A Duplicated Copy of the Meiotic Gene ZIP4 Preserves up to 50% Pollen Viability and Grain Number in Polyploid Wheat

SIMPLE SUMMARY: On wheat polyploidisation, the major meiotic gene ZIP4, duplicated and diverged, such that tetraploid and hexaploid wheat each carry three and four copies of ZIP4, respectively. Surprisingly, this study demonstrates that, in hexaploid wheat, despite the presence of the other three ZIP4 copies, the duplicated ZIP4 copy is required to prevent major abnormalities during meiosis. Although there is greater disruption of subsequent male rather than female fertility, the duplicated ZIP4 copy preserves up to 50% of the grain number. High wheat fertility is important since it is consumed by over 4.5 billion people on the planet, of whom 2.5 billion are dependent on it. This study highlights the potentially extraordinary value of the wheat ZIP4 duplication, mandating further studies to unravel the complexity of the ZIP4 phenotype in this global crop. ABSTRACT: Although most flowering plants are polyploid, little is known of how the meiotic process evolves after polyploidisation to stabilise and preserve fertility. On wheat polyploidisation, the major meiotic gene ZIP4 on chromosome 3B duplicated onto 5B and diverged (TaZIP4-B2). TaZIP4-B2 was recently shown to promote homologous pairing, synapsis and crossover, and suppress homoeologous crossover. We therefore suspected that these meiotic stabilising effects could be important for preserving wheat fertility. A CRISPR Tazip4-B2 mutant was exploited to assess the contribution of the 5B duplicated ZIP4 copy in maintaining pollen viability and grain setting. Analysis demonstrated abnormalities in 56% of meiocytes in the Tazip4-B2 mutant, with micronuclei in 50% of tetrads, reduced size in 48% of pollen grains and a near 50% reduction in grain number. Further studies showed that most of the reduced grain number occurred when Tazip4-B2 mutant plants were pollinated with the less viable Tazip4-B2 mutant pollen rather than with wild type pollen, suggesting that the stabilising effect of TaZIP4-B2 on meiosis has a greater consequence in subsequent male, rather than female gametogenesis. These studies reveal the extraordinary value of the wheat chromosome 5B TaZIP4-B2 duplication to agriculture and human nutrition. Future studies should further investigate the role of TaZIP4-B2 on female fertility and assess whether different TaZIP4-B2 alleles exhibit variable effects on meiotic stabilisation and/or resistance to temperature change.