Improved synapsis dynamics accompany meiotic stability in Arabidopsis arenosa autotetraploids

Abstract

During meiosis, the correct pairing, synapsis, and recombination of homologous chromosome pairs is critical for fertility of sexual eukaryotes. These processes are challenged in polyploids, which possess additional copies of each chromosome. Polyploidy thus provides a unique context to study how evolution can modify meiotic programs in response to challenges. We previously observed that in Arabidopsis arenosa newly formed (neo-)polyploids, synapsis defects precede chromosomes associating in aberrant multivalent and univalent configurations. Here we study synapsis dynamics in genotypes with varying levels of meiotic stability to ask whether efficient synaptic progression is a key component of evolving stable tetraploid meiosis. We develop a method to quantify synapsis dynamics using the progression of foci of the pro-crossover factor HEI10 as a reference. HEI10 initially appears at many small loci before accumulating only at crossover sites. In diploids, this transition begins while there is still significant asynapsis, which quickly declines as HEI10 accumulation to fewer foci progresses. In neo-tetraploids, suboptimal elongation of synaptic initiation sites, and perhaps defective pairing, precedes synapsis stalling before the onset of HEI10 accumulation. In established tetraploids, HEI10 accumulation begins only when asynapsis is minimal, suggesting an enhanced HEI10/synapsis co-dynamic (even compared to diploids). Hybrids generated by crossing neo- and established tetraploids exhibit intermediate phenotypes. We find the extent of asynapsis correlates positively with crossover numbers, as well as a higher frequency of multivalents and univalent, which can disturb chromosome segregation. Our work supports the hypothesis that improving the efficiency of synapsis is important for evolving polyploid meiotic stability. Significance StatementDuring meiosis, homologous chromosomes pair and subsequently form the synaptonemal complex, which provides a context for maturation of DNA recombination events. How synapsis and crossover formation are coordinated in polyploids, where multiple chromosome sets complicate pair-wise interactions, remains unclear. Leveraging the dynamics of the pro-crossover factor HEI10 as a developmental clock, we quantified synapsis progression in new and established tetraploids of Arabidopsis arenosa. Synapsis is severely compromised in neo-tetraploids, while in established ones it is more efficient even than diploids. Notably, the extent of synaptic defects correlated with excess crossovers, which compromises meiotic stability in tetraploids by connecting connect multiple homologs in multivalents. These findings highlight that improving synapsis dynamics are important for the evolution of meiotic stability in polyploids.