Redox-regulated plastoglobule ABC1K1-ABC1K3 kinase complex controls plastoquinone mobilization for chloroplast photosynthetic adaptation to red light.

Plastoglobules, lipoprotein particles associated with thylakoid membranes, serve as critical hubs for chloroplast acclimation to environmental perturbations. However, the molecular mechanisms underlying plastoglobules' signal perception and transduction remain poorly understood. Here, we identify a redox-regulated kinase complex in Arabidopsis that mediates plastoglobules' response to red light. Two plastoglobule-localized kinases, ACTIVITY OF BC1 COMPLEX KINASE 1 and 3 (ABC1K1 and ABC1K3), form a dynamic hetero-oligomeric complex essential for maintaining plastoquinone (PQ) pool homeostasis and optimizing photosynthetic efficiency. These kinases dynamically adjust their conformational states in response to PQ redox state changes induced by environmental light conditions. Under preferential photosystem II (PSII) excitation induced by red light, reduced PQ pool initiates a signaling cascade through activation of the thylakoid oxidoreductase LUMEN THIOL OXIDOREDUCTASE 1 (LTO1). Activated LTO1 then oxidizes ABC1K1 at Cys107, triggering its oligomerization via inter-molecular disulfide bond formation. This oligomeric state change leads to enhanced interaction between ABC1K1 and ABC1K3 oligomers, reconfiguring the kinase complex to relieve ABC1K3-mediated inhibition of PQ mobilization. Consequently, by restoring PQ pool homeostasis, the ABC1K1-ABC1K3 complex mitigates PSII photodamage and safeguards photosynthesis, thereby enabling chloroplast adaptation to red light. Thus, our findings reveal a redox regulation mechanism by which plastoglobules integrate environmental cues with chloroplast homeostasis, providing new insights into plastoglobule-mediated stress acclimation.