Marchantia TCP transcription factor activity correlates with three-dimensional chromatin structure

Karaaslan, Ezgi Süheyla; Wang, Nan; Faiss, Natalie; Liang, Yuyu; Montgomery, Sean A.; Laubinger, Sascha; Berendzen, Kenneth W.; Berger, Frédéric; Breuninger, Holger; Liu, Chang

doi:10.1038/s41477-020-00766-0

Cited by 61 publications

(49 citation statements)

References 80 publications

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“…Comparison of motif occurrences between co-accessible link edges indicated that ACRs in co-accessible links are more similar to one another than randomly linked ACRs (empirical: P < 1e-4; Figure S9E). Furthermore, we identified several cases where co-accessible ACR edges were reciprocally enriched for the same TF motif in both cell type- (Karaaslan et al, 2020;Liu et al, 2017;Peng et al, 2019;Sun et al, 2020). Consistent with these past studies, our results implicate independently evolved TF families with CTCF-like function capable of organizing higher-order chromatin architecture through DNA-protein interactions.…”

Section: Coordinated Dynamic Chromatin Accessibility Recapitulates In Vivo Chromatin Interactionssupporting

confidence: 91%

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Acis-regulatory atlas in maize at single-cell resolution

Marand

Chen

Gallavotti

et al. 2020

Preprint

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Cis-regulatory elements (CREs) encode the genomic blueprints for coordinating spatiotemporal gene expression programs underlying highly specialized cell functions. To identify CREs underlying cell-type specification and developmental transitions, we implemented single-cell sequencing of Assay for Transposase Accessible Chromatin in an atlas of Zea mays organs. We describe 92 distinct states of chromatin accessibility across more than 165,913 putative CREs, 56,575 cells, and 52 known cell-types in maize using a novel implementation of regularized quasibinomial logistic regression. Cell states were largely determined by combinatorial accessibility of transcription factors (TFs) and their binding sites. A neural network revealed that cell identity could be accurately predicted (>0.94) solely based on TF binding site accessibility. Co-accessible chromatin recapitulated higher-order chromatin interactions, with distinct sets of TFs coordinating cell type-specific regulatory dynamics. Pseudotime reconstruction and alignment with Arabidopsis thaliana trajectories identified conserved TFs, associated motifs, and cis-regulatory regions specifying sequential developmental progressions. Cell-type specific accessible chromatin regions were enriched with phenotype-associated genetic variants and signatures of selection, revealing the major cell-types and putative CREs targeted by modern maize breeding. Collectively, our analysis affords a comprehensive framework for understanding cellular heterogeneity, evolution, and cis-regulatory grammar of cell-type specification in a major crop species.

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Section: Coordinated Dynamic Chromatin Accessibility Recapitulates In Vivo Chromatin Interactionssupporting

confidence: 91%

“…7f, g ). A role in chromatin organization is supported by previous research demonstrating TCP motif overrepresentation in topologically associated domain-like (TAD) boundaries in Oryza sativa and Marchantia polymorpha, and the distal edges of chromatin loops in Zea mays 27, 28, 31, 32 .…”

Section: Main Textmentioning

confidence: 70%

Acis-regulatory atlas in maize at single-cell resolution

Marand

Chen

Gallavotti

et al. 2020

Preprint

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“…Moreover, inconsistent ChIP signals between individual MpNMCP:2HA tagging lines were found across the autosomes (data not shown). The ChIP experiments were performed in accordance with our working protocol that we used for MpTCP1 proteins (Karaaslan et al, 2020b), and we verified successful immunoprecipitation of MpNMCP:2HA proteins with Western blot (Supplementary Figure 8). Thus, our data suggest that MpNMCP proteins do not directly interact with chromatin at the nuclear periphery.…”

Section: Mpnmcp Indirectly Regulates Perinuclear Location Of Chromatinmentioning

confidence: 82%

“…The in situ Hi-C library preparation was strictly followed as described (Karaaslan et al, 2020b). In total, two replicates of 2week-old Tak-1 and Mpnmcp mutant thallus Hi-C libraries were made, and for each replicate, around 0.5 g of fixed sample was homogenized for nuclei isolation.…”

Section: In Situ Hi-c and Data Processingmentioning

confidence: 99%

Characterization of a Plant Nuclear Matrix Constituent Protein in Liverwort

et al. 2021

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The nuclear lamina (NL) is a complex network of nuclear lamins and lamina-associated nuclear membrane proteins, which scaffold the nucleus to maintain structural integrity. In animals, type V intermediate filaments are the main constituents of NL. Plant genomes do not encode any homologs of these intermediate filaments, yet plant nuclei contain lamina-like structures that are present in their nuclei. In Arabidopsis thaliana, CROWDED NUCLEI (CRWN), which are required for maintaining structural integrity of the nucleus and specific perinuclear chromatin anchoring, are strong candidates for plant lamin proteins. Recent studies revealed additional roles of Arabidopsis Nuclear Matrix Constituent Proteins (NMCPs) in modulating plants’ response to pathogen and abiotic stresses. However, detailed analyses of Arabidopsis NMCP activities are challenging due to the presence of multiple homologs and their functional redundancy. In this study, we investigated the sole NMCP gene in the liverwort Marchantia polymorpha (MpNMCP). We found that MpNMCP proteins preferentially were localized to the nuclear periphery. Using CRISPR/Cas9 techniques, we generated an MpNMCP loss-of-function mutant, which displayed reduced growth rate and curly thallus lobes. At an organelle level, MpNMCP mutants did not show any alteration in nuclear morphology. Transcriptome analyses indicated that MpNMCP was involved in regulating biotic and abiotic stress responses. Additionally, a highly repetitive genomic region on the male sex chromosome, which was preferentially tethered at the nuclear periphery in wild-type thalli, decondensed in the MpNMCP mutants and located in the nuclear interior. This perinuclear chromatin anchoring, however, was not directly controlled by MpNMCP. Altogether, our results unveiled that NMCP in plants have conserved functions in modulating stress responses.

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“…Plant genomes are known to lack homologs of the CCCTC-binding factor and insulators (Ong & Corces, 2009); instead, analysis of conserved sequence motifs at TAD borders has suggested that plant-specific TCP DOMAIN PROTEINS (TCPs) presumably control 3D chromatin packing (Liu et al, 2017). Consistently, the TCP1 of Marchantia polymorpha has been proven to establish TAD structure (Karaaslan et al, 2020). Interestingly, a significant portion of plant TCPs contain IDRs (Pontvianne & Liu, 2020) and are located in nuclear speckles (Valsecchi et al, 2013;Kubota et al, 2017;Mazur et al, 2017), further supporting that LLPS contributes to the 3D genome configuration in plants.…”

Section: Temperature Sensing Condensatesmentioning

confidence: 99%

Get closer and make hotspots: liquid–liquid phase separation in plants

Kim

Lee

et al. 2021

EMBO Reports

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Liquid-liquid phase separation (LLPS) facilitates the formation of membraneless compartments in a cell and allows the spatiotemporal organization of biochemical reactions by concentrating macromolecules locally. In plants, LLPS defines cellular reaction hotspots, and stimulus-responsive LLPS is tightly linked to a variety of cellular and biological functions triggered by exposure to various internal and external stimuli, such as stress responses, hormone signaling, and temperature sensing. Here, we provide an overview of the current understanding of physicochemical forces and molecular factors that drive LLPS in plant cells. We illustrate how the biochemical features of cellular condensates contribute to their biological functions. Additionally, we highlight major challenges for the comprehensive understanding of biological LLPS, especially in view of the dynamic and robust organization of biochemical reactions underlying plastic responses to environmental fluctuations in plants.

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Marchantia TCP transcription factor activity correlates with three-dimensional chromatin structure

Cited by 61 publications

References 80 publications

Acis-regulatory atlas in maize at single-cell resolution

Acis-regulatory atlas in maize at single-cell resolution

Characterization of a Plant Nuclear Matrix Constituent Protein in Liverwort

Get closer and make hotspots: liquid–liquid phase separation in plants

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