VAL1 Acts As an Assembly Platform Co-ordinating Co-transcriptional Repression and Chromatin Regulation at Arabidopsis FLC

Overview

Journal Nat Commun

Specialty Biology

Date 2022 Sep 21

PMID 36130923

Authors

Pawel Mikulski

Philip Wolff

Tiancong Lu

Mathias Nielsen

Elsa Franco Echevarria

Danling Zhu

Julia I Questa

Gerhard Saalbach

Carlo Martins

Caroline Dean

Affiliations

Soon will be listed here.

Abstract

Polycomb (PcG) silencing is crucial for development, but how targets are specified remains incompletely understood. The cold-induced Polycomb Repressive Complex 2 (PRC2) silencing of Arabidopsis thaliana FLOWERING LOCUS C (FLC) provides an excellent system to elucidate PcG regulation. Association of the DNA binding protein VAL1 to FLC PcG nucleation regionis an important step. VAL1 co-immunoprecipitates APOPTOSIS AND SPLICING ASSOCIATED PROTEIN (ASAP) complex and PRC1. Here, we show that ASAP and PRC1 are necessary for co-transcriptional repression and chromatin regulation at FLC. ASAP mutants affect FLC transcription in warm conditions, but the rate of FLC silencing in the cold is unaffected. PRC1-mediated H2Aub accumulation increases at the FLC nucleation region during cold, but unlike the PRC2-delivered H3K27me3, does not spread across the locus. H2Aub thus involved in the transition to epigenetic silencing at FLC, facilitating H3K27me3 accumulation and long-term epigenetic memory. Overall, our work highlights the importance of VAL1 as an assembly platform co-ordinating activities necessary for epigenetic silencing at FLC.

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References

Itoh Y, Woods E, Minami K, Maeshima K, Collepardo-Guevara R . Liquid-like chromatin in the cell: What can we learn from imaging and computational modeling?. Curr Opin Struct Biol. 2021; 71:123-135. DOI: 10.1016/j.sbi.2021.06.004. View

Qin F, Sakuma Y, Tran L, Maruyama K, Kidokoro S, Fujita Y . Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell. 2008; 20(6):1693-707. PMC: 2483357. DOI: 10.1105/tpc.107.057380. View

Yang H, Berry S, Olsson T, Hartley M, Howard M, Dean C . Distinct phases of Polycomb silencing to hold epigenetic memory of cold in . Science. 2017; 357(6356):1142-1145. DOI: 10.1126/science.aan1121. View

Alfieri C, Gambetta M, Matos R, Glatt S, Sehr P, Fraterman S . Structural basis for targeting the chromatin repressor Sfmbt to Polycomb response elements. Genes Dev. 2013; 27(21):2367-79. PMC: 3828522. DOI: 10.1101/gad.226621.113. View

Yuan L, Song X, Zhang L, Yu Y, Liang Z, Lei Y . The transcriptional repressors VAL1 and VAL2 recruit PRC2 for genome-wide Polycomb silencing in Arabidopsis. Nucleic Acids Res. 2020; 49(1):98-113. PMC: 7797069. DOI: 10.1093/nar/gkaa1129. View

Michaels S, Amasino R . FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell. 1999; 11(5):949-56. PMC: 144226. DOI: 10.1105/tpc.11.5.949. View

Yang H, Howard M, Dean C . Antagonistic roles for H3K36me3 and H3K27me3 in the cold-induced epigenetic switch at Arabidopsis FLC. Curr Biol. 2014; 24(15):1793-7. PMC: 4123163. DOI: 10.1016/j.cub.2014.06.047. View

Xu C, Wu Z, Duan H, Fang X, Jia G, Dean C . R-loop resolution promotes co-transcriptional chromatin silencing. Nat Commun. 2021; 12(1):1790. PMC: 7979926. DOI: 10.1038/s41467-021-22083-6. View

Sheldon C, Rouse D, Finnegan E, Peacock W, Dennis E . The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci U S A. 2000; 97(7):3753-8. PMC: 16312. DOI: 10.1073/pnas.97.7.3753. View

10.

Baile F, Merini W, Hidalgo I, Calonje M . EAR domain-containing transcription factors trigger PRC2-mediated chromatin marking in Arabidopsis. Plant Cell. 2021; 33(8):2701-2715. PMC: 8408475. DOI: 10.1093/plcell/koab139. View

11.

Sengupta A, Kuhrs A, Muller J . General transcriptional silencing by a Polycomb response element in Drosophila. Development. 2004; 131(9):1959-65. DOI: 10.1242/dev.01084. View

12.

Yang C, Bratzel F, Hohmann N, Koch M, Turck F, Calonje M . VAL- and AtBMI1-mediated H2Aub initiate the switch from embryonic to postgerminative growth in Arabidopsis. Curr Biol. 2013; 23(14):1324-9. DOI: 10.1016/j.cub.2013.05.050. View

13.

Csorba T, Questa J, Sun Q, Dean C . Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. Proc Natl Acad Sci U S A. 2014; 111(45):16160-5. PMC: 4234544. DOI: 10.1073/pnas.1419030111. View

14.

Sun Q, Csorba T, Skourti-Stathaki K, Proudfoot N, Dean C . R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science. 2013; 340(6132):619-21. PMC: 5144995. DOI: 10.1126/science.1234848. View

15.

Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C . Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science. 2000; 290(5490):344-7. DOI: 10.1126/science.290.5490.344. View

16.

Swiezewski S, Liu F, Magusin A, Dean C . Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature. 2009; 462(7274):799-802. DOI: 10.1038/nature08618. View

17.

Scelfo A, Fernandez-Perez D, Tamburri S, Zanotti M, Lavarone E, Soldi M . Functional Landscape of PCGF Proteins Reveals Both RING1A/B-Dependent-and RING1A/B-Independent-Specific Activities. Mol Cell. 2019; 74(5):1037-1052.e7. PMC: 6561742. DOI: 10.1016/j.molcel.2019.04.002. View

18.

Li P, Tao Z, Dean C . Phenotypic evolution through variation in splicing of the noncoding RNA COOLAIR. Genes Dev. 2015; 29(7):696-701. PMC: 4387712. DOI: 10.1101/gad.258814.115. View

19.

Xu L, Shen W . Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Curr Biol. 2008; 18(24):1966-71. DOI: 10.1016/j.cub.2008.11.019. View

20.

Zhu P, Lister C, Dean C . Cold-induced Arabidopsis FRIGIDA nuclear condensates for FLC repression. Nature. 2021; 599(7886):657-661. PMC: 8612926. DOI: 10.1038/s41586-021-04062-5. View