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The master growth regulator DELLA binding to histone H2A is essential for DELLA-mediated global transcription regulation

Nature Plants volume 9, pages 1291–1305 (2023)Cite this article

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Abstract

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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Fig. 1: All missense rga hypomorphs are clustered within the GRAS domain.
Fig. 2: Missense rga mutant proteins showed varying degrees of reduced activity.
Fig. 3: Y2H assay showed rga mutations in the LHR1 subdomain reduced interaction with BZR1, PIF3 and TCP14, whereas rga-2 and rga-11 in PFYRE did not.
Fig. 4: Pulldown and co-IP assays showed rga mutations in the LHR1 subdomain reduced interaction with BZR1, PIF3 and IDD3, whereas rga-2 and rga-11 in PFYRE did not.
Fig. 5: rga mutations in the PFYRE subdomain impaired association with target chromatin globally by ChIP–seq analysis.
Fig. 6: cis-Elements for bHLH, bZIP, TCP and IDD TFs were most enriched near RGA binding peaks associated with RGA direct target genes.
Fig. 7: rga-2 and rga-11 reduced RGA binding to histone H2A.
Fig. 8: Working model of DELLA-mediated transcriptional regulation.

Data availability

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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Acknowledgements

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.

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Author notes

  1. Hao Tian

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

  2. Jeongmoo Park

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

  3. Rodolfo Zentella

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

  4. Rodolfo Zentella

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

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

Authors and Affiliations

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

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

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

    Dong-Ha Oh & Maheshi Dassanayake

  3. 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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Contributions

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.

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Correspondence to Tai-Ping Sun.

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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 9, 1291–1305 (2023). https://doi.org/10.1038/s41477-023-01477-y

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