Diploid origins, adaptation to polyploidy, and the beginning of rediploidization in allotetraploid Arabidopsis suecica

Abstract

Polyploidization, followed by genome downsizing, is a recurrent evolutionary cycle that dramatically reshapes genome structure. Newly formed polyploids must quickly adjust their cell division machinery to maintain stable chromosome inheritance, while long-term stabilization involves rediploidization, returning the genome to a diploid-like state. Here, we investigate the origin and early genome evolution of Arabidopsis suecica, a hybrid polyploid derived from A. thaliana and A. arenosa Leveraging a recent genome assembly for A. suecica along with population level whole-genome resequencing of all three species, we identify the closest progenitors to A. suecica and use this knowledge to examine genes under positive selection and to assess compensatory dynamics between homeologs carrying loss-of-function mutations. Our findings show that both parental species were diploid, including the paternal A. arenosa progenitor. We identify evidence for de novo adaptation to allopolyploidy within the A. arenosa sub-genome of A. suecica, including genes involved in homolog pairing and recombination. Although relaxed purifying selection is evident, likely due to the genome-wide redundancy, we observe functional compensation between homeologous gene pairs in A. suecica: when one copy loses function, the other maintains it Together, these findings revise the origin of A. suecica and identify early genome stabilization mechanisms, including evidence for meiotic adaptation and mutational buffering through homeologous gene compensation.