Genetic Adaptation Associated with Genome-Doubling in Autotetraploid Arabidopsis arenosa

Abstract

Genome duplication, which results in polyploidy, is disruptive to fundamental biological processes. Genome duplications occur spontaneously in a range of taxa and problems such as sterility, aneuploidy, and gene expression aberrations are common in newly formed polyploids. In mammals, genome duplication is associated with cancer and spontaneous abortion of embryos. Nevertheless, stable polyploid species occur in both plants and animals. Understanding how natural selection enabled these species to overcome early challenges can provide important insights into the mechanisms by which core cellular functions can adapt to perturbations of the genomic environment. Arabidopsis arenosa includes stable tetraploid populations and is related to well-characterized diploids A. lyrata and A. thaliana. It thus provides a rare opportunity to leverage genomic tools to investigate the genetic basis of polyploid stabilization. We sequenced the genomes of twelve A. arenosa individuals and found signatures suggestive of recent and ongoing selective sweeps throughout the genome. Many of these are at genes implicated in genome maintenance functions, including chromosome cohesion and segregation, DNA repair, homologous recombination, transcriptional regulation, and chromatin structure. Numerous encoded proteins are predicted to interact with one another. For a critical meiosis gene, ASYNAPSIS1, we identified a non-synonymous mutation that is highly differentiated by cytotype, but present as a rare variant in diploid A. arenosa, indicating selection may have acted on standing variation already present in the diploid. Several genes we identified that are implicated in sister chromatid cohesion and segregation are homologous to genes identified in a yeast mutant screen as necessary for survival of polyploid cells, and also implicated in genome instability in human diseases including cancer. This points to commonalities across kingdoms and supports the hypothesis that selection has acted on genes controlling genome integrity in A. arenosa as an adaptive response to genome doubling.

Author Summary

Duplication of an entire set of chromosomes is a dramatic mutation disruptive to core cellular functions. Genome duplication and the genomic instability that generally follows can cause problems with fertility and viability, and in mammals is associated with cancer and spontaneous abortion. Yet, established polyploids occur naturally in both plants and animals. How do these organisms overcome these early problems and ultimately stabilize? The genetic basis of the adaptive response to polyploidy has remained almost completely unknown. We took advantage of modern genomic approaches to gain insight into this using a stable polyploid plant, Arabidopsis arenosa. We found evidence of selection in genes that control core genome maintenance processes. These overlap with genes or functions shown in yeast to be necessary for survival of polyploid cells and in humans implicated in cancer. Our results identify genes controlling core genome maintenance functions that may have undergone compensatory adaptation after genome doubling.