Genetic effect of the Ph1 locus on transcriptome atlas of anther development‐related genes, meiotic chromosome behavior and agronomic traits in bread wheat.

SUMMARY: Proper spatiotemporal expression of meiosis‐related genes (MRGs) and other male‐microsporogenesis/microgametogenesis‐related genes (MMRGs) is crucial for normal anther development, yet their expression patterns remain largely unknown in wheat. The Ph1 locus in wheat is known to contain the Ph1 gene that plays a dual role in promoting pairing between homologous chromosomes but repressing pairing between homoeologous chromosomes, but its genetic function is still unclear. Here, we investigated these issues by conducting a comprehensive transcriptome analysis during wheat anther development in Chinese Spring (CS) and its ph1b deletion mutant under greenhouse and field conditions. Our results revealed that MRGs and MMRGs are predominantly expressed during pre‐meiosis stages, with MMRGs also being highly expressed in meiotic‐II. Gene co‐expression analysis showed that C2H2 and B3 transcriptional factors (TFs) are associated with MRGs, and MYB regulators interacted mainly with MMRGs during microgametogenesis. Deletion of genes within the Ph1 locus failed to induce compensatory transcriptional activation of their homoeologous counterparts, while genes outside the Ph1 locus showed environmental‐specific responses, especially during meiotic‐II and mature pollen stages. Notably, early disjunction of bivalent chromosomes is a primary factor leading to defective meiocytes during metaphase I. Furthermore, the ph1b deletion mutant exhibited a substantially delayed heading date, potentially contributing to environment‐stable and environment‐specific alterations in fertility and grain‐related traits. Our study highlights the significant impact of the Ph1 locus on the transcriptome during anther development, and a previously unheeded effect on meiotic chromosome pairing and agronomic traits, suggesting potential for genetic manipulations within the Ph1 locus for wheat improvement. Significance Statement: This study addresses critical gaps by revealing the spatiotemporal expression dynamics of meiosis‐related genes in wheat and clarifying the genetic function of the Ph1 locus. It demonstrates the locus's dual regulatory impact on chromosome pairing and identifies environmental‐specific transcriptional responses, offering insights into genetic targets for improving wheat fertility and agronomic traits. [ABSTRACT FROM AUTHOR]