SlSMXL1 integrates strigolactone signaling and energy sensing to control tomato shoot branching under low light

Abstract

Strigolactone (SL) signaling pathways have been characterized in model and crop species. However, the critical components of SL signaling in tomato (Solanum lycopersicum) remain unclear. In this study, MORE AXILLARY GROWTH 2.1/2.2 (SlMAX2.1/2.2) and SUPPRESSOR OF MAX2 1-LIKE1/2 (SlSMXL1/2), which are the homologs of AtMAX2 and AtSMXL6/7/8 in Arabidopsis thaliana respectively, were identified in tomato. Protein–protein interaction assays revealed that SL receptor DWARF14 (SlD14), SlMAX2.1/2.2, and SlSMXL1 formed a ternary complex. Silencing of SlD14, SlMAX2.1 or SlMAX2.2 increased the accumulation of SlSMXL1 protein. Both slmax2.1 and slmax2.2 mutant showed increased branching, and the slmax2.1/2.2 double mutant exhibited a stronger branching phenotype than either single mutant. Furthermore, knockout of SlSMXL1, but not SlSMXL2, reduced bud growth, and silencing of SlSMXL1 suppressed shoot branching of the slmax2.1/2.2 double mutant. Low light (LL) or overexpression of Sucrose-nonfermenting 1-related kinase 1.1 (SlSnRK1.1) inhibited lateral bud growth and upregulated SL-related genes in lateral buds. Notably, lateral bud growth of slmax2.1/2.2 double mutant was suppressed by LL, and cosilencing of SlMAX2.1/2.2 was not able to fully restored the inhibition of lateral bud growth in OE-SlSnRK1.1 plant. Silencing of SlSnRK1.1 promoted lateral bud growth in wild type plants, but this effect was attenuated in the slsmxl1 mutant. Moreover, SlSnRK1.1 physically interacted with SlSMXL1, and silencing of SlSnRK1.1 increased SlSMXL1 protein abundance. Collectively, SlSMXL1 functions as a negative regulator of SL signaling to promote shoot branching, and SL signaling and SlSnRK1.1-mediated starvation response suppress shoot branching under LL, at least in part, by decreasing SlSMXL1 protein levels.