Positional differences of rice spikelet formation under high temperature are associated with sucrose utilization discrepancy

Abstract

In rice (Oryza sativa), the upper position (top 1/3) of the panicle exhibits superior spikelet development compared with the basal position (basal 1/3), particularly under high temperature (HT). In this study, the rice cultivar Yongyou 538 (susceptible to spikelet degeneration) was subjected to HT to investigate the physiological mechanism underlying positional differences in spikelet degeneration in the panicle by conducting comparative transcriptome and physiological analyses. The basal position of panicles showed more degenerated spikelets compared with the upper under normal temperature and HT, with HT aggravating this degeneration. Spikelet development depends on carbohydrate availability. In total, 1144 genes associated with spikelet development were differentially expressed in the upper and basal, primarily involving starch and sucrose metabolism. Under normal temperature and HT, the expression levels of sucrose transporter genes were lower in the basal, indicating sucrose transport was blocked there. Sucrose, a type of soluble sugar, accumulated more appreciably in the basal position under HT, whereas total soluble sugar content exhibited the opposite trend. It is associated with sucrose hydrolysis enzyme activities were markedly reduced, indicating impaired sucrose utilization. Simultaneously, decreased activities of TCA cycle-related enzymes led to NAD⁺ accumulation and increase in reactive oxygen species production. Lower antioxidant enzyme activities in the basal resulted in substantial reactive oxygen species accumulation. In conclusion, significant positional differences in spikelet formation along the panicle are characterized by extensive degeneration of spikelets in the basal position, owing to impaired sucrose utilization in this region, leading to peroxide accumulation and inhibition of spikelet development.