The T6P-KIN10-ORE1 regulatory axis acts downstream of TDIF-PXY signaling to connect phloem sugar transport with leaf senescence in Arabidopsis.

Abstract

The TDIF-PXY signaling module is best known for its role in vascular development, a process closely linked to phloem function and long-distance sugar transport. However, the molecular mechanisms by which TDIF-PXY-mediated vascular development links phloem sugar transport and signaling to leaf senescence remain largely unclear. Here, we show that Arabidopsis TDIF-PXY-defective mutants exhibit accelerated leaf senescence, accompanied by impaired phloem transport and increased vein callose deposition, together with transcriptional reprogramming of sugar metabolism and carbohydrate accumulation. Inducible PXY knockdown further suggests that changes in sugar metabolism-related gene expression associated with TDIF-PXY attenuation arise primarily from impaired phloem transport rather than from a direct transcriptional output of this pathway. Genetic and metabolic analyses identify trehalose-6-phosphate (T6P) as a key signal contributing to the premature senescence of the pxy mutant. Mechanistically, the T6P-inhibited SnRK1 catalytic subunit KIN10 directly interacts with and phosphorylates the senescence regulator ORE1 at S115, promoting ORE1 destabilization. Elevated T6P inhibits KIN10 activity, thereby reducing S115-dependent ORE1 phosphorylation and stabilizing ORE1. During natural leaf aging, the expression of TDIF-PXY pathway genes and phloem transport capacity decline, whereas T6P accumulation and vein callose deposition increase. Maintaining TDIF expression in phloem tissues preserves phloem transport and delays senescence. Together, these findings reveal a T6P-KIN10-ORE1 regulatory axis that links vascular function to leaf aging, supporting the idea that vascular status serves as an intrinsic cue for the onset of leaf senescence.