Integration of metabolomics and existing omics data reveals new insights into phytoplasma-induced metabolic reprogramming in host plants

Phytoplasmas are cell wall-less bacteria that induce abnormal plant growth and various diseases, causing severe economic loss. Phytoplasmas are highly dependent on nutrients imported from host cells because they have lost many genes involved in essential metabolic pathways during reductive evolution. However, metabolic crosstalk between phytoplasmas and host plants and the mechanisms of phytoplasma nutrient acquisition remain poorly understood. In this study, using metabolomics approach, sweet cherry virescence (SCV) phytoplasma-induced metabolite alterations in sweet cherry trees were investigated. A total of 676 metabolites were identified in SCV phytoplasma-infected and mock inoculated leaves, of which 187 metabolites were differentially expressed, with an overwhelming majority belonging to carbohydrates, fatty acids/lipids, amino acids, and flavonoids. Available omics data of interactions between plant and phytoplasma were also deciphered and integrated into the present study. The results demonstrated that phytoplasma infection promoted glycolysis and pentose phosphate pathway activities, which provide energy and nutrients, and facilitate biosynthesis of necessary low-molecular metabolites. Our findings indicated that phytoplasma can induce reprograming of plant metabolism to obtain nutrients for its own replication and infection. The findings from this study provide new insight into interactions of host plants and phytoplasmas from a nutrient acquisition perspective.