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H4 acetylation by the NuA4 complex is required for plastid transcription and chloroplast biogenesis

Abstract

Chloroplast biogenesis is crucial in plant development, as it is essential for the transition to autotrophic growth. This process is light-induced and relies on the orchestrated transcription of nuclear and plastid genes, enabling the effective assembly and regulation of the photosynthetic machinery. Here we reveal a new regulation level for this process by showing the involvement of chromatin remodelling in the nuclear control of plastid gene expression for proper chloroplast biogenesis and function. The two Arabidopsis homologues of yeast EPL1 protein, components of the NuA4 histone acetyltransferase complex, are essential for plastid transcription and correct chloroplast development and performance. We show that EPL1 proteins are light-regulated and necessary for concerted expression of nuclear genes encoding most components of chloroplast transcriptional machinery, directly mediating H4K5ac deposition at these loci and promoting the expression of plastid genes required for chloroplast biogenesis. These data unveil a NuA4-mediated mechanism regulating chloroplast biogenesis that links the transcription of nuclear and plastid genomes during chloroplast development.

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Fig. 1: Arabidopsis EPL1 proteins directly interact with NuA4 Piccolo subunits.
Fig. 2: EPL1 genes play a redundant role in early developmental stages of chloroplast biogenesis.
Fig. 3: EPL1 protein levels are regulated by light exposure.
Fig. 4: Transcriptomic profiling of epl1ab-1 mutant plants reveals the downregulation of genes involved in plastid transcription.
Fig. 5: Loss of EPL function causes lower H4K5 acetylation levels in genes involved in plastid transcription.
Fig. 6: EPL1B protein binds chromatin at key loci for plastid transcriptional machinery.
Fig. 7: Light promotes H4 acetylation at key loci for plastid transcription.

Data availability

The materials generated in this work are available upon request to the corresponding authors. Sequence data related to this article can be found in the Arabidopsis information portal (https://www.araport.org/) under the accession numbers EPL1A (At1g16690), EPL1B (At1g79020), HAM1 (At5g64610), ING2 (At1g54390) and EAF6 (At4g14385). The complete genome-wide data from this publication are already deposited in the Gene Expression Omnibus database (www.ncbi.nlm.nih.gov/geo/) under accession number GSE180614. Source data are provided with this paper.

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Acknowledgements

We thank T. Hernández-Verdeja for the critical reading of the manuscript and also V. M. Quesada (Univ. Miguel Hernandez, Elche, Spain) and M. Cheng (Duke University, Durham, NC, USA) for kindly providing sca3-2 (ref. 20) and hmr-22 (ref. 38) mutants, respectively. This work was funded by the Spanish Ministry of Economy, Industry, and Competitiveness (grant Nos. BIO2016-77559-R and PID2019-104899GB-I00 to M.P. and J.A.J. from MCIN/AEI/10.13039/501100011033 and FEDER; FPI fellowship No. BES-2017-07992 from MCIN/AEI/10.13039/501100011033 and FSE to L.B-M.) and INIA (FPI fellowship No. FPI-SGIT-2016-08 to L.E.-C.). We acknowledge the ‘Severo Ochoa Program for Centres of Excellence in R&D’ from the Agencia Estatal de Investigación of Spain (grant No. SEV-2016-0672 (2017-2021) from MCIN/AEI/10.13039/501100011033) for supporting the scientific services used in this work.

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M.P. and J.A.J. conceived this project; L.E.-C. analysed protein–protein interactions between NuA4-C subunits. J.B.-G. and L.B.-M. performed the rest of the experiments. J.B.-G., M.P. and J.A.J. designed all the experiments, analysed the data and wrote the paper.

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Correspondence to Manuel Piñeiro or José A. Jarillo.

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Nature Plants thanks Enrique Lopez-Juez and the other, anonymous, reviewer(s) for their contribution to the peer review of this work

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Supplementary Figs. 1–8, description of Supplementary tables and unmodified gel image of Supplementary Fig. 2.

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Unprocessed western blots.

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Unprocessed western blots.

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Statistical source data for Fig. 4.

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Barrero-Gil, J., Bouza-Morcillo, L., Espinosa-Cores, L. et al. H4 acetylation by the NuA4 complex is required for plastid transcription and chloroplast biogenesis. Nat. Plants 8, 1052–1063 (2022). https://doi.org/10.1038/s41477-022-01229-4

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