Histone acetyltransferase GCN5 is essential for heat stress‐responsive gene activation and thermotolerance in Arabidopsis

Abstract

SUMMARYExposure to temperatures exceeding the normal optimum levels, or heat stress (HS), constitutes an environmental disruption for plants, resulting in severe growth and development retardation. Here we show that loss of function of the Arabidopsis histone acetyltransferase GCN5 results in serious defects in terms of thermotolerance, and considerably impairs the transcriptional activation of HS-responsive genes. Notably, expression of several key regulators such as the HS transcription factors HSFA2 and HSFA3, Multiprotein Bridging Factor 1c (MBF1c) and UV-HYPERSENSITIVE 6 (UVH6) is down-regulated in the gcn5 mutant under HS compared with the wild-type. Chromatin immunoprecipitation (ChIP) assays indicated that GCN5 protein is enriched at the promoter regions of HSFA3 and UVH6 genes, but not in HSFA2 and MBF1c, and that GCN5 facilitates H3K9 and H3K14 acetylation, which are associated with HSFA3 and UVH6 activation under HS. Moreover, constitutive expression of UVH6 in the gcn5 mutant partially restores heat tolerance. Taken together, our data indicate that GCN5 plays a key role in the preservation of thermotolerance via versatile regulation in Arabidopsis. In addition, expression of the wheat TaGCN5 gene re-establishes heat tolerance in Arabidopsis gcn5 mutant plants, suggesting that GCN5-mediated thermotolerance may be conserved between Arabidopsis and wheat.

Histone acetyltransferase general control non‐repressed protein 5 (GCN5) affects the fatty acid composition of Arabidopsis thaliana seeds by acetylating fatty acid desaturase3 (FAD3)

“…C18:3, C16:3) content positively correlates with thermotolerance (Murakami et al ., ; Matsuda et al ., ; Roman et al ., ). Thus, the decreased ALA (C18:3) content in the gcn5 mutant leaves is inconsistent with our previous observation that the loss of GCN5 function results in significant defects in thermotolerance (Hu et al ., ), which indicates that GCN5‐mediated lipid metabolism and thermotolerance are relatively independent.…”

“…Histone acetylation/deacetylation is a dynamic process that plays an important role in gene regulation through the antagonist actions of HATs and HDACs. As a HAT, GCN5 is a versatile regulator of Arabidopsis biology, including floral meristem development, light responsiveness, root growth, thermotolerance and iron homeostasis (Bertrand et al ., ; Benhamed et al ., ; Kornet and Scheres, ; Hu et al ., ; Xing et al ., ). We observed that GCN5 is essential for lipid metabolism in Arabidopsis seeds.…”

“…Moreover, GCN5 is also involved in cell differentiation, shoot and floral meristem formation, light and abiotic stress (e.g. heat and cold) responses, and iron homeostasis in Arabidopsis (Laux et al ., ; Stockinger et al ., ; Benhamed et al ., ; Long et al ., ; Hu et al ., ; Xing et al ., ). In this study, we observed that in seeds harboring a GCN5 mutation, seed oil was significantly decreased compared with the wild‐type Arabidopsis.…”

Histone acetyltransferase GCN5 contributes to cell wall integrity and salt stress tolerance by altering the expression of cellulose synthesis genes

“…GCN5 is a versatile regulator of developmental and inducible gene expression in Arabidopsis and is required for the regulation of divergent sets of stress response genes (Servet et al ., ; Hu et al ., ; Xing et al ., ). To illustrate the mechanisms underlying the involvement of GCN5 in salt stress responses, we identified 1330 genes that were upregulated after salt stress, of which 471 are affected by GCN5.…”

Genome Wide Analysis of Fatty Acid Desaturation and Its Response to Temperature

“…Interestingly, Wang et al (2016) recently reported that Arabidopsis mutants in a number of histone deacetylases exhibit changes in seed fatty acid composition and that H3K9/14 acetylation of FAD3 influences its expression level (Wang et al, 2016). DNA acetylation in Arabidopsis has been implicated in heat stress-responsive gene expression (Hu et al, 2015). Therefore, although an hd2d mutant has yet to be analyzed, it is conceivable that this gene might play a role in controlling v-6 ΔDE.…”