MdERDL6-mediated glucose efflux to the cytosol promotes sugar accumulation in the vacuole through up-regulating TSTs in apple and tomato

Abstract

Sugar transport across tonoplasts is essential for maintaining cellular sugar homeostasis and metabolic balance in plant cells. It remains unclear, however, how this process is regulated among different classes of sugar transporters. Here, we identified a tonoplast H+/glucose symporter, MdERDL6-1, from apples, which was highly expressed in fruits and exhibited expression patterns similar to those of the tonoplast H+/sugar antiporters MdTST1 and MdTST2. Overexpression ofMdERDL6-1unexpectedly increased not only glucose (Glc) concentration but also that of fructose (Fru) and sucrose (Suc) in transgenic apple and tomato leaves and fruits. RNA sequencing (RNA-seq) and expression analyses showed an up-regulation ofTST1andTST2in the transgenic apple and tomato lines overexpressingMdERDL6-1. Further studies established that the increased sugar concentration in the transgenic lines correlated with up-regulation ofTST1andTST2expression. Suppression or knockout ofSlTST1andSlTST2in theMdERDL6-1–overexpressed tomato background reduced or abolished the positive effect ofMdERDL6-1on sugar accumulation, respectively. The findings demonstrate a regulation ofTST1andTST2byMdERDL6-1, in which Glc exported by MdERDL6-1 from vacuole up-regulatesTST1andTST2to import sugars from cytosol to vacuole for accumulation to high concentrations. The results provide insight into the regulatory mechanism of sugar accumulation in vacuoles mediated by the coordinated action of two classes of tonoplast sugar transporters.