Multi-omics dissection of panicle development reveals a GSE9-centered regulatory network controlling rice grain shape

Rice panicle development is a key agronomic trait that critically determining grain yield and quality. However, the underlying molecular networks, particularly those regulated by de novo genes, remain inadequately characterized.

To address this gap, we performed an integrated transcriptomic, metabolomic, and proteomic analysis of the de novo gene GRAIN SHAPE ON CHROMOSOME 9(GSE9) during panicle development.

Our findings demonstrate that GSE9 disruption activates extensive transcriptomic reprogramming during critical stages. Functional analyses revealed that GSE9 may direct a hierarchical regulatory network, possibly by modulating key transcription factors, such as ERF, WRKY, and bZIP, to integrate hormone signaling pathways, including gibberellin and abscisic acid. Concurrently, GSE9 deficiency led to widespread metabolic dysregulation, particularly in secondary metabolism involving phenylpropanoid and flavonoid biosynthesis that affects spikelet hull properties. A machine learning (KANMB) approach applied to the metabolomic data identified a core set of metabolites and co-expressed genes, indicating that GSE9 coordinately regulates starch metabolism and secondary metabolite biosynthesis. Proteomic profiling further confirmed alterations in these pathways. Critically,GSE9 knockout induced genome-wide transcriptional-translational decoupling, specifically impairing synchronous mRNA-protein coordination rather than simply introducing a temporal delay between transcription and translation. Further analysis revealed that this effect stems from a transcription-dominant regulatory mode, potentially accompanied by translational compensation, while direct evidence is lacking.

This study delineates a multi-level regulatory mechanism by which GSE9 determines grain shape and underscores the broad network-wide effects of gene editing, providing crucial insights for fundamental research and precision crop breeding.