Cis and trans determinants of epigenetic silencing by Polycomb repressive complex 2 in Arabidopsis

Xiao, Jun; Jin, Run; Yu, Xiang; Shen, Max W.; Wagner, John D.; Pai, Armaan; Song, Claire; Zhuang, Michael; Klasfeld, Samantha; He, Chongsheng; Santos, Alexandre Matte; Helliwell, Chris A.; Pruneda‐Paz, Jose L.; Kay, Steve A.; Lin, Xiaowei; Cui, Sujuan; García, Meilín Fernández; Clarenz, Oliver; Goodrich, Justin; Zhang, Xiaoyu; Austin, Ryan E; Bonasio, Roberto; Wagner, Doris

doi:10.1038/ng.3937

Cited by 235 publications

(242 citation statements)

References 75 publications

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“…The ChIP‐seq results were validated by ChIP‐quantitative PCR (ChIP‐qPCR) analyses on several randomly selected target genes (Supporting Information ). Furthermore, we also compared our CLF/SWN target genes with FIE target genes by taking advantage of the published datasets (Deng et al., ; Xiao et al., ). As shown in Supporting Information , CLF/SWN and FIE share a large fraction of targets (Supporting Information ).This result is understandable, given the fact that these experiments were carried out with plants of different ages.…”

Section: Resultsmentioning

confidence: 99%

“…Meanwhile, although a number of H3K27me3 genome‐wide profiling have been reported (Carter et al., ; Cui et al., ; Li et al., , ; Luo et al., ; Wang et al., ; Yang et al., ), works on genome‐wide occupancy of the CLF and SWN proteins are rather limited. The recently published CLF ChIP‐chip data were based on a transgenic line in which CLF was driven by a constitutive promoter (Xiao et al., ). Therefore, there is a pressing need to profile their genome‐wide occupancy for the plant biology community to dissect their functions comprehensively.…”

Section: Introductionmentioning

confidence: 99%

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Genome‐wide occupancy of histone H3K27 methyltransferases CURLY LEAF and SWINGER in Arabidopsis seedlings

et al. 2019

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The Polycomb Group (PcG) proteins form two protein complexes, PcG Repressive Complex 1 ( PRC 1) and PRC 2, which are key epigenetic regulators in eukaryotes. PRC 2 represses gene expression by catalyzing the trimethylation of histone H3 lysine 27 (H3K27me3). In Arabidopsis ( Arabidopsis thaliana ), CURLY LEAF ( CLF ) and SWINGER ( SWN ) are two major H3K27 methyltransferases and core components of PRC 2, playing essential roles in plant growth and development. Despite their importance, genome‐wide binding profiles of CLF and SWN have not been determined and compared yet. In this study, we generated transgenic lines expressing GFP ‐tagged CLF / SWN under their respective native promoters and used them for Ch IP ‐seq analyses to profile the genome‐wide distributions of CLF and SWN in Arabidopsis seedlings. We also profiled and compared the global H3K27me3 levels in wild‐type ( WT ) and PcG mutants ( clf , swn , and clf swn ). Our data show that CLF and SWN bind to almost the same set of genes, except that SWN has a few hundred more targets. Two short DNA sequences, the GAGA ‐like and Telo ‐box‐like motifs, were found enriched in the CLF and SWN binding regions. The H3K27me3 levels in clf , but not in swn , were markedly reduced compared with WT ; and the mark was undetectable in the clf swn double mutant. Further, we profiled the transcriptomes in clf , swn , and clf swn, and compared that with WT . Thus this work provides a useful resource for the plant epigenetics community for dissecting the functions of PRC 2 in plant growth and development.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Genome‐wide occupancy of histone H3K27 methyltransferases CURLY LEAF and SWINGER in Arabidopsis seedlings

et al. 2019

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“…Our results here extend this observation to another intronic RNA. The DNA region (+2616 to +3348 within AG intron 2) that we identified as CLF target also contains PREs which may recruit PRC2 for gene repression (Xiao et al ., ).…”

Section: Discussionmentioning

confidence: 97%

A noncoding RNA transcribed from the AGAMOUS (AG) second intron binds to CURLY LEAF and represses AG expression in leaves

Deng

et al. 2018

New Phytologist

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Dispersed H3K27 trimethylation (H3K27me3) of the AGAMOUS (AG) genomic locus is mediated by CURLY LEAF (CLF), a component of the Polycomb Repressive Complex (PRC) 2. Previous reports have shown that the AG second intron, which confers AG tissue-specific expression, harbors sequences targeted by several positive and negative regulators. Using RACE reverse transcription polymerase chain reaction, we found that the AG intron 2 encodes several noncoding RNAs. RNAi experiment showed that incRNA4 is needed for CLF repressive activity. AG-incRNA4RNAi lines showed increased leaf AG mRNA levels associated with a decrease of H3K27me3 levels; these plants displayed AG overexpression phenotypes. Genetic and biochemical analyses demonstrated that the AG-incRNA4 can associate with CLF to repress AG expression in leaf tissues through H3K27me3-mediated repression and to autoregulate its own expression level. The mechanism of AG-incRNA4-mediated repression may be relevant to investigations on tissue-specific expression of Arabidopsis MADS-box genes.

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“…In Drosophila PcG and TrxG proteins bind promoters and other specialized regulatory elements called Cell Memory Module (CMM) that convey epigenetic inheritance through cell division . In mammalian cells PcG proteins bind preferentially CpG islands close to TSS and recent evidence for CMM has been reported in plants …”

Section: Introductionmentioning

confidence: 99%

How Polycomb‐Mediated Cell Memory Deals With a Changing Environment

2018

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Cells and tissues are continuously exposed to a changing microenvironment, hence the necessity of a flexible modulation of gene expression that in complex organism have been achieved through specialized chromatin mechanisms. Chromatin-based cell memory enables cells to maintain their identity by fixing lineage specific transcriptional programs, ensuring their faithful transmission through cell division; in particular PcG-based memory system evolved to maintain the silenced state of developmental and cell cycle genes. In evolution the complexity of this system have increased, particularly in vertebrates, indicating combinatorial and dynamic properties of Polycomb proteins, in some cases even overflowing outside the cell nucleus. Therefore, their function may not be limited to the imposition of rigid states of genetic programs, but on the ability to recognize signals and allow plastic transcriptional changes in response to different stimuli. Here, we discuss the most novel PcG mediated memory functions in facing and responding to the challenges posed by a fluctuating environment.

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Cis and trans determinants of epigenetic silencing by Polycomb repressive complex 2 in Arabidopsis

Cited by 235 publications

References 75 publications

Genome‐wide occupancy of histone H3K27 methyltransferases CURLY LEAF and SWINGER in Arabidopsis seedlings

Genome‐wide occupancy of histone H3K27 methyltransferases CURLY LEAF and SWINGER in Arabidopsis seedlings

A noncoding RNA transcribed from the AGAMOUS (AG) second intron binds to CURLY LEAF and represses AG expression in leaves

How Polycomb‐Mediated Cell Memory Deals With a Changing Environment

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