The transcriptional repressors VAL1 and VAL2 mediate genome-wide recruitment of the CHD3 chromatin remodeler PICKLE in Arabidopsis

Abstract

PICKLE (PKL) is a Chromodomain Helicase DNA-binding domain 3 (CHD3) chromatin remodeler that plays essential roles in controlling the gene expression patterns that determine developmental identity in plants, but the molecular mechanisms through which PKL is recruited to its target genes remain elusive. Here, we define a cis-motif and trans-acting factors mechanism that governs the genomic occupancy profile of PKL in Arabidopsis thaliana. We show that two homologous trans-factors VIVIPAROUS1/ABI3-LIKE1 (VAL1) and VAL2, physically interact with PKL in vivo, localize extensively to PKL-occupied regions in the genome, and promote efficient PKL recruitment at thousands of target genes, including those involved in seed maturation. Transcriptome analysis and genetic interaction studies reveal a close cooperation of VAL1/VAL2 and PKL in regulating gene expression and developmental fate. We demonstrate that this recruitment operates at two master regulatory genes, ABSCISIC ACID INSENSITIVE3 (ABI3) and AGAMOUS-LIKE 15 (AGL15), to repress the seed maturation program and ensure the seed-to-seedling transition. Together, our work unveils a general rule through which the CHD3 chromatin remodeler PKL binds to its target chromatin in plants.

Recent progress in molecular genetics and omics-driven research in seed biology

“…This role has been confirmed for the activation of the FLOWERING LOCUS C (FLC) during early embryo development [66,67]. The LAFL antagonize VIVIPAROUS1/ABI3-LIKE1 (VAL1) and VAL2, two B3type TFs involved in recruiting PRC to FLC [68][69][70][71] or the CHD3 chromatin remodelling factor PICKLE to ABI3 and AGL15, to repress seed maturation [72]. Interestingly, FLC has been shown to be involved in the modulation of seed dormancy in response to temperature [73,74].…”

“…Ce rôle a été confirmé pour l'activation du gène FLOWERING LOCUS C (FLC) au cours du développement embryonnaire précoce [66,67]. Les LAFL antagonisent VIVIPAROUS1/ABI3-LIKE1 (VAL1) et VAL2, deux TFs également de type B3 impliqués dans le re-crutement des PRC au locus FLC [68][69][70][71] ou le facteur de remodelage de la chromatine CHD3 PICKLE aux locus ABI3 et AGL15, pour réprimer la maturation des graines [72]. Il est intéressant de noter que FLC est impliqué dans la modulation de la dormance des graines en réponse à la température [73,74].…”

PKL is stabilized by MMS21 to negatively regulate Arabidopsis drought tolerance through directly repressing AFL1 transcription

“…Moreover, it has been shown that PKL is enriched at genome loci decorated by H3K27me3 (Zhang et al ., 2008). A recent study revealed that PKL could interact with the transcription factors VAL1/2 to repress the expression of ABI3 and AGL15 in regulating the seed‐to‐seedling transition (Liang et al ., 2022). Our transcriptome analysis revealed that PKL represses the transcription of the drought tolerance‐related gene AFL1 (Fig.…”

“…In Arabidopsis , trimethylation of histone H3 Lys 27 (H3K27me3) is deposited by Polycomb Repressive Complex 2 (PRC2; Hinsch et al ., 2021). PICKLE (PKL) is an ATP‐dependent Chromodomain Helicase DNA‐binding domain type 3 (CHD3) chromatin remodeler that is required for H3K27me3 deposition at some genomic locations and regulates multiple plant developmental and physiological processes (Tong et al ., 1998; Ogas et al ., 1999; Fukaki et al ., 2006; Perruc et al ., 2007; Aichinger et al ., 2009, 2011; Furuta et al ., 2011; Jing et al ., 2013, 2019a,b; Zhang et al ., 2014; Xu et al ., 2016; Zha et al ., 2017, 2020; Yang et al ., 2019; Hinsch et al ., 2021; Hu et al ., 2022; Liang et al ., 2022). A recent study revealed that PKL could interact with the transcription factors VIVIPAROUS1/ABI3‐LIKE1/2 (VAL1/2) to repress the expression of ABA INSENSITIVE 3 ( ABI3 ) and AGAMOUS‐LIKE 15 ( AGL15 ) in regulating the seed‐to‐seedling transition (Liang et al ., 2022).…”