Asymmetric epigenome maps of subgenomes reveal imbalanced transcription and distinct evolutionary trends in Brassica napus

Abstract

The complexity of the epigenome landscape and transcriptional regulation is significantly increased during plant polyploidization, which drives genome evolution and contributes to the increased adaptability to diverse environments. However, a comprehensive epigenome map of Brassica napus is still unavailable. In this study, we performed integrative analysis of five histone modifications, RNA polymerase II occupancy, DNA methylation, and transcriptomes in two B. napus lines (2063A and B409), and established global maps of regulatory elements, chromatin states, and their dynamics for the whole genome (including the An and Cn subgenomes) in four tissue types (young leaf, flower bud, silique, and root) of these two lines. Approximately 65.8% of the genome was annotated with different epigenomic signals. Compared with the Cn subgenome, the An subgenome possesses a higher level of active epigenetic marks and lower level of repressive epigenetic marks. Genes from subgenome-unique regions contribute to the major differences between the An and Cn subgenomes. Asymmetric histone modifications between homeologous gene pairs reflect their biased expression patterns. We identified a novel bivalent chromatin state (with H3K4me1 and H3K27me3) in B. napus that is associated with tissue-specific gene expression. Furthermore, we observed that different types of duplicated genes have discrepant patterns of histone modification and DNA methylation levels. Collectively, our findings provide a valuable epigenetic resource for allopolyploid plants.

Asymmetric epigenetic modification and homoeolog expression bias in the establishment and evolution of allopolyploid Brassica napus

“…We found that the C subgenome was significantly DNA methylation dominant in both resynthesized and natural B. napus (Figs 2a, Fig. S3), which was consistent with the findings of previous studies (Chalhoub et al ., 2014; Bird et al ., 2021; Zhang et al ., 2021). Chalhoub et al .…”

A novel bivalent chromatin associates with rapid induction of camalexin biosynthesis genes in response to a pathogen signal in Arabidopsis

“…The biological function of bivalent chromatins has long been hypothesized to poise gene expression for rapid activation upon signal perception. To date, this model has been tested only in mammalian stem cells and cancer cells ( Zeng et al, 2019 ; Zhang et al, 2021 ; Deng et al, 2013 ), and no direct evidence is available in a whole organism context. As a first step to understand the role of the H3K27me3-H3K18ac bivalent chromatin on camalexin genes, we examined the transcriptional kinetics of camalexin biosynthesis genes under FLG22 induction in wild type and mutant lines with defective deposition of H3K27me3 or H3K18ac.…”

“…In plants, the H3K27m3-H3K4me3 bivalent chromatin has been observed at FLOWERING LOCUS C ( FLC ) ( Jiang et al, 2008 ) in A. thaliana and genes associated with cold stress in potato tuber ( Zeng et al, 2019 ). Recently, a novel bivalent chromatin formed by H3K27me3 and H3K4me1 was identified in Brassica napus ( Zhang et al, 2021 ). Therefore, bivalent chromatins can be formed by different pairs of epigenetic marks.…”

Rapid and Low-Input Profiling of Histone Marks in Plants Using Nucleus CUT&Tag

“…Enhanced ChIP-seq is an efficient protocol in profiling histone marks. It was used to map rice and B. napus reference epigenomes with considerably low background noise (Zhang et al, 2020;Zhao et al, 2020). To compare the signal-to-noise ratio of nCUT&Tag relative to eChIP-seq, we downsampled the sequencing reads at varying depth from 1-M to 24-M. Then we called peaks and calculated FRiP values under the same sequencing depth (Supplementary Table 3).…”

“…nCUT&Tag Is Scalable for Chromatin Profiling in Other Plant Species Enhanced ChIP-seq has been used to map high-quality reference epigenomes in rice and B. napus (Zhang et al, 2020;Zhao et al, 2020). To examine whether nCUT&Tag could be applied to other plant species, we generated the nCUT&Tag data of the H3K4me3 antibody with crosslinked leaves of the dicot rapeseed (B. napus) (Figure 6A).…”