Desynapsis in potato is caused by StMSH4 mutant alleles and leads to either highly uniform unreduced pollen or sterility

The balanced segregation of homologous chromosomes during meiosis is essential for fertility and is mediated by crossovers. A strong reduction of crossovers leads to desynapsis, a process in which pairing of homologous chromosomes is abolished before metaphase I. This results in a random segregation of univalent and the production of unbalanced and sterile gametes. However, if desynapsis is combined with another meiotic alteration that restitutes the first meiotic division, then uniform and balanced unreduced gametes, essentially composed of non-recombinant homologs, are produced. This mitosis-like division is of interest to breeders because it transmits most of the parental heterozygosity to the gametes. In potato, desynapsis is a recessive trait that was tentatively mapped to chromosome 8. In this article, we have fine-mapped the position of the desynapsis locus and identified StMSH4, an essential component of the class I crossover pathway, as the most likely candidate gene. A seven base-pair insertion in the second exon of StMSH4 was found to be associated with desynapsis in our mapping population. We also identified a second allele with a 3820 base-pair insertion and confirmed that both alleles cannot complement each other. Such non-functional alleles appeared to be common in potato cultivars. More than half of the varieties we tested are carriers of mutational load at the StMSH4 locus. With this new information, breeders can choose to remove desynaptic alleles from their germplasm to improve fertility or to use them to produce highly uniform unreduced gametes in alternative breeding schemes.