Sucrose metabolism and hormone interaction determine the fate of different florets within central spikelet of wheat

Highlights 1 Proximal floret (F1) developed earlier than distal floret (F5) within a spikelet. IAA-starch synergy in F1 establishes a competitive metabolic sink, whereas ABA-T6P interplay in F5 enforces developmental arrest. Tissue-specific regulation in fertile florets: lemmas supplied carbon by photosynthesis, anthers decomposed sucrose to synthesize starch, ovaries activated lipid biosynthesis for embryogenesis. In the central spikelet, floret primordia proximal to rachis typically develop into fertile florets, while those distal ones tend to abort. However, the mechanism driving these divergent outcomes remain unclear. To elucidate this mechanism, a two-year field experiment was conducted, analyzing the differences between fertile (floret 1) and abortive florets (floret 5) at phenotypic, physiological, cellular, and transcriptional levels. Our results showed that floret 1 (F1) developed earlier than floret 5 (F5), evidenced as distinct floret and anther cell morphology. This developmental difference was associated with distinct metabolic strategies: F1 prioritizes starch biosynthesis by enhancing photosynthetic efficiency and reducing thermal dissipation, while F5 diverts carbon to trehalose metabolism under resource constraints. Transcriptomic profiling revealed 17,711 differentially expressed genes, predominantly enriched in carbohydrate metabolism. Key starch-related genes ( WAXY , SS , GBE1 ) were upregulated in F1, while trehalose synthesis genes ( TPS.5 , TPS.6 , TPP.7 ) dominated in F5, reflecting a metabolic trade-off between growth and survival. Hormonal profiling revealed elevated indole-3-acetic acid (IAA) levels in F1, driven by upregulated genes encoding enzymes of TDC and YUCCA, whereas abscisic acid (ABA) level increased in F5, mediated by NCED. Specially, tissue-specific regulation in fertile floret was clarified: lemma tissues enriched in photosynthesis genes supplied localized carbon, anthers relied on sucrose cleavage genes to sustain pollen development, and ovary activated lipid biosynthesis genes for embryogenesis. Collectively, we propose a model where IAA-starch synergy in proximal florets establishes a competitive metabolic sink, whereas ABA-T6P interplay in distal florets enforces developmental arrest, thereby optimizing resource allocation and reproductive success. The proposed regulatory framework provides novel views for improving floret fertility through carbohydrate partitioning and hormone signal.