COMPASS-Like Complexes Mediate Histone H3 Lysine-4 Trimethylation to Control Floral Transition and Plant Development

English version České info

Histone H3 lysine-4 (H3K4) methylation is associated with transcribed genes in eukaryotes. In Drosophila and mammals, both di- and tri-methylation of H3K4 are associated with gene activation. In contrast to animals, in Arabidopsis H3K4 trimethylation, but not mono- or di-methylation of H3K4, has been implicated in transcriptional activation. H3K4 methylation is catalyzed by the H3K4 methyltransferase complexes known as COMPASS or COMPASS-like in yeast and mammals. Here, we report that Arabidopsis homologs of the COMPASS and COMPASS-like complex core components known as Ash2, RbBP5, and WDR5 in humans form a nuclear subcomplex during vegetative and reproductive development, which can associate with multiple putative H3K4 methyltransferases. Loss of function of ARABIDOPSIS Ash2 RELATIVE (ASH2R) causes a great decrease in genome-wide H3K4 trimethylation, but not in di- or mono-methylation. Knockdown of ASH2R or the RbBP5 homolog suppresses the expression of a crucial Arabidopsis floral repressor, FLOWERING LOCUS C (FLC), and FLC homologs resulting in accelerated floral transition. ASH2R binds to the chromatin of FLC and FLC homologs in vivo and is required for H3K4 trimethylation, but not for H3K4 dimethylation in these loci; overexpression of ASH2R causes elevated H3K4 trimethylation, but not H3K4 dimethylation, in its target genes FLC and FLC homologs, resulting in activation of these gene expression and consequent late flowering. These results strongly suggest that H3K4 trimethylation in FLC and its homologs can activate their expression, providing concrete evidence that H3K4 trimethylation accumulation can activate eukaryotic gene expression. Furthermore, our findings suggest that there are multiple COMPASS-like complexes in Arabidopsis and that these complexes deposit trimethyl but not di- or mono-methyl H3K4 in target genes to promote their expression, providing a molecular explanation for the observed coupling of H3K4 trimethylation (but not H3K4 dimethylation) with active gene expression in Arabidopsis.

Vyšlo v časopise: COMPASS-Like Complexes Mediate Histone H3 Lysine-4 Trimethylation to Control Floral Transition and Plant Development. PLoS Genet 7(3): e32767. doi:10.1371/journal.pgen.1001330
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001330

Souhrn

Zdroje

1. LanF

NottkeAC

ShiY

2008 Mechanisms involved in the regulation of histone lysine demethylases. Curr Opin Cell Biol 20 316 325

2. ShilatifardA

2008 Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation. Curr Opin Cell Biol 20 341 348

3. Santos-RosaH

SchneiderR

BannisterAJ

SherriffJ

BernsteinBE

2002 Active genes are tri-methylated at K4 of histone H3. Nature 419 407 411

4. SchubelerD

MacAlpineDM

ScalzoD

WirbelauerC

KooperbergC

2004 The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev 18 1263 1271

5. BernsteinBE

KamalM

Lindblad-TohK

BekiranovS

BaileyDK

2005 Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120 169 181

6. ZhangX

BernatavichuteYV

CokusS

PellegriniM

JacobsenSE

2009 Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10 R62

7. MillerT

KroganNJ

DoverJ

Erdjument-BromageH

TempstP

2001 COMPASS: a complex of proteins associated with a trithorax-related SET domain protein. Proc Natl Acad Sci U S A 98 12902 12907

8. SchneiderJ

WoodA

LeeJS

SchusterR

DuekerJ

2005 Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol Cell 19 849 856

9. DouY

MilneTA

RuthenburgAJ

LeeS

LeeJW

2006 Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat Struct Mol Biol 13 713 719

10. RuthenburgAJ

AllisCD

WysockaJ

2007 Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol Cell 25 15 30

11. SimsRJ

ReinbergD

2006 Histone H3 Lys 4 methylation: caught in a bind? Genes Dev 20 2779 2786

12. NgHH

RobertF

YoungRA

StruhlK

2003 Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 11 709 719

13. HeY

DoyleMR

AmasinoRM

2004 PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev 18 2774 2784

14. ZhuB

MandalSS

PhamAD

ZhengY

Erdjument-BromageH

2005 The human PAF complex coordinates transcription with events downstream of RNA synthesis. Genes Dev 19 1668 1673

15. OhS

ParkS

van NockerS

2008 Genic and global functions for Paf1c in chromatin modification and gene expression in Arabidopsis. PLoS Genet 4 e1000077 doi:10.1371/journal.pgen.1000077

16. HenikoffS

2008 Nucleosome destabilization in the epigenetic regulation of gene expression. Nat Rev Genet 9 15 26

17. SpringerNM

NapoliCA

SelingerDA

PandeyR

ConeKC

2003 Comparative analysis of SET domain proteins in maize and Arabidopsis reveals multiple duplications preceding the divergence of monocots and dicots. Plant Physiol 132 907 925

18. BaumbuschLO

ThorstensenT

KraussV

FischerA

NaumannK

2001 The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes. Nucleic Acids Res 29 4319 4333

19. Alvarez-VenegasR

AvramovaZ

2005 Methylation patterns of histone H3 Lys 4, Lys 9 and Lys 27 in transcriptionally active and inactive Arabidopsis genes and in atx1 mutants. Nucleic Acids Res 33 5199 5207

20. Alvarez-VenegasR

PienS

SadderM

WitmerX

GrossniklausU

2003 ATX-1, an Arabidopsis homolog of TRITHORAX, activates flower homeotic genes. Curr Biol 13 627 637

21. PienS

FleuryD

MylneJS

CrevillenP

InzeD

2008 ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone H3 lysine-4 trimethylation. Plant Cell 20 580 588

22. TamadaY

YunJY

WooSC

AmasinoRM

2009 ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C. Plant Cell 21 3257 3269

23. BerrA

XuL

GaoJ

CognatV

SteinmetzA

2009 SET DOMAIN GROUP25 encodes a histone methyltransferase and is involved in FLOWERING LOCUS C activation and repression of flowering. Plant Physiol 151 1476 1485

24. JiangD

GuX

HeY

2009 Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. Plant Cell 21 1733 1746

25. MichaelsSD

2009 Flowering time regulation produces much fruit. Curr Opin Plant Biol 12 75 80

26. BaurleI

DeanC

2006 The timing of developmental transitions in plants. Cell 125 655 664

27. ScortecciKC

MichaelsSD

AmasinoRM

2001 Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J 26 229 236

28. RatcliffeOJ

KumimotoRW

WongBJ

RiechmannJL

2003 Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. Plant Cell 15 1159 1169

29. GuX

JiangD

WangY

BachmairA

HeY

2009 Repression of the floral transition via histone H2B monoubiquitination. Plant J 57 522 533

30. SungS

AmasinoRM

2005 REMEMBERING WINTER: Toward a molecular understanding of vernalization. Annu Rev Plant Biol 56 491 508

31. HeY

2009 Control of the transition to flowering by chromatin modifications. Molecular Plant 2 554 564

32. SchubertD

PrimavesiL

BishoppA

RobertsG

DoonanJ

2006 Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. Embo J 25 4638 4649

33. WuK

ZhangL

ZhouC

YuCW

ChaikamV

2008 HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J Exp Bot 59 225 234

34. SchmitzRJ

SungS

AmasinoRM

2008 Histone arginine methylation is required for vernalization-induced epigenetic silencing of FLC in winter-annual Arabidopsis thaliana. Proc Natl Acad Sci U S A 105 411 416

35. WangX

ZhangY

MaQ

ZhangZ

XueY

2007 SKB1-mediated symmetric dimethylation of histone H4R3 controls flowering time in Arabidopsis. Embo J 26 1934 1941

36. LiuC

LuF

CuiX

CaoX

2010 Histone methylation in higher plants. Annu Rev Plant Biol 61 395 420

37. YuX

MichaelsSD

2010 The Arabidopsis Paf1c complex component CDC73 participates in the modification of FLC chromatin. Plant Physiol: 153 1074 1084

38. AqueaF

JohnstonAJ

CanonP

GrossniklausU

Arce-JohnsonP

2010 TRAUCO, a Trithorax-group gene homologue, is required for early embryogenesis in Arabidopsis thaliana. J Exp Bot 61 1215 1224

39. SessionsA

BurkeE

PrestingG

AuxG

McElverJ

2002 A high-throughput Arabidopsis reverse genetics system. Plant Cell 14 2985 2994

40. CraftJ

SamalovaM

BarouxC

TownleyH

MartinezA

2005 New pOp/LhG4 vectors for stringent glucocorticoid-dependent transgene expression in Arabidopsis. Plant J 41 899 918

41. PatelA

VoughtVE

DharmarajanV

CosgroveMS

2008 A conserved arginine-containing motif crucial for the assembly and enzymatic activity of the Mixed Lineage Leukemia Protein-1 core complex. J Biol Chem 283 32162 32175

42. Andreu-VieyraCV

ChenR

AgnoJE

GlaserS

AnastassiadisK

2010 MLL2 is required in oocytes for bulk Histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biol 8 e1000453 doi:10.1371/journal.pbio.1000453

43. SunB

XuY

NgKH

ItoT

2009 A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Genes Dev 23 1791 1804

44. ReddyGV

MeyerowitzEM

2005 Stem-cell homeostasis and growth dynamics can be uncoupled in the Arabidopsis shoot apex. Science 310 663 667

45. JohansonU

WestJ

ListerC

MichaelsS

AmasinoR

2000 Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290 344 347

46. KoJH

MitinaI

TamadaY

HyunY

ChoiY

Growth habit determination by the balance of histone methylation activities in Arabidopsis. Embo J 29 3208 3215

47. KwongRW

BuiAQ

LeeH

KwongLW

FischerRL

2003 LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development. Plant Cell 15 5 18

48. KarimiM

De MeyerB

HilsonP

2005 Modular cloning in plant cells. Trends Plant Sci 10 103 105

49. CurtisMD

GrossniklausU

2003 A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133 462 469

50. JiangD

YangW

HeY

AmasinoRM

2007 Arabidopsis relatives of the human Lysine-Specific Demethylase1 repress the expression of FWA and FLOWERING LOCUS C and thus promote the floral transition. Plant Cell 19 2975 2987

51. WoodCC

RobertsonM

TannerG

PeacockWJ

DennisES

2006 The Arabidopsis thaliana vernalization response requires a Polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc Natl Acad Sci U S A 103 14631 14636

52. JohnsonL

CaoX

JacobsenS

2002 Interplay between two epigenetic marks: DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12 1360 1367