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BHLH transcription factors cooperate with chromatin remodelers to regulate cell fate decisions during Arabidopsis stomatal development

ABSTRACT: The development of multi-cellular organisms requires coordinated changes in gene expression that are often mediated by the interaction between transcription factors (TFs) and their corresponding cis-regulatory elements (CREs). During development and differentiation, the accessibility of CREs is dynamically modulated by the epigenome. How the epigenome, CREs and TFs together exert control over cell fate commitment remains to be fully understood. In the Arabidopsis leaf epidermis, meristemoids undergo a series of stereotyped cell divisions, then switch fate to commit to stomatal differentiation. Newly created or reanalyzed scRNA-seq and ChIP-seq data confirm that stomatal development involves distinctive phases of transcriptional regulation and that differentially regulated genes are bound by the stomatal basic-helix-loop-helix (bHLH) TFs. Targets of the bHLHs often reside in repressive chromatin before activation. MNase-seq evidence further suggests that the repressive state can be overcome and remodeled upon activation by specific stomatal bHLHs. We propose that chromatin remodeling is mediated through the recruitment of a set of physical interactors that we identified through proximity labeling – the ATPase-dependent chromatin remodeling SWI/SNF complex and the histone acetyltransferase HAC1. The bHLHs and chromatin remodelers localize to overlapping genomic regions in a hierarchical order. Furthermore, plants with stage-specific knock-down of the SWI/SNF components or HAC1 fail to activate specific bHLH targets and display stomatal development defects. Together these data converge on a model for how stomatal TFs and epigenetic machinery cooperatively regulate transcription and chromatin remodeling during progressive fate specification.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE269849 | GEO | 2024/06/20

REPOSITORIES: GEO

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Project description:Stomata are pores in the epidermis of plants that can open and close, allowing for gas exchange with the environment, vital for photosynthesis, and regulating transpiration. They are formed from protodermal cells by a series of asymmetric and symmetric divisions and differentiation steps. Initiation into and progression within the stomatal lineage are driven by the consecutive expression and action of three sets of bHLH transcription factor dimers (SPCH, MUTE, FAMA plus their heterodimer partners SCRM or SCRM2) and is accompanied by massive changes in the transcriptome as well as the chromatin landscape. Strong shifts in chromatin accessibility have been observed specifically at the initiation stage and at the transition from division to differentiation. In line with this, FAMA, which promotes the differentiation of stomata, has been shown to interact with RBR, which can recruit the repressive PRC2 complex, to shut down the early stomatal lineage transcriptional program. Interestingly, several of the stomatal lineage bHLHs bind chromatin regions that are closed/inaccessible in a primordial state (the shoot apical meristem). This suggests that the stomatal lineage bHLHs could be able to access closed chromatin and that they might also be directly involved in opening (and closing) of chromatin at a subset of their target regions. In order to test this hypothesis and identify chromatin modifiers that associate with the stomatal lineage bHLH dimers, we did proximity labeling with TurboID fused to SCRM, which is expressed throughout the stomatal lineage and is the main heterodimerization partner of SPCH, MUTE and FAMA. We identified a number of proteins acting as chromatin modifiers and remodelers, including the histone acetyl transferase HAC1, which deposits activating marks on nucleosomes, and multiple subunits of the ATPase-dependent chromatin remodeling SWI/SNF complex. Together, these data support a role of SCRM and its partners in regulating target gene accessibility to impose lasting changes in gene expression within the stomatal lineage.

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BHLH transcription factors cooperate with chromatin remodelers to regulate cell fate decisions during Arabidopsis stomatal development

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