De Novo Mutation and Rapid Protein (Co-)evolution during Meiotic Adaptation in Arabidopsis arenosa

A sudden shift in environment or cellular context necessitates rapid adaptation. A dramatic example is genome duplication, which leads to polyploidy. In such situations, the waiting time for new mutations might be prohibitive; theoretical and empirical studies suggest that rapid adaptation will largely rely on standing variation already present in source populations. Here, we investigate the evolution of meiosis proteins in Arabidopsis arenosa, some of which were previously implicated in adaptation to polyploidy, and in a diploid, habitat. A striking and unexplained feature of prior results was the large number of amino acid changes in multiple interacting proteins, especially in the relatively young tetraploid. Here, we investigate whether selection on meiosis genes is found in other lineages, how the polyploid may have accumulated so many differences, and whether derived variants were selected from standing variation. We use a range-wide sample of 145 resequenced genomes of diploid and tetraploid A. arenosa, with new genome assemblies. We confirmed signals of positive selection in the polyploid and diploid lineages they were previously reported in and find additional meiosis genes with evidence of selection. We show that the polyploid lineage stands out both qualitatively and quantitatively. Compared with diploids, meiosis proteins in the polyploid have more amino acid changes and a higher proportion affecting more strongly conserved sites. We find evidence that in tetraploids, positive selection may have commonly acted on de novo mutations. Several tests provide hints that coevolution, and in some cases, multinucleotide mutations, might contribute to rapid accumulation of changes in meiotic proteins.

A novel allele of ASY3 promotes meiotic stability in autotetraploid Arabidopsis lyrata

In this study we performed a genotype-phenotype association analysis of meiotic stability in ten autotetraploid Arabidopsis lyrata and A. lyrata/A. arenosa hybrid populations collected from the Wachau region and East Austrian Forealps. The aim was to determine the effect of eight meiosis genes under extreme selection upon adaptation to whole genome duplication. Individual plants were genotyped by high-throughput sequencing of the eight meiosis genes (ASY1, ASY3, PDS5b, PRD3, REC8, SMC3, ZYP1a/b) implicated in synaptonemal complex formation and phenotyped by assessing meiotic metaphase I chromosome configurations. Our results reveal that meiotic stability varied greatly (20-100%) between individual tetraploid plants and was associated with segregation of a novel allele orthologous to the budding yeast RED1 chromosome axis protein, Asynapsis3 (ASY3), derived from A. lyrata. The adaptive ASY3 protein possesses a putative in-frame tandem duplication (TD) of a serine-rich region upstream of the coiled-coil domain that has arisen at sites of DNA microhomology. The frequency of multivalents observed in plants homozygous for the ASY3 TD haplotype was significantly lower than plants heterozygous for TD/ND (non-duplicated) ASY3 haplotypes. Chiasma distribution was significantly altered in the stable plants compared to the unstable plants with a shift from proximal and interstitial to predominantly distal locations. The number of HEI10 foci at pachtyene that mark class I crossovers was significantly reduced in meiotic nuclei from ASY3 TD homozygous plants compared to ASY3 ND/TD heterozygotes, indicating an adaptive consequence of the ASY3 TD allele. From the ten populations, fifty-eight alleles of these 8 meiosis genes were identified, demonstrating dynamic population variability at these loci which nevertheless exhibit signatures of strong hard selective sweeps. Widespread chimerism between alleles originating from A. lyrata/A. arenosa and diploid/tetraploids indicates that this group of rapidly evolving genes provide precise adaptive control over meiotic recombination in the tetraploids, the very process that gave rise to them.Author summaryWhole genome duplication can promote adaptability, but is a dramatic mutation usually resulting in meiotic catastrophe and genome instability. Here we focus on a case of coordinated stabilization of meiotic recombination in ten autotetraploid Arabidopsis lyrata and A. lyrata/A. arenosa hybrid populations from the Wachau region and East Austrian Forealps. We fuse population genomic data with a genotype-phenotype association study, concentrating on the effects of eight meiosis genes (ASY1, ASY3, PDS5b, PRD3, REC8, SMC3, ZYP1a/b) implicated in synaptonemal complex formation in the tetraploids under extreme selection. Our analysis demonstrates that a novel allele of the meiotic chromosome axis protein Asynapsis3 that contains an in-frame duplication of a serine-rich region is the major determinant of male meiotic stability. This adaptive restabilisation appears to be achieved by a reduction in the number of meiotic crossovers as well as a shift in their positioning towards the chromosome ends. Of the eight genes, fifty-eight alleles were identified, indicating dynamic population variability at these loci under extreme selection. In addition, widespread allelic chimerism between alleles originating from A. lyrata/A. arenosa and diploid/tetraploids indicates that this group of rapidly evolving genes provide precise adaptive control over meiotic recombination in the tetraploids, the very process that gave rise to them.

Multiple separate cases of pseudogenized meiosis genes Msh4 and Msh5 in Eurotiomycete fungi: associations with Zip3 sequence evolution and homothallism, but not Pch2 losses

The overall process of meiosis is conserved in many species, including some lineages that have lost various ancestrally present meiosis genes. The extent to which individual meiosis gene losses are independent from or dependent on one another is largely unknown. Various Eurotiomycete fungi were investigated as a case system of recent meiosis gene losses after BLAST and synteny comparisons found Msh4, Msh5, Pch2, and Zip3 to be either pseudogenized or undetected in Aspergillus nidulans yet intact in congeners such as A. fumigatus. Flanking gene-targeted degenerate PCR primers applied to 9 additional Aspergillus species found (i) Msh4, Msh5, and Zip3 pseudogenized in A. rugulosus (sister taxon to A. nidulans) but intact in all other amplified sequences; and (ii) Pch2 not present at the syntenic locus in most of the 9 species. Topology tests suggested two independent Pch2 losses in genus Aspergillus, neither directly coinciding with pseudogenization of the other three genes. The A. nidulans-A. conjunctus clade Pch2 loss was not associated with significant Ka/Ks changes for Msh4, Msh5, or Zip3; this suggests against prior Pch2 loss directly altering sequence evolution constraints on these three genes. By contrast, Zip3 Ka/Ks tended to be elevated in several other Eurotiomycete fungi with independently pseudogenized Msh4 and Msh5 (Talaromyces stipitatus, Eurotium herbariorum). The coinciding Ka/Ks elevation and/or clear pseudogenization of Zip3 in taxa with pseudogenized Msh4 and Msh5 is consistent with some degree of molecular coevolution. Possible molecular, environmental, and life history variables (e.g., homothallism) that may be associated with these numerous independent meiosis gene losses (Msh4: 3, Msh5: 3, Zip3: ≥ 1, Pch2: 4) are discussed.