Arabidopsis AL PHD-PRC1 complexes promote seed germination through H3K4me3-to-H3K27me3 chromatin state switch in repression of seed developmental genes.
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.
Institut de Biologie Moléculaire des Plantes du CNRS, Université de Strasbourg, Strasbourg, France.
Anne Marie
AM
Molitor
Institut de Biologie Moléculaire des Plantes du CNRS, Université de Strasbourg, Strasbourg, France ; State Key Laboratory of Genetic Engineering, International Associated Laboratory of CNRS-Fudan-HUNAU on Plant Epigenome Research, School of Life Sciences, Fudan University, Shanghai, PR China.
Zhongyuan
Z
Bu
State Key Laboratory of Genetic Engineering, International Associated Laboratory of CNRS-Fudan-HUNAU on Plant Epigenome Research, School of Life Sciences, Fudan University, Shanghai, PR China.
Yu
Y
Yu
Institut de Biologie Moléculaire des Plantes du CNRS, Université de Strasbourg, Strasbourg, France ; State Key Laboratory of Genetic Engineering, International Associated Laboratory of CNRS-Fudan-HUNAU on Plant Epigenome Research, School of Life Sciences, Fudan University, Shanghai, PR China.
Wen-Hui
WH
Shen
D017360:Arabidopsis; D029681:Arabidopsis Proteins / Q000235:genetics* / Q000378:metabolism; D002843:Chromatin / Q000235:genetics*; D004268:DNA-Binding Proteins / Q000235:genetics*; D018506:Gene Expression Regulation, Plant; D018525:Germination; D011495:Histone-Lysine N-Methyltransferase / Q000235:genetics* / Q000378:metabolism; D006657:Histones / Q000235:genetics; D018398:Homeodomain Proteins / Q000235:genetics*; D063150:Polycomb Repressive Complex 1 / Q000235:genetics; D011485:Protein Binding; D054829:RING Finger Domains / Q000235:genetics; D036226:Seedlings / Q000235:genetics / Q000254:growth & development; D012639:Seeds / Q000235:genetics* / Q000254:growth & development; D014157:Transcription Factors / Q000235:genetics*; D014158:Transcription, Genetic
C000588913:AL7 protein, Arabidopsis; C584518:ALFIN-LIKE 6 protein, Arabidopsis; D029681:Arabidopsis Proteins; D002843:Chromatin; D004268:DNA-Binding Proteins; D006657:Histones; D018398:Homeodomain Proteins; D014157:Transcription Factors; D011495:Histone-Lysine N-Methyltransferase; D063150:Polycomb Repressive Complex 1