SlBBX26 regulates vegetative growth, flowering and fruit development through the modulation of SlPIF4

Abstract

The BBX family of transcription factors regulate several physiological processes during plant vegetative and reproductive development, bridging light signaling to hormones metabolism. Here, we do an in-depth functional characterization of the tomato SlBBX26 (Solyc10g006750) gene by generating and phenotyping CRISPR/Cas9-mediated genome-edited and RNAi-mediated knockdown lines. We demonstrate that SlBBX26 regulates the negative factor of light signaling, PHYTOCHROME INTERACTING PROTEIN 4 (PIF4), which in turn modulates vegetative growth and flowering by controlling gibberellins (GAs) biosynthetic genes expression and signaling, respectively. Moreover, SlBBX26 regulates fruit growth modulating the expression of cell division- and expansion-related genes. SlBBX26 also influences fruit chloroplast ultrastructure and metabolism in an SlPIF4-mediated manner, leading to alterations in thylakoid stacking, plastoglobuli size, and chlorophyll content, through the regulation of genes involved in chloroplast differentiation and chlorophyll degradation. Finally, SlBBX26-SlPIF4 heterodimer is required to control GA and auxin signaling cascades, triggering the onset of fruit ripening. As such, our findings unveil how BBX proteins contribute to the regulation of main agronomic traits.

Keywords: BBX proteins; Flowering; Gibberellins; Ripening; Solanum lycopersicum; Tomato.