The Ph1 ZIP4 story stabilization of wheat as a polyploid and preservation of grain number

IWGSC webinar 04/21/2022 Presenter: Azahara Martin, John Innes Centre, UK Outline Meiosis is one of the biggest challenges facing a new polyploid. Multiple related chromosomes must be discriminated, ensuring regular chromosome segregation and fertility by allowing only homologous chromosomes to recombine. For 60 years, a locus named Ph1 (Pairing homoeologous 1), arising on chromosome 5B during polyploidization, has been considered responsible for stabilizing the wheat genome during meiosis, by preventing crossover between related (homoeologous) chromosomes. A 59.3 Mb deletion mutant (ph1b) has been used in breeding to allow recombination between wheat and its wild relatives. We have now identified the major meiotic gene ZIP4, as the gene inside the Ph1 locus responsible for wheat stabilization. On wheat polyploidization, ZIP4 duplicated from chromosome 3B onto 5B and diverged (ZIP4-B2). This duplicated gene performs two key meiotic functions: promotion of faithful chromosome pairing-synapsis, and suppression of related chromosome crossover. We obtained a CRISPR zip4-B2 mutant with loss of both functions. This mutation yielded 50% fewer grains, confirming the critical role of ZIP4-B2 in wheat fertility. Next, we generated a novel ‘separation of function’ zip4-B2 mutant named zip4-ph1d, with loss of the crossover suppression phenotype but retained ability to promote correct pairing-synapsis. Remarkably, this zip4-ph1d mutant maintained chromosome stability and preserved grain number. Thus, contrary to accepted wisdom, the key event stabilizing polyploid wheat is promotion of correct pairing-synapsis, rather than suppression of crossover between related chromosomes. We recommend the use of this new zip4-ph1d mutant in wheat breeding strategies to induce crossover between related chromosomes, rather than using the previously used ph1 mutants. Slides of the presentations can be downloaded here: https://tinyurl.com/4bfdchhk