Strigolactones restrict sugar acquisition in rice tiller buds to inhibit their outgrowth by suppressing the expression and polarized localization of two monosaccharide transporters.

Abstract

Strigolactones (SLs) are fundamental phytohormones that suppress tillering, whereas sugars act as both energy sources and signaling molecules to promote tillering. However, the molecular interplay between SLs and sugars remains largely underexplored. In this study, through isobaric tags for relative and absolute quantification-based quantitative proteomic analysis, we identified two highly homologous monosaccharide transporters, OsMST3 and OsMST6, showing increased protein abundance in the SL signaling mutant d3^s2-215 and biosynthesis mutant d10^XJ1705. Using feeding assays with fluorescence- or isotope-labeled sugars, we showed that OsMST3 and OsMST6 function as influx transporters of glucose and fructose, facilitating their translocation from leaf blades to tiller buds to promote bud outgrowth. Interestingly, glucose and fructose not only induce OsMST3 and OsMST6 expression but also promote polarized plasma membrane localization of their encoded proteins, both essential for bud outgrowth, whereas SLs suppress their expression and counteract sugar-induced polarized localization of OsMST3 and OsMST6. Furthermore, we revealed that OsTB1, a key transcription factor downstream of SL signaling, directly binds the OsMST3 and OsMST6 promoters to inhibit their transcription. Tiller bud outgrowth of the tb1^SG0312 mutant is severely inhibited by a non-metabolizable glucose analog (2-deoxy-D-glucose) and an inhibitor of sugar transporters (carbonyl cyanide m-chlorophenylhydrazone). Moreover, simultaneous knockout of OsMST3 and OsMST6 could rescue high-tillering phenotype of the d3^s2-215, d10^XJ1705, and tb1^SG0312 mutants. Collectively, our study reveals a novel mechanism by which SLs control tillering by limiting sugar allocation to buds through suppression of the monosaccharide transporters OsMST3 and OsMST6.