RNA silencing in fungi

doi:10.1007/s11515-010-0550-3

Front Biol

2010, Vol. 5

Issue (6) : 478-494 https://doi.org/10.1007/s11515-010-0550-3

REVIEW

RNA silencing in fungi

Ulrike SCHUMANN¹(

), Mick AYLIFFE¹, Kemal KAZAN², Ming-Bo WANG¹

1. Commonwealth Scientific and Industrial Research Organization Plant Industry, Canberra, ACT 2601, Australia; 2. Commonwealth Scientific and Industrial Research Organization Plant Industry, St. Lucia, QLD 4067, Australia

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Abstract

RNA silencing is an evolutionarily conserved mechanism in eukaryotic organisms induced by double-stranded RNA (dsRNA) and plays an essential role in regulating gene expression and maintaining genome stability. RNA silencing occurs at both posttranscriptional levels through sequence-specific RNA degradation or translational repression and at transcriptional levels through RNA-directed DNA methylation and/or heterochromatin formation. RNA silencing pathways have been relatively well characterized in plants and animals, and are now also being widely investigated in diverse fungi, some of which are important plant pathogens. This review focuses primarily on the current understanding of the dsRNA-mediated posttranscriptional gene silencing processes in fungi, but also discusses briefly the known gene silencing pathways that appear to be independent of the RNA silencing machineries. We review RNA silencing studies for a variety of fungi and highlight some of the mechanistic differences observed in different fungal organisms. As RNA silencing is being exploited as a technology in gene function studies in fungi as well as in engineering anti-fungal resistance in plants and animals, we also discuss the recent progress towards understanding dsRNA uptake in fungi.

Keywords RNA silencing gene silencing heterochromatin formation fungi small interfering RNA micro-RNA

Corresponding Author(s): SCHUMANN Ulrike,Email:ulrike.Schumann@csiro.au

Issue Date: 01 December 2010

Cite this article:

Ulrike SCHUMANN,Mick AYLIFFE,Kemal KAZAN, et al. RNA silencing in fungi[J]. Front Biol, 2010, 5(6): 478-494.

URL:

https://academic.hep.com.cn/fib/EN/10.1007/s11515-010-0550-3
https://academic.hep.com.cn/fib/EN/Y2010/V5/I6/478

Fig.1 . Within the plant genome RNA polymerase II (Pol II) transcribes miRNA genes giving rise to primary transcripts that have the ability to fold back to form hairpin structures. Natural sense and antisense transcripts produced by RNA Pol II have partial sequence overlap which can form double-stranded regions. TAS transcripts are produced by RNA Pol II and/or NRPD1a and serve as substrate to RdRP to produce dsRNA. All dsRNA molecules are processed by a specific DCL protein into sRNA species. These sRNAs are incorporated into RISC containing a specific AGO protein that mediates target transcript cleavage. rasiRNAs are generated by RNA Pol IV from repetitive DNA loci and direct sequence specific DNA methylation. The figure is adapted from Eamens et al., 2008 and simplified.

Fig.2 . Sequences were aligned using MAFFT and a rooted, neighbour joining tree was created in Mega4. 500 bootstrap trials were carried out and bootstrap values above 60% are shown. The asterisk (*) denotes genus in which some species have lost the RNA silencing machinery.

Fig.3 . Quelling occurs during vegetative growth of the fungus and can be induced by the introduction of transgenes. Transcripts are converted into dsRNA by the RdRP Qde-1 and subsequent DCL processing results in siRNA production. These siRNAs are incorporated into the RNA-induced silencing complex (RISC) that contains the AGO protein Qde-2 and mediates degradation of homologous mRNA. Meiotic silencing of unpaired DNA (MSUD) occurs only during the zygote stage. Unpaired alleles give rise to aberrant transcripts that mediate degradation of all homologous transcripts. Whether this process is mediated by the RNA silencing machinery is still unclear. Repeat induced point mutation (RIP) is functional only during the dikaryotic stage. RIP recognizes repetitive sequences and results in cytosine methylation. Subsequent deamination leads to irreversible C:G to T:A transitions. This figure is adapted from and simplified.

Tab.1 Isolated sRNA species associated with RNA silencing events in fungi

1	Ah-Fong A M V, Bormann-Chung C A, Judelson H S (2008). Optimization of transgene-mediated silencing in Phytophthora infestans and its association with small-interfering RNAs. Fungal Genet Biol , 45(8): 1197–1205 doi: 10.1016/j.fgb.2008.05.009
2	Barnes S E, Alcocer M J C, Archer D B (2008). siRNA as a molecular tool for use in Aspergillus niger. Biotechnol Lett , 30(5): 885–890 doi: 10.1007/s10529-007-9614-0
3	Blanco F A, Judelson H S (2005). A bZIP transcription factor from Phytophthora interacts with a protein kinase and is required for zoospore motility and plant infection. Mol Microbiol , 56(3): 638–648 doi: 10.1111/j.1365-2958.2005.04575.x
4	Bohse M L, Woods J P (2007). RNA interference-mediated silencing of the YPS3 gene of Histoplasma capsulatum reveals virulence defects. Infect Immun , 75(6): 2811–2817 doi: 10.1128/IAI.00304-07
5	Braumann I, van den Berg M, Kempken F (2008). Repeat induced point mutation in two asexual fungi, Aspergillus niger and Penicillium chrysogenum. Curr Genet , 53(5): 287–297 doi: 10.1007/s00294-008-0185-y
6	Buchon N, Vaury C (2006). RNAi: a defensive RNA-silencing against viruses and transposable elements. Heredity , 96(2): 195–202 doi: 10.1038/sj.hdy.6800789
7	Cam H P, Sugiyama T, Chen E S, Chen X, FitzGerald P C, Grewal S I S (2005). Comprehensive analysis of heterochromatin- and RNAi-mediated epigenetic control of the fission yeast genome. Nat Genet , 37(8): 809–819 doi: 10.1038/ng1602
8	Camblong J, Beyrouthy N, Guffanti E, Schlaepfer G, Steinmetz L M, Stutz F (2009). Trans-acting antisense RNAs mediate transcriptional gene cosuppression in S. cerevisiae. Genes Dev , 23(13): 1534–1545 doi: 10.1101/gad.522509
9	Camblong J, Iglesias N, Fickentscher C, Dieppois G, Stutz F (2007). Antisense RNA stabilization induces transcriptional gene silencing via histone deacetylation in S. cerevisiae. Cell , 131(4): 706–717
10	Cardoza R E, Hermosa M R, Vizcaíno J A, González F J, Llobell A, Monte E, Gutiérrez S (2007). Partial silencing of a hydroxy-methylglutaryl-CoA reductase-encoding gene in Trichoderma harzianum CECT 2413 results in a lower level of resistance to lovastatin and lower antifungal activity. Fungal Genet Biol , 44(4): 269–283 doi: 10.1016/j.fgb.2006.11.013
11	Cardoza R E, Vizcaíno J A, Hermosa M R, Sousa S, González F J, Llobell A, Monte E, Gutiérrez S (2006). Cloning and characterization of the erg1 gene of Trichoderma harzianum: effect of the erg1 silencing on ergosterol biosynthesis and resistance to terbinafine. Fungal Genet Biol , 43(3): 164–178 doi: 10.1016/j.fgb.2005.11.002
12	Caribé dos Santos A C, Sena J A L, Santos S C, Dias C V, Pirovani C P, Pungartnik C, Valle R R, Cascardo J C M, Vincentz M (2009). dsRNA-induced gene silencing in Moniliophthora perniciosa, the causal agent of witches’ broom disease of cacao. Fungal Genet Biol , 46(11): 825–836 doi: 10.1016/j.fgb.2009.06.012
13	Catalanotto C, Azzalin G, Macino G, Cogoni C (2000). Gene silencing in worms and fungi. Nature , 404(6775): 245 doi: 10.1038/35005169
14	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(7): 790–795 doi: 10.1101/gad.222402
15	Catalanotto C, Nolan T, Cogoni C (2006). Homology effects in Neurospora crassa. FEMS Microbiol Lett , 254(2): 182–189 doi: 10.1111/j.1574-6968.2005.00037.x
16	Catalanotto C, Pallotta M, ReFalo P, Sachs M S, Vayssie L, Macino G, Cogoni C (2004). Redundancy of the two dicer genes in transgeneinduced posttranscriptional gene silencing in Neurospora crassa. Mol Cell Biol , 24(6): 2536–2545 doi: 10.1128/MCB.24.6.2536-2545.2004
17	Cecere G, Cogoni C (2009). Quelling targets the rDNA locus and functions in rDNA copy number control. BMC Microbiol , 9(1): 44–54 doi: 10.1186/1471-2180-9-44
18	Choudhary S, Lee H C, Maiti M, He Q, Cheng P, Liu Q, Liu Y (2007). A double-stranded-RNA response program important for RNA interference efficiency. Mol Cell Biol , 27(11): 3995–4005 doi: 10.1128/MCB.00186-07
19	Cogoni C, Irelan J T, Schumacher M, Schmidhauser T J, Selker E U, Macino G (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 , 15(12): 3153–3163
20	Cogoni C, Macino G (1997). Isolation of quelling-defective (qde) mutants impaired in posttranscriptional transgene-induced gene silencing in Neurospora crassa. Proc Natl Acad Sci USA , 94(19): 10233–10238 doi: 10.1073/pnas.94.19.10233
21	Cogoni C, Macino G (1999a). Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature , 399(6732): 166–169 doi: 10.1038/20215
22	Cogoni C, Macino G (1999b). Posttranscriptional gene silencing in Neurospora by a RecQ DNA helicase. Science , 286(5448): 2342–2344 doi: 10.1126/science.286.5448.2342
23	Cogoni C, Romano N, Macino G (1994). Suppression of gene expression by homologous transgenes. Antonie van Leeuwenhoek , 65(3): 205–209 doi: 10.1007/BF00871948
24	Costa A M S B, Mills P R, Bailey A M, Foster G D, Challen M P (2008). Oligonucleotide sequences forming short self-complimentary hairpins can expedite the down-regulation of Coprinopsis cinerea genes. J Microbiol Methods , 75(2): 205–208 doi: 10.1016/j.mimet.2008.06.006
25	Costa A S M B, Thomas D J I, Eastwood D, Cutler S B, Bailey A M, Foster G D, Mills P R, Challen M P (2009). Quantifiable downregulation of endogenous genes in Agaricus bisporus mediated by expression of RNA hairpins. J Microbiol Biotechnol , 19(3): 271–276
26	Davis C A, Ares M Jr (2006). Accumulation of unstable promoter-associated transcripts upon loss of the nuclear exosome subunit Rrp6p in Saccharomyces cerevisiae. Proc Natl Acad Sci USA , 103(9): 3262–3267 doi: 10.1073/pnas.0507783103
27	de Haro J P, Calo S, Cervantes M, Nicolás F E, Torres-Martínez S, Ruiz-Vázquez R M (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(10): 1486–1497 doi: 10.1128/EC.00191-09
28	de Jong J F, Deelstra H J, W?sten H A B, Lugones L G (2006). RNA-mediated gene silencing in monokaryons and dikaryons of Schizophyllum commune. Appl Environ Microbiol , 72(2): 1267–1269 doi: 10.1128/AEM.72.2.1267-1269.2006
29	Der S D, Zhou A, Williams B R G, Silverman R H (1998). Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci USA , 95(26): 15623–15628 doi: 10.1073/pnas.95.26.15623
30	Disney M D, Haidaris C G, Turner D H (2003). Uptake and antifungal activity of oligonucleotides in Candida albicans. Proc Natl Acad Sci USA , 100(4): 1530–1534 doi: 10.1073/pnas.0337462100
31	Djupedal I, Kos-Braun I C, Mosher R A, S?derholm N, Simmer F, Hardcastle T J, Fender A, Heidrich N, Kagansky A, Bayne E, Wagner E G H, Baulcombe D C, Allshire R C, Ekwall K (2009). Analysis of small RNA in fission yeast; centromeric siRNAs are potentially generated through a structured RNA. EMBO J , 28(24): 3832–3844 doi: 10.1038/emboj.2009.351
32	Drinnenberg I A, Weinberg D E, Xie K T, Mower J P, Wolfe K H, Fink G R, Bartel D P (2009). RNAi in budding yeast. Science , 326(5952): 544–550 doi: 10.1126/science.1176945
33	Duxbury M S, Ashley S W, Whang E E (2005). RNA interference: a mammalian SID-1 homologue enhances siRNA uptake and gene silencing efficacy in human cells. Biochem Biophys Res Commun , 331(2): 459–463 doi: 10.1016/j.bbrc.2005.03.199
34	Eamens A, Wang M B, Smith N A, Waterhouse P M (2008). RNA silencing in plants: yesterday, today, and tomorrow. Plant Physiol , 147(2): 456–468 doi: 10.1104/pp.108.117275
35	Eastwood D C, Challen M P, Zhang C, Jenkins H, Henderson J, Burton K S (2008). Hairpin-mediated down-regulation of the urea cycle enzyme argininosuccinate lyase in Agaricus bisporus. Mycol Res , 112: 708–716 doi: 10.1016/j.mycres.2008.01.009
36	Fire A, Xu S, Montgomery M K, Kostas S A, Driver S E, Mello C C (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature , 391(6669): 806–811 doi: 10.1038/35888
37	Fitzgerald A, Van Kan J A L, Plummer K M (2004). Simultaneous silencing of multiple genes in the apple scab fungus, Venturia inaequalis, by expression of RNA with chimeric inverted repeats. Fungal Genet Biol , 41(10): 963–971 doi: 10.1016/j.fgb.2004.06.006
38	Freitag M, Lee D W, Kothe G O, Pratt R J, Aramayo R, Selker E U (2004). DNA methylation is independent of RNA interference in Neurospora. Science , 304(5679): 1939 doi: 10.1126/science.1099709
39	Galagan J E, Selker E U (2004). RIP: the evolutionary cost of genome defense. Trends Genet , 20(9): 417–423 doi: 10.1016/j.tig.2004.07.007
40	Gaulin E, Jauneau A, Villalba F, Rickauer M, Esquerré-Tugayé M T, Bottin A (2002). The CBEL glycoprotein of Phytophthora parasitica var. nicotianae is involved in cell wall deposition and adhesion to cellulosic substrates. J Cell Sci , 115(23): 4565–4575 doi: 10.1242/jcs.00138
41	Ghildiyal M, Zamore P D (2009). Small silencing RNAs: an expanding universe. Nat Rev Genet , 10(2): 94–108 doi: 10.1038/nrg2504
42	Goldoni M, Azzalin G, Macino G, Cogoni C (2004). Efficient gene silencing by expression of double stranded RNA in Neurospora crassa. Fungal Genet Biol , 41(11): 1016–1024 doi: 10.1016/j.fgb.2004.08.002
43	Goodbourn S, Didcock L, Randall R E (2000). Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J Gen Virol , 81(Pt 10): 2341–2364
44	Hamada W, Spanu P D (1998). Co-suppression of the hydrophobin gene HCf-1 is correlated with antisense RNA biosynthesis in Cladosporium fulvum. Mol Gen Genet , 259(6): 630–638 doi: 10.1007/s004380050857
45	Hammond T M, Bok J W, Andrewski M D, Reyes-Domínguez Y, Scazzocchio C, Keller N P (2008). RNA silencing gene truncation in the filamentous fungus Aspergillus nidulans. Eukaryot Cell , 7(2): 339–349 doi: 10.1128/EC.00355-07
46	Hammond T M, Keller N P (2005). RNA silencing in Aspergillus nidulans is independent of RNA-dependent RNA polymerases. Genetics , 169(2): 607–617 doi: 10.1534/genetics.104.035964
47	Heneghan M N, Costa A M S B, Challen M P, Mills P R, Bailey A, Foster G D (2007). A comparison of methods for successful triggering of gene silencing in Coprinus cinereus. Mol Biotechnol , 35(3): 283–296 doi: 10.1007/BF02686014
48	Himeno M, Maejima K, Komatsu K, Ozeki J, Hashimoto M, Kagiwada S, Yamaji Y, Namba S (2010). Significantly low level of small RNA accumulation derived from an encapsidated mycovirus with dsRNA genome. Virology , 396(1): 69–75 doi: 10.1016/j.virol.2009.10.008
49	Hinas A, Reimeg?rd J, Wagner E G, Nellen W, Ambros V R, S?derbom F (2007). The small RNA repertoire of Dictyostelium discoideum and its regulation by components of the RNAi pathway. Nucleic Acids Res , 35(20): 6714–6726 doi: 10.1093/nar/gkm707
50	Idnurm A, Howlett B J (2003). Analysis of loss of pathogenicity mutants reveals that repeat-induced point mutations can occur in the Dothideomycete Leptosphaeria maculans. Fungal Genet Biol , 39(1): 31–37 doi: 10.1016/S1087-1845(02)00588-1
51	Iida T, Nakayama J I, Moazed D (2008). siRNA-mediated heterochromatin establishment requires HP1 and is associated with antisense transcription. Mol Cell , 31: 178–189 doi: 10.1016/j.molcel.2008.07.003
52	Irelan J T, Selker E U (1996). Gene silencing in filamentous fungi: RIP, MIP and quelling. J Genet , 75(3): 313–324 doi: 10.1007/BF02966311
53	J?chl C, Loh E, Ploner A, Haas H, Hüttenhofer A (2009). Development-dependent scavenging of nucleic acids in the filamentous fungus Aspergillus fumigatus. RNA Biol 6(2): 178–186
54	J?chl C, Rederstorff M, Hertel J, Stadler P F, Hofacker I L, Schrettl M, Haas H, Hüttenhofer A (2008). Small ncRNA transcriptome analysis from Aspergillus fumigatus suggests a novel mechanism for regulation of protein synthesis. Nucleic Acids Res , 36(8): 2677–2689 doi: 10.1093/nar/gkn123
55	Judelson H S, Tani S (2007). Transgene-induced silencing of the zoosporogenesis-specific NIFC gene cluster of Phytophthora infestans involves chromatin alterations. Eukaryot Cell , 6(7): 1200–1209 doi: 10.1128/EC.00311-06
56	Kadotani N, Murata T, Quoc N B, Adachi Y, Nakayashiki H (2008). Transcriptional control and protein specialization have roles in the functional diversification of two dicer-like proteins in Magnaporthe oryzae. Genetics , 180(2): 1245–1249 doi: 10.1534/genetics.108.093922
57	Kadotani N, Nakayashiki H, Tosa Y, Mayama S (2003). RNA silencing in the phytopathogenic fungus Magnaporthe oryzae. Mol Plant Microbe Interact , 16(9): 769–776 doi: 10.1094/MPMI.2003.16.9.769
58	Kadotani N, Nakayashiki H, Tosa Y, Mayama S (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(43): 44467–44474 doi: 10.1074/jbc.M408259200
59	Kato H, Goto D B, Martienssen R A, Urano T, Furukawa K, Murakami Y (2005). RNA polymerase II is required for RNAi-dependent heterochromatin assembly. Science , 309(5733): 467–469 doi: 10.1126/science.1114955
60	Kemppainen M, Duplessis S, Martin F, Pardo A G (2009). RNA silencing in the model mycorrhizal fungus Laccaria bicolor: gene knock-down of nitrate reductase results in inhibition of symbiosis with Populus. Environ Microbiol , 11(7): 1878–1896 doi: 10.1111/j.1462-2920.2009.01912.x
61	Keon J P R, Owen J W, Hargreaves J A (1999). Lack of evidence for antisense suppression in the fungal plant pathogen Ustilago maydis. Antisense Nucleic Acid Drug Dev , 9(1): 101–104
62	Khatri M, Rajam M V (2007). Targeting polyamines of Aspergillus nidulans by siRNA specific to fungal ornithine decarboxylase gene. Med Mycol , 45(3): 211–220 doi: 10.1080/13693780601158779
63	Klattenhoff C, Theurkauf W (2008). Biogenesis and germline functions of piRNAs. Development , 135(1): 3–9 doi: 10.1242/dev.006486
64	Lacroix H, Spanu P D (2009). Silencing of six hydrophobins in Cladosporium fulvum: complexities of simultaneously targeting multiple genes. Appl Environ Microbiol , 75(2): 542–546 doi: 10.1128/AEM.01816-08
65	Latijnhouwers M, Govers F (2003). A Phytophthora infestans G-protein β subunit is involved in sporangium formation. Eukaryot Cell , 2(5): 971–977 doi: 10.1128/EC.2.5.971-977.2003
66	Laurie J D, Linning R, Bakkeren G (2008). Hallmarks of RNA silencing are found in the smut fungus Ustilago hordei but not in its close relative Ustilago maydis. Curr Genet , 53(1): 49–58 doi: 10.1007/s00294-007-0165-7
67	Lee H C, Chang S S, Choudhary S, Aalto A P, Maiti M, Bamford D H, Liu Y (2009). qiRNA is a new type of small interfering RNA induced by DNA damage. Nature , 459(7244): 274–277 doi: 10.1038/nature08041
68	Liu H, Cottrell T R, Pierini L M, Goldman W E, Doering T L (2002). RNA interference in the pathogenic fungus Cryptococcus neoformans. Genetics , 160(2): 463–470
69	Malone C D, Hannon G J (2009). Small RNAs as guardians of the genome. Cell , 136(4): 656–668
70	McDonald T, Brown D, Keller N P, Hammond T M (2005). RNA silencing of mycotoxin production in Aspergillus and Fusarium species. Mol Plant Microbe Interact , 18(6): 539–545 doi: 10.1094/MPMI-18-0539
71	Molnar A, Bassett A, Thueneman E, Schwach F, Karkare S, Ossowski S, Weigel D, Baulcombe D (2009). Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii. Plant J , 58(1): 165–174 doi: 10.1111/j.1365-313X.2008.03767.x
72	Molnár A, Schwach F, Studholme D J, Thuenemann E C, Baulcombe D C (2007). miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature , 447(7148): 1126–1129 doi: 10.1038/nature05903
73	Morin R D, Aksay G, Dolgosheina E, Ebhardt H A, Magrini V, Mardis E R, Sahinalp S C, Unrau P J (2008). Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Res , 18(4): 571–584 doi: 10.1101/gr.6897308
74	Moriwaki A, Ueno M, Arase S, Kihara J (2007). RNA-mediated gene silencing in the phytopathogenic fungus Bipolaris oryzae. FEMS Microbiol Lett , 269(1): 85–89 doi: 10.1111/j.1574-6968.2006.00606.x
75	Motamedi M R, Verdel A, Colmenares S U, Gerber S A, Gygi S P, Moazed D (2004). Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell , 119(6): 789–802
76	Mouyna I, Henry C, Doering T L, Latgé J P (2004). Gene silencing with RNA interference in the human pathogenic fungus Aspergillus fumigatus. FEMS Microbiol Lett , 237(2): 317–324
77	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(18): 5987–5994 doi: 10.1093/nar/gkm646
78	Nakayashiki H (2005). RNA silencing in fungi: mechanisms and applications. FEBS Lett , 579(26): 5950–5957 doi: 10.1016/j.febslet.2005.08.016
79	Nakayashiki H, Hanada S, Nguyen B Q, Kadotani N, Tosa Y, Mayama S (2005). RNA silencing as a tool for exploring gene function in ascomycete fungi. Fungal Genet Biol , 42(4): 275–283
80	Nakayashiki H, Kadotani N, Mayama S (2006). Evolution and diversification of RNA silencing proteins in fungi. J Mol Evol , 63(1): 127–135 doi: 10.1007/s00239-005-0257-2
81	Nakayashiki H, Nguyen Q B (2008). RNA interference: roles in fungal biology. Curr Opin Microbiol , 11(6): 494–502 doi: 10.1016/j.mib.2008.10.001
82	Namekawa S H, Iwabata K, Sugawara H, Hamada F N, Koshiyama A, Chiku H, Kamada T, Sakaguchi K (2005). Knockdown of LIM15/DMC1 in the mushroom Coprinus cinereus by double-stranded RNA-mediated gene silencing. Microbiology , 151(11): 3669–3678 doi: 10.1099/mic.0.28209-0
83	Nicolás F E, de Haro J P, Torres-Martínez S, Ruiz-Vázquez R M (2007). Mutants defective in a Mucor circinelloides dicer-like gene are not compromised in siRNA silencing but display developmental defects. Fungal Genet Biol , 44(6): 504–516 doi: 10.1016/j.fgb.2006.09.003
84	Nicolás F E, Torres-Martínez S, Ruiz-Vázquez R M (2003). Two classes of small antisense RNAs in fungal RNA silencing triggered by non-integrative transgenes. EMBO J , 22(15): 3983–3991 doi: 10.1093/emboj/cdg384
85	Nolan T, Cecere G, Mancone C, Alonzi T, Tripodi M, Catalanotto C, Cogoni C (2008). The RNA-dependent RNA polymerase essential for post-transcriptional gene silencing in Neurospora crassa interacts with replication protein A. Nucleic Acids Res , 36(2): 532–538 doi: 10.1093/nar/gkm1071
86	Osborne E A, Dudoit S, Rine J (2009). The establishment of gene silencing at single-cell resolution. Nat Genet , 41(7): 800–806 doi: 10.1038/ng.402
87	Rappleye C A, Engle J T, Goldman W E (2004). RNA interference in Histoplasma capsulatum demonstrates a role for α-(1,3)-glucan in virulence. Mol Microbiol , 53(1): 153–165 doi: 10.1111/j.1365-2958.2004.04131.x
88	Roignant J Y, Carré C, Mugat B, Szymczak D, Lepesant J A, Antoniewski C (2003). Absence of transitive and systemic pathways allows cell-specific and isoform-specific RNAi in Drosophila. RNA , 9(3): 299–308
89	Romano N, Macino G (1992). Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol , 6(22): 3343–3353 doi: 10.1111/j.1365-2958.1992.tb02202.x
90	Saleh M C, van Rij R P, Hekele A, Gillis A, Foley E, O’Farrell P H, Andino R (2006). The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nat Cell Biol , 8(8): 793–802 doi: 10.1038/ncb1439
91	Schuurs T A, Schaeffer E A M, Wessels J G H (1997). Homology-dependent silencing of the SC3 gene in Schizophyllum commune. Genetics , 147(2): 589–596
92	Segers G C, van Wezel R, Zhang X, Hong Y, 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(6): 896–904 doi: 10.1128/EC.00373-05
93	Segers G C, Zhang X, Deng F, Sun Q, Nuss D L (2007). Evidence that RNA silencing functions as an antiviral defense mechanism in fungi. Proc Natl Acad Sci USA , 104(31): 12902–12906 doi: 10.1073/pnas.0702500104
94	Sigova A, Rhind N, Zamore P D (2004). A single Argonaute protein mediates both transcriptional and posttranscriptional silencing in Schizosaccharomyces pombe. Genes Dev , 18(19): 2359–2367 doi: 10.1101/gad.1218004
95	Simmer F, Buscaino A, Kos-Braun I C, Kagansky A, Boukaba A, Urano T, Kerr A R W, Allshire R C (2010). Hairpin RNA induces secondary small interfering RNA synthesis and silencing in trans in fission yeast. EMBO Rep , 11(2): 112–118 doi: 10.1038/embor.2009.273
96	Smith N A, Singh S P, Wang M B, Stoutjesdijk P A, Green A G, Waterhouse P M (2000). Total silencing by intron-spliced hairpin RNAs. Nature , 407(6802): 319–320 doi: 10.1038/35030305
97	Sugiyama T, Cam H, Verdel A, Moazed D, Grewal S I S (2005). RNA-dependent RNA polymerase is an essential component of a self-enforcing loop coupling heterochromatin assembly to siRNA production. Proc Natl Acad Sci USA , 102(1): 152–157 doi: 10.1073/pnas.0407641102
98	Sun Q, Choi G H, Nuss D L (2009). A single argonaute gene is required for induction of RNA silencing antiviral defense and promotes viral RNA recombination. Proc Natl Acad Sci USA , 106(42): 17927–17932 doi: 10.1073/pnas.0907552106
99	Timmons L, Fire A (1998). Specific interference by ingested dsRNA. Nature , 395(6705): 854 doi: 10.1038/27579
100	van West P, Kamoun S, van’t Klooster J W, Govers F (1999). Internuclear gene silencing in Phytophthora infestans. Mol Cell , 3(3): 339–348 doi: 10.1016/S1097-2765(00)80461-X
101	van West P, Shepherd S J, Walker C A, Li S, Appiah A A, Grenville-Briggs L J, Govers F, Gow N A R (2008). Internuclear gene silencing in Phytophthora infestans is established through chromatin remodelling. Microbiology , 154(5): 1482–1490 doi: 10.1099/mic.0.2007/015545-0
102	Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal S I S, Moazed D (2004). RNAi-mediated targeting of heterochromatin by the RITS complex. Science , 303(5658): 672–676 doi: 10.1126/science.1093686
103	Verdel A, Vavasseur A, Le Gorrec M, Touat-Todeschini L (2009). Common themes in siRNA-mediated epigenetic silencing pathways. Int J Dev Biol , 53(2-3): 245–257 doi: 10.1387/ijdb.082691av
104	Volpe T A, Kidner C, Hall I M, Teng G, Grewal S I S, Martienssen R A (2002). Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science , 297(5588): 1833–1837 doi: 10.1126/science.1074973
105	W?lti M A, Villalba C, Buser R M, Grünler A, Aebi M, Künzler M (2006). Targeted gene silencing in the model mushroom Coprinopsis cinerea (Coprinus cinereus) by expression of homologous hairpin RNAs. Eukaryot Cell , 5(4): 732–744 doi: 10.1128/EC.5.4.732-744.2006
106	Waterhouse P M, Graham M W, Wang M B (1998). Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. Proc Natl Acad Sci USA , 95(23): 13959–13964 doi: 10.1073/pnas.95.23.13959
107	Waterhouse P M, Wang M B, Lough T (2001). Gene silencing as an adaptive defence against viruses. Nature , 411(6839): 834–842 doi: 10.1038/35081168
108	Whisson S C, Avrova A O, van West P, Jones J T (2005). A method for double-stranded RNA-mediated transient gene silencing in Phytophthora infestans. Mol Plant Pathol , 6(2): 153–163 doi: 10.1111/j.1364-3703.2005.00272.x
109	Winston W M, Molodowitch C, Hunter C P (2002). Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science , 295(5564): 2456–2459 doi: 10.1126/science.1068836
110	Yamada O, Ikeda R, Ohkita Y, Hayashi R, Sakamoto K, Akita O (2007). Gene silencing by RNA interference in the koji mold Aspergillus oryzae. Biosci Biotechnol Biochem , 71(1): 138–144 doi: 10.1271/bbb.60405
111	Zhang X, Segers G C, Sun Q, Deng F, Nuss D L (2008). Characterization of hypovirus-derived small RNAs generated in the chestnut blight fungus by an inducible DCL-2-dependent pathway. J Virol , 82(6): 2613–2619 doi: 10.1128/JVI.02324-07
112	Zhao T, Li G, Mi S, Li S, Hannon G J, Wang X J, Qi Y (2007). A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev , 21(10): 1190–1203 doi: 10.1101/gad.1543507
113	Zhao T, Wang W, Bai X, Qi Y (2009). Gene silencing by artificial miRNAs in Chlamydomonas. Plant J , 58: 157–164 doi: 10.1111/j.1365-313X.2008.03758.x

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