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. 2018 Sep 25;19(1):144.
doi: 10.1186/s13059-018-1533-y.

Dynamics and functional interplay of histone lysine butyrylation, crotonylation, and acetylation in rice under starvation and submergence

Yue Lu  1 , Qiutao Xu  1 , Yuan Liu  1 , Yue Yu  1 , Zhong-Yi Cheng  2 , Yu Zhao  1 , Dao-Xiu Zhou  3   4
Affiliations

Dynamics and functional interplay of histone lysine butyrylation, crotonylation, and acetylation in rice under starvation and submergence

Yue Lu et al. Genome Biol. .

Abstract

Background: Histone lysine acylations by short-chain fatty acids are distinct from the widely studied histone lysine acetylation in chromatin, although both modifications are regulated by primary metabolism in mammalian cells. It remains unknown whether and how histone acylation and acetylation interact to regulate gene expression in plants that have distinct regulatory pathways of primary metabolism.

Results: We identify 4 lysine butyrylation (Kbu) sites (H3K14, H4K12, H2BK42, and H2BK134) and 45 crotonylation (Kcr) sites on rice histones by mass spectrometry. Comparative analysis of genome-wide Kbu and Kcr and H3K9ac in combination with RNA sequencing reveals 25,306 genes marked by Kbu and Kcr in rice and more than 95% of H3K9ac-marked genes are marked by both. Kbu and Kcr are enriched at the 5' region of expressed genes. In rice under starvation and submergence, Kbu and Kcr appear to be less dynamic and display changes in different sets of genes compared to H3K9ac. Furthermore, Kbu seems to preferentially poise gene activation by external stresses, rather than internal circadian rhythm which has been shown to be tightly associated with H3K9ac. In addition, we show that rice sirtuin histone deacetylase (SRT2) is involved in the removal of Kcr.

Conclusion: Kbu, Kcr, and H3K9ac redundantly mark a large number of active genes but display different responses to external and internal signals. Thus, the proportion of rice histone lysine acetylation and acylation is dynamically regulated by environmental and metabolic cues, which may represent an epigenetic mechanism to fine-tune gene expression for plant adaptation.

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Figures

Fig. 1
Fig. 1
Identification of rice histone Kbu and Kcr modifications. a Detection by immunoblotting of Kbu and Kcr in histones isolated from rice, Arabidopsis, tobacco, and maize seedlings. b Rice histone Kbu and Kcr sites detected by mass spectrometry (see Additional file 1: Figure S1 and Additional file 2: Dataset 1)
Fig. 2
Fig. 2
Distribution of histone Kbu and Kcr modifications in the rice genome. a Distribution of histone Kbu/Kcr peaks in different regions of the rice genome. b Average genome-wide occupancies of Kbu and Kcr in different categories of genes. c Correlogram of Kbu, Kcr, and other histone modifications. The genome was divided into 1-kb bins and TPM values of each bin were used to calculate correlation coefficients
Fig. 3
Fig. 3
Different combinations of Kbu, Kcr, and H3K9ac modifications affect gene expression. a Venn diagram of Kbu/Kcr/H3K9ac modified genes. b Average genome-wide occupancies of H3K9ac, Kbu, and Kcr in all genes and genes with only Kbu and Kcr modifications (N = 4795). c Density curve of H3K9ac/Kbu/Kcr modification proportions in all genes. d Expression levels of genes with different modification profiles. Numbers of genes: H3K9ac (N = 418), H3K9ac + Kbu (N = 229), H3K9ac + Kcr (N = 217), H3K9ac + Kbu + Kcr (N = 20511), Kbu (N = 1234), Kcr (N = 784), Kbu + Kcr (N = 4795), all genes (N = 56384). Y-axis stands for gene expression levels calculated by log10 (FPKM + 0.001). e Expression levels of genes with different proportion of H3K9ac, Kbu, and Kcr under normal conditions. f Total acylation levels of genes with different combinations of the marks
Fig. 4
Fig. 4
Kbu, Kcr, and H3K9ac changes in rice under starvation and submergence. a Overlapping of genes with Kbu/Kcr/H3K9ac changes (increase and decrease) after starvation and submergence treatments. Genes with TPM changes > 1.5-fold in both replicates were taken into consideration. b Igv screenshots showing H3K9ac, Kbu, and Kcr peaks in different treatments. Arrow indicates a differentially modified region (see Additional file 1: Figure S5)
Fig. 5
Fig. 5
Role of Kbu, Kcr, and H3K9ac dynamics in stress-induced and diurnal gene expression. a Plots of Kbu, Kcr, and HK9ace changes of differentially expressed genes in rice under starvation and submergence. X-axis: gene expression fold change (log2); Y-axis: gene lysine acylation changes (log2); genes with acylation level (TPM) change > 1.5-fold are marked by colors. b Scatter plot showing the proportion change of H3K9ac and Kbu/Kcr in starvation/submergence DEGs. Proportion of each modification was calculated by its TPM in gene body divided by total acylation TPM value (K9ac + Kbu + Kcr) in each gene. c Enrichment of starvation and submergence upregulated genes with different combinations of the acylation marks. **Significant enrichments (p < 0.01). d Enrichment of circadian-regulated genes marked by different combinations of lysine acylations (see Additional file 1: Figure S6). **Significant enrichments (p < 0.01)
Fig. 6
Fig. 6
Rice SRT2 has a decrotonylase activity. a Histone H3K9ac, Kbu, and Kcr levels in SRT1 RNAi, srt2 CRISPR, and hda705 CRISPR plants compared to wild types (MH63, DJ, and ZH11) were detected by immunoblotting. Each sample was loaded twice and two replicates for each immunoblot are shown. Relative quantified signals of each band are indicated with the first wild type loading set as 1. b In vitro lysine decrotonylation activity of OsSRT2 by fluorometric assays. Left panel, assays with E. coli-produced OsSRT1-GST protein. GST and mutated OsSRT2 (S123 Y and H215 Y in the catalytic domain) were used as control. Right panel: assays with OsSRT1 protein produced in transient transfected tobacco cells. Bars are means ± SD from three biological replicates
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