AL PHD-PRC1 Complexes Promote Seed Germination through H3K4me3-to-H3K27me3 Chromatin State Switch in Repression of Seed Developmental Genes

English version České info

Seed germination and subsequent seedling growth define crucial steps for entry into the plant life cycle. For those events to take place properly, seed developmental genes need to be silenced whereas vegetative growth genes are activated. Chromatin structure is generally known to play crucial roles in gene transcription control. However, the transition between active and repressive chromatin states during seed germination is still poorly characterized and the underlying molecular mechanisms remain largely unknown. Here we identified the Arabidopsis PHD-domain H3K4me3-binding ALFIN1-like proteins (ALs) as novel interactors of the Polycomb Repressive Complex 1 (PRC1) core components AtBMI1b and AtRING1a. The interactions were confirmed by diverse in vitro and in vivo assays and were shown to require the AL6 N-terminus containing PAL domain conserved in the AL family proteins and the AtRING1a C-terminus containing RAWUL domain conserved in animal and plant PRC1 ring-finger proteins (including AtRNIG1a/b and AtBMI1a/b). By T-DNA insertion mutant analysis, we found that simultaneous loss of AL6 and AL7 as well as loss of AtBMI1a and AtBMI1b retards seed germination and causes transcriptional derepression and a delayed chromatin state switch from H3K4me3 to H3K27me3 enrichment of several seed developmental genes (e.g. ABI3, DOG1, CRU3, CHO1). We found that AL6 and the PRC1 H3K27me3-reader component LHP1 directly bind at ABI3 and DOG1 loci. In light of these data, we propose that AL PHD-PRC1 complexes, built around H3K4me3, lead to a switch from the H3K4me3-associated active to the H3K27me3-associated repressive transcription state of seed developmental genes during seed germination. Our finding of physical interactions between PHD-domain proteins and PRC1 is striking and has important implications for understanding the connection between the two functionally opposite chromatin marks: H3K4me3 in activation and H3K27me3 in repression of gene transcription.

Vyšlo v časopise: AL PHD-PRC1 Complexes Promote Seed Germination through H3K4me3-to-H3K27me3 Chromatin State Switch in Repression of Seed Developmental Genes. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1004091
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004091

Souhrn

Zdroje

1. BentsinkL, KoornneefM (2008) Seed dormancy and germination. Arabidopsis Book 6: e0119.

2. KoornneefM, HanhartCJ, HilhorstHW, KarssenCM (1989) In vivo inhibition of seed development and reserve protein accumulation in recombinants of abscisic acid biosynthesis and responsiveness mutants in Arabidopsis thaliana. Plant Physiol 90 : 463–469.

3. GiraudatJ, HaugeBM, ValonC, SmalleJ, ParcyF, et al. (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4 : 1251–1261.

4. ParcyF, ValonC, RaynalM, Gaubier-ComellaP, DelsenyM, et al. (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6 : 1567–1582.

5. MönkeG, SeifertM, KeilwagenJ, MohrM, GrosseI, et al. (2012) Toward the identification and regulation of the Arabidopsis thaliana ABI3 regulon. Nucleic Acids Res 40 : 8240–8254.

6. Alonso-BlancoC, BentsinkL, HanhartCJ, Blankestijn-de VriesH, et al. (2003) Analysis of natural allelic variation at seed dormancy loci of Arabidopsis thaliana. Genetics 164 : 711–729.

7. BentsinkL, JowettJ, HanhartCJ, KoornneefM (2006) Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc Natl Acad Sci U S A 103 : 17042–17047.

8. NakabayashiK, BartschM, XiangY, MiattonE, PellengahrS, et al. (2012) The time required for dormancy release in Arabidopsis is determined by DELAY OF GERMINATION1 protein levels in freshly harvested seeds. Plant Cell 24 : 2826–2838.

9. HaslekasC, VikenMK, GriniPE, NygaardV, NordgardSH, et al. (2003) Seed 1-cysteine peroxiredoxin antioxidants are not involved in dormancy, but contribute to inhibition of germination during stress. Plant Physiol 133 : 1148–1157.

10. YamagishiK, TatematsuK, YanoR, PrestonJ, KitamuraS, et al. (2009) CHOTTO1, a double AP2 domain protein of Arabidopsis thaliana, regulates germination and seedling growth under excess supply of glucose and nitrate. Plant Cell Physiol 50 : 330–340.

11. AichingerE, VillarCB, FarronaS, ReyesJC, HennigL, et al. (2009) CHD3 proteins and Polycomb group proteins antagonistically determine cell identity in Arabidopsis. PLoS Genet 5: e1000605.

12. BouyerD, RoudierF, HeeseM, AndersenED, GeyD, et al. (2011) Polycomb Repressive Complex 2 controls the embryo-to-seedling phase transition. PLoS Genet 7: e1002014.

13. KimSY, LeeJ, Eshed-WilliamsL, ZilbermanD, SungZR (2012) EMF1 and PRC2 cooperate to repress key regulators of Arabidopsis development. PLoS Genet 8: e1002512.

14. MullerK, BouyerD, SchnittgerA, KermodeAR (2012) Evolutionarily conserved histone methylation dynamics during seed life-cycle transitions. PLoS One 7: e51532.

15. ZhangH, BishopB, RingenbergW, MuirWM, OgasJ (2012) The CHD3 remodeler PICKLE associates with genes enriched for trimethylation of histone H3 lysine 27. Plant Physiol 159 : 418–432.

16. ZhengB, ChenX (2011) Dynamics of histone H3 lysine 27 trimethylation in plant development. Curr Opin Plant Biol 14 : 123–129.

17. PerrucE, KinoshitaN, Lopez-MolinaL (2007) The role of chromatin-remodeling factor PKL in balancing osmotic stress responses during Arabidopsis seed germination. Plant J 52 : 927–936.

18. SimonJA, KingstonRE (2009) Mechanisms of Polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 10 : 697–708.

19. MolitorA, ShenW-H (2013) The Polycomb complex PRC1: composition and function in plants. J Genet Genomics 40 : 231–238.

20. XuL, ShenW-H (2008) Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Curr Biol 18 : 1966–1971.

21. ChenD, MolitorA, LiuC, ShenW-H (2010) The Arabidopsis PRC1-like ring-finger proteins are necessary for repression of embryonic traits during vegetative growth. Cell Res 20 : 1332–1344.

22. BratzelF, Lopez-TorrejonG, KochM, Del PozoJC, CalonjeM (2010) Keeping cell identity in Arabidopsis requires PRC1 RING-finger homologs that catalyze H2A monoubiquitination. Curr Biol 20 : 1853–1859.

23. YangC, BratzelF, HohmannN, KochM, TurckF, et al. (2013) VAL -⁠ and AtBMI1-mediated H2Aub initiate the switch from embryonic to postgerminative growth in Arabidopsis. Curr Biol 23 : 1324–1329.

24. LeeWY, LeeD, ChungWI, KwonCS (2009) Arabidopsis ING and Alfin1-like protein families localize to the nucleus and bind to H3K4me3/2 via plant homeodomain fingers. Plant J 58 : 511–524.

25. Sanchez-PulidoL, DevosD, SungZR, CalonjeM (2008) RAWUL: a new ubiquitin-like domain in PRC1 ring finger proteins that unveils putative plant and worm PRC1 orthologs. BMC Genomics 9 : 308.

26. LatrasseD, GermannS, Houba-HerinN, DuboisE, Bui-ProdhommeD, et al. (2011) Control of flowering and cell fate by LIF2, an RNA binding partner of the Polycomb complex component LHP1. PLoS One 6: e16592.

27. DerkachevaM, SteinbachY, WildhaberT, MozgovaI, MahrezW, et al. (2013) Arabidopsis MSI1 connects LHP1 to PRC2 complexes. EMBO J 32 : 2073–2085.

28. TurckF, RoudierF, FarronaS, Martin-MagnietteML, GuillaumeE, et al. (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3: e86.

29. ZhangX, GermannS, BlusBJ, KhorasanizadehS, GaudinV, et al. (2007) The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat Struct Mol Biol 14 : 869–871.

30. GuérillonC, LarrieuD, PedeuxR (2013) ING1 and ING2: multifaceted tumor suppressor genes. Cell Mol Life Sci 70 : 3753–3772.

31. GaudinV, LibaultM, PouteauS, JuulT, ZhaoG, et al. (2001) Mutations in LIKE HETEROCHROMATIN PROTEIN 1 affect flowering time and plant architecture in Arabidopsis. Development 128 : 4847–4858.

32. GraeberK, LinkiesA, MüllerK, WunchovaA, RottA, et al. (2010) Cross-species approaches to seed dormancy and germination: conservation and biodiversity of ABA-regulated mechanisms and the Brassicaceae DOG1 genes. Plant Mol Biol 73 : 67–87.

33. KhandelwalA, ChoS, MarellaH, SakataY, PerroudP-F, et al. (2010) Role of ABA and ABI3 in desiccation tolerance. Science 327 : 546–546.

34. BasselGW, LanH, GlaabE, GibbsDJ, GerjetsT, et al. (2011) Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc Natl Acad Sci U S A 108 : 9709–9714.

35. AzuaraV, PerryP, SauerS, SpivakovM, JorgensenHF, et al. (2006) Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8 : 532–538.

36. BernsteinBE, MikkelsenTS, XieX, KamalM, HuebertDJ, et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125 : 315–326.

37. AbedJA, JonesRS (2012) H3K36me3 key to Polycomb-mediated gene silencing in lineage specification. Nat Struct Mol Biol 19 : 1214–1215.

38. De LuciaF, CrevillenP, JonesAM, GrebT, DeanC (2008) A PHD-polycomb Repressive Complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci U S A 105 : 16831–16836.

39. BarreroMJ, Izpisua BelmonteJC (2013) Polycomb complex recruitment in pluripotent stem cells. Nat Cell Biol 15 : 348–350.

40. HeJ, ShenL, WanM, TaranovaO, WuH, et al. (2013) Kdm2b maintains murine embryonic stem cell status by recruiting PRC1 complex to CpG islands of developmental genes. Nat Cell Biol 15 : 373–384.

41. YuY, DongA, ShenW-H (2004) Molecular characterization of the tobacco SET domain protein NtSET1 unravels its role in histone methylation, chromatin binding, and segregation. Plant J 40 : 699–711.

42. Onate-SanchezL, Vicente-CarbajosaJ (2008) DNA-free RNA isolation protocols for Arabidopsis thaliana, including seeds and siliques. BMC Res Notes 1 : 93.

43. RamakersC, RuijterJM, DeprezRH, MoormanAF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci lett 339 : 62–66.

44. CzechowskiT, StittM, AltmannT, UdvardiMK, ScheibleWR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139 : 5–17.

45. BerrA, McCallumEJ, AliouaA, HeintzD, HeitzT, et al. (2010) Arabidopsis histone methyltransferase SET DOMAIN GROUP8 mediates induction of the jasmonate/ethylene pathway genes in plant defense response to necrotrophic fungi. Plant Physiol 154 : 1403–1414.