#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

MoSET1 (Histone H3K4 Methyltransferase in ) Regulates Global Gene Expression during Infection-Related Morphogenesis


This paper provides two major contributions to the field of genetics. First, we systematically studied the biological roles of eight histone lysine methyltransferase (KMT) genes in the phytopathogenic fungus Magnaporthe oryzae. We investigated their roles, especially focusing on their involvement in infection-related morphogenesis and pathogenicity. The results showed that the eight KMTs were involved in various infection processes to varying degrees, and that MoSET1, one of the KMTs catalyzing methylation at histone H3 lysine 4 (H3K4), had the largest impact on the pathogenicity of the fungus. Second, we focused on the role of MoSET1 in global gene regulation. H3K4 methylation is generally believed to be an epigenetic mark for gene activation in higher eukaryotes. However, in Saccharomyces cerevisiae, SET1 was originally characterized as being required for transcriptional silencing of silent mating-type loci. We addressed this apparent discrepancy by examining genome-wide gene expression and H3K4 methylation during infection-related morphogenesis in M. oryzae. RNA-seq analysis of a MoSET1 deletion mutant revealed that MoSET1 was indeed required for proper gene activation and repression. ChIP-seq analyses of H3K4 methylation and MoSET1 suggested that MoSET1 could directly play a role in gene activation while MoSET1-dependent gene repression may be caused by indirect effects.


Vyšlo v časopise: MoSET1 (Histone H3K4 Methyltransferase in ) Regulates Global Gene Expression during Infection-Related Morphogenesis. PLoS Genet 11(7): e32767. doi:10.1371/journal.pgen.1005385
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005385

Souhrn

This paper provides two major contributions to the field of genetics. First, we systematically studied the biological roles of eight histone lysine methyltransferase (KMT) genes in the phytopathogenic fungus Magnaporthe oryzae. We investigated their roles, especially focusing on their involvement in infection-related morphogenesis and pathogenicity. The results showed that the eight KMTs were involved in various infection processes to varying degrees, and that MoSET1, one of the KMTs catalyzing methylation at histone H3 lysine 4 (H3K4), had the largest impact on the pathogenicity of the fungus. Second, we focused on the role of MoSET1 in global gene regulation. H3K4 methylation is generally believed to be an epigenetic mark for gene activation in higher eukaryotes. However, in Saccharomyces cerevisiae, SET1 was originally characterized as being required for transcriptional silencing of silent mating-type loci. We addressed this apparent discrepancy by examining genome-wide gene expression and H3K4 methylation during infection-related morphogenesis in M. oryzae. RNA-seq analysis of a MoSET1 deletion mutant revealed that MoSET1 was indeed required for proper gene activation and repression. ChIP-seq analyses of H3K4 methylation and MoSET1 suggested that MoSET1 could directly play a role in gene activation while MoSET1-dependent gene repression may be caused by indirect effects.


Zdroje

1. Strathl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41–45. 10638745

2. Shilatifard A (2008) Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation. Curr Opin Cell Biol 20: 341–8. doi: 10.1016/j.ceb.2008.03.019 18508253

3. Lachner M, Jenuwein T (2002) The many faces of histone lysine methylation. Curr Opin Cell Biol 14: 286–98. 12067650

4. Copeland RA, Solomon ME, Richon VM (2009) Protein methyltransferases as a target class for drug discovery. Nat Rev Drug Discov 8: 724–732. doi: 10.1038/nrd2974 19721445

5. Bedford MT, Richard S (2005) Arginine methylation an emerging regulator of protein function. Mol Cell 18: 263–272. 15866169

6. Allis CD, Berger SL, Cote J, Dent S, Jenuwien T, Kouzarides T, Pillus L, Reinberg D, Shi Y, Shiekhattar R, Shilatifard A, Workman J, Zhang Y (2007) New nomenclature for chromatin-modifying enzymes. Cell 131: 633–636. 18022353

7. Schotta G1, Ebert A, Krauss V, Fischer A, Hoffmann J, Rea S, Jenuwein T, Dorn R, Reuter G (2002) Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J. 21:1121–1131. 11867540

8. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI (2001) Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292:110–113. 11283354

9. Tamaru H, Selker EU (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414: 277–283. 11713521

10. 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. 9398665

11. Mozer BA, Dawid IB (1989) Cloning and molecular characterization of the trithorax locus of Drosophila melanogaster. Proc Nat Acad Sci USA 86: 3738–3742. 2566995

12. Mareike A, Kristian H (2010) Histone methyltransferases in cancer. Semin Cell Dev Biol 21: 209–220 doi: 10.1016/j.semcdb.2009.10.007 19892027

13. Zhou Z, Rune T, Søren K, Anders LN (2010) The NSD3L histone methyltransferase regulates cell cycle and cell invasion in breast cancer cells. Biochem Biophys Res Commun 398: 565–570. doi: 10.1016/j.bbrc.2010.06.119 20599755

14. Tamaru H, Zhang X, McMillen D, Singh PB, Nakayama J, Grewal SI, Allis CD, Cheng X, Selker EU (2003) Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet 34:75–79. 12679815

15. Zachary AL, Adhvaryu KK, Honda S, Shiver A, Selker UE (2010) Identification of DIM-7, a protein required to target the DIM-5 H3 methyltransferase to chromatin. Proc Nat Acad Sci USA 107: 8310–8315. doi: 10.1073/pnas.1000328107 20404183

16. Keyur KA, Morris SA, Strahl BD, Selker EU (2005) Methylation of histone H3 Lysine 36 is required for normal development in Neurospora crassa. Eukaryot Cell 4: 1455–1464. 16087750

17. Jamieson K1, Rountree MR, Lewis ZA, Stajich JE, Selker EU (2013) Regional control of histone H3 lysine 27 methylation in Neurospora. Proc Nat Acad Sci USA 110:6027–6032. doi: 10.1073/pnas.1303750110 23530226

18. Connolly LR, Smith KM, Freitag M. (2013) The Fusarium graminearum histone H3 K27 methyltransferase KMT6 regulates development and expression of secondary metabolite gene clusters. PLoS Genet 9:e1003916. doi: 10.1371/journal.pgen.1003916 24204317

19. Chujo T, Scott B. (2014) Histone H3K9 and H3K27 methylation regulates fungal alkaloid biosynthesis in a fungal endophyte-plant symbiosis. Mol Microbiol 92:413–34 doi: 10.1111/mmi.12567 24571357

20. Soyer JL, El Ghalid M, Glaser N, Ollivier B, Linglin J, Grandaubert J, Balesdent MH, Connolly LR, Freitag M, Rouxel T, Fudal I. (2014) Epigenetic control of effector gene expression in the plant pathogenic fungus Leptosphaeria maculans. PLoS Genet 10:e1004227. doi: 10.1371/journal.pgen.1004227 24603691

21. 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. doi: 10.1038/nchembio.177 19448638

22. 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. Peer J 1: e4. doi: 10.7717/peerj.4 23638376

23. 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. 11751634

24. 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. doi: 10.1101/gad.458008 18316478

25. Cheng J1, Blum R1, Bowman C1, Hu D, Shilatifard A, Shen S, Dynlacht BD (2014) A role for H3K4 monomethylation in gene repression and partitioning of chromatin readers. Mol Cell 2014 53:979–992.

26. Xu JR, Zhao X, Dean RA (2007) From genes to genomes; a new paradigm for studying fungal pathogenesis in Magnaporthe oryzae. Adv Genet 57: 175–218. 17352905

27. Wilson RA, Talbot NJ (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol 7: 185–195. doi: 10.1038/nrmicro2032 19219052

28. 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, RL-SAGE, and oligo array methods. BMC Genomics 7: 310. 17156450

29. Mathioni SM, Belo A, Rizzo CJ, Dean RA, Donofrio NM (2011) Transcriptome profiling of the rice blast fungus during invasive plant infection and in vitro stress. BMC Genomics. 12:49. doi: 10.1186/1471-2164-12-49 21247492

30. Soanes DM, Chakrabarti A, Paszkiewicz KH, Dawe AL, Talbot NJ (2012) Genome-wide transcriptional profiling of appressorium development by the rice blast fungus Magnaporthe oryzae. PloS Pathogen 8: e1002514.

31. Vu VB, Pham TMK, Nakayashiki H (2013) Substrate-induced transcriptional activation of the MoCel7C cellulase gens is associated with methylation of histone H3 at lysine 4 in the rice blast fungus Magnaporthe oryzae. Appl Environ Microbiol 79: 6823–6832. doi: 10.1128/AEM.02082-13 23995923

32. Fu J, Hettler E, Wickes BL (2005) Split marker transformation increases homologous integration frequency in Cryptococcus neoformans. Fungal Genet Biol 43: 200–212

33. Hyon G, Nguyen TTN, Chuma I, Inoue Y, Asano H, Murata N, Kusaba M, Tosa Y (2012) Charaterization of interactions between barley and various host-specific subgroups of Magnaporthe oryzae and M. grisea. J Gen Plant Pathol 78: 237–246.

34. Ngueyn QB, Kadotani N, Kasahara S, Tosa Y, Mayama S, Nakayashiki H (2008) Systemic functional analysis of calcium signaling protein in the genome of the rice blast fungus, Magnaporthe oryzae, using a high-throughput RNA silencing system. Mol Microbiol 68: 1348–1365. doi: 10.1111/j.1365-2958.2008.06242.x 18433453

35. Gilbert RD, Johnson AM, Dean RA (1996) Chemical signals responsible for appressoirum formation n the rice blast fungus M. grisea. Physiol Mol Plant Pathol 48: 335–346.

36. Lee YH, Dean RA (1993) cAMP regulates infection structure formation in the plant pathogenic fungus Magnaporthegrisea. Plant Cell 5: 693–700. 12271080

37. Mitchell TK, Dean RA (2005) The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe oryzae. Plant Cell 7: 1869–1878.

38. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10: 57–63. doi: 10.1038/nrg2484 19015660

39. 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. 16122420

40. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823–837. 17512414

41. Van DK, Ding Y, Malkaram S, Riethoven JJ, Liu R, Yang J, Laczko P, Chen H, Xia Y, Ladunga I, Avramova Z, Fromm M (2010) Dynamic changes in genome-wide histone H3 lysine 4 methylation patterns in response to dehydration stress in Arabidopsis thaliana. BMC Plant Biol 10: 238. doi: 10.1186/1471-2229-10-238 21050490

42. Gilbert MJ, Thornton CR, Wakley GE, Talbot NJ (2006) A P-type ATPase required for rice blast disease and induction of host resistance. Nature 440: 535–539. 16554820

43. James TC, Elgin SC (1986) Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol Cell Biol 6: 3862–3872. 3099166

44. Bannister AJ, Schneider R, Myers FA, Thorne AW, Crane-Robinson C, Kouzarides T (2005) Spatial distribution of di- and tri-methyl lysine 36 of histone H3 at active genes. J Biol Chem 280: 17732–17736. 15760899

45. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130: 77–88. 17632057

46. Gregory GD, Vakoc CR, Rozovskaia T, Zheng X, Patel S, Nakamura T, Canaani E, Blobel GA (2007) Mammalian ASH1L is a histone methyltransferase that occupies the transcribed region of active genes. Mol Cell Biol 27: 8466–8479. 17923682

47. Tanaka Y, Kawahashi K, Katagiri Z, Nakayama Y, Mahajan M, Kioussis D (2011) Dual function of histone H3 lysine 36 methyltransferase ASH1 in regulation of Hox gene expression. PLoS ONE 6: e28171. doi: 10.1371/journal.pone.0028171 22140534

48. Jeon J, Goh J, Yoo S, Chi MH, Choi J, Rho HS, Park J, Han SS, Kim BR, Park SY, Kim S, Lee YH (2008) A putative MAP kinase kinase kinase, MCK1, is required for cell wall integrity and pathogenicity of the rice blast fungus, Magnaporthe oryzae. Mol Plant Microbe Interact 21: 525–34. doi: 10.1094/MPMI-21-5-0525 18393612

49. Liu XH, Lu JP, Zhang L, Dong B, Min H, Lin FC (2007) Involvement of a Magnaporthe grisea serine/threonine kinase gene, MgATG1, in appressorium turgor and pathogenesis. Eukaryot Cell 6: 997–1005. 17416896

50. Nguyen BQ, Itoh K, Vu VB, Nakayashiki H (2012) Simultaneous silencing of endo-β-1,4xylanase genes reveals their roles in the virulence of Magnaporthe oryzae. Mol Microbiol 81: 1008–1019.

51. Vu VB, Itoh K, Nguyen BQ, Tosa Y, Nakayashiki H (2012) Cellulose belonging to glycoside hydrolase family 6 ans 7 contribute to the virulence of Magnaporthe oryzae. Mol Plant Microbe Interact 25: 1135–1141. doi: 10.1094/MPMI-02-12-0043-R 22852807

52. 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. doi: 10.1074/jbc.M112.359935 23319591

53. 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 homolog of retrotransposon MGR583. Annu Phytopathol Soc Jpn 65: 429–436.

54. Nakayashiki H, Kiyotomi K, Tosa Y, Mayama S (1999) Transposition of the retrotransposon MAGGY in heterologous species of filamentous fungi. Genetics 153: 693–703 10511549

55. Morita Y1, 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 alternate Japanese pear pathotype. Mol Plant Pathol. 14:365–378. doi: 10.1111/mpp.12013 23279187

56. Kadotani N, Nakayashiki H, Tosa Y, Mayama S (2003) RNA silencing in the phytopathogenic fungus Magnaporthe oryzae. Mol Plant Microbe Interact 16: 769–775. 12971600

57. Murakami J, Tosa Y, Kataoka T, Tomita R, Kawasaki J, Chuma I, et al. (2000) Analysis of host species specificity of Magnaporthe grisea toward wheat using a genetic cross between isolates from wheat and foxtail milliet. Phytopathology 90: 1060–1067. doi: 10.1094/PHYTO.2000.90.10.1060 18944467

58. Zhang SW, Mayama S, Tosa Y (2008) Identification of two genes for resistance to Triticum isolates of Maganporthe oryzae in wheat. Genome 56: 216–221.

59. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2011) TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology 14:R36.

60. Li H., Durbin R. (2009) Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics 25:1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

61. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative Genomics Viewer. Nature Biotechnology 29:24–26. doi: 10.1038/nbt.1754 21221095

62. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140 doi: 10.1093/bioinformatics/btp616 19910308

63. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.

64. Robinson MD, Oshlack A (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biology 11:R25. doi: 10.1186/gb-2010-11-3-r25 20196867

65. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57: 289–300.

66. Falcon S., Gentleman R. (2007) Using GOstats to test gene lists for GO term association. Bioinformatics 23:257–258. 17098774

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 7
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#