Concerted genomic and epigenomic changes accompany stabilization of Arabidopsis allopolyploids

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.

Gradual evolution of allopolyploidy in Arabidopsis suecica

Most diploid organisms have polyploid ancestors. The evolutionary process of polyploidization is poorly understood but has frequently been conjectured to involve some form of ‘genome shock’, such as genome reorganization and subgenome expression dominance. Here we study polyploidization in Arabidopsis suecica, a post-glacial allopolyploid species formed via hybridization of Arabidopsis thaliana and Arabidopsis arenosa. We generated a chromosome-level genome assembly of A. suecica and complemented it with polymorphism and transcriptome data from all species. Despite a divergence around 6 million years ago (Ma) between the ancestral species and differences in their genome composition, we see no evidence of a genome shock: the A. suecica genome is colinear with the ancestral genomes; there is no subgenome dominance in expression; and transposon dynamics appear stable. However, we find changes suggesting gradual adaptation to polyploidy. In particular, the A. thaliana subgenome shows upregulation of meiosis-related genes, possibly to prevent aneuploidy and undesirable homeologous exchanges that are observed in synthetic A. suecica, and the A. arenosa subgenome shows upregulation of cyto-nuclear processes, possibly in response to the new cytoplasmic environment of A. suecica, with plastids maternally inherited from A. thaliana. These changes are not seen in synthetic hybrids, and thus are likely to represent subsequent evolution.

Gradual evolution of allopolyploidy in Arabidopsis suecica

The majority of diploid organisms have polyploid ancestors. The evolutionary process of polyploidization (and subsequent re-diploidization) is poorly understood, but has frequently been conjectured to involve some form of “genome shock” — partly inspired by studies in crops, many of which are polyploid, and in which polyploidy has frequently been linked to dramatic genomic changes such as subgenome expression dominance and genome reorganization. It is unclear, however, whether domesticated polyploids are representative of natural ones. Here, we study polyploidization in Arabidopsis suecica (n = 13), a post-glacial allopolyploid species formed via hybridization of A. thaliana (n = 5) and A. arenosa (n = 8). We generated a chromosome-level genome assembly of A. suecica and complemented it with polymorphism and transcriptome data from multiple individuals of all species. Despite a divergence of ~6 Mya between the two ancestral species and appreciable differences in their genome composition, we see no evidence of a genome shock: the A. suecica genome is highly colinear with the ancestral genomes, there is no subgenome dominance in expression, and transposable element dynamics appear to be stable. We do, however, find strong evidence for changes suggesting gradual adaptation to polyploidy. In particular, the A. thaliana subgenome shows upregulation of meiosis-related genes, possibly in order to prevent aneuploidy and undesirable homeologous exchanges that are frequently observed in experimentally generated A. suecica, and the A. arenosa subgenome shows upregulation of cyto-nuclear related processes, possibly in response to the new cytoplasmic environment of A. suecica, with plastids maternally inherited from A. thaliana.

Homoeologous exchanges occur through intragenic recombination generating novel transcripts and proteins in wheat and other polyploids

Recombination between homeologous chromosomes, also known as homeologous exchange (HE), plays a significant role in shaping genome structure and gene expression in interspecific hybrids and allopolyploids of several plant species. However, the molecular mechanisms that govern HEs are not well understood. Here, we studied HE events in the progeny of a nascent allotetraploid (genome AADD) derived from two diploid progenitors of hexaploid bread wheat using cytological and whole-genome sequence analyses. In total, 37 HEs were identified and HE junctions were mapped precisely. HEs exhibit typical patterns of homologous recombination hotspots, being biased toward low-copy, subtelomeric regions of chromosome arms and showing association with known recombination hotspot motifs. But, strikingly, while homologous recombination preferentially takes place upstream and downstream of coding regions, HEs are highly enriched within gene bodies, giving rise to novel recombinant transcripts, which in turn are predicted to generate new protein fusion variants. To test whether this is a widespread phenomenon, a dataset of high-resolution HE junctions was analyzed for allopolyploid Brassica, rice, Arabidopsis suecica, banana, and peanut. Intragenic recombination and formation of chimeric genes was detected in HEs of all species and was prominent in most of them. HE thus provides a mechanism for evolutionary novelty in transcript and protein sequences in nascent allopolyploids.