Concerted genomic and epigenomic changes accompany stabilization of Arabidopsis allopolyploids

Arabidopsis suecica is an allotetraploid derived from Arabidopsisthaliana and Arabidopsisarenosa. Analysis of resynthesized and natural allotetraploid A. suecica shows balanced genomic variation accompanied by convergent and concerted changes in DNA methylation and gene expression between two subgenomes that probably contributed to genome stability during polyploid evolution. During evolution successful allopolyploids must overcome 'genome shock' between hybridizing species but the underlying process remains elusive. Here, we report concerted genomic and epigenomic changes in resynthesized and natural Arabidopsis suecica (TTAA) allotetraploids derived from Arabidopsisthaliana (TT) and Arabidopsisarenosa (AA). A. suecica shows conserved gene synteny and content with more gene family gain and loss in the A and T subgenomes than respective progenitors, although A. arenosa-derived subgenome has more structural variation and transposon distributions than A. thaliana-derived subgenome. These balanced genomic variations are accompanied by pervasive convergent and concerted changes in DNA methylation and gene expression among allotetraploids. The A subgenome is hypomethylated rapidly from F-1 to resynthesized allotetraploids and convergently to the T-subgenome level in natural A. suecica, despite many other methylated loci being inherited from F-1 to all allotetraploids. These changes in DNA methylation, including small RNAs, in allotetraploids may affect gene expression and phenotypic variation, including flowering, silencing of self-incompatibility and upregulation of meiosis- and mitosis-related genes. In conclusion, concerted genomic and epigenomic changes may improve stability and adaptation during polyploid evolution.

Automated summary

Arabidopsis suecica is an allotetraploid derived from Arabidopsisthaliana and Arabidopsisarenosa, showing balanced genomic variation and concerted changes in DNA methylation and gene expression. These concerted genomic and epigenomic changes may improve stability and adaptation during polyploid evolution.