The synaptonemal complex stabilizes meiosis in allotetraploid Brassica napus and autotetraploid Arabidopsis thaliana

Abstract

Summary Polyploidy plays a key role in genome evolution and crop improvement. The formation of bivalents rather than multivalents during meiosis of polyploids is essential to ensure meiotic stability and optimal fertility of the species. However, the mechanisms preventing multivalent recombination in polyploids remain obscure. We studied the role of the synaptonemal complex in polyploid meiosis by mutating the transverse filament component ZYP1 in allotetraploid Brassica napus and autotetraploid Arabidopsis. In B. napus, a mutation of all four ZYP1 copies results in multivalent pairing accompanied by pairing partner switches, nonhomologous recombination, and interlocks, leading to severe chromosome entanglement and fertility abortion. The presence of only one functional allele of ZYP1 compromises synapsis and multivalent associations occur at nonsynaptic regions. Moreover, the disruption of ZYP1 causes a complete shift from predominantly multivalent pairing to exclusively multivalent pairing in pachytene cells of synthetic autotetraploid Arabidopsis thaliana, resulting in a dramatic increase in the frequency of multivalents at metaphase I. We conclude that the ZYP1‐mediated assembly of the synaptonemal complex facilitates the pairwise homologous pairing and recombination in both allopolyploid and autopolyploid species and plays a key role in ensuring a diploid‐like bivalent formation in polyploid meiosis.