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The master growth regulator DELLA binding to histone H2A is essential for DELLA

Jun 25, 2023Jun 25, 2023

Nature Plants (2023)Cite this article

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The DELLA genes, also known as ‘Green Revolution’ genes, encode conserved master growth regulators that control plant development in response to internal and environmental cues. Functioning as nuclear-localized transcription regulators, DELLAs modulate expression of target genes via direct protein–protein interaction of their carboxy-terminal GRAS domain with hundreds of transcription factors (TFs) and epigenetic regulators. However, the molecular mechanism of DELLA-mediated transcription reprogramming remains unclear. Here by characterizing new missense alleles of an Arabidopsis DELLA, repressor of ga1-3 (RGA), and co-immunoprecipitation assays, we show that RGA binds histone H2A via the PFYRE subdomain within its GRAS domain to form a TF–RGA–H2A complex at the target chromatin. Chromatin immunoprecipitation followed by sequencing analysis further shows that this activity is essential for RGA association with its target chromatin globally. Our results indicate that, although DELLAs are recruited to target promoters by binding to TFs via the LHR1 subdomain, DELLA–H2A interaction via the PFYRE subdomain is necessary to stabilize the TF–DELLA–H2A complex at the target chromatin. This study provides insights into the two distinct key modular functions in DELLA for its genome-wide transcription regulation in plants.

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Raw and processed ChIP–seq data and ATAC-seq data have been deposited at the National Center for Biotechnology Information’s Gene Expression Omnibus (accession numbers GSE220898 and GSE233124, respectively). Source data are provided with this paper.

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We thank G. Choi for helpful discussions and for sharing Arabidopsis lines and constructs. This work was supported by the National Institutes of Health (R01 GM100051 to T.-P.S.) and the National Science Foundation (MCB-1818161 to T.-P.S., and NSF-EDGE-1923589 to D.-H.O. and M.D.). We also acknowledge Louisiana State University High Performance Computing services for providing computational resources.

Hao Tian

Present address: Department of Botany and Plant Sciences, University of California, Riverside, Riverside, CA, USA

Jeongmoo Park

Present address: Syngenta, Research Triangle Park, Raleigh, NC, USA

Rodolfo Zentella

Present address: Agricultural Research Service, Plant Science Research Unit, US Department of Agriculture, Raleigh, NC, USA

Rodolfo Zentella

Present address: Department of Crop and Soil Sciences, North Carolina State University, Raleigh, NC, USA

These authors contributed equally: Xu Huang, Hao Tian, Jeongmoo Parkg.

Department of Biology, Duke University, Durham, NC, USA

Xu Huang, Hao Tian, Jeongmoo Park, Jianhong Hu, Rodolfo Zentella & Tai-Ping Sun

Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, USA

Dong-Ha Oh & Maheshi Dassanayake

Institute for Cellular and Molecular Biology and Department of Molecular Biosciences, The University of Texas at Austin, Austin, TX, USA

Hong Qiao

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J.P. and T.-P.S. conceived and designed the research project. R.Z. provided helpful suggestions. H.Q. provided constructs and protocols. X.H., H.T., J.P., J.H. and R.Z. performed experiments. X.H., H.T., J.P., J.H., R.Z. and T.-P.S. analysed the data and generated figures. D.-H.O., J.P., H.T. and M.D. performed analysis for the ChIP–seq data and generated figures. T.-P.S. wrote the paper with input from all co-authors.

Correspondence to Tai-Ping Sun.

The authors declare no competing interests.

Nature Plants thanks the anonymous reviewers for their contribution to the peer review of this work.

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Supplementary Figs. 1–11; Fig. 11 is the source data figure for the supplementary figures.

Supplementary Tables 1–10.

Statistical source data for Supplementary Figs. 1–3.

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Unprocessed blots and gels.

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Huang, X., Tian, H., Park, J. et al. The master growth regulator DELLA binding to histone H2A is essential for DELLA-mediated global transcription regulation. Nat. Plants (2023). https://doi.org/10.1038/s41477-023-01477-y

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Received: 14 December 2022

Accepted: 04 July 2023

Published: 03 August 2023

DOI: https://doi.org/10.1038/s41477-023-01477-y

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