Gibberellin and the miRNA156-targeted SlSBPs synergistically regulate tomato floral meristem determinacy and ovary patterning.

Many developmental processes associated with fruit development occur at the floral meristem (FM). Age-regulated microRNA156 (miR156) and gibberellins (GA) interact to control flowering time, but their interplay in subsequent stages of reproductive development is poorly understood. Here, we show GA and miR156-targeted SlSBPs interact in tomato FM and ovary patterning. High GA responses or overexpression of miR156 (156OE), which leads to low levels of miR156-silenced SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL/SBP), resulted in enlarged FMs, ovary indeterminacy, and fruits with increased locule number. Conversely, low GA responses reduced indeterminacy and locule number, and overexpression of a miR156-resistant SlSBP15 allele (rSBP15) reduced FM size and locule number. GA responses were partially required for the defects observed in 156OE and rSBP15 fruits. Transcriptome analysis and genetic interactions revealed shared and divergent functions of miR156-targeted SlSBPs, PROCERA/DELLA and the classical WUSCHEL/CLAVATA pathway, which has been previously associated with meristem size and determinacy. Our findings reveal the miR156/SlSBP/GA regulatory module is deployed differently depending on developmental stage and create novel opportunities to fine-tune aspects of fruit development that have been important for tomato domestication.