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Profiling chromatin accessibility during stomatal development

ABSTRACT: Plant cells are totipotent and hence can dedifferentiate and re-differentiate, making it possible to clone entire plant parts from a single cell. It is hence critical for plant cells to maintain specific cell-states during and after differentiation. Stomata, microscopic valves on the plant epidermis required for efficient gas exchange and water management, have emerged as a powerful model system for understanding how de novo lineage-specific stem cell initiate, proliferate and differentiate into specialized cell types during their development of the plant epidermis. The stomatal lineage emerged from a subpopulation of protodermal cells as meristemoid mother cells (MMCs) that undergoes an asymmetric entry division to give a rise meristemoid and its sister cell called the stomatal-lineage ground cell (SLGC). After several rounds of asymmetric cell division, meristemoids differentiate into round guard mother cells (GMC), which divide symmetrically and terminally differentiate into paired guard cells (GCs). We have adapted the INTACT (Isolation of Nuclei TAgged in Specific Cell Types) system to isolate each stomatal lineage-specific nuclei followed by ATACseq (Assay for Transposase-Accessible Chromatin). We showed that chromatin accessibility is dynamic throughout the stomatal lineage progression. Further, the analysis of TF binding sites in differentially accessible regions led to discover that combinatorial cis-regulatory elements and transcription factor circuits controls lineage specific cell state transition during stomatal development.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE190753 | GEO | 2022/12/28

REPOSITORIES: GEO

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Project description:Stomata are pores in the epidermis of plants that can open and close and allow for gas exchange vital for photosynthesis and regulate transpiration. Stomatal development is driven by a set of conserved bHLH transcription factors (SPCH, MUTE, FAMA, and their heterodimerization partners ICE1, SCRM2), that initiate and promote progression of cell fates in the stomatal lineage. Due to the shared ancestry of SPCH, MUTE and FAMA (subgroup Ia) and ICE1 and SCRM2 (subgroup IIIb) their DNA binding specificity is similar and there is some functional redundancy. However, individual bHLHs also have unique functions. For example, SPCH is required for initiation of the stomatal lineage, while FAMA is responsible for terminal differentiation of the guard cell pair. In grasses, the stomatal complex comprises the guard cell pair, and two flanking subsidiary cells. Recruitment of the latter from neighboring cell filed during development requires expression of MUTE. Remarkably, while MUTE is absolutely required for the promotion of guard mother cell fate in maize and rice, this is not the case in Brachypodium. This suggests that another TF can at least partially substitute for MUTE in this function. While different expression profiles of the bHLH dimers within the stomatal lineage may partially responsible for distinct functions of each pair, it is likely that each pair forms different transcriptional complexes and that interaction with other transcriptional regulators affects the dimer’s binding DNA binding and gene regulation properties. Given the differences in bHLH function between dicots and grasses and even within the grass family, we were interested in elucidating the protein interaction networks of the stomatal lineage regulators in Brachypodium. To this end, we performed co-immunoprecipitation coupled to LC-MS/MS of BdSPCH2-YFP, YFP-BdMUTE, YFP-BdFAMA, YFP-ICE1 and YFP-SCRM2 from the developmental zone of young B. distachyon leaves using GFP-Trap beads. All YFP-fusion proteins were expressed under the endogenous promoter in the Bd21-3 background. The only exception was BdICE1, which was expressed under the ZmUBI promoter, but was nevertheless mostly restricted to the stomatal lineage. As control lines we use the Bd21-3 wild type and a line expressing 3x YFPnls (nuclear YFP) under the MUTE promoter. Comparison of proteins enriched with the bHLH fusion proteins vs. the controls revealed overlapping and distinct putative interactors, which is in agreement with the assumption that these transcription factors have both shared and unique functions. Notably, in addition to the presumed hetero-dimerization partners, we found a number of other bHLH transcription factors that were identified with one or more of the bait proteins. This suggests the presence of a larger bHLH network acting in the stomatal lineage.

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Profiling chromatin accessibility during stomatal development

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