The interaction of fungi with the environment orchestrated by RNAi

Mycologia

Volumn 108, Issue 3, 2016, Pages 556-571

  Villalobos Escobedo, José Manuel ^a   Herrera Estrella, Alfredo ^a   Carreras Villaseñor, Nohemí ^b  

^a Cinvestav Campus Guanajuato   (Mexico)

^b StelaGenomics Mexico S de RL de CV   (Mexico)

Author keywords

Argonaute; Dicer; Gene expression; MicroRNA; Small RNA

Indexed keywords

ANTIBIOTIC RESISTANCE; DNA; ENVIRONMENTAL RESPONSE; FUNGUS; GENE EXPRESSION; GENETIC ANALYSIS; GENOME; RNA;

BOTRYOTINIA FUCKELIANA; FILOBASIDIELLA NEOFORMANS; FUNGI; MAGNAPORTHE ORYZAE; MUCOR CIRCINELLOIDES; NEUROSPORA CRASSA; TRICHODERMA ATROVIRIDE;

FUNGAL PROTEIN; FUNGAL RNA;

ECOSYSTEM; FUNGUS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE;

ECOSYSTEM; FUNGAL PROTEINS; FUNGI; GENE EXPRESSION REGULATION, FUNGAL; RNA INTERFERENCE; RNA, FUNGAL;

EID: 84975034074     PISSN: 00275514     EISSN: 15572536     Source Type: Journal    
DOI: 10.3852/15-246     Document Type: Article

References (101)

1. Aguirre A, Montserrat N, Zacchigna S, Nivet E, Hishida T, Krause MN, Kurian L, Ocampo A, Vazquez-Ferrer E, Rodriguez-Esteban C, Kumar S, Moresco JJ, Yates JR, Campistol JM, Sancho-Martinez I, Giacca M, Izpisua Belmonte JCI. 2014. In vivo activation of a conserved microRNA program induces mammalian heart regeneration. Cell Stem Cell 15:589-604, doi:10.1016/j.stem. 2014.10.003.
2. Alexander WG, Raju NB, Xiao H, Hammond TM, Perdue TD, Metzenberg RL, Pukkila PJ, Shiu PK. 2008. DCL-1 colocalizes with other components of the MSUD machinery and is required for silencing. Fungal Genet Biol 45:719-727, doi:10.1016/j.fgb.2007.10.006.
3. Ameres SL, Zamore PD. 2013. Diversifying microRNA sequence and function. Nat Rev Mol Cell Biol 14:475-488, doi:10.1038/nrm3611.
4. Aramayo R, Metzenberg RL. 1996. Meiotic transvection in fungi. Cell 86:103-113, doi:10.1016/S0092-8674(00) 80081-1.
5. Arteaga-Vázquez M, Caballero-Pérez J, Vielle-Calzada J-P. 2006. A family of microRNAs present in plants and animals. Plant Cell 18:3355-3369.
6. Axtell MJ, Westholm JO, Lai EC. 2011. Vive la différence bio-genesis and evolution of microRNAs in plants and animals. Genome Biol 12:221, doi:10.1101/gr.101386.109.
7. Bai Y, Lan F, Yang W, Zhang F, Yang K, Li Z, Gao P, Wang S. 2015. sRNA profiling in Aspergillus flavus reveals differentially expressed miRNA-like RNAs response to water activity and temperature. Fungal Genet Biol 81:113-119, doi:10.1016/j.fgb.2015.03.004.
8. Bartel DP. 2004. MicroRNAs: genomics, biogenesis, mechanism and function. Cell 116:281-297, doi:10.1016/S0092-8674(04)000455.
9. Biggar KK, Storey KB. 2015. Insight into post-transcriptional gene regulation: stress-responsive microRNAs and their role in the environmental stress survival of tolerant animals. J Exp Biol 218:1281-1289, doi:10.1242/jeb. 104828.
10. Billmyre RB, Calo S, Feretzaki M, Wang X, Heitman J. 2013. RNAi function, diversity and loss in the fungal kingdom. Chromosome Res 21:561-572, doi:10.1007/s10577-013-9388-2.
11. Blair C, Olson K. 2015. The role of RNA interference (RNAi) in arbovirus-vector interactions. Viruses 7:820-843, doi:10.3390/v7020820.
12. Calo S, Nicolás FE, Vila A, Torres-Martínez S, Ruiz-vázquez RM. 2012. Two distinct RNA-dependent RNA polymerases are required for initiation and amplification of RNA silencing in the basal fungus Mucor circinelloides. Mol Microbiol 83:379-394, doi:10.1111/j.1365-2958. 2011.07939.x.
13. Calo S, Shertz-Wall C, Lee SC, Bastidas RJ, Nicolás FE, Granek JA, Mieczkowski P, Torres-Martínez S, RuizVázquez RM, Cardenas ME, Heitman J. 2014. Antifungal drug resistance evoked via RNAi-dependent epimutations. Nature 513:555-558, doi:10.1038/nature13575.
14. Carreras-Villaseñor N, Esquivel-Naranjo EU, Villalobos-Escobedo JM, Abreu-Goodger C, Herrera-Estrella A. 2013. The RNAi machinery regulates growth and development in the filamentous fungus Trichoderma atroviride. Mol Microbiol 89:96-112.
15. Carreras-Villaseñor N, Sánchez-Arreguin JA, Herrera-Estrella AH. 2012. Trichoderma: sensing the environment for survival and dispersal. Microbiology 158:3-16.
16. Carthew RW, Sontheimer EJ. 2009. Origins and mechanisms of miRNAs and siRNAs. Cell 136:642-655, doi:10.1016/j. cell.2009.01.035.
17. Catalanotto C, Azzalin G, Macino G, Cogoni C. 2000. Gene silencing in worms and fungi. Nature 404:245, doi:10.1038/35005169.
18. Catalanotto C, Azzalin G, Macino G, Cogoni C. 2002. Involvement of small RNAs and role of the qde genes in the gene-silencing pathway in Neurospora. Genes Dev 16:790-795.
19. Catalanotto C, Pallotta M, ReFalo P, Sachs MS, Vayssie L, Macino G, Cogoni C. 2004. Redundancy of the two dicer genes in transgene-induced posttranscriptional gene silencing in Neurospora crassa. Mol Cell Biol 24:2536-2545.
20. Cervantes M, Vila A, Nicolás FE, Moxon S, de Haro JP, Dalmay T, Torres-Martínez S, Ruiz-Vázquez RM. 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, doi:10.1371/journal.pone.0069283.s015.
21. Chang SS, Zhang Z, Liu Y. 2012. RNA interference path ways in fungi: mechanisms and functions. Annu Rev Microbiol 66:305-323, doi:10.1146/annurev-micro-092611-150138.
22. Chávez-Montes RA, Rosas-Cárdenas FF, de Paoli E, Accerbi M, Rymarquis LA, Mahalingam G, Marsch-Martínez N, Meyers BC, Green PJ, de Folter S. 2014. Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs. Nat Commun 5:3722.
23. Chen H, Kobayashi K, Miyao A, Hirochika H, Yamaoka N, Nishiguchi M. 2013. Both OsRecQ1 and OsRDR1 are required for the production of small RNA in response to DNA damage in rice. PLoS One 8:e55252, doi:10.1371/journal.pone.0055252.g005.
24. Chen R, Jiang N, Jiang Q, Sun X, Wang Y, Zhang H, Hu Z. 2014. Exploring microRNA-like small RNAs in the filamentous fungus Fusarium oxysporum. PLoS One 9: e104956, doi:10.1371/journal.pone.0104956.s012.
25. Chicas A, Cogoni C, Macino G. 2004. RNAi-dependent and RNAi-independent mechanisms contribute to the silencing of RIPed sequences in Neurospora crassa. Nucleic Acids Res 32:4237-4243.
26. Choi J, Kim KT, Jeon J, Wu J, Song H, Asiegbu FO, Lee YH. 2014. funRNA: a fungi-centered genomics platform for genes encoding key components of RNAi. BMC Genomics 15:S14, doi:10.1101/gr.849004.
27. Cogoni C, Macino G. 1997. Isolation of quelling-defective (qde) mutants impaired in posttranscriptional trans-gene-induced gene silencing in Neurospora crassa. Proc Natl Acad Sci U S A 94:10233-10238, doi:10.1073/ pnas.94.19.10233.
28. Cogoni C, Macino G. 1999. Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature 399:166-169.
29. Dahlmann TA, Kück U. 2015. Dicer-dependent biogenesis of small RNAs and evidence for microRNA-like RNAs in the penicillin producing fungus Penicillium chrysogenum. PLoS One 10:e0125989, doi:10.1371/journal.pone.0125989. s012.
30. Dang Y, Li L, Guo W, Xue Z, Liu Y. 2013. Convergent transcription induces dynamic DNA methylation at disiRNA loci. PLoS Genet 9:e1003761, doi:10.1371/journal. pone.0125989.s012.
31. de Haro JP, Calo S, Cervantes M, Nicolás FE, Torres-Martínez S, Ruiz-Vázquez RM. 2009. A single dicer gene is required for efficient gene silencing associated with two classes of small antisense RNAs in Mucor circinelloides. Eukaryot Cell 8:1486-1497, doi:10.1371/journal.pgen. 1003761.s012.
32. Decker LM, Boone EC, Xiao H, Shanker BS, Boone SF, Kingston SL, Lee SA, Hammond TM, Shiu PK. 2015. Complex formation of RNA silencing proteins in the perinuclear region of Neurospora crassa. Genetics 199:1017-1021, doi:10.1534/genetics.115.174623.
33. Drinnenberg IA, Fink GR, Bartel DP. 2011. Compatibility with killer explains the rise of RNAi-deficient fungi. Science 333:1592, doi:10.1126/science.1209575.
34. Drinnenberg IA, Weinberg DE, Xie KT, Mower JP, Wolfe KH, Fink GR, Bartel DP. 2009. RNAi in budding yeast. Science 326:544-550.
35. Driver F, Milner RJ, Trueman JW. 2000. A taxonomic revision of Metarhizium based on a phylogenetic analysis of rDNA sequence data. Mycol Res 104:134-150.
36. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP. 2011. Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749-759, doi:10.1038/nrmicro2637.
37. Duan G, Saint RB, Helliwell CA, Behm CA, Wang MB, Waterhouse PM, Gordon KH. 2013. C. elegans RNA-dependent RNA polymerases rrf-1 and ego-1 silence Drosophila trans-genes by differing mechanisms. Cell Mol Life Sci 70:1469-1481, doi:10.1007/s00018-012-1218-8.
38. Eichhorn SW, Guo H, McGeary SE, Rodriguez-Mias RA, Shin C, Baek D, Hsu S, Ghoshal K, Villén J, Bartel DP. 2014. mRNA destabilization is the dominant effect of mammalian microRNAs by the time substantial repression ensues. Mol Cell 56:104-115, doi:10.1016/j.molcel. 2014.08.028.
39. Francia S, Michelini F, Saxena A, Tang D, de Hoon M, Anelli V, Mione M, Carninci P, di Fagagna FDA. 2012. Site-specific dicer and drosha RNA products control the DNA damage response. Nature 488:231-235, doi:10. 1038/nature11179.
40. Ge X, Lei P, Wang H, Zhang A, Han Z, Chen X, Li S, Jiang R, Kang C, Zhang J. 2014. miR-21 improves the neurological outcome after traumatic brain injury in rats. Scien-tific Rep 4:6718, doi:10.1038/srep06718.
41. Goodwin SB, M'Barek SB, Dhillon B, Wittenberg AH, Crane CF, Hane JK, Foster AJ, van der Lee TAJ, Grimwood J, Aerts A, Antoniw J, Bailey A, Bluhm B, Bowler J, Bristow J, van der Burgt A, Canto-Canché B, Churchill ACL, Conde-Ferràez L, Cools HJ, Coutinho PM, Csukai M, Dehal P, de Wit P, Donzelli B, van de Geest HC, van Ham RCHJ, Hammond-Kosack KE, Henrissat B, Kilian A, Kobayashi AK, Koopmann E, Kourmpetis Y, Kuzniar A, Lindquist E, Lombard V., Maliepaard C, Martins N, Mehrabi R, Nap JPH, Ponomarenko A, Rudd JJ, Salamov A, Schmutz J, Schouten HJ, Shapiro H, Stergiopoulos I, Torriani SFF, Tu H, de Vries RP, Waalwijk C, Ware SB, Wiebenga A, Zwiers L-H, Oliver RP, Grigoriev IV, Kema GHJ. 2011. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity and stealth pathogenesis. PLoS Genet 7:e1002070, doi:10.1371/journal. pgen.1002070.s022.
42. Grimson A, Srivastava M, Fahey B, Woodcroft BJ, Chiang HR, King N, Degnan BM, Rokhsar DS, Bartel DP. 2008. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455:1193-1197, doi:10.1038/nature07415.
43. Ha M, Kim VN. 2014. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 15:509-524, doi:10.1038/nrm3838.
44. Hammond TM, Andrewski MD, Roossinck MJ, Keller NP. 2008. Aspergillus mycoviruses are targets and suppressors of RNA silencing. Eukaryot Cell 7:350-357, doi:10.1128/ EC.00356-07.
45. Hammond TM, Xiao H, Boone EC, Perdue TD, Pukkila PJ, Shiu PK. 2011. SAD-3, a putative helicase required for meiotic silencing by unpaired DNA, interacts with other components of the silencing machinery. Genes Genomes Genet 1:369-376.
46. Hernández-Oñate MA, Esquivel-Naranjo EU, Mendoza-Mendoza A, Stewart A, Herrera-Estrella A. 2012. An injury response mechanism conserved across kingdoms determines entry of the fungus Trichoderma atroviride into development. Proc Natl Acad Sci U S A 109:14918-14923.
47. Hernández-Oñate MA, Herrera-Estrella A. 2015. Damage response involves mechanisms conserved across plants, animals and fungi. Curr Genet 61:359-372.
48. Hertel J, Stadler PF. 2015. The expansion of animal microRNA families revisited. Life 5:905-920, doi:10.3390/life5010905.
49. Janbon G, Maeng S, Yang DH, Ko YJ, Jung KW, Moyrand F, Floyd A, Heitman J, Bahn YS. 2010. Characterizing the role of RNA silencing components in Cryptococcus neofor-mans. Fungal Genet Biol 47:1070-1080, doi:10.1016/j. fgb.2010.10.005.
50. Jiang N, Yang Y, Janbon G, Pan J, Zhu X. 2012. Identification and functional demonstration of miRNAs in the fungus Cryptococcus neoformans. PLoS One 7:e52734, doi:10.1371/journal.pone.0052734.t004.
51. Kang K, Zhong J, Jiang L, Liu G, Gou CY, Wu Q, Wang Y, Luo J, Gou D. 2013. Identification of microRNA-like RNAs in the filamentous fungus Trichoderma reesei by Solexa sequencing. PloS one 8:e76288.
52. Kato A, Akamatsu Y, Sakuraba Y, Inoue H. 2004. The Neurospora crassa mus-19 gene is identical to the qde-3 gene, which encodes a ReqQ homolog and is involved in recombination repair and postreplication repair. Curr Genet 45:37-44, doi:10.1371/journal.pone.0076288.s008.
53. Kruszka K, Pieczynski M, Windels D, Bielewicz D, Jarmolowski A, Szweykowska-Kulinska Z, Vazquez F. 2012. Role of microRNAs and other sRNAs of plants in their changing environments. J Plant Physiol 169:1664-1672, doi:10.1016/j.jplph.2012.03.009.
54. Kubicek CP, Herrera-Estrella A, Seidl V, le Crom S, Zeilinger S, Druzhinina IS, Hermosa R, Casas-Flores S, Horwitz BA, Mukherjee PK, Mukherjee M, Kredics L, Alcaraz LD, Aerts A, Antal Z, Atanasova L, Cervantes-Badillo MG, Challacombe J, Chertkov O, McCluskey K, Coulpier F, Deshpande N, von Döhren H, Ebbole DJ, EsquivelNaranjo EU, Fekete E, Flipphi M, Glaser F, Gómez-Rodríguez EY, Gruber S, Hans C, Henrissat B, Hernández-Oñate M, Karaffa L, Kosti I, Lindquist E, Lucas S, Lübeck M, Lübeck PS, Margeot A, Metz B, Misra M, Nevalainen H, Omann M, Packer N, Perrone G, Uresti-Rivera EE, Salamov A, Schmoll M, Seiboth B, Shapiro H, Sukno S, Tamayo-Ramos JA, Thon M, Tisch D, Wiest A, Wilkinson HH, Zhang M, Coutinho PM, Kenerley CM, Monte E, Baker SE, Grigoriev IV. 2011. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 12:R40, doi:10.1093/bioinformatics/ btm076.
55. Lau SK, Chow WN, Wong AY, Yeung JM, Bao J, Zhang N, Lok S, Woo PC, Yuen KY. 2013. Identification of microRNA-like RNAs in mycelial and yeast phases of the thermal dimorphic fungus Penicillium marneffei. PLoS Negl Trop Dis 7:e2398.
56. Lee DW, Pratt RJ, McLaughlin M, Aramayo R. 2003. An Argonaute-like protein is required for meiotic silenc-ing. Genetics 164:821-828, doi:10.1371/journal.pntd. 0002398.s001.
57. Lee HC, Aalto AP, Yang Q, Chang SS, Huang G, Fisher D, Cha J, Poranen MM, Bamford DH, Liu Y. 2010. The DNA/RNA-dependent RNA polymerase QDE-1 generates aberrantRNA and dsRNA for RNAi in a process requiring replication protein A and a DNA helicase. PLoS Biol 8:e1000496.
58. Lee HC, Chang SS, Choudhary S, Aalto AP, Maiti M, Bamford DH, Liu Y. 2009. qiRNA is a new type of small interfering RNA induced by DNA damage. Nature 459:274-277, doi:10.1371/journal.pbio.1000496.s003.
59. Lee HC, Li L, Gu W, Xue Z, Crosthwaite SK, Pertsemlidis A, Lewis ZA, Freitag M, Selker EU, Mello CC, Liu Y. 2010. Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. Mol Cell 38:803-814.
60. Lin JS, Lin CC, Lin HH, Chen YC, Jeng ST. 2012. microR828 regulates lignin and H2O2 accumulation in sweet potato on wounding. New Phytol 196:427-440, doi:10.1111/j.1469-8137.2012.04277.x.
61. Lin YL, Ma LT, Lee YR, Lin SS, Wang S-Y, Chang TT, Shaw JF, Li WH, Chu FH. 2015. microRNA-like small RNAs prediction in the development of Antrodia cinnamomea. PLoS One. 10:e0123245, doi:10.1371/journal.pone.0123245. s005.
62. Luo J, Qiu H, Cai G, Wagner NE, Bhattacharya D, Zhang N. 2015. Phylogenomic analysis uncovers the evolutionary history of nutrition and infection mode in rice-blast fungus and other Magnaporthales. Sci Rep 5:9448, doi:10.1038/srep09448.
63. Maiti M, Lee HC, Liu Y. 2007. QIP, a putative exonuclease, interacts with the Neurospora Argonaute protein and facilitates conversion ofduplex siRNA into single strands. Genes Dev 21:590-600, doi:10.1101/gad.1497607.
64. Medina-Castellanos E, Esquivel-Naranjo EU, Heil M, Herrera-Estrella A. 2014. Extracellular ATP activates MAPK and ROS signaling during injury response in the fungus Trichoderma atroviride. Front Plant Sci 5:659.
65. Michalik KM, Böttcher R, Förstemann K. 2012. A small RNA response at DNA ends in Drosophila. Nucleic Acids Res 40:9596-9603, doi:10.1093/nar/gks711.
66. Molnar A, Schwach F, Studholme DJ, Thuenemann EC, Baulcombe DC. 2007. miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447:1126-1129.
67. Mukherjee PK, Horwitz BA, Herrera-Estrella A, Schmoll M, Kenerley CM. 2013. Trichoderma research in the genome era. Annu Rev Phytopathol 51:105-129, doi:10.1146/ annurev-phyto-082712-102353.
68. Murata T, Kadotani N, Yamaguchi M, Tosa Y, Mayama S, Nakayashiki H. 2007. siRNA-dependent and independent post-transcriptional cosuppression of the LTR-retrotransposon MAGGY in the phytopathogenic fungus Magnaporthe oryzae. Nucleic Acids Res 35:5987-5994, doi:10.1093/nar/gkm646.
69. Napoli C, Lemieux C, Jorgensen R. 1990. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279-289, doi:10.1105/tpc.2.4.279.
70. Nicolás FE, de Haro JP, Torres-Martínez S, Ruiz-Vázquez RM. 2007. Mutants defective in a Mucor circinelloides dicer-like gene are not compromised in siRNA silencing but display developmental defects. Fungal Genet Biol 44:504-516.
71. Nicolás FE, Moxon S, de Haro J, Calo S, Grigoriev IV, TorresMartínez S, Moulton V, Ruiz-Vázquez RM, Dalmay T. 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 38:5535-5541.
72. Nicolás FE, Torres-Martínez S, Ruiz-Vázquez RM. 2003. Two classes of small antisense RNAs in fungal RNA silencing triggered by non-integrative transgenes. EMBO J 22: 3983-3991.
73. Nicolás FE, Vila A, Moxon S, Cascales MD, Torres-Martínez S, Ruiz-Vázquez RM, Garre V. 2015. The RNAi machinery controls distinct responses to environmental signals in the basal fungus Mucor circinelloides. BMCGenomics 16:1-14.
74. Nolan T, Braccini L, Azzalin G, De Toni A, Macino G, Cogoni C. 2005. The post-transcriptional gene silencing machinery functions independently of DNA methylation to repress a LINE1-like retrotransposon in Neurospora crassa. Nucleic Acids Res 33:1564-1573, doi:10.1093/ nar/gki300.
75. Nunes CC, Gowda M, Sailsbery J, Xue M, Chen F, Brown DE, Oh Y, Mitchell TK, Dean RA. 2011. Diverse and tissue-enriched small RNAs in the plant pathogenic fungus Magnaporthe oryzae. BMC Genomics 12:288, doi:10.1101/gr.849004.
76. Panda SK, Sunkar R. 2015. Nutrient-and other stress-responsive microRNAs in plants: role for thiol-based redox signaling. Plant Signaling Behavior 10:e1010916.
77. Raman V, Simon SA, Romag A, Demirci F, Mathioni SM, Zhai, J., Meyers BC, Donofrio NM. 2013. Physiological stressors and invasive plant infections alter the small RNA transcriptome of the rice blast fungus, Magnaporthe oryzae. BMC Genomics 14:326, doi:10.1002/yea.817.
78. Romano N, Macino G. 1992. Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol 6:3343-3353, doi:10.1111/j.1365-2958.1992.tb02202.x.
79. Samarajeewa DA, Sauls PA, Sharp KJ, Smith ZJ, Xiao H, Groskreutz KM, Malone TL, Boone EC, Edwards KA, Shiu PKT, Larson ED, Hammond TM. 2014. Efficient detection of unpaired DNA requires a member of the rad54-like family of homologous recombination proteins. Genetics 198:895-904.
80. Saugstad JA. 2010. MicroRNAs as effectors of brain function with roles in ischemia and injury, neuroprotection and neurodegeneration. J Cereb Blood Flow Metab 30: 1564-1576, doi:10.1038/jcbfm.2010.101.
81. Schommer C, Palatnik JF, Aggarwal P, Chételat A, Cubas P, Farmer EE, Nath U, Weigel D. 2008. Control of jasmo-nate biosynthesis and senescence by miR319 targets. PLoS Biol. 6:1991-2001.
82. Segers GC, Zhang X, Deng F, Sun Q, Nuss DL. 2007. Evidence that RNA silencing functions as an antiviral defense mechanism in fungi. Proc Natl Acad Sci U S A 104:12902-12906, doi:10.1073/pnas.0702500104.
83. Shiu PK, Raju NB, Zickler D, Metzenberg RL. 2001. Meiotic silencing by unpaired DNA. Cell 107:905-916, doi:10.1016/S0092-8674(01)00609-2.
84. Shiu PK, Zickler D, Raju NB, Ruprich-Robert G, Metzenberg RL. 2006. SAD-2 is required for meiotic silencing by unpaired DNA and perinuclear localization of SAD-1 RNA-directed RNA polymerase. Proc Natl Acad Sci U S A 103:2243-2248.
85. Sun Q, Choi GH, Nuss DL. 2009. A single Argonaute gene is required for induction of RNA silencing antiviral defense and promotes viral RNA recombination. Proc Natl Acad Sci U S A. 106:17927-17932, doi:10.1073/ pnas.0907552106.
86. Tabach Y, Billi AC, Hayes GD, Newman MA, Zuk O, Gabel H, Kamath R, Yacoby K, Chapman B, Garcia SM, Borowsky M, Kim JK, Ruvkun G. 2013. Identification of small RNA pathway genes using patterns of phylogenetic conservation and divergence. Nature 493:694-698.
87. Thomson RC, Plachetzki DC, Mahler DL, Moore BR. 2014. A critical appraisal of the use of microRNA data in phylogenetics. Proc Natl Acad Sci U S A 111:E3659-E3668, doi:10.1073/pnas.1407207111.
88. Trieu TA, Calo S, Nicolás FE, Vila A, Moxon S, Dalmay T, Torres-Martínez S, Garre V, Ruiz-Vázquez RM. 2015. A non-canonical RNA silencing pathway promotes mRNA degradation in basal fungi. PLOS Genet 11:e1005168.
89. Wang X, Hsueh YP, Li W, Floyd A, Skalsky R, Heitman J. 2010. Sex-induced silencing defends the genome of Cryptococcus neoformans via RNAi. Genes Dev 24:2566-2582, doi:10.1371/journal.pgen.1005168.s022.
90. Wang X, Wang P, Sun S, Darwiche S, Idnurm A, Heitman J. 2012. Transgene induced co-suppression during vegetative growth in Cryptococcus neoformans. PLoS Genet 8:1-13.
91. Wei W, Ba Z, Gao M, Wu Y, Ma Y, Amiard S, White CI, Daniel-sen JMR, Yang YG, Qi Y. 2012. A role for small RNAs in DNA double-strand break repair. Cell 149:101-112, doi:10.1016/j.cell.2012.03.002.
92. Weiberg A, Wang M, Lin F-M, Zhao H, Zhang Z, Kaloshian I, Huang H-D, Jin H. 2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118-123, doi:10.1126/science. 1239705.
93. Xiao H, Alexander WG, Hammond TM, Boone EC, Perdue TD, Pukkila PJ, Shiu PK. 2010. QIP, a protein that converts duplex siRNA into single strands, is required for meiotic silencing by unpaired DNA. Genetics 186:119-126, doi:10.1534/genetics.110.118273.
94. Yang Q, Ye QA, Liu Y. 2015. Mechanism of siRNA production from repetitive DNA. Genes Dev 29:526-537, doi:10.1101/gad.255828.114.
95. Zhang DX, Nuss DL. 2008. A host dicer is required for defective viral RNA production and recombinant virus vector RNA instability for a positive sense RNA virus. Proc Natl Acad Sci U S A 105:16749-16754, doi:10.1073/pnas. 0807225105.
96. Zhang DX, Spiering MJ, Nuss DL. 2014a. 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.
97. Zhang Z, Chang SS, Zhang Z, Xue Z, Zhang H, Li S, Liu Y. 2013. Homologous recombination as a mechanism to recognize repetitive DNA sequences in an RNAi pathway. Genes Dev 27:145-150.
98. Zhang Z, Yang Q, Sun G, Chen S, He Q, Li S, Liu Y. 2014b. His-tone H3K56 acetylation is required for quelling-induced small RNA production through its role in homologous recombination. J Biol Chem 289:9365-9371.
99. Zhou J, Fu Y, Xie J, Li B, Jiang D, Li G, Cheng J. 2012a. Identification of microRNA-like RNAs in a plant pathogenic fungus Sclerotinia sclerotiorum by high-throughput sequencing. Mol Genet Genomics 287:275-282, doi:10. 1007/s00438-012-0678-8.
100. Zhou Q, Wang Z, Zhang J, Meng H, Huang B. 2012b. Ge-nomewide identification and profiling of microRNA-like RNAs from Metarhizium anisopliae during development. Fungal Biol 116:1156-1162, doi:10.1016/j.funbio.2012.09.001.
101. Zong J, Yao X, Yin J, Zhang D, Ma H. 2009. Evolution of the RNA-dependent RNA polymerase (RdRP) genes: duplications and possible losses before and after the divergence of major eukaryotic groups. Gene 447:29-39, doi:10.1016/j.gene.2009.07.004.