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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.
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.
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.
Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM) – Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)/CSIC, Campus
Montegancedo UPM, Pozuelo de Alarcón (Madrid), Madrid, Spain
Javier Barrero-Gil, Laura Bouza-Morcillo, Loreto Espinosa-Cores, Manuel Piñeiro & José A. Jarillo
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.
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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