Genomic asymmetry of the Brassica napus seed: epigenetic contributions of DNA methylation and small RNAs to subgenome bias

Abstract

Polyploidy is a persistent phenomenon in angiosperm genome evolution that is hypothesized to have contributed to the diversity of extant flowering plants. Brassica napus, one of the world's most important angiosperm oilseed species, originated from the interspecific hybridization of Brassica rapa (A n ) and Brassica oleracea (C n ). While the trends of genome dominance in transcriptomics are beginning to emerge, less is known about the epigenetic and small RNA landscapes in polyploids during reproductive development. The seed is the pivotal developmental transition into the new sporophytic generation, and experiences substantial epigenetic modifications over time. Here, we investigated the prevalence of bias in the contexts of DNA methylation and small interfering (si)RNA profiles in both subgenomes (A n and C n ), as well as the ancestral fractionated genomes across B. napus seed development. We report ubiquitous C n subgenome bias of siRNA expression and cytosine methylation, with DNA methylation being particularly abundant on gene promoters in the C n subgenome. Further, we provide evidence that siRNA transcriptional patterns were conserved within the ancestral triplicated subgenomes of B. napus, but not across the A n and C n subgenomes. We discuss how methylation patterns in the B. napus seed relate to genes, promoter regions, siRNA loci and transposable elements through the lens of genome fractionation and polyploidization. Taken together we provide evidence for epigenetic regulation selectively silencing the C n subgenome during seed development, and explore the impact of genome fractionation on the epigenetic components of the B. napus seed.

Genomic asymmetric epigenetic modification of transposable elements is involved in gene expression regulation of allopolyploid Brassica napus

“…The TEs of the C n subgenome in B. napus were more densely and abundantly distributed in and around these genes (Figure 1a; Table S2). We also observed higher TE methylation levels in the C n subgenome (Figure 6a), similar to those observed in B. napus seeds (Ziegler et al, 2023). However, TEs on the A n subgenome seemed to be more susceptible to epigenetic modification, and TE methylation levels were more likely to be altered in the in silico 'hybrid', resynthesized, and natural B. napus (Figure 6e).…”

“…As a critical component of the RdDM pathway, 24-nt siRNAs are the most abundant small RNA in plant genomes (Chow & Mosher, 2023), direct TE methylation to regulate gene expression, and control rice tillering and stress resistance (Sun et al, 2021;Xu et al, 2020). The number of siRNAs originating from TEs increases during seed development in B. napus, promoting selective subgenome silencing (Ziegler et al, 2023). The CHH methylation level of TEs has been shown to change in the early stage of allopolyploid formation and gradually return to parental level over time during its evolution (Edger et al, 2017).…”