<i>Botrytis cinerea</i> Targets Chloroplast to Suppress Photosynthesis and Enhance Susceptibility by Attenuating Degradation of SlBIUPa in Tomato

Chloroplasts are central to plant immunity, but how the necrotrophic pathogen Botrytis cinerea (B. cinerea) manipulates chloroplast function to suppress host defences remains largely unknown. Here, we identified and characterised SlBIUPa, a B. cinerea-induced unknown protein in tomato critical for plant response to the pathogen. Overexpression of SlBIUPa disrupts chloroplast function, while the SlBIUPa mutant increased chloroplast content, reduced photosynthesis damage, and decreased reactive oxygen species accumulation, thereby conferring remarkable resistance to B. cinerea. Mechanistically, SlBIUPa interacts with the Rubisco small subunit SlRBCS3B, inhibiting its expression and reducing Rubisco activity. Under normal conditions, the SlBIUPa is ubiquitinated and degraded via the 26S proteasome-dependent pathway; however, B. cinerea infection attenuates this degradation, leading to SlBIUPa accumulation and increased susceptibility. Significantly, the SlBIUPa and homologue gene SlBIUPb double mutant enhanced plant resistance and increased lycopene and carotenoid content in fruits without any fitness costs. These findings offer a potential strategy for breeding tomatoes with enhanced disease resistance and improved fruit quality.