TY - JOUR
T1 - GCN5 modulates salicylic acid homeostasis by regulating H3K14ac levels at the 5' and 3' ends of its target genes.
AU - Kim, SoonKap
AU - Piquerez, Sophie J M
AU - Ramirez-Prado, Juan S
AU - Mastorakis, Emmanouil
AU - Veluchamy, Alaguraj
AU - Latrasse, David
AU - Manza-Mianza, Deborah
AU - Brik-Chaouche, Rim
AU - Huang, Ying
AU - Rodriguez-Granados, Natalia Y
AU - Concia, Lorenzo
AU - Blein, Thomas
AU - Citerne, Sylvie
AU - Bendahmane, Abdelhafid
AU - Bergounioux, Catherine
AU - Crespi, Martin
AU - Mahfouz, Magdy M.
AU - Raynaud, Cécile
AU - Hirt, Heribert
AU - Ntoukakis, Vardis
AU - Benhamed, Moussa
N1 - KAUST Repository Item: Exported on 2020-12-08
Acknowledgements: Agence Nationale de la Recherche (ANR) [EPICLISPE ANR-18-CE20-0015]; Institut Universitaire de France (IUF); Biotechnology and Biological Science Research Council [BB/L019345/1, BB/M017982/1 to V.N., in part]; V.N. is also supported by the Royal Society. Funding for open access charge: ANR research grant.
PY - 2020/5/13
Y1 - 2020/5/13
N2 - 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.
AB - 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.
UR - http://hdl.handle.net/10754/666299
UR - https://academic.oup.com/nar/article/48/11/5953/5836186
UR - http://www.scopus.com/inward/record.url?scp=85086522843&partnerID=8YFLogxK
U2 - 10.1093/nar/gkaa369
DO - 10.1093/nar/gkaa369
M3 - Article
C2 - 32396165
SN - 0305-1048
VL - 48
SP - 5953
EP - 5966
JO - Nucleic acids research
JF - Nucleic acids research
IS - 11
ER -