A novel allele of ASY3 is associated with greater meiotic stability in autotetraploid Arabidopsis lyrata
Abstract
In this study we performed a genotype-phenotype association analysis of meiotic stability in 10 autotetraploidArabidopsis lyrataandA.lyrata/A.arenosahybrid 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 associated with segregation of a novelASYNAPSIS3(ASY3) allele derived fromA.lyrata.
TheASY3allele that associates with meiotic stability possesses a putative in-frame tandem duplication (TD) of a serine-rich region upstream of the coiled-coil domain that appears to have arisen at sites of DNA microhomology. The frequency of multivalents observed in plants homozygous for theASY3 TDhaplotype was significantly lower than in plants heterozygous forASY3 TD/ND(non-duplicated) 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 pachytene that mark class I crossovers was significantly reduced in a plant homozygous forASY3 TDcompared to a plant heterozygous forASY3 ND/TD.
Fifty-eight alleles of the 8 meiosis genes were identified from the 10 populations analysed, demonstrating dynamic population variability at these loci. Widespread chimerism between alleles originating fromA.lyrata/A.arenosaand diploid/tetraploids indicates that this group of rapidly evolving genes may provide precise adaptive control over meiotic recombination in the tetraploids, the very process that gave rise to them.
Author summary Whole 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 10 autotetraploidArabidopsis lyrataandA.lyrata/A.arenosahybrid 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,ZYP1aandZYP1b) implicated in synaptonemal complex formation in the tetraploids under extreme selection. Our analysis demonstrates that segregation of a novel allele of the meiotic chromosome axis protein ASYNAPSIS3 is associated with male meiotic stability.
Adaptive restabilisation of meiotic recombination appears to be achieved by a reduction in the number of crossovers as well as a shift in their positioning towards the chromosome ends. Of the eight genes, 58 alleles were identified, indicating dynamic population variability at these loci under extreme selection.
In addition, widespread allelic chimerism between alleles originating fromA.lyrata/A.arenosaand diploid/tetraploids indicates that this group of rapidly evolving genes may provide precise adaptive control over meiotic recombination in the tetraploids, the very process that gave rise to them.