Partial cytological diploidization of neoautotetraploid meiosis by induced cross- over rate reduction

Polyploids, which arise from whole-genome duplication events, have contributed to genome evolution throughout eukaryotes. Among plants, novel features of neopoly-ploids include traits that can be evolutionarily or agriculturally beneficial, such as increased abiotic stress tolerance. Thus, in addition to being interesting from an evolutionary perspective, genome duplication is also increasingly recognized as a promising crop improvement tool. However, newly formed (neo)polyploids commonly suffer from fertility problems, which have been attributed to abnormal associations among the multiple homologous chromosome copies during meiosis (multivalents). Here, we test the long-standing hypothesis that reducing meiotic cross-over number may be sufficient to limit multivalent formation, favoring diploid-like bivalent associations (cytological diploidization). To do so, we developed Arabidopsis thaliana lines with low cross-over rates by combining mutations for HEI10 and TAF4b. Double mutants showed a reduction of similar to 33% in cross-over numbers in diploids without compromising meiotic stability. Neopolyploids derived from the double mutant show a cross-over rate reduction of about 40% relative to wild-type neotetraploids, and groups of four homologs indeed formed fewer multivalents and more bivalents. However, we also show that the reduction in multivalents comes with the cost of a slightly increased frequency of univalents and that it does not rescue neopolyploid fertility. Thus, while our results do show that reducing cross-over rates can reduce multivalent frequency in neopolyploids, they also emphasize that there are additional factors affecting both meiotic stability and neopolyploid fertility that will need to be considered in solving the neopolyploid fertility challenge.

Automated summary

Polyploids, which result from genome duplication events, play an important role in genome evolution in eukaryotes and offer potential benefits for crop improvement. This study investigates the hypothesis that reducing meiotic cross-over rates can limit the formation of abnormal chromosomal associations, called multivalents, in polyploids. The researchers developed Arabidopsis thaliana lines with low cross-over rates and found that the reduction in cross-overs decreased multivalent formation in polyploids, but also resulted in increased univalent frequency and did not improve polyploid fertility. These findings highlight the complexity of factors affecting meiotic stability and fertility in polyploids.