Tomato miR156-targeted SlSBP15 represses shoot branching by modulating hormone dynamics and interacting with GOBLET and BRANCHED1b.

Abstract

The microRNA156 (miR156)/SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE (SPL/SBP) regulatory hub is highly conserved among phylogenetically distinct species, but how it interconnects multiple pathways to converge to common integrators controlling shoot architecture is still unclear. Here, we demonstrated that the miR156/SlSBP15 node modulates tomato shoot branching (SB) by connecting multiple phytohormones with classical genetic pathways regulating both axillary bud (AB) development and outgrowth. MiR156-overexpressing plants (156-OE) displayed high SB, whereas plants overexpressing a miR156-resistant SlSBP15 allele (rSBP15) showed arrested SB. Importantly, the rSBP15 allele was able to partially restore the wild-type SB phenotype in 156-OE background. rSBP15 plants have tiny ABs, and their activation is dependent on shoot apex-derived auxin transport inhibition. Hormonal measurements revealed that Indole-3-acetic acid (IAA) and abscisic acid (ABA) concentrations were lower in 156-OE and higher in rSBP15 ABs, respectively. Genetic and molecular data indicated that SlSBP15 regulates AB development and outgrowth by inhibiting auxin transport and GOBLET (GOB) activity, and by interacting with tomato BRANCHED1b (SlBRC1b) to control ABA levels within ABs. Collectively, our data provide a new mechanism by which the miR156/SPL/SBP hub regulates SB, and suggest that modulating SlSBP15 activity might have potential applications in shaping tomato shoot architecture.