Abstract
Comprehensive phylogenetic analyses of fungal Argonaute, Dicer, and RNA-dependent RNA polymerase-like proteins have been performed to gain insights into the diversification of RNA silencing pathways during the evolution of fungi. A wide range of fungi including ascomycetes, basidiomycetyes, and zygomycetes possesses multiple RNA silencing components in the genome, whereas a portion of ascomycete and basidiomycete fungi apparently lacks the whole or most of the components. The number of paralogous silencing proteins in the genome differs considerably among fungal species, suggesting that RNA silencing pathways have diversified significantly during evolution in parallel with developing the complexity of life cycle or in response to environmental conditions. Interestingly, orthologous silencing proteins from different fungal clades are often clustered more closely than paralogous proteins in a fungus, indicating that duplication events occurred before speciation events. Therefore, the origin of multiple RNA silencing pathways seems to be very ancient, likely having occurred prior to the divergence of the major fungal lineages.
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Altschul S, Madden T, Schaffer A, Zhang J, Zhang Z, Miller W, Lipman D (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Aramayo R, Metzenberg RL (1996) Meiotic transvection in fungi. Cell 86:103–113
Aravind L, Watanabe H, Lipman DJ, Koonin EV (2000) Lineage–specific loss and divergence of functionally linked genes in eukaryotes. Proc Natl Acad Sci USA 97:11319–11324
Barnett JA, Payne RW, Yarrow D (1990) Yeasts: Characterisation and identification. Cambridge University Press, Cambridge
Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer EL (2002) The Pfam protein families database. Nucleic Acids Res. 30:276–280
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
Chicas A, Forrest EC, Sepich S, Cogoni C, Macino G (2005) Small interfering RNAs that trigger posttranscriptional gene silencing are not required for the histone H3 Lys9 methylation necessary for transgenic tandem repeat stabilization in Neurospora crassa. Mol Cell Biol 25:3793–3801
Cogoni C, Macino G (1999) Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature 399:166–169
Cogoni C, Macino G (2000) Post-transcriptional gene silencing across kingdoms. Curr Opin Genet 10:638–643
Couch BC, Kohn LM (2002) A multilocus gene genealogy concordant with host preference indicates segregation of a new species, Magnaporthe oryzae, from M. grisea. Mycologia 94:683–693
Dalmay T, Hamilton A, Rudd S, Angell S, Baulcombe DC (2000) An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101:543–553
Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811
Fitzgerald A, Kan JALv, Plummer KM (2004) Simultaneous silencing of multiple genes in the apple scab fungus, Venturia inaequalis, by expression of RNA with chimeric inverted repeats. Fungal Genet Biol 41:963–971
Freitag M, Lee DW, Kothe GO, Pratt RJ, Aramayo R, Selker EU (2004) DNA methylation is independent of RNA interference in Neurospora. Science 304:1939
Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, Fitzhugh W, Ma L-J, Smirnov S, Purcell S, Rehman B, Elkins T, Engels R, Wang S, Nielsen CB, Butler J, Endrizzi M, Qui D, Ianakiev P, Bell-Pedersen D, Nelson MA, Werner-Washburne M, Selitrennikoff CP, Kinsey JA, Braun EL, Zelter A, Schulte U, Kothe GO, Jedd G, Mewes W, Staben C, Marcotte E, Greenberg D, Roy A, Foley K, Naylor J, Stange-Thomann N, Barrett R, Gnerre S, Kamal M, Kamvysselis M, Mauceli E, Bielke C, Rudd S, Frishman D, Krystofova S, Rasmussen C, Metzenberg RL, Perkins DD, Kroken S, Cogoni C, Macino G, Catcheside D, Li W, Pratt RJ, Osmani SA, Desouza CPC, Glass L, Orbach MJ, Berglund JA, Voelker R, Yarden O, Plamann M, Seiler S, Dunlap J, Radford A, Aramayo R, Natvig DO, Alex LA, Mannhaupt G, Ebbole DJ, Freitag M, Paulsen I, Sachs MS, Lander ES, Nusbaum C, Birren B (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859–868
Hammond TM, Keller NP (2005) RNA silencing in Aspergillus nidulans is independent of RNA-dependent RNA polymerases. Genetics 169:607–617
Kadotani N, Nakayashiki H, Tosa Y, Mayama S (2003) RNA silencing in the phytopathogenic fungus Magnaporthe oryzae. Mol Plant Microbe Interact 16:769–776
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 siRNA accumulation. J Biol Chem 279:44467–44474
Kato H, Yamamoto M, Yamaguchi-Ozaki T, Kadouchi H, Iwamoto Y, Nakayashiki H, Tosa Y, Mayama S, Mori N (2000) Pathogenicity, mating ability and DNA restriction fragment length polymorphisms of Pyricularia populations isolated from Gramineae, Bambusideae and Zingiberaceae plants. J Gen Plant Pathol 66:30–47
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
Kurtzman CP, Robnett CJ (2003) Phylogenetic relationships among yeasts of the ‘Saccharomyces complex’ determined from multigene sequence analyses. FEMS Yeast Res 3:417–432
Latijnhouwers M, Ligterink W, Vleeshouwers VGAA, West Pv, Govers F (2004) A Galpha subunit controls zoospore motility and virulence in the potato late blight pathogen Phytophthora infestans. Mol Microbiol 51:925–936
Lee DW, Pratt RJ, McLaughlin M, Aramayo R (2003) An argonaute-like protein is required for meiotic silencing. Genetics 164:821–828
Lee YS, Nakahara K, Pham JW, Kim K, He Z, Sontheimer EJ, Carthew RW (2004) Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117:69–81
Liu H, Cottrell TR, Pierini LM, Goldman WE, Doering TL (2002) RNA interference in the pathogenic fungus Cryptococcus neoformans. Genetics 160:463–470
Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ, Hammond SM, Joshua-Tor L, Hannon GJ (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305:1437–1441
Martens H, Novotny J, Oberstrass J, Steck TL, Postlethwait P, Nellen W (2002) RNAi in Dictyostelium: the role of RNA-directed RNA polymerases and double-stranded RNase. Mol Biol Cell 13:445–453
Matzke MA, Birchler JA (2005) RNAi–mediated pathways in the nucleus. Nat Rev Genet 6:24–35
Mlotshwa S, Voinnet O, Mette MF, Matzke M, Vaucheret H, Ding SW, Pruss G, Vance VB (2002) RNA silencing and the mobile silencing signal. Plant Cell 14:S289–301
Mochizuki K, Gorovsky MA (2005) A Dicer-like protein in Tetrahymena has distinct functions in genome rearrangement, chromosome segregation, and meiotic prophase. Genes Dev 19:77–89
Mourrain P, Beclin C, Elmayan T, Feuerbach F, Godon C, Morel JB, Jouette D, Lacombe AM, Nikic S, Picault N, Remoue K, Sanial M, Vo TA, Vaucheret H (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101:533–542
Mouyna I, Henry C, Doering TL, Latge JP (2004) Gene silencing with RNA interference in the human pathogenic fungus Aspergillus fumigatus. FEMS Microbiol Lett 237:317–324
Ngo H, Tschudi C, Gull K, Ullu E (1998) Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc Natl Acad Sci USA 95:14687–14692
Nicolas FE, Torres-Martinez S, Ruiz-Vazquez RM (2003) Two classes of small antisense RNAs in fungal RNA silencing triggered by non-integrative transgenes. EMBO J 22:3983–3991
Okamura K, Ishizuka A, Siomi H, Siomi MC (2004) Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev 18:1655–1666
Rappleye CA, Engle JT, Goldman WE (2004) RNA interference in Histoplasma capsulatum demonstrates a role for alpha-(1,3)-glucan in virulence. Mol Microbiol 53:153–165
Romano N, Macino G (1992) Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol 6:3343–3353
Shiu PKT, Raju NB, Zickler D, Metzenberg RL (2001) Meiotic silencing by unpaired DNA. Cell 107:905–916
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Tomari Y, Zamore PD (2005) Perspective: machines for RNAi. Genes Dev 19:517–529
Ullu E, Tschudi C, Chakraborty T (2004) RNA interference in protozoan parasites. Cell Microbiol 6:509–519
Van der Krol AR, Mur LA, Beld M, Mol JN, Stuitje AR (1990) Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2:291–299
Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal SI, Moazed D (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303:672–676
Wood V, Gwilliam R, Rajandream M-A, et al. (2002) The genome sequence of Schizosaccharomyces pombe. Nature 415:871–880
Acknowledgments
We are grateful to Naoki Mori, Kobe University, for useful discussion. We also thank Michael Freitag, University of Oregon, for providing helpful comments. This work was supported by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan.
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Nakayashiki, H., Kadotani, N. & Mayama, S. Evolution and Diversification of RNA Silencing Proteins in Fungi. J Mol Evol 63, 127–135 (2006). https://doi.org/10.1007/s00239-005-0257-2
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DOI: https://doi.org/10.1007/s00239-005-0257-2