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.

Brassica napus and its diploid progenitors (B. rapa and B. oleracea) are suitable for studying the problems associated with polyploidization. As an important anti-stress protein, RCI2 proteins widely exist in various tissues of plants, and are crucial to plant growth, development, and stress response. In this study, the RCI2 gene family was comprehensively identified and analyzed, and 9, 9, and 24 RCI2 genes were identified in B. rapa, B. oleracea, and B. napus, respectively. Phylogenetic analysis showed that all of the identified RCI2 genes were divided into two groups, and further divided into three subgroups. Ka/Ks analysis showed that most of the identified RCI2 genes underwent a purifying selection after the duplication events. Moreover, gene structure analysis showed that the structure of RCI2 genes is largely conserved during polyploidization. The promoters of the RCI2 genes in B. napus contained more cis-acting elements, which were mainly involved in plant development and growth, plant hormone response, and stress responses. Thus, B. napus might have potential advantages in some biological aspects. In addition, the changes of RCI2 genes during polyploidization were also discussed from the aspects of gene number, gene structure, gene relative location, and gene expression, which can provide reference for future polyploidization analysis.

The nucleosomes occupying the chromosomal start sites of transcription contain the histone H2A variant H2A.Z in place of H2A. Upon galactose induction, nucleosomes are evicted from the GAL1 locus in Saccharomyces cerevisiae cells. H2A.Z (which is encoded by the HTZ1 gene in S. cerevisiae) is required for the eviction of the GAL1 promoter nucleosome and for the transcriptional activation of the GAL1 gene; however, histones are also important for transcriptional repression and we asked in the present paper if H2A.Z also plays a role in the glucose repression of the GAL1 promoter. With the help of a fusion of the URA3 ORF (open reading frame) to the GAL1 promoter, we were able to detect two different epigenetic transcription states of the GAL1 promoter in glucose-grown cells lacking H2A.Z: a repressed state that is occupied by a H2A-containing nucleosome and a derepressed state that is nucleosome-free. These two chromatin states are inherited stably through many cell divisions. According to the model described in the present paper, the role of H2A.Z is to facilitate the addition and removal of promoter nucleosomes and to prevent the formation of unfavourable stable epigenetic chromatin structures, which are not in accordance with the environmental conditions.