Transcription factor OsbZIP10 modulates rice grain quality by regulating OsGIF1

• Published in: The Plant journal : for cell and molecular biology Vol. 119; no. 5; pp. 2181 - 2198
• Main Authors: Jiang, Meng, Zhang, Huali, Song, Yue, Chen, Jiale, Bai, Jianjiang, Tang, Jianhao, Wang, Qing, Fotopoulos, Vasileios, Zhu, Qian‐Hao, Yang, Ruifang, Li, Ruiqing
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.09.2024
• Subjects: AGPS1; Amylose; Biological activity; Cell walls; Crop yield; Eating quality; Genes; Genetic analysis; Genetic engineering; Grain; grain filling; Haplotypes; Homeostasis; Impact analysis; Invertase; natural variation; Oryza sativa indica; Oryza sativa japonica; Reactive oxygen species; Rice; seed formation; Seeds; starch synthesis; Transcription factors; starch synthesis; amylose; seed formation; AGPS1; grain filling; natural variation
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.16911

SUMMARY Understanding and optimizing the process of grain filling helps the quest to maximize rice (Oryza sativa L.) seed yield and quality, yet the intricate mechanisms at play remain fragmented. Transcription factors (TFs) are major players in the gene networks underlying the grain filling process. Here, we employed grain incomplete filling (OsGIF1)/cell wall invertase 2, a key gene involved in grain filling, to explore its upstream TFs and identified a bZIP family TF, OsbZIP10, to be a transcriptional activator of OsGIF1. Rice grains of the knockouts of OsbZIP10 showed increased white‐core rates but lower amylose content (AC), leading to better eating and cooking qualities in all genetic backgrounds investigated, though the impact of mutations in OsbZIP10 on grain weight depended on genetic background. Multi‐omics analyses suggested that, in addition to OsGIF1, multiple genes involved in different biological processes contributing to grain filling were targeted by OsbZIP10, including OsAGPS1, a gene encoding the ADP‐Glc pyrophosphorylase (AGPase) small subunit, and genes contributing to homeostasis of reactive oxygen species. Distinct genetic make‐up was observed in OsbZIP10 between japonica and indica rice varieties, with the majority varieties of each subspecies belonging to two different haplotypes that were closely associated with AC. Overexpressing the haplotype linked to high‐AC in the low‐AC genetic background increased AC. Overall, this study sheds crucial light on the significance of the OsbZIP10–OsGIF1 module in the determination of rice grain quality, offering a potential avenue for genetic engineering of rice to produce seeds with tailored attributes. Significance Statement Proposed model explaining the contributions of OsbZIP10 to seed quality. OsbZIP10 exerts a direct influence on the expression of OsGIF1 and OsAGPS1, genes fundamental to the synthesis of starch. The regulation of OsbZIP10 over these genes is, therefore, instrumental in determining the quality of the seed. Concomitantly, the influence of OsbZIP10 extends beyond starch synthesis to encompass the regulation of antioxidant genes, such as OsAPX1, OsCAT2 and OsPRX47. This oversight ensures the activity of key antioxidant enzymes, including POD, CAT and APX, which are vital in maintaining a balance of ROS within the seed. This balance is, in turn, crucial for the proper functioning of starch biosynthetic enzymes, thereby linking OsbZIP10's role in seed quality to its influence on redox homeostasis. The interplay between OsbZIP10 and these genes underscores the complexity o regulatory networks that govern seed development and quality. We here revealed that OsbZIP10 acts as a positive regulator of OsGIF1 and OsAGPS1, and that the affection of OsbZIP10 on grain formation is tightly associated with redox homeostasis, which, in turn, is crucial for the proper functioning of starch biosynthetic enzymes. Overall, this study sheds crucial light on the significance of the OsbZIP10–OsGIF1 module in determining rice grain quality, offering a potential avenue for genetic engineering to produce rice seeds with tailored attributes.