Changing Host Photosynthetic, Carbohydrate, and Energy Metabolisms Play Important Roles in Phytoplasma Infection

Phytoplasmas parasitize plant phloem tissue and cause many economically important plant diseases. Jujube witches'-broom disease is a destructive phytoplasma disease of Chinese jujube (Ziziphus jujuba). To elucidate the influence of phytoplasma on host photosynthetic, carbohydrate and energy metabolisms, four types of jujube tissues showing disease symptoms with different severity were investigated at the structural, physiological, and molecular levels. Quantitative real-time PCR and high-performance liquid chromatography results showed that the down-regulation of genes related to photosynthesis and the lower contents of chlorophyll in diseased leaves. This clearly inhibited the light-harvesting and photosystem II activity of photosynthesis; however, overexpression of genes related to starch, sucrose and glucose synthesis led to higher contents of these carbohydrates. Meanwhile, transmission electron microscopy images revealed that dense amounts of phytoplasmas accumulated in the sieve elements of diseased petiole phloem, and the structure of the grana and stroma lamellae of chloroplasts in the diseased leaves was destroyed. Phytoplasma infection inhibited photosynthesis and led to abnormal carbohydrate accumulation in the diseased leaves. Furthermore, comparative metabolite analysis indicated that phytoplasma infection also stimulated amino acids and energy metabolisms of the diseased leaves. Continually inhibiting the photosynthetic process and stimulating carbohydrate and energy metabolisms of diseased trees may exhaust their nutrients. Our results highlight the importance of changing host metabolisms during the pathogenic process.