Deep karyotypic and genomic changes drive the evolution of Oxalis subgenus Thamnoxys (Oxalidaceae)

Oxalis subgenus Thamnoxys comprises 90 species across nine taxonomic sections endemic to the Americas. It exhibits remarkable genome size and karyotype variation compared with other angiosperms. In this manuscript we aimed to assess the impact of chromosomal changes on the split of new evolutionary lineages in this subgenus.

To evaluate the impact of this variability on the evolution of O. subg. Thamnoxys, we analysed cytologically 46 species from eight of its sections, along with four representatives of Averrhoa and Biophytum. For most species, chromosome number and morphology, meiotic behaviour, heterochromatic banding pattern and DNA content are reported here for the first time within an ITS-based phylogenetic framework for 37 species of the subgenus plus 25 outgroup taxa.

Our results reveal two main clades: one with base number of x = 6 and another with x = 5 and x = 6. Polyploid species or cytotypes, as well as karyotypes dominated by metacentric and submetacentric chromosomes, were largely confined to sects. Thamnoxys and Foliosae. In contrast, other sections primarily included diploids with acrocentric chromosomes that exhibited heterogeneity in size and variable DNA content. Averrhoa (x = 6) and Biophytum (x = 7) showed chromosomal traits more similar to O. sect. Thamnoxys. Each section displayed a distinct karyotype, and some included one or more atypical karyotypes. Phylogenetic analysis clustered most species with atypical ones separately from those with typical ones within each section.

Comparative data suggest that the ancestral karyotype of O. subg. Thamnoxys was probably symmetrical, with x = 6 and a small genome. The diversification of the subgenus into distinct evolutionary lineages was apparently triggered by extensive chromosomal reshuffling and genome size variation, giving rise to at least 14 different karyotype formulas without major changes in floral or vegetative characters.