9Background: Whole-genome duplications (WGD) have dominated the evolutionary 10 history of plants. One consequence of WGD is a dramatic restructuring of the genome as 11 it undergoes diploidization, a process under which deletions and rearrangements of 12 various sizes scramble the genetic material, leading to a repacking of the genome and 13 eventual return to diploidy. Here, we investigate the history of WGD in the columbine 14 genus Aquilegia, a basal eudicot, and use it to illuminate the origins of the core eudicots.
15Results: Within-genome synteny confirms that columbines are ancient tetraploids, and 16 comparison with the grape genome reveals that this tetraploidy appears to be shared 17 with the core eudicots. Thus, the ancient gamma hexaploidy found in all core eudicots 18 must have involved a two-step process: first tetraploidy in the ancestry of all eudicots, 19 then hexaploidy in the ancestry of core eudicots. Furthermore, the precise pattern of 20 synteny sharing suggests that the latter involved allopolyploidization, and that core 21 eudicots thus have a hybrid origin.
22Conclusions: Novel analyses of synteny sharing together with the well-preserved 23 structure of the columbine genome reveal that the gamma hexaploidy at the root of core 24 eudicots is likely a result of hybridization between a tetraploid and a diploid species. 25 26 Background 27 Whole-genome duplication (WGD) is common in the evolutionary history of plants 28 [reviewed in 1,2]. All flowering plants are descended from a polyploid ancestor, which in 29 turn shows evidence of an even older WGD shared by all seed plants [3]. These repeated 30 cycles of polyploidy dramatically restructure plant genomes. Presumably driven by the 31 "diploidization" process, whereby genomes are returned to an effectively diploid state, 32 chromosomes are scrambled via fusions and fissions, lose both repetitive and genic 33sequences, or are lost entirely [4][5][6][7][8][9][10][11]. Intriguingly, gene loss after WGD is non-random: 34 not only is there a bias against the retention of certain genes [12,13], but also against the 35 retention of one of the WGD-derived paralog chromosomes [6,9,[14][15][16].
37We investigated the history of WGDs in the columbine genus Aquilegia for two reasons.
38The first is related to its phylogenetic position: columbines are "basal" eudicots, having 39 diverged early from the remaining "core" eudicots [17,18]. This matters because our 40 understanding of eudicot karyotype evolution is limited to the heavily sampled core 41 eudicots. Using the recently published Aquilegia coerulea genome [19], we were able to 42 address key questions about the history of polyploidization in all eudicots. Second, we 43 traced the origins of the columbine chromosomes with a particular focus on the strange 44 chromosome 4, which differs from the rest of the genome many ways. In particular, it 45 harbors more genetic polymorphism and transposable elements, has lower gene density 46 and reduced gene expression, and appears to migrate more,...