Phytochrome-interacting factors integrate environmental signals to regulate tomato growth and development

Plants respond to environmental cues, such as light and temperature, which regulate their growth and development. In the model plant Arabidopsis (Arabidopsis thaliana), PHYTOCHROME-INTERACTING FACTORS (PIFs) are central regulators of both shade-avoidance and thermomorphogenesis. However, their functional roles in crop species are less well known. Here, we generated a tomato (Solanum lycopersicum) mutant lacking all eight known PIF genes (slpifo), to investigate their roles under controlled and field conditions. We showed that SlPIFs are essential for shade responses, while thermomorphogenesis-induced elongation is largely independent of SlPIFs, revealing species-specific differences in regulatory mechanisms. Under low-red to far-red light (low R/FR), slpifo plants failed to exhibit characteristic wild-type responses, including shoot elongation, expansion and thinning of leaf blades, and depletion of leaf chlorophyll. We further identified redundant roles for SlPIF1a, SlPIF4, and SlPIF8a in regulating stem elongation and chlorophyll depletion in response to low R/FR. In addition, slpifo plants exhibited reduced overall growth, fruit size, fruit number, and seed dormancy under field conditions, highlighting broader roles for SlPIFs beyond neighbor detection. These findings provide insights into how PIFs orchestrate organ-specific developmental plasticity in tomato, offering avenues to optimize light responsiveness for crop improvement.