Applied Microbiology and Biotechnology

, Volume 89, Issue 3, pp 501–512

RNAi as a potential tool for biotechnological applications in fungi

  • Tomer M. Salame
  • Carmit Ziv
  • Yitzhak Hadar
  • Oded Yarden
Mini-Review

Abstract

RNA interference (RNAi) is a post-transcriptional gene-silencing (PTGS) phenomenon in which double-stranded RNA (dsRNA) triggers the degradation of homologous mRNA species, thereby reducing gene expression. In fungi, the use of RNAi as a tool for reverse genetics, aimed at modification of gene expression, is constantly growing, with more than 40 species already proven to be responsive. This technology has the ability to co-down-regulate the expression of several genes; however, this trait also makes it susceptible to non-target effects, which can be addressed using both available and developing bioinformatic tools. Moreover, the functionality of absorbed exogenous RNAi molecules, and the various classes of small RNAs found in fungi, offer great versatility and flexibility in acquiring the desired effects on gene expression, even without the necessity to genetically modify the targeted strain. There is an emerging role for RNAi as a potential tool for biotechnological applications. This is evident from current investigations in fungi, demonstrating the contribution of RNAi to progress research and applications in biomaterials production, bioconversion, plant fungal interactions and virulence factors of human pathogens. Possible problems and prospects for the use of RNAi in fungal biotechnology are discussed.

Keywords

RNA interference (RNAi) RNA silencing 

References

  1. Agrawal N, Dasaradhi PVN, Mohmmed A, Malhotra P, Bhatnagar RK, Mukherjee SK (2003) RNA interference: biology, mechanism and applications. Microbiol Mol Biol Rev 67:657–685Google Scholar
  2. Ah Fong A, Judelson HS (2003) Cell cycle regulator Cdc14 is expressed during sporulation but not hyphal growth in the fungus-like oomycete Phytophthora infestans. Mol Microbiol 50:487–494Google Scholar
  3. Archer DB, Mackenzie DA, Jeenes DJ, Roberts IN (1992) Proteolytic degradation of heterologous proteins expressed in Aspergillus niger. Biotechnol Lett 14:357–362Google Scholar
  4. Bacon JS, Jones D, Farmer VC, Webley DM (1968) The occurrence of alpha-(1–3)-glucan in Cryptococcus, Schizosaccharomyces and Polyporus species, and its hydrolysis by a Streptomyces culture filtrate lysing cell walls of Cryptococcus. Biochim Biophys Acta 158:313–315Google Scholar
  5. Baldo A, Mathy A, Tabart J, Camponova P, Vermout S, Massart L, Maréchal F, Galleni M, Mignon B (2010) Secreted subtilisin Sub3 from Microsporum canis is required for adherence to but not for invasion of the epidermis. Br J Dermatol 162:990–997Google Scholar
  6. Barton LM, Prade RA (2008) Inducible RNA interference of brlAbeta in Aspergillus nidulans. Eukaryot Cell 7:2004–2007Google Scholar
  7. Bernard M, Latge JP (2001) Aspergillus fumigates cell wall: composition and biosynthesis. Med Mycol 39:9–17Google Scholar
  8. Bicanic T, Wood R, Bekker LG, Darder M, Meintjes G, Harrison TS (2005) Antiretroviral roll-out, antifungal roll-back: access to treatment for cryptococcal meningitis. Lancet Infect Dis 5:530–531Google Scholar
  9. Brody H, Suchindra M (2009) RNAi-mediated gene silencing of highly expressed genes in the industrial fungi Trichoderma reesei and Aspergillus niger. Ind Biotechnol 5:53–60Google Scholar
  10. Bromley M, Gordon C, Rovira-Graells N, Oliver J (2006) The Aspergillus fumigatus cellobiohydrolase B (cbhB) promoter is tightly regulated and can be exploited for controlled protein expression and RNAi. FEMS Microbiol Lett 264:246–254Google Scholar
  11. Brotman Y, Briff E, Viterbo A, Chet I (2008) Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol 147:779–6789Google Scholar
  12. Cardoza RE, Vizcaíno JA, Hermosa MR, Sousa S, González FJ, 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 43:164–178Google Scholar
  13. Catalanotto C, Azzalin G, Macino G, Cogoni C (2000) Gene silencing in worms and fungi. Nature 404:245Google Scholar
  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 16:790–795Google Scholar
  15. Chang YC, Kwon-Chung KJ (1994) Complementation of a capsule-deficient mutation of Cryptococcus neoformans restores its virulence. Mol Cell Biol 14:4912–4919Google Scholar
  16. 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 94:10233–10238Google Scholar
  17. Cogoni C, Macino G (1999a) Posttranscriptional gene silencing in Neurospora by a RecQ DNA helicase. Science 286:2342–2344Google Scholar
  18. Cogoni C, Macino G (1999b) Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature 399:166–169Google Scholar
  19. Cogoni C, Irelan JT, Schumacher M, Schmidhauser TJ, Selker EU, 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 15:3153–3163Google Scholar
  20. Cohen R, Persky L, Hadar Y (2002) Biotechnological applications and potential of wood-degrading mushrooms of the genus Pleurotus. Appl Microbiol Biotechnol 58:582–594Google Scholar
  21. Cole GT, Hung CY (2001) The parasitic cell wall of Coccidioides immitis. Med Mycol 39:31–40Google Scholar
  22. Costa AM, Mills PR, Bailey AM, Foster GD, Challen MP (2008) Oligonucleotide sequences forming short self-complimentary hairpins can expedite the down-regulation of Coprinopsis cinerea genes. J Microbiol Methods 75:205–208Google Scholar
  23. Costa ASMB, Thomas DJI, Eastwood D, Cutler SB, Bailey AM, Foster GD, Mills PR, Challen MP (2009) Quantifiable downregulation of endogenous genes in Agaricus bisporus mediated by expression of RNA hairpin. J Microbiol Biotechnol 19:271–276Google Scholar
  24. Cottrell TR, Doering TL (2003) Silence of the strands: RNA interference in eukaryotic pathogens. Trends Microbiol 11:37–43Google Scholar
  25. de Backer MD, Neilssen B, Logghe M, Viaene J, Loonen I, Vandoninck S, de Hoogt R, Dewaele S, Simons FA, Verhasselt P, Vanhoof G, Contreras R, Luyten WH (2001) An antisense-based functional genomics approach for identification of genes critical for growth of Candida albicans. Nat Biotechnol 19:235–241Google Scholar
  26. de Backer MD, Raponi M, Arndt GM (2002) RNA-mediated gene silencing in non-pathogenic and pathogenic fungi. Curr Opin Microbiol 5:323–329Google Scholar
  27. de Jong JF, Deelstra HJ, Wosten HA, Lugones LG (2006) RNA-mediated gene silencing in monokaryons and dikaryons of Schizophyllum commune. Appl Environ Microbiol 72:1267–1269Google Scholar
  28. Dean RA (1997) Signal pathways and appressorium morphogenesis. Annu Rev Phytopathol 35:211–234Google Scholar
  29. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu JR, Pan H, Read ND, Lee YH, Carbone I, Brown D, Oh YY, Donofrio N, Jeong JS, Soanes DM, Djonovic S, Kolomiets E, Rehmeyer C, Li W, Harding M, Kim S, Lebrun MH, Bohnert H, Coughlan S, Butler J, Calvo S, Ma LJ, Nicol R, Purcell S, Nusbaum C, Galagan JE, Birren BW (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434:980–986Google Scholar
  30. dos Santos ACC, Sena JAL, Santos SC, Dias CV, Pirovani CP, Pungartnik C, Valle RR, Cascardo JCM, Vincentz M (2009) dsRNA-induced gene silencing in Moniliophthora perniciosa, the causal agent of witches’ broom disease of cacao. Fungal Genet Biol 46:825–836Google Scholar
  31. Emmet RW, Parberry DG (1975) Appressoria. Ann Rev Phytopathol 13:147–167Google Scholar
  32. Engh I, Nowrousian M, Kück U (2007) Regulation of melanin biosynthesis via the dihydroxynaphthalene pathway is dependent on sexual development in the ascomycete Sordaria macrospora. FEMS Microbiol Lett 275:62–70Google Scholar
  33. Erental A, Harel A, Yarden O (2007) Type 2A phosphoprotein phosphatase is required for asexual development and pathogenesis of Sclerotinia sclerotiorum. Mol Plant Microb Interact 20:944–954Google Scholar
  34. 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 391:806–811Google Scholar
  35. Fitzgerald A, Van Kan JA, 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 41:963–971Google Scholar
  36. Goldoni M, Azzalin G, Macino G, Cogoni C (2004) Efficient gene silencing by expression of double stranded RNA in Neurospora crassa. Fungal Genet Biol 41:1016–1024Google Scholar
  37. Haas BJ, Kamoun S, Zody MC, Jiang RH, Handsaker RE, Cano LM, Grabherr M, Kodira CD, Raffaele S, Torto-Alalibo T, Bozkurt TO, Ah-Fong AM, Alvarado L, Anderson VL, Armstrong MR, Avrova A, Baxter L, Beynon J, Boevink PC, Bollmann SR, Bos JI, Bulone V, Cai G, Cakir C, Carrington JC, Chawner M, Conti L, Costanzo S, Ewan R, Fahlgren N, Fischbach MA, Fugelstad J, Gilroy EM, Gnerre S, Green PJ, Grenville-Briggs LJ, Griffith J, Grünwald NJ, Horn K, Horner NR, Hu CH, Huitema E, Jeong DH, Jones AM, Jones JD, Jones RW, Karlsson EK, Kunjeti SG, Lamour K, Liu Z, Ma L, Maclean D, Chibucos MC, McDonald H, McWalters J, Meijer HJ, Morgan W, Morris PF, Munro CA, O’Neill K, Ospina-Giraldo M, Pinzón A, Pritchard L, Ramsahoye B, Ren Q, Restrepo S, Roy S, Sadanandom A, Savidor A, Schornack S, Schwartz DC, Schumann UD, Schwessinger B, Seyer L, Sharpe T, Silvar C, Song J, Studholme DJ, Sykes S, Thines M, van de Vondervoort PJ, Phuntumart V, Wawra S, Weide R, Win J, Young C, Zhou S, Fry W, Meyers BC, van West P, Ristaino J, Govers F, Birch PR, Whisson SC, Judelson HS, Nusbaum C (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393–398Google Scholar
  38. Hamilton A, Voinnet O, Chappell L, Baulcombe D (2002) Two classes of short interfering RNA in RNA silencing. EMBO J 21:4671–4679Google Scholar
  39. Hammond TM, Keller NP (2005) RNA silencing in Aspergillus nidulans is independent of RNA-dependent RNA polymerases. Genetics 169:607–617Google Scholar
  40. Heneghan MN, Costa AMSB, Challen MP, Mills PR, Bailey A, Foster GD (2007) A comparison of methods for successful triggering of gene silencing in Coprinus cinereus. Mol Biotechnol 35:283–294Google Scholar
  41. Henry C, Mouyna I, Latge JP (2007) Testing the efficacy of RNA interference constructs in Aspergillus fumigatus. Curr Genet 51:277–284Google Scholar
  42. Hogan LH, Klein BS (1994) Altered expression of surface alpha-1, 3-glucan in genetically related strains of Blastomyces dermatitidis that differ in virulence. Infect Immun 62:3543–3546Google Scholar
  43. Hutvagner G, Zamore PD (2002) RNAi: nature abhors a double-strand. Curr Opin Genet Dev 12:225–232Google Scholar
  44. Jana S, Chakraborty C, Nandi S (2004) Mechanisms and roles of the RNA-based gene silencing. Electron J Biotechnol 7:324–335Google Scholar
  45. Janus D, Hoff B, Hofmann E, Kück U (2007) An efficient fungal RNA-silencing system using the DsRed reporter gene. Appl Environ Microbiol 73:962–970Google Scholar
  46. Janus D, Hoff B, Kück U (2009) Evidence for Dicer-dependent RNA interference in the industrial penicillin producer Penicillium chrysogenum. Microbiology 155:3946–3956Google Scholar
  47. Kadotani N, Nakayashiki H, Tosa Y, Mayama S (2003) RNA silencing in the phytopathogenic fungus Magnaporthe oryzae. Mol Plant Microb Interact 16:769–776Google Scholar
  48. 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 279:44467–44474Google Scholar
  49. Kemppainen MJ, Pardo AG (2010) pHg/pSILBAgamma vector system for efficient gene silencing in homobasidiomycetes: optimization of ihpRNA-triggering in the mycorrhizal fungus Laccaria bicolor. Microb Biotechnol 3:178–200Google Scholar
  50. Kemppainen MJ, Duplessis S, Martin F, Pardo AG (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 11:1878–1896Google Scholar
  51. Khatri M, Rajam MV (2007) Targeting polyamines of Aspergillus nidulans by siRNA specific to fungal ornithine decarboxylase gene. Med Mycol 45:211–220Google Scholar
  52. Kitamoto N, Yoshino S, Ohmiya K, Tsukagoshi N (1999) Sequence analysis, overexpression, and antisense inhibition of a beta-xylosidase gene, xylA, from Aspergillus oryzae KBN616. Appl Environ Microbiol 65:20–24Google Scholar
  53. Klimpel KR, Goldman WE (1987) Isolation and characterization of spontaneous avirulent variants of Histoplasma capsulatum. Infect Immun 55:528–533Google Scholar
  54. Klimpel KR, Goldman WE (1988) Cell walls from avirulent variants of Histoplasma capsulatum lack α-(1, 3)-glucan. Infect Immun 56:2997–3000Google Scholar
  55. Krajaejun T, Gauthier GM, Rappleye CA, Sullivan TD, Klein BS (2007) Development and application of a green fluorescent protein sentinel system for identification of RNA interference in Blastomyces dermatitidis illuminates the role of septin in morphogenesis and sporulation. Eukaryot Cell 6:1299–1309Google Scholar
  56. Kück U, Hoff B (2010) New tools for the genetic manipulation of filamentous fungi. Appl Microbiol Biotechnol 86:51–62Google Scholar
  57. Latijnhouwers M, Ligterink W, Vleeshouwers VG, van West P, Govers F (2004) A Galpha subunit controls zoospore motility and virulence in the potato late blight pathogen Phytophthora infestans. Mol Microbiol 51:925–936Google Scholar
  58. Li L, Chang S, Liu Y (2010) RNA interference pathways in filamentous fungi. Cell Mol Life Sci. doi:10.1007/s00018-010-0471-y Google Scholar
  59. Liu H, Cottrell TR, Pierini LM, Goldman WE, Doering TL (2002) RNA interference in the pathogenic fungus Cryptococcus neoformans. Genetics 160:463–470Google Scholar
  60. Liu H, Zhang B, Li C, Bao X (2010) Knock down of chitosanase expression in phytopathogenic fungus Fusarium solani and its effect on pathogenicity. Curr Genet 56:275–281Google Scholar
  61. Machida M, Yamada O, Gomi K (2008) Genomics of Aspergillus oryzae: learning from the history of koji mold and exploration of its future. DNA Res 15:173–183Google Scholar
  62. 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 13:445–453Google Scholar
  63. Martin F, Aerts A, Ahrén D, Brun A, Danchin EG, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buée M, Brokstein P, Canbäck B, Cohen D, Courty PE, Coutinho PM, Delaruelle C, Detter JC, Deveau A, DiFazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I, Gay G, Grimwood J, Hoegger PJ, Jain P, Kilaru S, Labbé J, Lin YC, Legué V, Le Tacon F, Marmeisse R, Melayah D, Montanini B, Muratet M, Nehls U, Niculita-Hirzel H, Oudot-Le Secq MP, Peter M, Quesneville H, Rajashekar B, Reich M, Rouhier N, Schmutz J, Yin T, Chalot M, Henrissat B, Kües U, Lucas S, Van de Peer Y, Podila GK, Polle A, Pukkila PJ, Richardson PM, Rouzé P, Sanders IR, Stajich JE, Tunlid A, Tuskan G, Grigoriev IV (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88–92Google Scholar
  64. Matityahu A, Hadar Y, Dosoretz CG, Belinky PA (2008) Gene silencing by RNA interference in the white rot fungus Phanerochaete chrysosporium. Appl Environ Microbiol 74:5359–5365Google Scholar
  65. Matzke MA, Birchler JA (2005) RNAi-mediated pathways in the nucleus. Nat Rev Genet 6:24–35Google Scholar
  66. McDonald T, Brown D, Keller NP, Hammond TM (2005) RNA silencing of mycotoxin production in Aspergillus and Fusarium species. Mol Plant Microb Interact 18:539–545Google Scholar
  67. Moreno RE, Kanetsuna F, Carbonell LM (1969) Isolation of chitin and glucan from the cell wall of the yeast form of Paracoccidioides brasiliensis. Arch Biochem Biophys 130:212–217Google Scholar
  68. Moriwaki A, Ueno M, Arase S, Kihara J (2007) RNA-mediated gene silencing in the phytopathogenic fungus Bipolaris oryzae. FEMS Microbiol Lett 269:85–89Google Scholar
  69. Moriwaki A, Katsube H, Ueno M, Arase S, Kihara J (2008) Cloning and characterization of the BLR2, the homologue of the blue-light regulator of Neurospora crassa WC-2, in the phytopathogenic fungus Bipolaris oryzae. Curr Microbiol 56:115–121Google Scholar
  70. Mouyna I, Henry C, Doering TL, Latge JP (2004) Gene silencing with RNA interference in the human pathogenic fungus Aspergillus fumigatus. FEMS Microbiol Lett 237:317–324Google Scholar
  71. Nakayashiki H (2005) RNA silencing in fungi: mechanisms and applications. FEBS Lett 579:5950–5957Google Scholar
  72. Nakayashiki H, Nguyen QB (2008) RNA interference: roles in fungal biology. Curr Opin Microbiol 11:494–502Google Scholar
  73. Nakayashiki H, Hanada S, Nguyen BQ, Kadotani N, Tosa Y, Mayama S (2005) RNA silencing as a tool for exploring gene function in ascomycete fungi. Fungal Genet Biol 42:275–283Google Scholar
  74. Nakayashiki H, Kadotani N, Mayama S (2006) Evolution and diversification of RNA silencing proteins in fungi. J Mol Evol 63:127–135Google Scholar
  75. Namekawa SH, Iwabata K, Sugawara H, Hamada FN, 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 151:3669–3678Google Scholar
  76. Ngiam C, Jeenes DJ, Punt PJ, Van Den Hondel CA, Archer DB (2000) Characterization of a foldase, protein disulfide isomerase A, in the protein secretory pathway of Aspergillus niger. Appl Environ Microbiol 66:775–782Google Scholar
  77. Nguyen QB, Kadotani N, Kasahara S, Tosa Y, Mayama S, Nakayashiki H (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 68:1348–1365Google Scholar
  78. 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 22:3983–3991Google Scholar
  79. 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 44:504–516Google Scholar
  80. 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 33:1564–1573Google Scholar
  81. Novick P, Field C, Schekman R (1980) Identification of 23 complementation groups required for posttranslational events in the yeast secretory pathway. Cell 21:205–215Google Scholar
  82. Oliveira JM, van der Veen D, de Graaff LH, Qui L (2008) Efficient cloning system for construction of gene silencing vectors in Aspergillus niger. Appl Microbiol Biotechnol 80:917–924Google Scholar
  83. Panepinto J, Komperda K, Frases S, Park YD, Djordjevic JT, Casadevall A, Williamson PR (2009) Sec6-dependent sorting of fungal extracellular exosomes and laccase of Cryptococcus neoformans. Mol Microbiol 71:1165–1176Google Scholar
  84. Patel RM, van Kan JA, Bailey AM, Foster GD (2008) RNA mediated gene silencing of superoxide dismutase (bcsod1) in Botrytis cinerea. Phytopathology 98:1334–1339Google Scholar
  85. Raponi M, Arndt GM (2003) Double-stranded RNA-mediated gene silencing in fission yeast. Nucleic Acids Res 31:4481–4489Google Scholar
  86. Rappleye CA, Engle JT, Goldman WE (2004) RNA interference in Histoplasma capsulatum demonstrates a role for alpha-(1, 3)-glucan in virulence. Mol Microbiol 53:153–165Google Scholar
  87. Renckens S, De Greve H, Van Montagu M, Hernalsteens JP (1992) Petunia plants escape from negative selection against a transgene by silencing the foreign DNA via methylation. Mol Gen Genet 233:53–64Google Scholar
  88. Romano N, Macino G (1992) Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol 6:3343–3353Google Scholar
  89. Rukavtsova EB, Alekseeva VV, Buryanov YI (2010) The use of RNA interference for the metabolic engineering of plants (Review). Bioorg Khim 36:146–156Google Scholar
  90. Salame TM, Yarden O, Hadar Y (2010) Pleurotus ostreatus manganese-dependent peroxidase silencing impairs decolourization of Orange II. Microb Biotechnol 3:93–106Google Scholar
  91. Schümann J, Hertweck C (2007) Molecular basis of cytochalasan biosynthesis in fungi: gene cluster analysis and evidence for the involvement of a PKS-NRPS hybrid synthase by RNA silencing. J Am Chem Soc 129:9564–9565Google Scholar
  92. Segers GC, van Wezel R, Zhang X, Hong Y, Nuss DL (2006) Hypovirus papain-like protease p29 suppresses RNA silencing in the natural fungal host and in a heterologous plant system. Eukaryot Cell 5:896–904Google Scholar
  93. Shafran H, Miyara I, Eshed R, Prusky D, Sherman A (2008) Development of new tools for studying gene function in fungi based on the Gateway system. Fungal Genet Biol 45:1147–1154Google Scholar
  94. Silva CL, Alves LM, Figueiredo F (1994) Involvement of cell wall glucans in the genesis and persistence of the inflammatory reaction caused by the fungus Paracoccidioides brasiliensis. Microbiology 140:1189–1194Google Scholar
  95. Singh S, Braus-Stromeyer SA, Timpner C, Tran VT, Lohaus G, Reusche M, Knufer J, Teichmann T, von Tiedemann A, Braus GH (2009) Silencing of Vlaro2 for chorismate synthase revealed that the phytopathogen Verticillium longisporum induces the cross-pathway control in the xylem. Appl Microbiol Biotechnol 85:1961–1976Google Scholar
  96. Smith TF, Waterman MS (1981) Identification of common molecular subsequences. J Mol Biol 147:195–197Google Scholar
  97. Spiering MJ, Moon CD, Wilkinson HH, Schardl CL (2005) Gene clusters for insecticidal loline alkaloids in the grass-endophytic fungus Neotyphodium uncinatum. Genetics 3:1403–1414Google Scholar
  98. Takeno S, Sakuradani E, Tomi A, Inohara-Ochiai M, Kawashima H, Ashikari T, Shimizu S (2005) Improvement of the fatty acid composition of an oil-producing filamentous fungus, Mortierella alpina 1 S-4, through RNA interference with delta12-desaturase gene expression. Appl Environ Microbiol 71:5124–5128Google Scholar
  99. Tanguay P, Bozza S, Breuil C (2006) Assessing RNAi frequency and efficiency in Ophiostoma floccosum and O. piceae. Fungal Genet Biol 43:804–812Google Scholar
  100. Tinoco MLP, Dias BBA, Dall’Astta RC, Pamphile JA, Aragão FJL (2010) In vivo trans-specific gene silencing in fungal cells by in planta expression of a double-stranded RNA. BMC Biol 8:27. doi:10.1186/1741-7007-8-27 Google Scholar
  101. Ullán RV, Godio RP, Teijeira F, Vaca I, Garcia-Estrada C, Feltrer R, Kosalkova K, Martin JF (2008) RNA-silencing in Penicillium chrysogenum and Acremonium chrysogenum: validation studies using beta-lactam genes expression. J Microbiol Methods 75:209–218Google Scholar
  102. 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 2:291–299Google Scholar
  103. van West P, Kamoun S, van’t Klooster JW, Govers F (1999) Internuclear gene silencing in Phytophthora infestans. Mol Cell 3:339–348Google Scholar
  104. Vermout S, Tabart J, Baldo A, Monod M, Losson B, Mignon B (2007) RNA silencing in the dermatophyte Microsporum canis. FEMS Microbiol Lett 275:38–45Google Scholar
  105. Viterbo A, Landau U, Kim S, Chernin L, Chet I (2010) Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiol Lett 305:42–48Google Scholar
  106. Wani SH (2010) Inducing fungus-resistance into plants through biotechnology. Not Sci Biol 2:14–21Google Scholar
  107. Whisson SC, Avrova AO, Van West P, Jones JT (2005) A method for double-stranded RNA-mediated transient gene silencing in Phytophthora infestans. Mol Plant Pathol 6:153–163Google Scholar
  108. Wilson RA, Talbot NJ (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol 7:185–195Google Scholar
  109. Yamada T, Morishita S (2005) Accelerated off-target search algorithm for siRNA. Bioinformatics 21:1316–1324Google Scholar
  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 71:138–144Google Scholar
  111. Zamore PD, Tuschl T, Sharp PA, Bartel DP (2000) RNAi: Double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101:25–33Google Scholar
  112. Zheng XF, Kobayashi Y, Takeuchi M (1998) Construction of a low-serine-type-carboxypeptidase-producing mutant of Aspergillus oryzae by the expression of antisense RNA and its use as a host for heterologous protein secretion. Appl Microbiol Biotechnol 49:39–44Google Scholar
  113. Ziv C, Yarden O (2010) Gene silencing for functional analysis: assessing RNAi as a tool for manipulation of gene expression. Methods Mol Biol 638:77–100Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Tomer M. Salame
    • 1
  • Carmit Ziv
    • 1
  • Yitzhak Hadar
    • 1
  • Oded Yarden
    • 1
  1. 1.Department of Plant Pathology and Microbiology and the Otto Warburg Minerva Center for Agricultural Biotechnology, The Robert H. Smith Faculty of Agriculture, Food and EnvironmentThe Hebrew University of JerusalemRehovotIsrael

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