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.

Department of Botany Faculty of Science Charles University 12800 Prague Czech Republic

Department of Chromosome Biology Max Planck Institute for Plant Breeding Research 50829 Cologne Germany

Department of Plant Biotechnology and Bioinformatics Ghent University 9052 Ghent Belgium

Department of Plant Sciences University of Cambridge CB23EA Cambridge UK

VIB UGent Center for Plant Systems Biology Ghent 9052 Belgium

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