Glucose- and sucrose-signaling modules regulate the Arabidopsis juvenile-to-adult phase transition

Cytosolic invertase 1 (CINV1), which converts sucrose into glucose and fructose is a key entry point of carbon into cellar metabolism and Hexokinase 1 (HXK1) functions as a pivotal sensor for glucose. Further, it is well established that sugar signaling can regulate plant gene expression, for example, the Production of Anthocyanin Pigment 1 (PAP1) / MYB75 transcription factor is specifically induced by sucrose accumulation. Exogenous sugars are also thought to trigger the juvenile-to-adult phase transition via a miR156A/SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) module. However, the endogenous factors that regulate this process have remained undetermined. Here we show that sucrose induced expression of the PAP1 transcription factor increases CINV1 activity by direct binding to CINV1 promoter. Further, we identify a glucose feed-forward loop (Sucrose-CINV1-Glucose-HXK1-miR156-SPL9-PAP1-CINV1-Glucose) that controls CINV1 activity to convert sucrose into glucose signaling to dynamically control the juvenile-to-adult phase transition. Moreover, PAP1 directly binds to the SPL9 promoter, activating SPL9 expression, triggering sucrose signaling that mediates the juvenile-to-adult phase transition. Therefore, a glucose signaling feed-forward loop and a sucrose signaling pathway synergistically regulate the Arabidopsis juvenile-to-adult phase transition. Collectively, we identify a molecular link between the major photosynthate sucrose, the entry point of carbon into cellar metabolism and a key developmental process, the juvenile-to-adult phase transition.