Abstract
Polyploidization plays a crucial role in the evolution of angiosperm species. Almost all newly formed polyploids encounter genetic or epigenetic instabilities. However, the molecular mechanisms contributing to genomic instability in synthetic polyploids have not been clearly elucidated. Here, we performed a comprehensive transcriptomic and methylomic analysis of natural and synthetic polyploid rapeseeds (Brassica napus). Our results showed that the CHG methylation levels of synthetic rapeseed in different genomic contexts (genes, transposon regions, and repeat regions) were significantly lower than those of natural rapeseed. The total number and length of CHG-DMRs between natural and synthetic polyploids were much greater than those of CG-DMRs and CHH-DMRs, and the genes overlapping with these CHG-DMRs were significantly enriched in DNA damage repair and nucleotide metabolism pathways. These results indicated that CHG methylation may be more sensitive than CG and CHH methylation in regulating the stability of the polyploid genome of B. napus. In addition, many genes involved in DNA damage repair, nucleotide metabolism, and cell cycle control were significantly differentially expressed between natural and synthetic rapeseeds. Our results highlight that the genes related to DNA repair and nucleotide metabolism display differential CHG methylation patterns between natural and synthetic polyploids and reveal the potential connection between the genomic instability of polyploid plants with DNA methylation defects and dysregulation of the DNA repair system. In addition, it was found that the maintenance of CHG methylation in B. napus might be partially regulated by MET1. Our study provides novel insights into the establishment and evolution of polyploid plants and offers a potential idea for improving the genomic stability of newly formed Brassica polyploids.
Highlights
Polyploidization is an important driving force in the evolution of angiosperms[1,2,3]
It was found that the expression levels of other genes involved in the establishment, maintenance, and removal of DNA methylation were relatively low, and there were no obvious differences between natural B. napus and the synthetic rapeseeds (Table S2, Fig. S1)
The mechanisms for the successful establishment of polyploid species remain largely unclear, and the molecular mechanisms leading to genomic instability in synthetic polyploids have not been clearly elucidated[37,38]
Summary
Polyploidization is an important driving force in the evolution of angiosperms[1,2,3]. Previous studies have demonstrated that synthetic B. napus has extensive changes in DNA methylation relative to its diploid parents (B. rapa and B. oleracea), which may contribute to the stability of its genome[15,16,17,21]. Changes in DNA methylation occurred as early as the first generation in synthetic B. napus, and most of these changes remained fixed in their fifth selfpollinated generation[15,16]. These studies have provided valuable insights into the effects of polyploidization on DNA methylation. These results were based on the techniques of restriction fragment length polymorphism[15,16] or methylation-sensitive amplification polymorphism[17,21], which could not accurately reflect changes in DNA methylation at the genome-wide level
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