Transposable elements and their epigenetic modifications mediate gene expression and subgenome dominance in Brassica carinata.

Abstract

Key message: Subgenome-specific TE expansion and multilayered epigenetic modifications synergistically and antagonistically mediate gene expression, shaping subgenome dominance in B. carinata. Transposable elements (TEs) are major components of plant genomes and play pivotal roles in subgenome differentiation and gene expression regulation in allopolyploid plants; however, the regulatory effects mediated by epigenetic modifications of TEs remain poorly understood. Here, using allotetraploid Brassica carinata (B_cB_cC_cC_c genome) as a model, we systematically investigated the regulatory roles of TE on gene expression by inserting genes, capturing genes, and multiple epigenetic modifications (DNA methylation and histone modifications) within TE regions. Distinct TE superfamilies exhibited differential expansion and dynamic evolutionary patterns between the B_c and C_c subgenomes, LTR retrotransposons expanded more prominently in the B_c subgenome, whereas TIR transposons exhibited stronger expansion in the C_c subgenome, contributing to subgenome structural divergence. TE insertions and TE-mediated gene capture regulate the expression of both neighboring and distal genes through synergistic and antagonistic interactions among multiple epigenetic modifications. Notably, the dominant B_c subgenome exhibits stronger H3K9me2 enrichment and lower DNA methylation in TE regions, while TEs in the C_c subgenome display higher DNA methylation and more diverse histone modifications. Collectively, TEs and their multilayered epigenetic modifications jointly shape the asymmetric subgenome expression landscape of B. carinata, providing new insights into the establishment of subgenome dominance in allopolyploid plants.