endogenous DNA double-strand breaks. Nucleic
Acids Res 46:11869–11882
Borgognone A, Castanera R, Morselli M, Lo ´pez-Varas
L, Rubbi L, Pisabarro AG, Pellegrini M, Ramı ´rez L
(2018) Transposon-associated epigenetic silencing
during Pleurotus ostreatus life cycle. DNA Res
25:451–464
Butler DK (1992) Ribosomal DNA is a site of chromosome breakage in aneuploid strains of Neurospora.
Genetics 131:581–592
Bzymek M, Lovett ST (2001) Instability of repetitive
DNA sequences: the role of replication in multiple
mechanisms. Proc Natl Acad Sci 98:8319–8325
Cai Q, He B, Kogel K-H, Jin H (2018a) Cross-kingdom
RNA trafficking and environmental RNAi — nature’s blueprint for modern crop protection strategies. Curr Opin Microbiol 46:58–64
Cai Q, Qiao L, Wang M, He B, Lin FM, Palmquist J, Da
Huang S, Jin H (2018b) Plants send small RNAs in
extracellular vesicles to fungal pathogen to silence
virulence genes. Science 360:1126–1129
Calo S, Shertz-Wall C, Lee SC, Bastidas RJ, Nicola ´s FE,
Granek JA, Mieczkowski P, Torres-Martı ´nez S,
Ruiz-Va ´zquez RM, Cardenas ME et al (2014) Antifungal drug resistance evoked via RNAidependent epimutations. Nature 513:555–558
Calo S, Nicola ´s FE, Lee SC, Vila A, Cervantes M, TorresMartinez S, Ruiz-Vazquez RM, Cardenas ME,
Heitman J (2017) A non-canonical RNA degradation pathway suppresses RNAi-dependent epimutations in the human fungal pathogen Mucor
circinelloides. PLoS Genet 13:e1006686
Campbell JL, Turner BC (1987) Recombination block in
the spore killer region of Neurospora. Genome
29:129–135
Campo S, Gilbert KB, Carrington JC (2016) Small RNAbased antiviral defense in the phytopathogenic
fungus Colletotrichum higginsianum. PLoS Pathog
12:e1005640
Carreras-Villasen ˜or
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
Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–655
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
Cerutti H, Casas-Mollano JA (2006) On the origin and
functions of RNA-mediated silencing: from protists to man. Curr Genet 50:81–99
Cervantes M, Vila A, Nicola ´s FE, Moxon S, de Haro JP,
Dalmay T, Torres-Martı ´nez S, Ruiz-Va ´zquez 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
Chang S-S, Zhang Z, Liu Y (2012) RNA interference
pathways in fungi: mechanisms and functions.
Annu Rev Microbiol 66:305–323
Chang Z, Billmyre RB, Lee SC, Heitman J (2019) Broad
antifungal resistance mediated by RNAi-dependent
epimutation in the basal human fungal pathogen
Mucor circinelloides. PLoS Genet 15:e1007957
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
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
Cogoni C, Irelan JT, Schumacher M, Schmidhauser TJ,
Selkerl EU, Macino G, Umana B, Cellulare B (1996)
Transgene silencing of the al-1 gene in vegetative
cells of Neurospora is mediated by a cytoplasmic
effector and does not depend on DNA-DNA interactions or DNA methylation. EMBO J 1:3153–3163
Dahlmann TA, Ku ¨ck U (2015) Dicer-dependent biogenesis of small RNAs and evidence for microRNAlike RNAs in the penicillin producing fungus Penicillium chrysogenum. PLoS One 10:e0125989
Dang Y, Li L, Guo W, Xue Z, Liu Y (2013) Convergent
transcription induces dynamic DNA methylation
at disiRNA loci. PLoS Genet 9:e1003761
Dang Y, Cheng J, Sun X, Zhou Z, Liu Y (2016) Antisense
transcription licenses nascent transcripts to mediate transcriptional gene silencing. Genes Dev
30:2417–2432
de Haro JP, Calo S, Cervantes M, Nicola ´s FE, TorresMartı ´nez S, Ruiz-Va ´zquez 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
Donaldson ME, Saville BJ (2012) Natural antisense
transcripts in fungi. Mol Microbiol 85:405–417
Donaldson ME, Saville BJ (2013) Ustilago maydis
natural antisense transcript expression alters
mRNA stability and pathogenesis. Mol Microbiol
89:29–51
Drinnenberg IA, Weinberg DE, Xie KT, Mower JP,
Wolfe KH, Fink GR, Bartel DP (2009) RNAi in
budding yeast. Science 326:544–550
Drinnenberg IA, Fink GR, Bartel DP (2011) Compatibility with killer explains the rise of RNAi-deficient
fungi. Science 333:1592
Dumesic PA, Natarajan P, Chen C, Drinnenberg IA,
Schiller BJ, Thompson J, Moresco JJ, Yates JR,
Bartel DP, Madhani HD (2013) Stalled spliceosomes are a signal for RNAi-mediated genome
defense. Cell 152:957–968
Ellendorff U, Fradin EF, De Jonge R, Thomma BPHJ
(2009) RNA silencing is required for Arabidopsis
118
F. E. Nicola ´s et al.
Acids Res 46:11869–11882
Borgognone A, Castanera R, Morselli M, Lo ´pez-Varas
L, Rubbi L, Pisabarro AG, Pellegrini M, Ramı ´rez L
(2018) Transposon-associated epigenetic silencing
during Pleurotus ostreatus life cycle. DNA Res
25:451–464
Butler DK (1992) Ribosomal DNA is a site of chromosome breakage in aneuploid strains of Neurospora.
Genetics 131:581–592
Bzymek M, Lovett ST (2001) Instability of repetitive
DNA sequences: the role of replication in multiple
mechanisms. Proc Natl Acad Sci 98:8319–8325
Cai Q, He B, Kogel K-H, Jin H (2018a) Cross-kingdom
RNA trafficking and environmental RNAi — nature’s blueprint for modern crop protection strategies. Curr Opin Microbiol 46:58–64
Cai Q, Qiao L, Wang M, He B, Lin FM, Palmquist J, Da
Huang S, Jin H (2018b) Plants send small RNAs in
extracellular vesicles to fungal pathogen to silence
virulence genes. Science 360:1126–1129
Calo S, Shertz-Wall C, Lee SC, Bastidas RJ, Nicola ´s FE,
Granek JA, Mieczkowski P, Torres-Martı ´nez S,
Ruiz-Va ´zquez RM, Cardenas ME et al (2014) Antifungal drug resistance evoked via RNAidependent epimutations. Nature 513:555–558
Calo S, Nicola ´s FE, Lee SC, Vila A, Cervantes M, TorresMartinez S, Ruiz-Vazquez RM, Cardenas ME,
Heitman J (2017) A non-canonical RNA degradation pathway suppresses RNAi-dependent epimutations in the human fungal pathogen Mucor
circinelloides. PLoS Genet 13:e1006686
Campbell JL, Turner BC (1987) Recombination block in
the spore killer region of Neurospora. Genome
29:129–135
Campo S, Gilbert KB, Carrington JC (2016) Small RNAbased antiviral defense in the phytopathogenic
fungus Colletotrichum higginsianum. PLoS Pathog
12:e1005640
Carreras-Villasen ˜or
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
Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–655
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
Cerutti H, Casas-Mollano JA (2006) On the origin and
functions of RNA-mediated silencing: from protists to man. Curr Genet 50:81–99
Cervantes M, Vila A, Nicola ´s FE, Moxon S, de Haro JP,
Dalmay T, Torres-Martı ´nez S, Ruiz-Va ´zquez 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
Chang S-S, Zhang Z, Liu Y (2012) RNA interference
pathways in fungi: mechanisms and functions.
Annu Rev Microbiol 66:305–323
Chang Z, Billmyre RB, Lee SC, Heitman J (2019) Broad
antifungal resistance mediated by RNAi-dependent
epimutation in the basal human fungal pathogen
Mucor circinelloides. PLoS Genet 15:e1007957
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
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
Cogoni C, Irelan JT, Schumacher M, Schmidhauser TJ,
Selkerl EU, Macino G, Umana B, Cellulare B (1996)
Transgene silencing of the al-1 gene in vegetative
cells of Neurospora is mediated by a cytoplasmic
effector and does not depend on DNA-DNA interactions or DNA methylation. EMBO J 1:3153–3163
Dahlmann TA, Ku ¨ck U (2015) Dicer-dependent biogenesis of small RNAs and evidence for microRNAlike RNAs in the penicillin producing fungus Penicillium chrysogenum. PLoS One 10:e0125989
Dang Y, Li L, Guo W, Xue Z, Liu Y (2013) Convergent
transcription induces dynamic DNA methylation
at disiRNA loci. PLoS Genet 9:e1003761
Dang Y, Cheng J, Sun X, Zhou Z, Liu Y (2016) Antisense
transcription licenses nascent transcripts to mediate transcriptional gene silencing. Genes Dev
30:2417–2432
de Haro JP, Calo S, Cervantes M, Nicola ´s FE, TorresMartı ´nez S, Ruiz-Va ´zquez 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
Donaldson ME, Saville BJ (2012) Natural antisense
transcripts in fungi. Mol Microbiol 85:405–417
Donaldson ME, Saville BJ (2013) Ustilago maydis
natural antisense transcript expression alters
mRNA stability and pathogenesis. Mol Microbiol
89:29–51
Drinnenberg IA, Weinberg DE, Xie KT, Mower JP,
Wolfe KH, Fink GR, Bartel DP (2009) RNAi in
budding yeast. Science 326:544–550
Drinnenberg IA, Fink GR, Bartel DP (2011) Compatibility with killer explains the rise of RNAi-deficient
fungi. Science 333:1592
Dumesic PA, Natarajan P, Chen C, Drinnenberg IA,
Schiller BJ, Thompson J, Moresco JJ, Yates JR,
Bartel DP, Madhani HD (2013) Stalled spliceosomes are a signal for RNAi-mediated genome
defense. Cell 152:957–968
Ellendorff U, Fradin EF, De Jonge R, Thomma BPHJ
(2009) RNA silencing is required for Arabidopsis
118
F. E. Nicola ´s et al.