Cotton solanesyl diphosphate synthases GhSPS1/2 catalyzes plastoquinone-9 (PQ-9) biosynthesis associating with...

Solanesyl diphosphate synthases (SPSs) are essential in the biosynthesis of plastoquinone-9 (PQ-9), a critical molecule for plant growth, development, and metabolism. However, how PQ-9 is promptly synthetized during photosynthesis remains unclear. Here, we revealed that Gossypium hirsutum SPS1/SPS2 (GhSPS1/2) catalyzed PQ-9 biosynthesis, which mitigates the effects of singlet oxygen (¹O₂) generated during photosynthesis. The simultaneous knockdown or knockout of GhSPS1/2 significantly reduced PQ-9 levels, increased ¹O₂ accumulation, and decreased carotenoid and chlorophyll levels, leading to the appearance of albino phenotypes. Yeast two-hybrid and split luciferase complementation assays suggested that GhSPS1/2 interacts with both GhPsbO1 (oxygen-evolving enhancer protein 1) and GhCAB-151 (the light-harvesting chlorophyll a/b binding protein 151). Interestingly, silencing GhPsbO1 was able to reduce PQ-9 levels, increase ¹O₂ accumulation, and decrease carotenoid and chlorophyll contents, which led to albino phenotype, but silencing GhCAB-151 did not. The functional role of SPS1/2 was further validated in tobacco and Arabidopsis, where they exhibited similar activities to GhSPS1/2. Collectively, these findings demonstrate that the interaction between SPS1/2 and PsbO1 possibly facilitates local biosynthesis of PQ-9 around photosystem II for photoprotection mechanism in plants.