SlBBX19 modulates plant development and negatively regulates chilling tolerance in tomato

Abstract

SUMMARY Chilling stress severely restricts tomato cultivation and productivity, yet the mechanisms by which a single regulator integrates photosynthetic efficiency, developmental progression, and chilling tolerance remain to be elucidated. Here, we characterized SlBBX19, a chilling‐inducible B‐box transcription factor in tomato (Solanum lycopersicum). SlBBX19 is nucleus‐localized, functions as a negative regulator of vegetative growth and photosynthetic capacity under normal conditions, while simultaneously promoting fruit ripening and suppressing inflorescence branching. Under chilling stress, SlBBX19 acts as a negative regulator of chilling tolerance: overexpression exacerbates reactive oxygen species (ROS) accumulation, membrane damage, and suppresses COR pathway activation, whereas knockout lines exhibit enhanced chilling resistance. Transcriptomic and molecular analyses reveal that SlBBX19 directly binds to G‐box elements in the promoters of light‐harvesting chlorophyll a/b‐binding genes SlLhcb2.2 and SlLhca4.1 to repress their transcription. Virus‐induced gene silencing of these targets recapitulated the overexpression phenotypes, confirming that SlBBX19 compromises photosynthetic efficiency and chilling tolerance primarily through SlLhc downregulation. Collectively, our findings establish SlBBX19 as a key integrator of development and environmental acclimation, revealing a novel regulatory module that links photosynthetic antenna dynamics to chilling stress adaptation. This work may provide a promising genetic target for engineering chilling‐tolerant and physiologically optimized tomato varieties.