β-Carbonic anhydrases integrate CO2 and light cues to coordinate photosynthesis in tomato.

Abstract

Optimization of photosynthesis requires precise coordination between electron transport and CO₂ assimilation, but how plants maintain this coordination under suboptimal CO₂ and light conditions remains poorly understood. Here, we identify two tomato (Solanum lycopersicum) β-carbonic anhydrases (βCAs) responsive to deficient CO₂. Although both are required for biomass accumulation and efficient photosynthesis, the chloroplast βCA1 does not directly participate in carbon assimilation but instead specifically coordinates photosystem performance and leaf internal structure. This role is distinct from the cytosol/plasma-membrane βCA2 that supports carbon assimilation and overall growth. We demonstrate that βCA1 buffers light-induced stromal pH changes, thereby optimizing proton motive force (pmf) and stabilizing photosystem II performance. The absence of βCA1 increases photosystem sensitivity to high-light intensities, resulting in increased photoprotective responses and adaptive thylakoid re-organization when environmental CO₂ becomes limiting relative to irradiance. Our findings establish chloroplast βCA1 as a key integrator of CO₂ and light cues that optimizes photosystem performance through modulation of pmf partitioning and reveal stromal pH regulation as a previously unrecognized mechanism for optimizing photosynthesis under suboptimal CO₂ and light conditions.