Advantageous spike-to-stem competition for assimilates contributes to the reduction in grain number loss in wheat spikes under water deficit stress

This study was conducted to investigate the mechanisms of assimilate distribution and sugar metabolism in spike-stem that inhibit the formation of fertile florets and grains per spike in winter wheat under pre-reproductive drought stress. Two winter wheat cultivars, CH58 (relatively strongly drought tolerant) and LH6 (relatively weakly drought tolerant), were subjected to successive soil drought treatments from jointing to heading during the 2020–2022 growing seasons. The results showed that pre-reproductive drought stress intensified the degradation and abortion of wheat florets. Compared to CH58, the decrease in the number of fertile florets and grains per spike of LH6 under drought stress increased by an average of 5.3%−8.0% and 8.3%−9.0%, respectively. Drought significantly inhibited the distribution of 13C-photosynthates in wheat spikes (15.7%−24.7%) and stems (8.5%−11.7%) during the booting stage. The number of differentially expressed genes enriched in starch and sucrose metabolic pathways was much higher in the spike and stem of LH6 than in those of CH58. Drought significantly reduced sucrose and hexose in young spikes but increased hexose and fructan concentrations in stems. Compared to LH6, the higher invertase activity and accompanying high expression of sugar transporter protein (STP) in CH58 spikes under drought stress contributed to the utilization of sucrose in young spikes. Additionally, under severe drought, the higher fructan concentration and expression of sugar transport proteins (SWEET and SUT) in the stem of CH58 improved the ability of the stem to transport assimilates to young spikes and thus alleviated the loss of grain number per spike. Exogenous spermidine optimized hexose and sucrose allocation in young wheat spikes and stems after drought stress, thereby increasing the number of fertile florets under drought stress. Overall, the ability of the dominant spike to utilize sugar and the ability to compete for assimilates between the spike and stem contribute to the resistance to drought stress-induced grain reduction in the spike. Exogenous chemicals can regulate the number of fertile florets through this pathway, thereby promoting the formation of wheat grain number.