SlBBX20 is a regulator of plant development in response to shade in tomato

An early light signal detected by plants is the reduction of red/far-red ratio (R/FR), triggering the shade avoidance syndrome (SAS), a set of developmental, growth, and biochemical responses that improve plant competition for light. B-box (BBX) transcription factors are key regulators of light-mediated responses in Arabidopsis thaliana; however, their roles in crop species remain elusive. Here, we investigated the function of SlBBX20 (Solyc12g089240) in the SAS of tomato (Solanum lycopersicum, cv. Micro-Tom) by a deep physiological and photosynthesis characterization with biochemical, phytohormone and gene expression analysis in leaves and stems. We conducted simulated shade experiments by reducing the R/FR with the addition of FR light horizontally, using green filters, and increasing plant density. Wild-type (WT) plants exhibited significant shade-avoidance responses in plant height and internode length, whereas Slbbx20 mutant plants showed reduced SAS. In WT plants, the expression of SlBBX20 was inhibited by low R/FR, and shade-induced genes were significantly promoted in the stems but not in the leaves. The expression of SlPAR1 and auxin-related (SlIAA7, SlIAA14 and SlIAA19) genes was significantly reduced in the Slbbx20 mutant under low R/FR. These results correlated with the lower levels of IAA auxin phytohormone in the Slbbx20 leaves. Further, Slbbx20 plants produced lower levels of anthocyanins than WT under high R/FR with constitutive low expression of SlCHS1, SlCHS2 and SlFLS genes in leaves. In greenhouse experiments with natural radiation, Slbbx20 plants showed lower photosynthesis and stomatal conductance than WT under sunlight, correlated with a lower number of stomata and fruit production. These findings suggest that SlBBX20 is a regulator of light responses, improving the fine-tuning of plant growth in different light environments with high and low R/FR ratios.