Integrated carbon metabolism-transcriptomics-proteomics reveals physiological and molecular mechanisms underlying sour jujube resistance to witches’ broom disease

Phytoplasma-mediated witches' broom disease (WBD) causes abnormal growth and inhibits fruit formation in sour jujube trees, causing significant economic damage. Research on the pathogenic mechanisms of WBD and the disease resistance mechanisms of sour jujube tree remains poorly understood. In this study, these mechanisms were investigated using healthy resistant jujube branches that had been grafted onto WBD-infected trees and grown for seven years. Leaves were collected from both healthy resistant branches (KB) and WBD-affected branches (ZFB) to analyze differences in plant physiological indicators, carbon metabolic processes, and transcriptional and protein regulatory mechanisms. The results indicated that, compared with the ZFB group, the KB group had significantly greater levels of photosynthetic indicators, including the transpiration rate, net photosynthetic rate, stomatal conductance, and photosynthetically active radiation. Nutrient absorption and metabolic indicators, such as soluble proteins, were also higher in KB than in ZFB, whereas soluble sugar and starch concentrations were lower. Carbon metabolism profiling revealed that the KB group showed increased fatty acid synthesis for sustained energy production, whereas the ZFB group presented disrupted central carbon flux through an impaired TCA cycle, glycolysis, and pentose phosphate pathways. In addition, ferredoxin (Fd) was identified as a key resistance determinant in jujube trees against WBD phytoplasma. Genes and proteins associated with the photosynthesis pathway exhibited elevated expression levels in KB leaves, particularly those encoding Fd. High Fd expression enhances NADPH and ATP production, accelerates the Calvin cycle, and promotes carbohydrate synthesis. This enhancement supports various biological pathways, including the assimilation of carbon and nitrogen, chlorophyll metabolism, and the synthesis of photosynthetic pigments and fatty acids. In summary, our study reveals that an intact photosynthetic system and its associated metabolism protect resistant branches against WBD, providing a theoretical basis for breeding resistant cultivars.