A DNA adenine demethylase impairs PRC2-mediated repression of genes marked by a specific chromatin signature.

BACKGROUND: The Fe (II)- and α-ketoglutarate-dependent AlkB family dioxygenases are implicated in nucleotide demethylation. AlkB homolog1 (ALKBH1) is shown to demethylate DNA adenine methylation (6mA) preferentially from single-stranded or unpaired DNA, while its demethylase activity and function in the chromatin context are unclear. RESULTS: Here, we find that loss-of-function of the rice ALKBH1 gene leads to increased 6mA in the R-loop regions of the genome but has a limited effect on the overall 6mA level. However, in the context of mixed tissues, rather than on individual loci, the ALKBH1 mutation or overexpression mainly affects the expression of genes with a specific combination of chromatin modifications in the body region marked with H3K4me3 and H3K27me3 but depleted of DNA CG methylation. In the similar context of mixed tissues, further analysis reveals that the ALKBH1 protein preferentially binds to genes marked by the chromatin signature and has a function to maintain a high H3K4me3/H3K27me3 ratio by impairing the binding of Polycomb repressive complex 2 (PRC2) to the targets, which is required for both the basal and stress-induced expression of the genes. CONCLUSION: Our findings unravel a function of ALKBH1 to control the balance between the antagonistic histone methylations for gene activity and provide insight into the regulatory mechanism of PRC2-mediated H3K27me3 deposition within the gene body region.

An enhanced network of energy metabolism, lysine acetylation, and growth-promoting protein accumulation is associated with heterosis in elite hybrid rice.

Heterosis refers to the superior performance of a hybrid compared with its parental lines. Although several genetic and molecular models have been proposed to explain heterosis, it remains unclear how hybrid cells integrate complementary gene expression or activity to drive heterotic growth. In this work, we show that accumulation of growth-promoting and energy metabolism proteins, enhanced energy metabolism activities, and increased protein lysine acetylation were associated with superior growth of the panicle meristem in the elite hybrid rice Shanyou 63 relative to its parental varieties. Metabolism of nuclear/cytosolic acetyl-coenzyme A was also enhanced in the hybrid, which paralleled increases in histone H3 acetylation to selectively target the expression of growth-promoting and metabolic genes. Lysine acetylation of cellular proteins, including TARGET OF RAPAMYCIN complex 1, ribosomal proteins, and energy metabolism enzymes, was also augmented and/or remodeled to modulate their activities. The data indicate that an enhanced network of energy-producing metabolic activity and growth-promoting histone acetylation/gene expression in the hybrid could contribute to its superior growth rate and may constitute a model to explain heterosis.

Parental variation in CHG methylation is associated with allelic-specific expression in elite hybrid rice.

Heterosis refers to the superior performance of hybrid lines over inbred parental lines. Besides genetic variation, epigenetic differences between parental lines are suggested to contribute to heterosis. However, the precise nature and extent of differences between the parental epigenomes and the reprograming in hybrids that govern heterotic gene expression remain unclear. In this work, we analyzed DNA methylomes and transcriptomes of the widely cultivated and genetically studied elite hybrid rice (Oryza sativa) SY63, the reciprocal hybrid, and the parental varieties ZS97 and MH63, for which high-quality reference genomic sequences are available. We showed that the parental varieties displayed substantial variation in genic methylation at CG and CHG (H = A, C, or T) sequences. Compared with their parents, the hybrids displayed dynamic methylation variation during development. However, many parental differentially methylated regions (DMRs) at CG and CHG sites were maintained in the hybrid. Only a small fraction of the DMRs displayed non-additive DNA methylation variation, which, however, showed no overall correlation relationship with gene expression variation. In contrast, most of the allelic-specific expression (ASE) genes in the hybrid were associated with DNA methylation, and the ASE negatively associated with allelic-specific methylation (ASM) at CHG. These results revealed a specific DNA methylation reprogramming pattern in the hybrid rice and pointed to a role for parental CHG methylation divergence in ASE, which is associated with phenotype variation and hybrid vigor in several plant species.