnological applications in fungi. Appl. Microbiol. Biotechnol. 89:501–12 [Google Scholar]
  98. Segers GC, van Wezel R, Zhang X, Hong Y, Nuss DL. 98.  2006. Hypovirus papain-like protease p29 suppresses RNA silencing in the natural fungal host and in a heterologous plant system. Eukaryot. Cell 6:896–904 [Google Scholar]
  99. Segers GC, Zhang X, Deng F, Sun Q, Nuss DL. 99.  2007. Evidence that RNA silencing functions as an antiviral defense mechanism in fungi. PNAS 104:12902–6 [Google Scholar]
  100. Sesma A, von der Haar T. 100. , eds. 2014. Fungal RNA Biology. Cham, Switz.: Springer Int. Publ. [Google Scholar]
  101. Shafran H, Miyara I, Eshed R, Prusky D, Sherman A. 101.  2008. Development of new tools for studying gene function in fungi based on the Gateway system. Fungal Genet. Biol. 45:1147–54 [Google Scholar]
  102. Shiu PK, Metzenberg RL. 102.  2002. Meiotic silencing by unpaired DNA: properties, regulation and suppression. Genetics 161:1483–95 [Google Scholar]
  103. Shiu PK, Raju NB, Zickler D, Metzenberg RL. 103.  2001. Meiotic silencing by unpaired DNA. Cell 107:905–16 [Google Scholar]
  104. Shiu PK, Zickler D, Raju NB, Ruprich-Robert G, Metzenberg RL. 104.  2006. SAD-2 is required for meiotic silencing by unpaired DNA and perinuclear localization of SAD-1 RNA-directed RNA polymerase. PNAS 7:2243–48 [Google Scholar]
  105. Son H, Min K, Lee J, Raju NB, Lee YW. 105.  2011. Meiotic silencing in the homothallic fungus Gibberella zeae. Fungal Biol. 12:1290–302 [Google Scholar]
  106. Son H, Park AR, Lim JY, Shin C, Lee YW. 106.  2017. Genome-wide exonic small interference RNA-mediated gene silencing regulates sexual reproduction in the homothallic fungus Fusarium graminearum. PLOS Genet. 13:e1006595 [Google Scholar]
  107. Soyer JL, El Ghalid M, Glaser N, Ollivier B, Linglin J. 107.  et al. 2014. Epigenetic control of effector gene expression in the plant pathogenic fungus Leptosphaeria maculans. . PLOS Genet. 10:e1004227 [Google Scholar]
  108. Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME. 108.  et al. 2016. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–46 [Google Scholar]
  109. Sun Q, Choi GH, Nuss DL. 109.  2009. A single Argonaute gene is required for induction of RNA silencing antiviral defense and promotes viral RNA recombination. PNAS 106:17927–32 [Google Scholar]
  110. Thran M, Link K, Sonnewald U. 110.  2012. The Arabidopsis DCP2 gene is required for proper mRNA turnover and prevents transgene silencing in Arabidopsis. Plant J. 72:368–77 [Google Scholar]
  111. Torres-Martínez S, Ruiz-Vázquez RM. 111.  2016. RNAi pathways in Mucor: a tale of proteins, small RNAs and functional diversity. Fungal Genet. Biol. 90:44–52 [Google Scholar]
  112. Trieu TA, Calo S, Nicolás FE, Vila A, Moxon S. 112.  et al. 2015. A non-canonical RNA silencing pathway promotes mRNA degradation in basal fungi. PLOS Genet 11:e1005168 [Google Scholar]
  113. Trieu TA, Navarro-Mendoza MI, Pérez-Arques C, Sanchis M, Capilla J. 113.  et al. 2017. RNAi-based functional genomics identifies new virulence determinants in mucormycosis. PLOS Pathog 13:1e1006150 [Google Scholar]
  114. Tucker JF, Ohle C, Schermann G, Bendrin K, Zhang W. 114.  et al. 2016. A novel epigenetic silencing pathway involving the highly conserved 5′-3′ exoribonuclease Dhp1/Rat1/Xrn2 in Schizosaccharomyces pombe. PLOS Genet. 12:e1005873 [Google Scholar]
  115. Vetukuri RR, Åsman AK, Tellgren-Roth C, Jahan SN, Reimegard J. 115.  et al. 2012. Evidence for small RNAs homologous to effector-encoding genes and transposable elements in the oomycete Phytophthora infestans. PLOS ONE 7:e51399 [Google Scholar]
  116. Villalobos-Escobedo JM, Herrera-Estrella A, Carreras-Villaseñor N. 116.  2016. The interaction of fungi with the environment orchestrated by RNAi. Mycologia 108:556–71 [Google Scholar]
  117. Voinnet O. 117.  2008. Use, tolerance and avoidance of amplified RNA silencing by plants. Trends Plant Sci 13:317–28 [Google Scholar]
  118. Wang M, Weiberg A, Lin FM, Thomma BP, Huang HD, Jin H. 118.  2016. Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nat. Plants 2:16151 [Google Scholar]
  119. Wang X, Darwiche S, Heitman J. 119.  2013. Sex-induced silencing operates during opposite-sex and unisexual reproduction in Cryptococcus neoformans. Genetics 193:1163–74 [Google Scholar]
  120. Wang X, Hsueh YP, Li W, Floyd A, Skalsky R, Heitman J. 120.  2010. Sex-induced silencing defends the genome of Cryptococcus neoformans via RNAi. Genes Dev 24:2566–82 [Google Scholar]
  121. Wang X, Wang P, Sun S, Darwiche S, Idnurm A. 121.  et al. 2012. Transgene induced co-suppression during vegetative growth in Cryptococcus neoformans. PLOS Genet 8:e1002885 [Google Scholar]
  122. Wang Y, Smith KM, Taylor JW, Freitag M, Stajich JE. 122.  2015. Endogenous small RNA mediates meiotic silencing of a novel DNA transposon. G3 5:1949–60 [Google Scholar]
  123. Wei W, Ba Z, Gao M, Wu Y, Ma Y. 123.  et al. 2012. A role for small RNAs in DNA double-strand break repair. Cell 149:101–12 [Google Scholar]
  124. Weiberg A, Bellinger M, Jin H. 124.  2015. Conversations between kingdoms: small RNAs. Curr. Opin. Biotechnol. 32:207–15 [Google Scholar]
  125. Weiberg A, Jin H. 125.  2015. Small RNAs—the secret agents in the plant-pathogen interactions. Curr. Opin. Plant Biol. 26:87–94 [Google Scholar]
  126. Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z. 126.  et al. 2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–23 [Google Scholar]
  127. Whisson S, Vetukuri R, Avrova A, Dixelius C. 127.  2012. Can silencing of transposons contribute to variation in effector gene expression in Phytophthora infestans?. Mob. Genet. Elem. 2:110–14 [Google Scholar]
  128. Xiao H, Alexander WG, Hammond TM, Boone EC, Perdue TD. 128.  et al. 2010. QIP, a protein that converts duplex siRNA into single strands, is required for meiotic silencing by unpaired DNA. Genetics 186:119–26 [Google Scholar]
  129. Xue Z, Ye Q, Anson SR, Yang J, Xiao G. 129.  et al. 2014. Transcriptional interference by antisense RNA is required for circadian clock function. Nature 514:650–53 [Google Scholar]
  130. Xue Z, Yuan H, Guo J, Liu Y. 130.  2012. Reconstitution of an Argonaute-dependent small RNA biogenesis pathway reveals a handover mechanism involving the RNA exosome and the exonuclease QIP. Mol. Cell 46:299–310 [Google Scholar]
  131. Yaegashi H, Yoshikawa N, Ito T, Kanematsu S. 131.  2013. A mycoreovirus suppresses RNA silencing in the white root rot fungus, Rosellinia necatrix. Virology 444:409–16 [Google Scholar]
  132. Yang Q, Li L, Xue Z, Ye Q, Zhang L. 132.  et al. 2013. Transcription of the major Neurospora crassa microRNA-like small RNAs relies on RNA polymerase III. PLOS Genet 9:e1003227 [Google Scholar]
  133. Yang Q, Ye QA, Liu Y. 133.  2015. Mechanism of siRNA production from repetitive DNA. Genes Dev 29:526–37 [Google Scholar]
  134. Ye W, Ma W. 134.  2016. Filamentous pathogen effectors interfering with small RNA silencing in plant hosts. Curr. Opin. Microbiol. 32:1–6 [Google Scholar]
  135. Zhang DX, Spiering MJ, Nuss DL. 135.  2014. Characterizing the roles of Cryphonectria parasitica RNA-dependent RNA polymerase-like genes in antiviral defense, viral recombination and transposon transcript accumulation. PLOS ONE 9:e108653 [Google Scholar]
  136. Zhang T, Zhao YL, Zhao JH, Wang S, Jin Y. 136.  et al. 2016. Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat. Plants 2:16153 [Google Scholar]
  137. Zhang X, Nuss DL. 137.  2008. A host Dicer is required for defective viral RNA production and recombinant virus vector RNA instability for a positive sense RNA virus. PNAS 105:16749–54 [Google Scholar]
  138. Zhang X, Segers GC, Sun Q, Deng F, Nuss DL. 138.  2008. Characterization of hypovirus-derived small RNAs generated in the chestnut blight fungus by an inducible DCL-2-dependent pathway. J. Virol. 6:2613–19 [Google Scholar]
  139. Zhang Z, Chang SS, Zhang Z, Xue Z, Zhang H. 139.  et al. 2013. Homologous recombination as a mechanism to recognize repetitive DNA sequences in an RNAi pathway. Genes Dev 27:145–50 [Google Scholar]
  140. Zhou J, Fu Y, Xie J, Li B, Jiang D. 140.  et al. 2012. Identification of microRNA-like RNAs in a plant pathogenic fungus Sclerotinia sclerotiorum by high-throughput sequencing. Mol. Genet. Genom. 287:275–82 [Google Scholar]
  141. Zhou Q, Wang Z, Zhang J, Meng H, Huang B. 141.  2012. Genome-wide identification and profiling of microRNA-like RNAs from Metarhizium anisopliae during development. Fungal Biol 116:1156–62 [Google Scholar]
  142. Zhou R, Rana TM. 142.  2013. RNA-based mechanisms regulating host-virus interactions. Immunol. Rev. 253:97–111 [Google Scholar]
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