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

Abstract

Summary This study explores how allopolyploidization reshapes the biased expression and asymmetric epigenetic modification of homoeologous gene pairs, and examines the regulation types and epigenetic basis of expression bias. We analyzed the gene expression and four epigenetic modifications (DNA methylation, H3K4me3, H3K27me3 and H3K27ac) of 29 976 homoeologous gene pairs in resynthesized, natural allopolyploid Brassica napus and an in silico ‘hybrid’. We comprehensively elucidated the biased gene expression, asymmetric epigenetic modifications and the generational transmission characteristics of these homoeologous gene pairs in B. napus. We analyzed cis/trans effects and the epigenetic basis of homoeolog expression bias. There was a significant positive correlation between two active histone modifications and biased gene expression. We revealed that parental legacy was the dominant principle in the remodeling of homoeolog expression bias and asymmetric epigenetic modifications in B. napus, and further clarified that this depends on whether there were differences in the expression/epigenetic modifications of gene pairs in parents/progenitors. The maternal genome was dominant in the homoeolog expression bias of resynthesized B. napus, and this phenomenon was attenuated in natural B. napus. Furthermore, cis rather than trans effects were dominant when epigenetic modifications potentially affected biased expression of gene pairs in B. napus.

Asymmetric subgenomic chromatin architecture impacts on gene expression in resynthesized and natural allopolyploid Brassica napus

“…Our results showed that approximately 64 million ( B. rapa , A2) to 102 million ( B. oleracea , C2) raw reads were obtained from ATAC-Seq, more than 96% of which were clean reads in all samples (Table S1 ). According to previous studies 38 , 40 , we constructed an in silico ‘hybrid’ (A_C), which can fuse well with parental data for the convenience of subsequent studies, by mixing the reads of B. rapa and B. oleracea in equal proportions. As shown in Table S1 , an average of approximately 94.7%, 95.6%, 93.0%, and 98.0% of clean reads from the ATAC-Seq data of B. rapa , B. oleracea , resynthesized B. napus , and natural B. napus were mapped to the genome of B. napus 35 , and the GC content of each sample was higher than 40%.…”

“…14b–d and 17 ). To further explore the cause of the differences between the two subgenomes, we divided the genes of each genotype into homeologous genes and subgenome-unique genes according to our previous study 38 . As shown in Fig.…”

“…According to our previous study 38 , homeologous gene pairs were divided into A-/C-biased expression genes (A-/C-BEGs) and no biased expression genes (no-BEGs). The distribution of gene expression levels of homeologous gene pairs is shown in Fig.…”

“…With the whole genomes of these three species sequenced, they became a model system for studying allopolyploidization 35 – 37 . Although the asymmetric gene distribution 35 , asymmetric epigenetic modification 8 , 38 and bias gene expression 8 , 38 , 39 of subgenomes of B. napus have been revealed gradually, the differences in chromatin accessibility between subgenomes and the evolutionary changes of ACRs have not been reported in the allopolyploid B. napus . In this study, we generated genome-wide chromatin accessibility of natural B. napus , resynthesized B. napus and in silico ‘hybrid’ constructed by two progenitors.…”

Spatial and Temporal Transcriptomic Heredity and Asymmetry in an Artificially Constructed Allotetraploid Wheat (AADD)

“…tauschii (~5.5 MYA) (Glémin et al, 2019 ) and between far source parents of allopolyploids (Shi et al, 2012 ), which enabled the accumulation of genetic variations in cis elements, such as promoters, enhancers, and gene bodies. Additionally, recent studies in wheat and Brassica have suggested subgenome-specific epigenetic modifications are also key factors regulating homoeolog expression bias (Li M. et al, 2021 ; Wang et al, 2021 ); however, those latter factors still need further validation in multiple tissues or at different developmental stages in synthesis and natural allopolyploid systems. Notably, despite its prevalence among HSE patterns, the cis -only pattern was not particularly conserved among tissues, suggesting that trans effects, especially tissue-specific trans effects, may balance expression differences between homoeolog mates and play a further fine-tuning role in HSE regulation.…”