Increased sugar content impairs pollen fertility and reduces seed-setting in high-photosynthetic-efficiency rice

Abstract

Crop yield depends on biomass, which is primarily associated with photosynthesis. We previously demonstrated that two photorespiratory bypasses, i.e., GOC (glycolate oxidase + oxalate oxidase + catalase) and GCGT (glycolate oxidase + catalase + glyoxylate carboligase + tartronic semialdehyde reductase), significantly increased photosynthesis, biomass, and grain yield, but decreased seed-setting rates in rice. This study explored the underlying mechanism of how elevated photosynthetic efficiency impacted the seed-setting. First, pollen germination assessed in vivo and in vitro, revealed a reduced germination rate in GCGT rice. Subsequent analysis found that photosynthates highly accumulated in the leaves and stems; sucrose and soluble sugar levels were increased but the starch level was reduced in the anthers. Uridine diphosphate glucose (UDP-Glc) was increased but uridine diphosphate galactose (UDP-Gal) was unaltered, thus causing an imbalance in the UDP-Glc/UDP-Gal ratio in GCGT anthers. Most anthers in GCGT plants had two locules in contrast to four in the wild-type (WT). Pollen tapetum was developmentally abnormal, and genes related to sucrose synthesis, transport, and tapetal programmed cell death (PCD) were upregulated, whereas those involved in starch synthesis and conversion were downregulated in GCGT anthers. Taken together, our results demonstrated that an increase in sugar content was the primary factor causing reduced seed-setting rates in high photosynthetic efficiency rice, during which metabolic disorder of sugars and UDP sugar imbalance in anthers lead to impaired pollen fertility.