#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

H3K27me3 Profiling of the Endosperm Implies Exclusion of Polycomb Group Protein Targeting by DNA Methylation


Polycomb group (PcG) proteins act as evolutionary conserved epigenetic mediators of cell identity because they repress transcriptional programs that are not required at particular developmental stages. Each tissue is likely to have a specific epigenetic profile, which acts as a blueprint for its developmental fate. A hallmark for Polycomb Repressive Complex 2 (PRC2) activity is trimethylated lysine 27 on histone H3 (H3K27me3). In plants, there are distinct PRC2 complexes for vegetative and reproductive development, and it was unknown so far whether these complexes have target gene specificity. The FERTILIZATION INDEPENDENT SEED (FIS) PRC2 complex is specifically expressed in the endosperm and is required for its development; loss of FIS function causes endosperm hyperproliferation and seed abortion. The endosperm nourishes the embryo, similar to the physiological function of the placenta in mammals. We established the endosperm H3K27me3 profile and identified specific target genes of the FIS complex with functional roles in endosperm cellularization and chromatin architecture, implicating that distinct PRC2 complexes have a subset of specific target genes. Importantly, our study revealed that selected transposable elements and protein coding genes are specifically targeted by the FIS PcG complex in the endosperm, whereas these elements and genes are densely marked by DNA methylation in vegetative tissues, suggesting that DNA methylation prevents targeting by PcG proteins in vegetative tissues.


Vyšlo v časopise: H3K27me3 Profiling of the Endosperm Implies Exclusion of Polycomb Group Protein Targeting by DNA Methylation. PLoS Genet 6(10): e32767. doi:10.1371/journal.pgen.1001152
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001152

Souhrn

Polycomb group (PcG) proteins act as evolutionary conserved epigenetic mediators of cell identity because they repress transcriptional programs that are not required at particular developmental stages. Each tissue is likely to have a specific epigenetic profile, which acts as a blueprint for its developmental fate. A hallmark for Polycomb Repressive Complex 2 (PRC2) activity is trimethylated lysine 27 on histone H3 (H3K27me3). In plants, there are distinct PRC2 complexes for vegetative and reproductive development, and it was unknown so far whether these complexes have target gene specificity. The FERTILIZATION INDEPENDENT SEED (FIS) PRC2 complex is specifically expressed in the endosperm and is required for its development; loss of FIS function causes endosperm hyperproliferation and seed abortion. The endosperm nourishes the embryo, similar to the physiological function of the placenta in mammals. We established the endosperm H3K27me3 profile and identified specific target genes of the FIS complex with functional roles in endosperm cellularization and chromatin architecture, implicating that distinct PRC2 complexes have a subset of specific target genes. Importantly, our study revealed that selected transposable elements and protein coding genes are specifically targeted by the FIS PcG complex in the endosperm, whereas these elements and genes are densely marked by DNA methylation in vegetative tissues, suggesting that DNA methylation prevents targeting by PcG proteins in vegetative tissues.


Zdroje

1. SchuettengruberB

CavalliG

2009 Recruitment of Polycomb group complexes and their role in the dynamic regulation of cell fate choice. Development 136 3531 3542

2. HennigL

DerkachevaM

2009 Diversity of Polycomb group complexes in plants: same rules, different players? Trends Genet 25 414 423

3. ChaudhuryAM

MingL

MillerC

CraigS

DennisES

1997 Fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci USA 94 4223 4228

4. CostaLM

Gutierrez-MarcosJF

DickinsonHG

2004 More than a yolk: the short life and complex times of the plant endosperm. Trends Plant Sci 9 507 514

5. KöhlerC

MakarevichG

2006 Epigenetic mechanisms governing seed development in plants. EMBO Rep 7 1223 1227

6. KöhlerC

HennigL

SpillaneC

PienS

GruissemW

2003 The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev 17 1540 1553

7. MakarevichG

LeroyO

AkinciU

SchubertD

ClarenzO

2006 Different Polycomb group complexes regulate common target genes in Arabidopsis. EMBO Rep 7 947 952

8. BarouxC

GagliardiniV

PageDR

GrossniklausU

2006 Dynamic regulatory interactions of Polycomb group genes: MEDEA autoregulation is required for imprinted gene expression in Arabidopsis. Genes Dev 20 1081 1086

9. GehringM

HuhJH

HsiehTF

PentermanJ

ChoiY

2006 DEMETER DNA glycosylase establishes MEDEA Polycomb gene self-imprinting by allele-specific demethylation. Cell 124 495 506

10. JullienPE

KatzA

OlivaM

OhadN

BergerF

2006 Polycomb group complexes self-regulate imprinting of the Polycomb group gene MEDEA in Arabidopsis. Curr Biol 16 486 492

11. ZhangX

ClarenzO

CokusS

BernatavichuteYV

PellegriniM

2007 Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5 e129 doi:10.1371/journal.pbio.0050129

12. SantosF

HendrichB

ReikW

DeanW

2002 Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 241 172 182

13. HsiehTF

IbarraCA

SilvaP

ZemachA

Eshed-WilliamsL

2009 Genome-wide demethylation of Arabidopsis endosperm. Science 324 1451 1454

14. GehringM

BubbKL

HenikoffS

2009 Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324 1447 1451

15. JullienPE

MosqunaA

IngouffM

SakataT

OhadN

2008 Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. PLoS Biol 6 e194 doi:10.1371/journal.pbio.0060194

16. ChoiY

GehringM

JohnsonL

HannonM

HaradaJJ

2002 DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110 33 42

17. MosherRA

MelnykCW

KellyKA

DunnRM

StudholmeDJ

2009 Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature 460 283 286

18. MosherRA

MelnykCW

2010 siRNAs and DNA methylation: seedy epigenetics. Trends Plant Sci 15 204 210

19. 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

20. YuanGC

LiuYJ

DionMF

SlackMD

WuLF

2005 Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309 626 630

21. OzsolakF

SongJS

LiuXS

FisherDE

2007 High-throughput mapping of the chromatin structure of human promoters. Nat Biotechnol 25 244 248

22. SpiesN

NielsenCB

PadgettRA

BurgeCB

2009 Biased chromatin signatures around polyadenylation sites and exons. Mol Cell 36 245 254

23. KöhlerC

PageDR

GagliardiniV

GrossniklausU

2005 The Arabidopsis thaliana MEDEA Polycomb group protein controls expression of PHERES1 by parental imprinting. Nat Genet 37 28 30

24. GehringM

HuhJH

HsiehTF

PentermanJ

ChoiY

2006 DEMETER DNA glycosylase establishes MEDEA Polycomb gene self-imprinting by allele-specific demethylation. Cell 124 495 506

25. MathieuO

ProbstAV

PaszkowskiJ

2005 Distinct regulation of histone H3 methylation at lysines 27 and 9 by CpG methylation in Arabidopsis. EMBO J 24 2783 2791

26. KangIH

SteffenJG

PortereikoMF

LloydA

DrewsGN

2008 The AGL62 MADS domain protein regulates cellularization during endosperm development in Arabidopsis. Plant Cell 20 635 647

27. ErilovaA

BrownfieldL

ExnerV

RosaM

TwellD

2009 Imprinting of the Polycomb group gene MEDEA serves as a ploidy sensor in Arabidopsis. PLoS Genet 5 e1000663 doi:10.1371/journal.pgen.1000663

28. MinicZ

JouaninL

2006 Plant glycoside hydrolases involved in cell wall polysaccharide degradation. Plant Physiol Biochem 44 435 449

29. SorensenMB

ChaudhuryAM

RobertH

BancharelE

BergerF

2001 Polycomb group genes control pattern formation in plant seed. Curr Biol 11 277 281

30. SchmidM

DavisonTS

HenzSR

PapeUJ

DemarM

2005 A gene expression map of Arabidopsis thaliana development. Nat Genet 37 501 506

31. DealRB

HenikoffS

2010 A simple method for gene expression and chromatin profiling of individual cell types within a tissue. Dev Cell 18 1030 1040

32. Boisnard-LorigC

Colon-CarmonaA

BauchM

HodgeS

DoernerP

2001 Dynamic analyses of the expression of the histone::YFP fusion protein in Arabidopsis show that syncytial endosperm is divided in mitotic domains. Plant Cell 13 495 509

33. MohnF

SchübelerD

2009 Genetics and epigenetics: stability and plasticity during cellular differentiation. Trends Genet 25 129 136

34. BrackenAP

DietrichN

PasiniD

HansenKH

HelinK

2006 Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 20 1123 1136

35. SquazzoSL

O'GeenH

KomashkoVM

KrigSR

JinVX

2006 Suz12 binds to silenced regions of the genome in a cell-type-specific manner. Genome Res 16 890 900

36. RingroseL

ParoR

2007 Polycomb/Trithorax response elements and epigenetic memory of cell identity. Development 134 223 232

37. PellouxJ

RusterucciC

MellerowiczEJ

2007 New insights into pectin methylesterase structure and function. Trends Plant Sci 12 267 277

38. KirmizisA

BartleySM

KuzmichevA

MargueronR

ReinbergD

2004 Silencing of human Polycomb target genes is associated with methylation of histone H3 Lys 27. Genes Dev 18 1592 1605

39. SchwartzYB

KahnTG

StenbergP

OhnoK

BourgonR

2010 Alternative epigenetic chromatin states of Polycomb target genes. PLoS Genet 6 e1000805 doi:10.1371/journal.pgen.1000805

40. NaumannK

FischerA

HofmannI

KraussV

PhalkeS

2005 Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis. EMBO J 24 1418 1429

41. LindrothAM

ParkYJ

McLeanCM

DokshinGA

PerssonJM

2008 Antagonism between DNA and H3K27 methylation at the imprinted Rasgrf1 locus. PLoS Genet 4 e1000145 doi:10.1371/journal.pgen.1000145

42. SazeH

ScheidOM

PaszkowskiJ

2003 Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet 34 65 69

43. WeigelD

GlazebrookJ

2002 Arabidopsis-a laboratory manual New York Cold Spring Harbor Laboratory Press

44. SimonP

2003 Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics 19 1439 1440

45. AcevedoLG

IniguezAL

HolsterHL

ZhangX

GreenR

2007 Genome-scale ChIP-chip analysis using 10,000 human cells. Biotechniques 43 791 797

46. RehrauerH

AquinoC

GruissemW

HenzS

HilsonP

2010 AGRONOMICS1 - A new resource for Arabidopsis transcriptome profiling. Plant Physiol 152 487 499

47. R Core Development Team 2009 A language and environment for statistical computing Vienna R foundation for statistical computing

48. JohnsonWE

LiW

MeyerCA

GottardoR

CarrollJS

2006 Model-based analysis of tiling-arrays for ChIP-chip. Proc Natl Acad Sci USA 103 12457 12462

49. BengtssonH

SimpsonK

BullardJ

HansenK

2008 Aroma.affymetrix: A generic framework in R for analyzing small to very large Affymetrix data sets in bounded memory Berkeley Department of Statistics

50. GottardoR

LiW

JohnsonWE

LiuXS

2008 A flexible and powerful bayesian hierarchical model for ChIP-Chip experiments. Biometrics 64 468 478

51. NicolJW

HeltGA

BlanchardSGJr

RajaA

LoraineAE

2009 The Integrated Genome Browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics 25 2730 2731

52. WuZ

IrizarryRA

GentlemanR

MurilloFM

SpencerF

2003 A model based background adjustment for oligonucleotide expression arrays Baltimore John Hopkins University, Department of Biostatistics

53. BreitlingR

ArmengaudP

AmtmannA

HerzykP

2004 Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 573 83 92

54. SaeedAI

SharovV

WhiteJ

LiJ

LiangW

2003 TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34 374 378

55. BenjaminiY

HochbergY

1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Ser B 57 289 300

56. ZilbermanD

GehringM

TranRK

BallingerT

HenikoffS

2007 Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39 61 69

57. 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

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2010 Číslo 10
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#