Abstract
INTRODUCTION: Gibberellins are essential phytohormones that regulate plant growth and development. Gibberellin 2-oxidases (GA2oxs) deactivate bioactive gibberellin isoforms and many GA2ox genes have been validated as key regulators of agronomic traits in model plants and crops. However, there are few studies on GA2ox genes in wheat, one of the most important staple crops. OBJECTIVE: This study aims to identify favorable alleles of wheat GA2ox genes (TaGA2oxs) and assess their application in wheat improvement. METHODS: We developed an efficient pipeline that integrates population genomics, transgene, transcriptome and evolutionary analyses to systemically dissect genetic effects of TaGA2ox variations on agronomic traits. RESULTS: We identified 40 TaGA2oxs by genome-wide in silico cloning, defined 25 C19-type and 15 C20-type members based on sequence similarity and specified TaGA2ox family expansion by genomic polyploidization, duplication and translocation events. Functional TaGA2oxs were predicted by spatiotemporal expression assays, genetic meta-analysis and genome microsynteny-based phylogeny. We retrieved 52 major haplotypes at 19 TaGA2ox loci based on genome resequencing data for representative wheat cultivars and developed diagnostic molecular markers. In addition to previously-validated favorable haplotypes Rht12b and Rht24b that reduce plant height and have no yield penalty, eight new favorable haplotypes of TaGA2oxs were identified by marker-trait association analysis. Among them, TaGA2ox8-B1-1_hap1, TaGA2ox8-B1-2_hap1 and TaGA2ox8-B1-3_hap1 formed a tandem duplicate gene cluster associated with reduced plant height and increased grain yield. TaGA2ox8-B1-2 as proof of concept was functionally validated to modulate major agronomic traits by transgene assays; its downstream genes and effect on gibberellin homeostasis were also identified by transcriptome, enzyme activity and hormone quantitative analyses. We further traced the origin, spread and distribution of favorable haplotypes to clarify their evolutionary history and application prospects. CONCLUSION: These findings not only provide valuable genetic resources and molecular tools for wheat improvement but also broaden genetic insight into gibberellin-mediated wheat morphogenesis, acclimation and yield formation.