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

• Published in: The Plant cell 2023-09, Vol.35 (9), p.3522-3543
• Main Authors: Chen, Huiqiong, Zhang, Shuqing, Li, Ruiqi, Peng, Guoqing, Chen, Weipan, Rautengarten, Carsten, Liu, Minglong, Zhu, Liya, Xiao, Yueping, Song, Fengshun, Ni, Jinlong, Huang, Jilei, Wu, Aimin, Liu, Zhenlan, Zhuang, Chuxiong, Heazlewood, Joshua L, Xie, Yongyao, Chu, Zhizhan, Zhou, Hai
• Format: Article
• Language: English
• Subjects: Apoptosis; Gene Expression Regulation, Plant; Homeostasis; Oryza - metabolism; Plant Proteins - genetics; Plant Proteins - metabolism; Pollen - metabolism; Reactive Oxygen Species - metabolism; Sugars - metabolism; Uridine Diphosphate - metabolism
• ISSN: 1040-4651; 1532-298X; 1532-298X
• DOI: 10.1093/plcell/koad181

Abstract Uridine 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. UDP-Glc and its derivatives induce the expression of NADPH oxidase genes, inducing ROS-triggered PCD as signaling molecules, but also regulate pollen wall development as metabolites.