Arabidopsis GCN5, HD1, and TAF1/HAF2 Interact to Regulate Histone Acetylation Required for Light-Responsive Gene Expression

Abstract

We previously showed that Arabidopsis thaliana histone acetyltransferase TAF1/HAF2 is required for the light regulation of growth and gene expression, and we show here that histone acetyltransferase GCN5 and histone deacetylase HD1/HDA19 are also involved in such regulation. Mutation of GCN5 resulted in a long-hypocotyl phenotype and reduced light-inducible gene expression, whereas mutation of HD1 induced opposite effects. The double mutant gcn5 hd1 restored a normal photomorphogenic phenotype. By contrast, the double mutant gcn5 taf1 resulted in further loss of light-regulated gene expression. gcn5 reduced acetylation of histones H3 and H4, mostly on the core promoter regions, whereas hd1 increased acetylation on both core and more upstream promoter regions. GCN5 and TAF1 were both required for H3K9, H3K27, and H4K12 acetylation on the target promoters, but H3K14 acetylation was dependent only on GCN5. Interestingly, gcn5 taf1 had a cumulative effect mainly on H3K9 acetylation. On the other hand, hd1 induced increased acetylation on H3K9, H3K27, H4K5, and H4K8. GCN5 was also shown to be directly associated with the light-responsive promoters. These results suggest that acetylation of specific histone Lys residues, regulated by GCN5, TAF1, and HD1, is required for light-regulated gene expression.

Arabidopsis histone deacetylase 6: a green link to RNA silencing

“…Antisense knockdown plants or stable insertion mutants of AtHda19 exhibit pleiotropic developmental phenotypes, such as early senescence, reduced apical dominance, homeotic changes, heterochronic developmental shifts and flower defects coupled with male and female sterility, thus highlighting an essential function of AtHDA19 in plant development (Tian and Chen, 2001;Tian et al, 2003). Furthermore, AtHDA19 antagonizes the histone acetyltransferase AtGCN5 in regulating the maintenance of embryo axis formation and light-responsive gene expression, respectively (Benhamed et al, 2006;Long et al, 2006). Besides development, AtHDA19 is required for jasmonic acid-and ethylene-mediated plant responses to plant pathogens, for responses of cultured cells to sucrose starvation and for transcriptional repression in response to abscisic acid, drought and salt stress (Song et al, 2005;Zhou et al, 2005;Nicolai et al, 2006;Song and Galbraith, 2006).…”

Histone acetyltransferase GCN5 interferes with the miRNA pathway in Arabidopsis

“…In addition, accumulation of a subset of miRNAs was decreased in hda19/hd1 and hda9 mutants (Figure 7). HDA19/AtHD1 has been shown to be a general HDAC required for the expression of a large number of genes and functions together with GCN5 as an antagonistic couple in a few regulatory pathways [9,35]. However, HDA19 seemed to play a less important role than HDA9 in MIRNA gene expression (Figure 7) …”

“…Aliquots of the dilution were used for an immunoprecipitation assay. The antibody of GCN5 was described in Benhamed et al [9]. Immunoprecipitated DNA was analyzed by PCR using primer sets listed in Supplementary information, Table S2.…”

“…gcn5-2, the association was much reduced (Figure 5A), suggesting that these MIRNA genes may be direct targets of GCN5. As GCN5 is required for acetylation of histone H3 lysine 14 (H3K14) [9,32], ChIP assays were performed with antibodies against acetylated H3K14. The analysis revealed that in the mutants H3K14 acetylation was reduced mainly on the GCN5 targets ( Figure 5B).…”

“…An ortholog found in Arabidopsis is also called HAG1 [7]. T-DNA insertion mutations of Arabidopsis GCN5 induce pleiotropic defects that alter many aspects of plant development and 900 npg responses to environmental conditions, such as light and cold [8][9][10]. Arabidopsis GCN5 found to be involved mostly in the acetylation of histone H3K9, K14 and K27, is shown to be required for the expression of a large number of genes [8,11,12], suggesting that this protein is involved in both long-term epigenetic regulation of chromatin modification and short-term control of transcriptional switches.…”