Global epigenomic analysis indicates that Epialleles contribute to Allele-specific expression via Allele-specific histone modifications in hybrid rice

Background

For heterozygous genes, alleles on the chromatin from two different parents exhibit histone modification variations known as allele-specific histone modifications (ASHMs). The regulation of allele-specific gene expression (ASE) by ASHMs has been reported in animals. However, to date, the regulation of ASE by ASHM genes remains poorly understood in higher plants.

Results

We used chromatin immunoprecipitation followed by next-generation sequencing (ChIP-seq) to investigate the global ASHM profiles of trimethylation on histone H3 lysine 27 (H3K27me3) and histone H3 lysine 36 (H3K36me3) in two rice F1 hybrids. A total of 522 to 550 allele-specific H3K27me3 genes and 428 to 494 allele-specific H3K36me3 genes were detected in GL × 93-11 and GL × TQ, accounting for 11.09% and 26.13% of the total analyzed genes, respectively. The epialleles between parents were highly related to ASHMs. Further analysis indicated that 52.48% to 70.40% of the epialleles were faithfully inherited by the F1 hybrid and contributed to 33.18% to 46.55% of the ASHM genes. Importantly, 66.67% to 82.69% of monoallelic expression genes contained the H3K36me3 modification. Further studies demonstrated a significant positive correlation of ASE with allele-specific H3K36me3 but not with H3K27me3, indicating that ASHM-H3K36me3 primarily regulates ASE in this study.

Conclusions

Our results demonstrate that epialleles from parents can be inherited by the F1 to produce ASHMs in the F1 hybrid. Our findings indicate that ASHM-H3K36me3, rather than H3K27me3, mainly regulates ASE in hybrid rice.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1454-z) contains supplementary material, which is available to authorized users.     

Histone H3 lysine 4 mono-methylation does not require ubiquitination of histone H2B

The yeast Set1-complex catalyzes histone H3 lysine 4 (H3K4) methylation. Using N-terminal Edman sequencing, we determined that 50% of H3K4 is methylated and consists of roughly equal amounts of mono, di and tri-methylated H3K4. We further show that loss of either Paf1 of the Paf1 elongation complex, or ubiquitination of histone H2B, has only a modest effect on bulk histone mono-methylation at H3K4. Despite the fact that Set1 recruitment decreases in paf1delta cells, loss of Paf1 results in an increase of H3K4 mono-methylation at the 5' coding region of active genes, suggesting a Paf1-independent targeting of Set1. In contrast to Paf1 inactivation, deleting RTF1 affects H3K4 mono-methylation at the 3' coding region of active genes and results in a decrease of global H3K4 mono-methylation. Our results indicate that the requirements for mono-methylation are distinct from those for H3K4 di and tri-methylation, and point to differences among members of the Paf1 complex in the regulation of H3K4 methylation.     

植物组蛋白赖氨酸甲基化建立过程及其遗传性研究进展

表观遗传学主要包括DNA甲基化、组蛋白修饰和非编码RNA,组蛋白甲基化作为组蛋白修饰中的一种重要修饰,在植物体的发育和环境适应中发挥着重要作用。组蛋白甲基化主要发生在赖氨酸残基上,同时根据不同的赖氨酸位点和每个赖氨酸位点甲基化程度的不同,形成了不同的赖氨酸甲基化修饰。根据对基因的不同功能,通常将组蛋白赖氨酸甲基化修饰分为2大类:(1)能够促进基因表达的,如H3K4me3和H3K36me3;(2)能够抑制基因表达的,如H3K9me2和H3K27me3。不同的组蛋白赖氨酸甲基化去甲基化过程需要相应的阅读(reader)、书写(writer)和擦除(eraser)3种蛋白。同时,组蛋白赖氨酸甲基化的遗传性质目前还不是很清楚。综述了植物中组蛋白赖氨酸甲基化建立与去除过程,以及对组蛋白赖氨酸甲基化可遗传性的探讨。