Sugar Depletion in Korean Pine Infected with Cronartium ribicola, Alongside Metabolic Reprogramming by the T6P–Tre Signaling Module

In diseased Korean pine trees (Pinus koraiensis), Cronartium ribicola develops aecia only in the bole, where sugar is initially sufficient. However, the molecular mechanisms underlying sugar depletion in diseased Korean pine trees remain unelucidated, hindering sugar-targeted control strategies. Focusing on host responses, this study integrated metabolomics, transcriptomics, and targeted glycomics based on spatial partitioning to investigate sugar metabolic reprogramming in the bole of diseased pines. Multi-omics revealed severe sugar depletion in the blister area, which was significantly correlated with relative C. ribicola DNA level. However, the transcription of sugar synthesis genes was upregulated, while sugar degradation genes were downregulated, indicating decoupling between sugar metabolism and transcription. Concurrently, T6P–Tre-centered reprogramming was identified: Pktppd and Pktpp4, encoding enzymes that convert T6P into Tre, were downregulated, leading to elevated T6P and reduced Tre levels. This T6P–Tre shift likely acts as a signal to activate genes related to sugar accumulation in response to sugar depletion, thereby explaining the observed transcriptional-metabolic decoupling. Targeting the T6P–Tre module to modulate host sugar allocation and restrict sugar availability to the pathogen may offer a novel strategy for the targeted control of Korean pine blister rust (KPBR).