Integrated metabolomic, lipidomic and proteomic analysis define the metabolic changes occurring in curled areas in leaves with leaf peach curl disease

Peach Leaf Curl Disease, caused by Taphrina deformans, is characterized by reddish hypertrophic and hyperplasic leaf areas. To comprehend the biochemical imbalances caused by the fungus, dissected symptomatic (C) and asymptomatic areas (N) from leaves with increasing disease extension were analyzed by an integrated approach including metabolomics, lipidomics, proteomics, and complementary biochemical techniques. Drastic metabolic differences were identified in C areas with respect to either N areas or healthy leaves, including altered chloroplastic functioning and composition, which differs from the typical senescence process. In C areas, alteration in redox-homoeostasis proteins and in triacylglycerols content, peroxidation and double bond index were observed. Proteomic data revealed induction of host enzymes involved in auxin and jasmonate biosynthesis and an upregulation of phenylpropanoid and mevalonate pathways and downregulation of the plastidic methylerythritol phosphate route. Amino acid pools were affected, with upregulation of proteins involved in asparagine synthesis. Curled areas exhibited a metabolic shift towards functioning as a sink tissue importing sugars, probably from N areas, and producing energy through fermentation and respiration and reductive power via the pentose phosphate route. Identifying the metabolic disturbances leading to disease symptoms is a key step in designing strategies to prevent or delay the progression of the disease.