Abstract

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 F1 to resynthesized allotetraploids and convergently to the T-subgenome level in natural A. suecica, despite many other methylated loci being inherited from F1 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.

Highlights

  • During evolution successful allopolyploids must overcome ‘genome shock’ between hybridizing species but the underlying process remains elusive

  • Our findings indicate that balanced genomic diversifications in allotetraploids are accompanied by convergent and concerted changes in DNA methylation and gene expression between two subgenomes

  • To overcome the heterozygosity issue, we sequenced the genome of a resynthesized allotetraploid, Allo[738], that had been maintained by self-pollination for ten or more generations (Fig. 1a)[11,19,27]

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Summary

Introduction

During evolution successful allopolyploids must overcome ‘genome shock’ between hybridizing species but the underlying process remains elusive. A. suecica shows conserved gene synteny and content with more gene family gain and loss in the A and T subgenomes than respective progenitors, 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. Our findings indicate that balanced genomic diversifications in allotetraploids are accompanied by convergent and concerted changes in DNA methylation and gene expression between two subgenomes This example of genomic and epigenomic reconciliation may provide a basis for stabilizing subgenomic structure and function to improve adaptation during polyploid evolution

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