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.

The BOY NAMED SUE Quantitative Trait Locus Confers Increased Meiotic Stability to an Adapted Natural Allopolyploid of Arabidopsis

“…Similar to the results presented here, new tetraploids of A. arenosa (diploids tetraploidized in the laboratory) exhibit more meiotic abnormalities than their natural autotetraploid counterparts (Hollister et al, 2012). Recent work comparing diploid and autotetraploid populations of A. arenosa has identified several genomic regions specifically associated with tetraploidy in this species (Hollister et al, 2012;Yant et al, 2013). The genes located within these regions are enriched in meiosis-related genes, confirming that rare variants or mutations that result in increased meiotic stability in a polyploid context have been selected upon tetraploidizaton in A. arenosa (Yant et al, 2013).…”

“…It may be an allopolyploid-specific adaptation (i.e., beneficial only in allopolyploids and even detrimental in autotetraploids). Similar to the results presented here, new tetraploids of A. arenosa (diploids tetraploidized in the laboratory) exhibit more meiotic abnormalities than their natural autotetraploid counterparts (Hollister et al, 2012). Recent work comparing diploid and autotetraploid populations of A. arenosa has identified several genomic regions specifically associated with tetraploidy in this species (Hollister et al, 2012;Yant et al, 2013).…”

“…A key adaptation involves chromosome pairing and recombination during meiosis. Evidence for meiotic gene adaptation to autopolyploidy, involving more than two equivalent pairing partners, has been recently described (Hollister et al, 2012;Yant et al, 2013). In allopolyploids, pairing should be limited to two homologous partners (Comai, 2005;Cifuentes et al, 2010), as opposed to homoeologous partners, which originate from different parents.…”

The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications

“…Thus, meiotic stability is a key hurdle that must be overcome following WGD and is one of the hallmarks of an adapted polyploid. Indeed, loci that encode genes controlling meiotic recombination and crossovers are strongly implicated in adaptation to WGD (Hollister et al, 2012;Yant et al, 2013).…”

Evolutionary mysteries in meiosis

“…This mechanism seems particularly important in autopolyploids and may be achieved through increasing CO interference (see §5b for definition) [54]. Several candidate genes that may effect such modifications have been identified in the autotetraploid Arabidopsis arenosa [51,55]. In allopolyploids, there is evidence for genes that have been selected to strengthen the preferential pairing of homologous (i.e.…”