Abstract
Polyploidy, which results from whole genome duplication (WGD), has shaped the long-term evolution of eukaryotic genomes in all kingdoms. Polyploidy is also implicated in adaptation, domestication, and speciation. Yet when WGD newly occurs, the resulting neopolyploids face numerous challenges. A particularly pernicious problem is the segregation of multiple chromosome copies in meiosis. Evolution can overcome this challenge, likely through modification of chromosome pairing and recombination to prevent deleterious multivalent chromosome associations, but the molecular basis of this remains mysterious. We study mechanisms underlying evolutionary stabilization of polyploid meiosis using Arabidopsis arenosa, a relative of A. thaliana with natural diploid and meiotically stable autotetraploid populations. Here we investigate the effects of ancestral (diploid) versus derived (tetraploid) alleles of two genes, ASY1 and ASY3, that were among several meiosis genes under selection in the tetraploid lineage. These genes encode interacting proteins critical for formation of meiotic chromosome axes, long linear multiprotein structures that form along sister chromatids in meiosis and are essential for recombination, chromosome segregation, and fertility. We show that derived alleles of both genes are associated with changes in meiosis, including reduced formation of multichromosome associations, reduced axis length, and a tendency to more rod-shaped bivalents in metaphase I. Thus, we conclude that ASY1 and ASY3 are components of a larger multigenic solution to polyploid meiosis in which individual genes have subtle effects. Our results are relevant for understanding polyploid evolution and more generally for understanding how meiotic traits can evolve when faced with challenges.
Highlights
Polyploidy, which results from whole genome duplication (WGD), has shaped the long-term evolution of eukaryotic genomes in all kingdoms
Genes encoding two interacting meiotic chromosome axis proteins were among the strongest genome-wide outliers for evidence of selection during evolution of tetraploid A. arenosa, suggesting that they might play a role in meiotic stabilization of the polyploid lineage [14, 26]
We test the functional consequences of their divergence and show that derived alleles of ASY1 and to a lesser extent ASY3, are associated with subtle effects on several key features that are likely important for stable tetraploid meiosis: 1) a reduction in multivalent formation rates, 2) a trend toward more “rod-shaped” bivalents in metaphase that could reflect increased chromatin condensation, and 3) a reduction in the length of the chromosome axes
Summary
Polyploidy, which results from whole genome duplication (WGD), has shaped the long-term evolution of eukaryotic genomes in all kingdoms. A pernicious problem is the segregation of multiple chromosome copies in meiosis Evolution can overcome this challenge, likely through modification of chromosome pairing and recombination to prevent deleterious multivalent chromosome associations, but the molecular basis of this remains mysterious. We use Arabidopsis arenosa as a model to understand the molecular basis of autopolyploid meiotic stabilization This species is a close relative of A. thaliana with naturally occurring diploid and autotetraploid populations [21, 22]. Genome duplication is an important factor in the evolution of eukaryotic lineages, but it poses challenges for the regular segregation of chromosomes in meiosis and fertility. We test the role that derived alleles of two genes under selection in tetraploid A. arenosa might have in meiotic stabilization in tetraploids
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