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GCN5 modulates salicylic acid homeostasis by regulating H3K14ac levels at the 5ʹ and 3ʹ ends of its target genes

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Kim, Soonkap, Piquerez, Sophie J. M. , Ramirez-Prado, Juan S., Mastorakis, Emmanouil, Veluchamy, Alaguraj, Latrasse, David , Manza-Mianza, Deborah, Brik-Chaouche, Rim , Huang, Ying, Rodriguez-Granados, Natalia Y. et al.
(2020) GCN5 modulates salicylic acid homeostasis by regulating H3K14ac levels at the 5ʹ and 3ʹ ends of its target genes. Nucleic Acids Research, 48 (11). pp. 5953-5966. doi:10.1093/nar/gkaa369 ISSN 0305-1048.

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Official URL: https://doi.org/10.1093/nar/gkaa369

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Abstract

The modification of histones by acetyl groups has a key role in the regulation of chromatin structure and transcription. The Arabidopsis thaliana histone acetyltransferase GCN5 regulates histone modifications as part of the Spt-Ada-Gcn5 Acetyltransferase (SAGA) transcriptional coactivator complex. GCN5 was previously shown to acetylate lysine 14 of histone 3 (H3K14ac) in the promoter regions of its target genes even though GCN5 binding did not systematically correlate with gene activation. Here, we explored the mechanism through which GCN5 controls transcription. First, we fine-mapped its GCN5 binding sites genome-wide and then used several global methodologies (ATAC-seq, ChIP-seq and RNA-seq) to assess the effect of GCN5 loss-of-function on the expression and epigenetic regulation of its target genes. These analyses provided evidence that GCN5 has a dual role in the regulation of H3K14ac levels in their 5′ and 3′ ends of its target genes. While the gcn5 mutation led to a genome-wide decrease of H3K14ac in the 5′ end of the GCN5 down-regulated targets, it also led to an increase of H3K14ac in the 3′ ends of GCN5 up-regulated targets. Furthermore, genome-wide changes in H3K14ac levels in the gcn5 mutant correlated with changes in H3K9ac at both 5′ and 3′ ends, providing evidence for a molecular link between the depositions of these two histone modifications. To understand the biological relevance of these regulations, we showed that GCN5 participates in the responses to biotic stress by repressing salicylic acid (SA) accumulation and SA-mediated immunity, highlighting the role of this protein in the regulation of the crosstalk between diverse developmental and stress-responsive physiological programs. Hence, our results demonstrate that GCN5, through the modulation of H3K14ac levels on its targets, controls the balance between biotic and abiotic stress responses and is a master regulator of plant-environmental interactions.

Item Type: Journal Article
Subjects: Q Science > QH Natural history > QH426 Genetics
Divisions: Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH): Genetic regulation, Chromatin, Arabidopsis thaliana -- Genetics, Eukaryotic cells - Genetics
Journal or Publication Title: Nucleic Acids Research
Publisher: Oxford University Press
ISSN: 0305-1048
Official Date: 19 June 2020
Dates:
DateEvent
19 June 2020Published
12 May 2020Available
2 May 2020Accepted
Volume: 48
Number: 11
Page Range: pp. 5953-5966
DOI: 10.1093/nar/gkaa369
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access (Creative Commons)
Date of first compliant deposit: 12 May 2020
Date of first compliant Open Access: 2 June 2020
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
[EPICLISPE ANR-18-CE20-0015[ANR] Agence Nationale de la Recherchehttp://dx.doi.org/10.13039/501100001665
UNSPECIFIEDInstitut Universitaire de Francehttp://dx.doi.org/10.13039/501100004795
BB/L019345/1[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
BB/M017982/1[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
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