Gradual evolution of allopolyploidy inArabidopsis suecica

Abstract

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.

Inference of polyploid origin and inheritance mode from population genomic data

“…This is clearly demonstrated in the case of A. suecica , a known allopolyploid (hybridization between A. arenosa & A. thaliana ) which we expect to exhibit preferential (bivalent) chromosome pairing and thus disomic inheritance. Figure 2c shows a stretch of chromosome 1 with a different inferred inheritance mode than the rest of the genome; this is a previously described (12) homeologous exchange between the first chromosome of A. suecica ( A. thaliana subgenome) and the sixth chromosome of A. suecica ( A. arenosa subgenome) in SRR3123767 (AS530) accession. This region of almost 16Mb of the A. arenosa subgenome has been exchanged for the A. thaliana copy.…”

“…The origin of polyploids often dictates the way we tend to analyse genome sequencing data. Sequencing data from allopolyploids with sufficient divergence between subgenomes can often be split either by mapping to the combined reference of the parental genomes with subsequent filtering for primary alignment in proper pairs (12, 13) or by using SNP markers specific for each parent (14, 15) . Divided subgenomes are then analysed as if they were separate taxa.…”

“…PrBn locus in oilseed rape ( Brassica napus ) has a similar effect (28) . Preferential homeologous pairing in A. suecica also has a genetic basis (29) ( BOY NAMED SUE locus) but also appears to be regulated on the transcriptional level of meiotic genes (12) . This suggests that homeologous exchanges are mostly deleterious and allopolyploids do not only rely on the divergence levels between the subgenomes to prevent these generally undesirable genome reshufflings.…”

The nature of intraspecific genome size variation in taxonomically complex eyebrights

“…This discrepancy may have originated from genome downsizing, commonly seen during re-diploidisation. It may also be explained by the fusion of two diverged diploid genomes of different size, as seen in allopolyploid Gossypium (Hendrix & Stewart, 2005) and Arabidopsis suecica (Burns et al ., 2021). However, the absence of interploidy repeat divergence in Euphrasia differs from other allotetraploid systems, where diverged sub-genomes tend to show differences in genomic repeats (Zhao et al ., 1998; Hawkins et al ., 2006; Renny-Byfield et al ., 2015; Dodsworth et al ., 2020).…”

Nuclear-cytoplasmic balance: whole genome duplications induce elevated organellar genome copy number

“…A similar, but evolutionarily independent history of WGD resulted in allotetraploid Arabidopsis suecica (2n = 4x) and is thought to have originated from an allopolyploidization event between an unreduced A. thaliana (2n = 2x) ovule and tetraploid A. arenosa (4n = 4x) pollen ca . 16,000 years ago (Jakobsson et al ., 2006; Novikova et al ., 2017; Burns et al ., 2021). Together, these independent allopolyploids provide a useful comparative context to investigate the evolved cytonuclear stoichiometric responses to WGD.…”