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. 2019 Nov 27;12(1):86.
doi: 10.1186/s12284-019-0342-6.

Genome-wide Profiling of Histone Lysine Butyrylation Reveals its Role in the Positive Regulation of Gene Transcription in Rice

Shuai Liu  1   2 , Guanqing Liu  1   2 , Peifeng Cheng  3 , Chao Xue  1   2 , Yong Zhou  1   2 , Xu Chen  1   2 , Lu Ye  1   2 , Zhongying Qiao  4 , Tao Zhang  5 , Zhiyun Gong  6
Affiliations

Genome-wide Profiling of Histone Lysine Butyrylation Reveals its Role in the Positive Regulation of Gene Transcription in Rice

Shuai Liu et al. Rice (N Y). .

Abstract

Background: Histone modifications play important roles in growth and development of rice (Oryza sativa L.). Lysine butyrylation (Kbu) with a four-carbon chain is a newly-discovered histone acylation modification in rice.

Main body: In this study, we performed chromatin immunoprecipitation sequencing (ChIP-seq) analyses, the result showed that major enrichment of histone Kbu located in genebody regions of rice genome, especially in exons. The enrichment level of Kbu histone modification is positively correlated with gene expression. Furthermore, we compared Kbu with DNase-seq and other histone modifications in rice. We found that 60.06% Kub enriched region co-located with DHSs in intergenic regions. The similar profiles were detected among Kbu and several acetylation modifications such as H3K4ac, H3K9ac, and H3K23ac, indicating that Kbu modification is an active signal of transcription. Genes with both histone Kbu and one other acetylation also had significantly increased expression compared with genes with only one acetylation. Gene Ontology (GO) enrichment analysis revealed that these genes with histone Kbu can regulate multiple metabolic process in different rice varieties.

Conclusion: Our study showed that the lysine butyrylation modificaiton may promote gene expression as histone acetylation and will provide resources for futher studies on histone Kbu and other epigenetic modifications in plants.

Keywords: ChIP-seq; Histone modification; Lysine butyrylation (Kbu); Oryza sativa; Transcriptional regulation.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
An overview of Kbu modifications in rice. a lysine butyrylation was detected in the nucleus and cytoplasm of two-week-old rice root cells by immunofluorescence using an anti-Kbu antibody (green), and the nuclei were stained with DAPI (red). Scale bars: 5 μm. b Western blot analysis of histones in 14-day-old rice seedling leaves with anti-Kbu antibody
Fig. 2
Fig. 2
The genomic distribution of histone Kbu-enriched regions in rice. a Genome-wide distribution of histone Kbu in the rice genome. The promoter regions are defined as the 1 kb of DNA sequence directly upstream of the gene transcription start site (TSS). b Mapping of Kbu sites, RNA-seq reads and gene loci in a 60,000 base pair region on Chr2:8,100,000 – 8,160,000. c Distribution of Kbu density around differentially expressed genes. The Kbu modification level was calculated by the number of reads per kilobase in the mapped genomic region. The arrow indicates the direction of transcription from the transcription start site (TSS). The rice genes were divided into six categories based the expression level from the top 20% to the bottom 0% based on published RNA-seq data from seedlings of the same rice cultivar at the same stage of development (Zhang et al. 2012)
Fig. 3
Fig. 3
Gene transcription in the rice genome and the genomic distribution of histone Kbu and other modifications. Visualization of the Kbu sites and 12 other histone modifications against 10 gene loci in a 100,000 base pair region on Chr2:12,839,000 – 12,939,000
Fig. 4
Fig. 4
The percentage of histone Kbu-enriched regions that overlap with regions enriched with 12 other histone modifications. a Heatmap b Histogram
Fig. 5
Fig. 5
Heatmaps of histone Kbu, H3K9ac, H3K27me3, and DHS in gene regions and intergenic regions. The DNA regions 1 kb upstream and 1 kb downstream of the transcription start sites were analyzed. Density was calculated by the number of reads per kilobase region per million mapped reads
Fig. 6
Fig. 6
Comparisons of the expression of genes associated with different combinations of histone modifications. The non-TE gene expression values (FPKM: Fragments per Kilobase Million) of each combination are indicated by box plots. All: all rice genes. Kbu: all genes with Kbu modifications. Both: genes with both Kbu and one of the other nine modifications as shown. The asterisks (*) indicate a significant difference between the pairwise combinations (p < 2.2e-16, Kolmogorov-Smirnov test)
Fig. 7
Fig. 7
Functional annotation of the lysine butyrylome. Representative GO annotations of histone Kbu sites for genes in the three primary GO categories “biological process”, “molecular function”, and “cellular component”. Gene ontology (GO) analysis was performed on 1480 genes that showed significant histone Kbu enrichment out of 14,808 Kbu-related genes in this study
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