Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis

EMBO Journal

Volumn 24, Issue 7, 2005, Pages 1418-1429

  Naumann, Kathrin ^a   Fischer, Andreas ^a   Hofmann, Ingo ^a   Krauss, Veiko ^b   Phalke, Sameer ^a   Irmler, Kristina ^a   Hause, Gerd ^a   Aurich, Anne Cathleen ^a   Dorn, Rainer ^a   Jenuwein, Thomas ^c   Reuter, Gunter ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

Author keywords

DNA methylation; Gene silencing; Heterochromatin; Histone methylation

Indexed keywords

HISTONE; METHYLTRANSFERASE; SU(VAR) PROTEIN; SUVH PROTEIN; SUVH1 PROTEIN; SUVH2 PROTEIN; UNCLASSIFIED DRUG;

ANGIOSPERM; ARABIDOPSIS; ARTICLE; DEMETHYLATION; DNA METHYLATION; ELECTRON MICROSCOPY; EPIGENETICS; GENE DOSAGE; GENE MUTATION; GENE SILENCING; HETEROCHROMATIN; IMMUNOHISTOCHEMISTRY; MULTIGENE FAMILY; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; TRANSGENE; WESTERN BLOTTING;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; BLOTTING, WESTERN; CROSSES, GENETIC; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA MUTATIONAL ANALYSIS; DNA PRIMERS; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; GENE SILENCING; GENETIC VECTORS; GENOTYPE; HETEROCHROMATIN; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; IMMUNOHISTOCHEMISTRY; LUCIFERASES; METHYLATION; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PHYLOGENY; RHIZOBIUM RADIOBACTER; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS; TRANSFECTION; TRANSGENES;

EID: 17844387167     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600604     Document Type: Article

References (47)

1. Aagaard L, Laible G, Selenko P, Schmid M, Dorn R, Schotta G, Kuhfittig S, Wolf A, Lebersorger A, Singh PB, Reuter G, Jenuwein T (1999) Functional mammalian homologues of the Drosophila PEV-modifier Su(var)3-9 encode centromere-associated proteins which complex with the heterochromatin component M31. EMBO J 18: 1923-1938
2. Alvarez-Venegas R, Pien S, Sadder M, Witmer X, Grossniklaus U, Avramova Z (2003) ATX-1, an Arabidopsis homolog of trithorax, activates flower homeotic genes. Curr Biol 13: 627-637
3. Aoyama T, Chua N-H (1997) A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J 11: 605-612
4. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815
5. Baumbusch LO, Thorstensen T, Krauss V, Fischer A, Naumann K, Assalkhou R, Schulz I, Reuter G, Aalen R (2001) The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionary conserved classes. Nucleic Acid Res 29: 4319-4333
6. Cao X, Jacobsen SE (2002) Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc Natl Acad Sci USA 99: 16491-16498
7. Ebert A, Schotta G, Lein S, Kubicek S, Krauss V, Jenuwein T, Reuter G (2004) Su(var) genes regulate the balance between euchromatin and heterochromatin in Drosophila. Genes Dev 18: 2973-2983
8. Finnegan EJ, Kovac KA (2000) Plant DNA methyltransferases. Plant Mol Biol 43: 189-201
9. Fischle W, Wang Y, Allis CD (2003) Extending the histone code: modification cassettes and switches. Nature 425: 475-479
10. Fransz P, Armstrong S, de Jong JH, Parnell LD, van Drunen C, Dean C, Zabel P, Bisseling T, Jones GH (2000) Integrated cytogenetic map of chromosome arm 4S of A. thaliana: structural organization of heterochromatic knob and centromere regions. Cell 100: 367-376
11. Gendrel A-V, Lippman Z, Yordan C, Colot V, Martienssen RA (2002) Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297: 1871-1873
12. Goodrich J, Puangsomiee P, Martin M, Long D, Meyerowitz E, Coupland G (1997) A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386: 44-51
13. Grossniklaus U, Vielle-Calzada JP, Hoeppner MA, Gagliano WB (1998) Maternal control of embryogenesis by MEDEA, a Polycomb group gene in Arabidopsis. Science 280: 446-450
14. Grunau G, Clark SJ, Rosenthal A (2001) Bisulfite genomic sequencing: systematic investigation of critical experimental parameters. Nucleic Acid Res 29: e65
15. Hause G, Hahn H (1998) Cytological characterization of multicellular structures in embryogenic microspore cultures of Brassica napus L. Bot Acta 111: 204-211
16. Ivanova AV, Bonaduce MJ, Ivanov SV, Klar AJS (1998) The chromo and SET domains of the Clr4 protein are essential for silencing in fission yeast. Nat Genet 19: 192-195
17. Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPONITE histone H3 methyltransferase. Nature 416: 556-560
18. Jasencakova Z, Soppe WJJ, Meister A, Gernand D, Turner B, Schubert I (2003) Histone modification in Arabidopsis-high methylation of H3 lysine 9 is dispensable for constitutive heterochromatin. Plant J 33: 471-480
19. Jeddeloh JA, Stokes TL, Richards FJ (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22: 94-97
20. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293: 1074-1080
21. Jenuwein T, Laible G, Dorn R, Reuter G (1998) SET domain proteins modulate chromatin domains in eu- and heterochromatin. Cell Mol Life Sci 54: 80-93
22. Johnson LM, Vao X, Jacobsen SE (2002) Interplay between two epigenetic marks: DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12: 1360-1367
23. Koncz C, Schell J (1986) The promotor of TL-DNA gene 5 controls the tissue specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204: 383-396
24. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116-120
25. Lindroth MA, Shultis D, Jasencakova Z, Fuchs J, Johnson L, Schubert D, Patnaik D, Pradhan S, Goodrich J, Schubert I, Jenuwein T, Khorasanizadeh S, Jacobsen SE (2004) Dual histone H3 methylation marks at lysine 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J 23: 4146-4155
26. Malagnac F, Bartee L, Bender J (2002) An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J 21: 6842-6852
27. Martienssen RA, Colot V (2001) DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293: 1070-1074
28. Mindrinos M, Katagiri F, Yu GL, Asubel FM (1994) The A. thaliana disease resistance gene RPS encodes a protein containing nucleotide-binding site and leucine-rich repeats. Cell 78: 1089-1099
29. Mittelsten Scheid O, Asfar K, Paszkowski J (1998) Release of epigenetic silencing by trans-acting mutations in Arabidopsis. Proc Natl Acad Sci USA 95: 632-637
30. Nakayama J, Rice JD, Strahl BD, Allis CD, Grewal SIS (2001) Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292: 110-113
31. Neff MM, Neff JD, Chory J, Pepper AE (1998) DCAPS a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J 14: 387-392
32. Pandey R, Muller A, Napoli CA, Selinger DA, Pikaard CS, Richards EJ, Bender J, Mount DW, Jorgensen RA (2002) Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acid Res 30: 5036-5055
33. Peters AHFM, Kubicek S, Mechtler K, O'Sullivan J, Derijck AAHA, Perez-Burgos L, Kohlmaier A, Opravil S, Tachibana M, Shinkai Y, Martens JHA, Jenuwein T (2003) Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell 12: 1577-1589
34. Peters AHFM, O'Carroll D, Scherthan H, Mechtler K, Sauer S, Schöfer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, Opravil S, Doyle M, Sibilia M, Jenuwein T (2001) Loss of the Suv39h histone methyltransferase impairs mammalian heterochromatin and genome stability. Cell 107: 323-337
35. Rea S, Eisenhaber F, O'Carroll D, Strahl BD, Sun Z-W, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, Jenuwein T (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406: 593-599
36. Schotta G, Ebert A, Krauss V, Fischer A, Hoffmann J, Rea S, Jenuwein T, 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
37. Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, Reuter G, Reinberg D, Jenuwein T (2004) A silencing pathway to induce H3-K9 and H4-K20 tri-methylation at constitutive heterochromatin. Genes Dev 18: 1251-1262
38. Selker EU (2002) Repeat-induced gene silencing in fungi. Adv Genet 46: 439-450
39. Soppe WJ, Jasencakova Z, Houben A, Kakutani T, Meister A, Huang MS, Jacobsen SE, Schubert I, Fransz P (2002) DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J 21: 6549-6559
40. Stahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41-45
41. Tamaru H, Selker EU (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414: 277-283
42. Tariq M, Saze H, Probst A, Lichota J, Habu Y, Paszkowski J (2003) Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin. Proc Natl Acad Sci USA 100: 8823-8827
43. Töpfer R, Matzeit V, Gronenborn B, Schell J, Steinbiss HH (1987) A set of plant expression vectors for transcriptional and translational fusions. Nucleic Acids Res 15: 5890
44. Tschiersch B, Hofmann A, Krauss V, Dorn R, Korge G, Reuter G (1994) The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J 13: 3822-3831
45. Vielle-Calcada JP, Thomas J, Spillane C, Coluccio A, Hoeppner MA, Grossniklaus U (1999) Maintenance of genomic imprinting at the Arabidopsis MEDEA locus requires zygotic DDM1 activity. Genes Dev 13: 2971-2982
46. Vongs A, Kakutani T, Matienssen RA, Richards EJ (1993) Arabidopsis thaliana DNA methylation mutants. Science 260: 1926-1928
47. Zemach A, Grafi G (2003) Characterization of Arabidopsis thaliana methyl-CpG-binding domain (MBD) proteins. Plant J 34: 565-572