Substrate-induced transcriptional activation of the MoCel7C cellulase gene is associated with methylation of histone H3 at lysine 4 in the rice blast fungus Magnaporthe oryzae

Applied and Environmental Microbiology

Volumn 79, Issue 21, 2013, Pages 6823-6832

  Van Vu, Ba ^a   Minh Pham, Kieu Thi ^a   Nakayashiki, Hitoshi ^a  

^a KOBE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYMETHYLCELLULOSE; CELLO-OLIGOSACCHARIDES; CHROMATIN IMMUNOPRECIPITATION ASSAY; ENVIRONMENTAL SIGNALS; GREEN FLUORESCENT PROTEIN; MAGNAPORTHE ORYZAE; METHYLTRANSFERASES; TRANSCRIPTIONAL ACTIVATIONS;

ALKYLATION; AMINO ACIDS; GENE ENCODING; GENE EXPRESSION; METHYLATION;

PROTEINS;

BIOACTIVITY; BIOASSAY; FUNGUS; GENE EXPRESSION; GLUCOSE; HISTOLOGY; METHYLATION; PROTEIN; RICE; SUBSTRATE;

CELLULASE; GREEN FLUORESCENT PROTEIN; HISTONE; LYSINE; PRIMER DNA;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; DNA SEQUENCE; ENZYMOLOGY; FUNGAL GENE; GENE INACTIVATION; GENE VECTOR; GENETICS; MAGNAPORTHE; METABOLISM; METHYLATION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION; WESTERN BLOTTING;

BASE SEQUENCE; BLOTTING, WESTERN; CELLULASE; CHROMATIN IMMUNOPRECIPITATION; DNA PRIMERS; GENE KNOCKOUT TECHNIQUES; GENES, FUNGAL; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HISTONES; LYSINE; MAGNAPORTHE; METHYLATION; MOLECULAR SEQUENCE DATA; REAL-TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; TRANSCRIPTIONAL ACTIVATION;

EID: 84886922600     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02082-13     Document Type: Article

References (60)

1. Faulk C, Dolinoy DC. 2011. Timing is everything: the when and how of environmentally induced changes in the epigenome of animals. Epigenetics 6:791-797.
2. Turner BM. 2011. Environmental sensing by chromatin: an epigenetic contribution to evolutionary change. FEBS Lett. 585:2032-2040.
3. Chinnusamy V, Zhu JK. 2009. Epigenetic regulation of stress responses in plants. Curr. Opin. Plant Biol. 12:133-139.
4. Cortessis VK, Thomas DC, Levine AJ, Breton CV, Mack TM, Siegmund KD, Haile RW, Laird PW. 2012. Environmental epigenetics: prospects for studying epigenetic mediation of exposure-response relationships. Hum. Genet. 131:1565-1589.
5. Smith KM, Phatale PA, Bredeweg EL, Connolly LR, Pomraning KR, Freitag M. 2012. Epigenetics of filamentous fungi, p 1-43. In Meyers RA (ed), Encyclopedia of molecular cell biology and molecular medicine. Wiley- VCH Verlag GmBH &Co., Weinheim, Germany.
6. Grimaldi B, Coiro P, Filetici P, Berge E, Dobosy JR, Freitag M, Selker EU, Ballario P. 2006. The Neurospora crassa White Collar-1 dependent blue light response requires acetylation of histone H3 lysine 14 by NGF-1. Mol. Biol. Cell 17:4576-4583.
7. Shwab EK, Bok JW, Tribus M, Galehr J, Graessle S, Keller NP. 2007. Histone deacetylase activity regulates chemical diversity in Aspergillus. Eukaryot. Cell 6:1656-1664.
8. Bok JW, Chiang YM, Szewczyk E, Reyes-Dominguez Y, Davidson AD, Sanchez JF, Lo HC, Watanabe K, Strauss J, Oakley BR, Wang CC, Keller NP. 2009. Chromatin-level regulation of biosynthetic gene clusters. Nat. Chem. Biol. 5:462-464.
9. Palmer JM, Bok JW, Lee S, Dagenais TR, Andes DR, Kontoyiannis DP, Keller NP. 2013. Loss of CclA, required for histone 3 lysine 4 methylation, decreases growth but increases secondary metabolite production in Aspergillus fumigatus. PeerJ 1:e4. doi:10.7717/peerj.4.
10. Bok JW, Keller NP. 2004. LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot. Cell 3:527-535.
11. Strauss J, Reyes-Dominguez Y. 2011. Regulation of secondary metabolism by chromatin structure and epigenetic codes. Fungal Genet. Biol. 48:62-69.
12. Xu J-R, Zhao X, Dean RA. 2007. From genes to genomes; a new paradigm for studying fungal pathogenesis in Magnaporthe oryzae. Adv. Genet. 57: 175-218.
13. Gowda M, Venu RC, Raghupathy MB, Nobuta K, Li H, Wing R, Stahlberg E, Couglan S, Haudenschild CD, Dean R, Nahm BH, Meyers BC, Wang GL. 2006. Deep and comparative analysis of the mycelium and appressorium transcriptomes of Magnaporthe grisea using MPSS, RLSAGE, and oligoarray methods. BMC Genomics 7:310.
14. Vu VB, Itoh K, Nguyen QB, Tosa Y, Nakayashiki H. 2012. Cellulases belonging to glycoside hydrolase families 6 and 7 contribute to the virulence of Magnaporthe oryzae. Mol. Plant Microbe Interact. 25:1135-1141.
15. Mandels M, Reese ET. 1957. Induction of cellulase in Trichoderma viride as influenced by carbon sources and metals. J. Bacteriol. 73:269-278.
16. Bisaria VS, Mishra S. 1989. Regulatory aspects of cellulase biosynthesis and secretion. CRC Crit. Rev. Biotechnol. 9:61-113.
17. Schmoll M, Kubicek CP. 2003. Regulation of Trichoderma cellulase formation: lessons in molecular biology from an industrial fungus. A review. Acta Microbiol. Immunol. Hung. 50:125-145.
18. Peterson R, Nevalainen H. 2012. Trichoderma reesei RUT-C30-thirty years of strain improvement. Microbiology 158:58-68.
19. Aro N, Ilmen M, Saloheimo A, Penttila M. 2003. ACEI of Trichoderma reesei is a repressor of cellulase and xylanase expression. Appl. Environ. Microbiol. 69:56-65.
20. Aro N, Saloheimo A, Ilmen M, Penttila M. 2001. ACEII, a novel transcriptional activator involved in regulation of cellulase and xylanase genes of Trichoderma reesei. J. Biol. Chem. 276:24309-24314.
21. Takashima S, Iikura H, Nakamura A, Masaki H, Uozumi T. 1996. Analysis of Cre1 binding sites in the Trichoderma reesei cbh1 upstream region. FEMS Microbiol. Lett. 145:361-366.
22. Ling M, Qin Y, Li N, Liang Z. 2009. Binding of two transcriptional factors, Xyr1 and ACEI, in the promoter region of cellulase cbh1 gene. Biotechnol. Lett. 31:227-231.
23. Seiboth B, Karimi RA, Phatale PA, Linke R, Hartl L, Sauer DG, Smith KM, Baker SE, Freitag M, Kubicek CP. 2012. The putative protein methyltransferase LAE1 controls cellulase gene expression in Trichoderma reesei. Mol. Microbiol. 84:1150-1164.
24. Urashima AS, Hashimoto Y, Don LD, Kusaba M, Tosa Y, Nakayashiki H, Mayama S. 1999. Molecular analysis of the wheat blast population in Brazil with a homologue of retrotransposon MGR583. Ann. Phytopathol. Soc. Jpn. 65:429-436.
25. Kadotani N, Nakayashiki H, Tosa Y, Mayama S. 2003. RNA silencing in the phytopathogenic fungus Magnaporthe oryzae. Mol. Plant Microbe Interact. 16:769-776.
26. 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 highthroughput RNA-silencing system. Mol. Microbiol. 68:1348-1365.
27. Nakayashiki H, Kiyotomi K, Tosa Y, Mayama S. 1999. Transposition of the retrotransposon MAGGY in heterologous species of filamentous fungi. Genetics 153:693-703.
28. Fairhead C, Llorente B, Denis F, Soler M, Dujon B. 1996. New vectors for combinatorial deletions in yeast chromosomes and for gap-repair cloning using 'split-marker' recombination. Yeast 12:1439-1457.
29. Morita Y, Hyon GS, Hosogi N, Miyata N, Nakayashiki H, Muranaka Y, Inada N, Park P, Ikeda K. 2013. Appressorium-localized NADPH oxidase B is essential for aggressiveness and pathogenicity in the host-specific, toxin-producing fungus Alternaria alternata Japanese pear pathotype. Mol. Plant Pathol. 14:365-378.
30. Namiki F, Matsunaga M, Okuda M, Inoue I, Nishi K, Fujita Y, Tsuge T. 2001. Mutation of an arginine biosynthesis gene causes reduced pathogenicity in Fusarium oxysporum f. sp. melonis. Mol. Plant Microbe Interact. 14:580-584.
31. 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. 42:275-283.
32. Zhou J, Zheng XZ, Lan L, Lin CZ, Wu YB, Lin XJ, Ebbole D, Lu GD, Wang ZH. 2008. Biochemical and molecular characterization of a putative endoglucanase in Magnaporthe grisea. Curr. Genet. 53:217-224.
33. Bernstein BE, Humphrey EL, Erlich RL, Schneider R, Bouman P, Liu JS, Kouzarides T, Schreiber SL. 2002. Methylation of histone H3 Lys 4 in coding regions of active genes. Proc. Natl. Acad. Sci. U.S.A. 99:8695-8700.
34. Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey DK, Huebert DJ, McMahon S, Karlsson EK, Kulbokas EJ, III, Gingeras TR, Schreiber SL, Lander ES. 2005. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120:169-181.
35. Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NC, Schreiber SL, Mellor J, Kouzarides T. 2002. Active genes are tri-methylated at K4 of histone H3. Nature 419:407-411.
36. Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee TI, Bell GW, Walker K, Rolfe PA, Herbolsheimer E, Zeitlinger J, Lewitter F, Gifford DK, Young RA. 2005. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122:517-527.
37. Zhang X, Clarenz O, Cokus S, Bernatavichute YV, Pellegrini M, Goodrich J, Jacobsen SE. 2007. Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 5:e129. doi:10.1371/journal .pbio.0050129.
38. Henrissat B, Bairoch A. 1996. Updating the sequence-based classification of glycosyl hydrolases. Biochem. J. 316:695-696.
39. Kouzarides T. 2007. Chromatin modifications and their function. Cell 128:693-705.
40. Berger H, Pachlinger R, Morozov I, Goller S, Narendja F, Caddick M, Strauss J. 2006. The GATA factor AreA regulates localization and in vivo binding site occupancy of the nitrate activator NirA. Mol. Microbiol. 59: 433-446.
41. Nislow C, Ray E, Pillus L. 1997. SET1, a yeast member of the trithorax family, functions in transcriptional silencing and diverse cellular processes. Mol. Biol. Cell 8:2421-2436.
42. Briggs SD, Bryk M, Strahl BD, Cheung WL, Davie JK, Dent SY, Winston F, Allis CD. 2001. Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev. 15:3286-3295.
43. Berretta J, Pinskaya M, Morillon A. 2008. A cryptic unstable transcript mediates transcriptional trans-silencing of the Ty1 retrotransposon in S. cerevisiae. Genes Dev. 22:615-626.
44. Raduwan H, Isola AL, Belden WJ. 2013. Methylation of histone H3 on lysine 4 by the lysine methyltransferase SET1 protein is needed for normal clock gene expression. J. Biol. Chem. 288:8380-8390.
45. Zeilinger S, Schmoll M, Pail M, Mach RL, Kubicek CP. 2003. Nucleosome transactions on the Hypocrea jecorina (Trichoderma reesei) cellulase promoter cbh2 associated with cellulase induction. Mol. Genet. Genomics 270:46-55.
46. El-Gogary S, Leite A, Crivellaro O, Eveleigh DE, El-Dorry H. 1989. Mechanism by which cellulose triggers cellobiohydrolase I gene expression in Trichoderma reesei. Proc. Natl. Acad. Sci. U.S.A. 86:6138-6141.
47. Dekker RFH. 1981. Induction, localization and characterization of ß-Dglucosidase produced by a species of Monilia. J. Gen. Microbiol. 127:177-184.
48. Johnson EA, Bouchot F, Demain AL. 1985. Regulation of cellulase formation in Clostridium thermocellum. J. Gen. Microbiol. 131:2303-2308.
49. Murray WD. 1987. Effects of cellobiose and glucose on cellulose hydrolysis by both growing and resting cells of Bacteroides cellulosolvens. Biotechnol. Bioeng. 29:1151-1154.
50. Mishra S, Beguin P, Aubert JP. 1991. Transcription of Clostridium thermocellum endoglucanase genes celF and celD. J. Bacteriol. 173:80-85.
51. Kubicek CP, Penttila ME. 1998. Regulation of production of plant polysaccharide degrading enzymes by Trichoderma, p 49-72. In Harman GE, Kubicek CP (ed), Trichoderma and Gliocladium, vol 2. Taylor & Francis Ltd., London, United Kingdom.
52. Znameroski EA, Coradetti ST, Roche CM, Tsai JC, Iavarone AT, Cate JHD, Glass NL. 2012. Induction of lignocellulose-degrading enzymes in Neurospora crassa by cellodextrins. Proc. Natl. Acad. Sci. U.S.A. 109: 6012-6017.
53. Bellemare DR, Sanschagrin M, Beaudoin J, Labbe S. 2001. A novel copper-regulated promoter system for expression of heterologous proteins in Schizosaccharomyces pombe. Gene 273:191-198.
54. Tada S, Gomi K, Kitamoto K, Takahashi K, Tamura G, Hara S. 1991. Construction of a fusion gene comprising the Taka-amylase A promoter and the Escherichia coli beta-glucuronidase gene and analysis of its expression in Aspergillus oryzae. Mol. Gen. Genet. 229:301-306.
55. Shoji JY, Maruyama J, Arioka M, Kitamoto K. 2005. Development of Aspergillus oryzae thiA promoter as a tool for molecular biological studies. FEMS Microbiol. Lett. 244:41-46.
56. Gwynne DI, Buxton FP, Williams SA, Sills AM, Johnstone JA, Buch JK, Guo ZM, Drake D, Westphal M, Davies RW. 1989. Development of an expression system in Aspergillus nidulans. Biochem. Soc. Trans. 17:338-340.
57. Vogt K, Bhabhra R, Rhodes JC, Askew DS. 2005. Doxycycline-regulated gene expression in the opportunistic fungal pathogen Aspergillus fumigatus. BMC Microbiol. 5:1.
58. Wang ZY, Thornton CR, Kershaw MJ, Debao L, Talbot NJ. 2003. The glyoxylate cycle is required for temporal regulation of virulence by the plant pathogenic fungus Magnaporthe grisea. Mol. Microbiol. 47:1601-1612.
59. Harkki A, Mantyla A, Penttila M, Muttilainen S, Buhler R, Suominen P, Knowles J, Nevalainen H. 1991. Genetic engineering of Trichoderma to produce strains with novel cellulase profiles. Enzyme Microb. Technol. 13:227-233.
60. Keranen S, Penttila M. 1995. Production of recombinant proteins in the filamentous fungus Trichoderma reesei. Curr. Opin. Biotechnol. 6:534-537.