BOTRYOID POLLEN 1 regulates ROS-triggered PCD and pollen wall development by controlling UDP-sugar homeostasis in rice

• DOI: 10.1093/plcell/koad181
• Publication Date: 2023-06-24T22:41:38Z
• Authors: Huiqiong Chen; Shuqing Zhang; Ruiqi Li; Guoqing Peng; Weipan Chen; Carsten Rautengarten; Minglong Liu; Liya Zhu; Yueping Xiao; Fengshun Song; Jinlong Ni; Jilei Huang; Aimin Wu; Zhenlan Liu; Chuxiong Zhuang; Joshua L Heazlewood; Yongyao Xie; Zhizhan Chu; Hai Zhou
• Keywords: Gene Expression Regulation, Plant; Pollen; Homeostasis; Oryza; Apoptosis; Reactive Oxygen Species; Sugars; Uridine Diphosphate; Plant Proteins

AbstractUridine diphosphate (UDP)-sugars are important metabolites involved in the biosynthesis of polysaccharides and may be important signaling molecules. UDP-glucose 4-epimerase (UGE) catalyzes the interconversion between UDP-Glc and UDP-Gal, whose biological function in rice (Oryza sativa) fertility is poorly understood. Here, we identify and characterize the botryoid pollen 1 (bp1) mutant and show that BP1 encodes a UGE that regulates UDP-sugar homeostasis, thereby controlling the development of rice anthers. The loss of BP1 function led to massive accumulation of UDP-Glc and imbalance of other UDP-sugars. We determined that the higher levels of UDP-Glc and its derivatives in bp1 may induce the expression of NADPH oxidase genes, resulting in a premature accumulation of reactive oxygen species (ROS), thereby advancing programmed cell death (PCD) of anther walls but delaying the end of tapetal degradation. The accumulation of UDP-Glc as metabolites resulted in an abnormal degradation of callose, producing an adhesive microspore. Furthermore, the UDP-sugar metabolism pathway is not only involved in the formation of intine but also in the formation of the initial framework for extine. Our results reveal how UDP-sugars regulate anther development and provide new clues for cellular ROS accumulation and PCD triggered by UDP-Glc as a signaling molecule.