Multi-omics identifies key genetic and metabolic networks regulating spike organ development in wheat

Abstract Wheat (Triticum aestivum L.) spike development is tightly regulated by genetic and metabolic programs that drive organ growth and morphological changes. However, the dynamic interplay between metabolic shifts, gene expression patterns, and their regulatory roles during spike development, remains poorly characterized. To address this knowledge gap, we performed integrated metabolomic and transcriptomic profiling across 12 stages of wheat spike organ development. Our analysis detected 1,105 metabolites in 233 spike, spikelet, and floret samples, uncovering an uneven distribution of phytohormone-related metabolites. The exogenous phytohormone treatments validated the regulatory roles of phytohormones in spike morphogenesis. High-resolution spatiotemporal data from carpel organs enabled the reconstruction of a regulatory network, identifying key genes (including 12-oxo-phytodienoic acid reductase3 (TaOPR3), Grain Length1 (GL1), and Grain Length2 (GL2)) as critical determinants of grain size. Genomic analyses revealed geographical differentiation in gene haplotypes and their selective retention during breeding, with superior alleles associated with increased grain size. This comprehensive dataset provides a valuable resource for understanding the molecular basis of wheat grain yield and offers potential targets for crop improvement.