Vitamin B1 THIAMIN REQUIRING1 synthase mediates the maintenance of chloroplast function by regulating sugar and fatty acid metabolism in rice

• Published in: Journal of integrative plant biology 2022-08, Vol.64 (8), p.1575-1595
• Main Authors: Nie, Yanshen, Yu, Li, Mao, Lianlian, Zou, Wenxuan, Zhang, Xiufeng, Zhao, Jie
• Format: Article
• Language: English
• Subjects: Alternative splicing; Biosynthesis; chloroplast; Chloroplasts; Cytosol; fatty acid metabolism; Fatty acids; Gene expression; Genes; Kinases; Membranes; Metabolism; Mutation; Pentose; Pentose phosphate pathway; Phosphomethylpyrimidine kinase; Rice; Seedlings; Splicing; Sucrose; Sugar; sugar metabolism; THIAMIN REQUIRING1; Thiamine; Thiamine diphosphate; Tricarboxylic acid cycle; Vitamin B; Vitamin B1
• ISSN: 1672-9072; 1744-7909
• DOI: 10.1111/jipb.13283

ABSTRACT Vitamin B1 (VB1), including thiamin, thiamin monophosphate (TMP), and thiamin pyrophosphate (TPP), is an essential micronutrient for all living organisms. Nevertheless, the precise function of VB1 in rice remains unclear. Here, we described a VB1 auxotrophic mutant, chlorotic lethal seedling (cles) from the mutation of OsTH1, which displayed collapsed chloroplast membrane system and decreased pigment content. OsTH1 encoded a phosphomethylpyrimidine kinase/thiamin‐phosphate pyrophosphorylase, and was expressed in various tissues, especially in seedlings, leaves, and young panicles. The VB1 content in cles was markedly reduced, despite an increase in the expression of VB1 synthesis genes. The decreased TPP content affected the tricarboxylic acid cycle, pentose phosphate pathway, and de novo fatty acid synthesis, leading to a reduction in fatty acids (C16:0 and C18:0) and sugars (sucrose and glucose) of cles. Additionally, irregular expression of chloroplast membrane synthesis genes led to membrane collapse. We also found that alternative splicing and translation allowed OsTH1 to be localized to both chloroplast and cytosol. Our study revealed that OsTH1 was an essential enzyme in VB1 biosynthesis and played crucial roles in seedling growth and development by participating in fatty acid and sugar metabolism, providing new perspectives on VB1 function in rice. Loss‐function of the Oryza sativa vitamin B1 biosynthesis gene OsTH1 led to a reduction of vitamin B1 content, thus affecting sugar metabolism and fatty acid synthesis, leading to the membrane collapse of chloroplast, defective growth and development, resulting in a chlorotic phenotype.