A chloroplast sulphate transporter modulates glutathione‐mediated redox cycling to regulate cell division

• Published in: Plant, cell and environment cell and environment, 2024-12, Vol.47 (12), p.5391-5410
• Main Authors: Huang, Pin‐jui, Lin, Yen‐Ling, Chen, Chun‐Han, Lin, Hsiang‐Yin, Fang, Su‐Chiung
• Format: Article
• Language: English
• Subjects: Anion Transport Proteins - genetics; Anion Transport Proteins - metabolism; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Basal bodies; Biosynthesis; Cell cycle; Cell Division; Cell size; Chlamydomonas reinhardtii; Chloroplasts; Chloroplasts - metabolism; Cycles; Cytosol; Cytosol - metabolism; G1 phase; Glutamate-Cysteine Ligase - genetics; Glutamate-Cysteine Ligase - metabolism; Glutathione; Glutathione - metabolism; Mutants; Mutation; Oxidation-Reduction; Phenotypes; Redox properties; Sulfates; Sulfates - metabolism; sulphate homoeostasis
• ISSN: 0140-7791; 1365-3040; 1365-3040
• DOI: 10.1111/pce.15113

Glutathione redox cycling is important for cell cycle regulation, but its mechanisms are not well understood. We previously identified a small‐sized mutant, suppressor of mat3 15‐1 (smt15‐1) that has elevated cellular glutathione. Here, we demonstrated that SMT15 is a chloroplast sulphate transporter. Reducing expression of γ‐GLUTAMYLCYSTEINE SYNTHETASE, encoding the rate‐limiting enzyme required for glutathione biosynthesis, corrected the size defect of smt15‐1 cells. Overexpressing GLUTATHIONE SYNTHETASE (GSH2) recapitulated the small‐size phenotype of smt15‐1 mutant, confirming the role of glutathione in cell division. Hence, SMT15 may regulate chloroplast sulphate concentration to modulate cellular glutathione levels. In wild‐type cells, glutathione and/or thiol‐containing molecules (GSH/thiol) accumulated in the cytosol at the G1 phase and decreased as cells entered the S/M phase. While the cytosolic GSH/thiol levels in the small‐sized mutants, smt15‐1 and GSH2 overexpressors, mirrored those of wild‐type cells (accumulating during G1 and declining at early S/M phase), GSH/thiol was specifically accumulated in the basal bodies at early S/M phase in the small‐sized mutants. Therefore, we propose that GSH/thiol‐mediated redox signalling in the basal bodies may regulate mitotic division number in Chlamydomonas reinhardtii. Our findings suggest a new mechanism by which glutathione regulates the multiple fission cell cycle in C. reinhardtii. Summary Statement The cell cycle is associated with periodic oscillation of the cellular redox environment. Our investigation of subcellular glutathione and thiol‐containing molecules in Chlamydomonas reinhardtii has provided new insights into their role in regulating the cell cycle.