The root-derived syringic acid and shoot-to-root phytohormone signaling pathways play a critical role in preventing apple scab disease

Abstract

Apple scab is a serious disease that has a huge economic impact. While some cultivars of apple are scab-resistant, most are not. Growing research has suggested that root-derived metabolites play a vital role in conferring resistance to aboveground pathogens through the long-distance signaling system between shoot and root. In this work, leaves of scab-resistant cultivar ‘Prima’ (PRM) and scab-susceptible cultivar 'Red Delicious' (RD) were challenged by Venturia inaequalis, and the resulting metabolic reprogramming in root tissues was monitored using gas chromatography-mass spectrometry-based metabolomics in time-course fashion. Metabolomics has revealed that scab fungus causes metabolic reprogramming in underground root tissue when above-ground parts (leaves) are infected. After scab infection in the above-ground leaf tissue, syringic acid is synthesized in the root tissue and transported from the root to the aerial part through vascular tissue. The increased level of reactive oxygen species and jasmonic acid (JA) across roots suggests a signaling pathway from infected leaves triggered by hydrogen peroxide (H₂O₂). In this study, it was found that leaf infection with scab produces H₂O₂. In aerial parts infected with scab, H₂O₂ may act as a signaling molecule to trigger JA production. By travelling from the aerial part (shoot) to the root, H₂O₂ and JA act as long-distance signaling molecules, stimulating magnesium uptake, and eventually enhancing phenylalanine ammonia-lyase (PAL) activity. A metabolic reprogramming of the root tissue is initiated by H₂O₂, JA and PAL activity. Root metabolic reprograming results in the formation of syringic acid, which travels from the roots to the aerial part through vascular tissue and helps fight scab fungal infections. The present study demonstrated that scab infection in apple leaves is associated with long distance signaling from shoot to root, in which root-derived specialized metabolites make their way to aerial parts and confer resistance to scab.