Excess endopolyploidy associated with cellular defects in neo-autotetraploid Arabidopsis arenosa is in part corrected by a naturally evolved allele of CYCD3;2.

Endopolyploidy (within-organism polyploidy) is an often-beneficial aspect of development. But polyploids, which have a higher baseline genome content, have been reported to have less endoreduplication than diploid relatives. Why has remained unclear; we explored this in Arabidopsis arenosa. We measured endopolyploidy levels and phenotyped cellular traits, comparing diploids, neo-autotetraploids, and established autotetraploids of A. arenosa. We used a genetic approach to ask whether CYCD3;2, a polyploidy regulator with evidence of selection in tetraploids, might be responsible for endopolyploidy-related phenotypic differences between neo- and established polyploids, and whether there are associated costs. Neo-tetraploids had the most 16C and 32C cells, whereas established tetraploids have proportions of 16C and 32C cells comparable to diploids. Tetraploid plants homozygous for a novel allele of CYCD3;2 have reduced endopolyploidy compared to homozygotes for the diploid allele and, surprisingly, also show cellular defects seen in neo-tetraploids. Suggesting this link is specific, we find that A. thaliana cycd3;2 mutants have not only increased endopolyploidy but also root hair defects like neo-tetraploids. Our results suggest reverting endopolyploidy in polyploids to diploid-like levels could be advantageous, and that one driver might be cellular defects that arise with excess high-ploidy cells.