Integrated Dual-Transcriptome and Metabolome Analyses Provide Insights into Fruit Symptom Development Caused By Huanglongbing in Citrus reticulata Blanco cv. Wokan

Citrus Huanglongbing (HLB), caused by the phloem-limited bacterium ‘Candidatus Liberibacter asiaticus’ (CLas), severely threatens global citrus production. Infected fruits showed a lopsided shape and color inversion (‘Red-nose’ fruit), but the mechanisms are unclear. We analyzed CLas–host interactions underlying symptom development using integrated transcriptomic and metabolomic profiling of the fruit pith and pericarp from 30 to 240 days after flowering (DAF). “Red-nose” symptoms emerged at 180 DAF and intensified as CLas titers peaked at 240 DAF. CLas transcriptomes indicated that early colonization (30–90 DAF) involved enhanced proliferation, nutrient uptake, stress tolerance, and secretion, whereas later stages (180–240 DAF) exhibited global metabolic downregulation with sustained transporter and surface-structure activity. CLas infection altered host metabolism by promoting sucrose degradation, suppressing sucrose synthesis, disrupting auxin and cytokinin signaling, and perturbing pigment pathways. Defense metabolites were depleted early but accumulated during ripening. These results illustrate how CLas temporally modulates host growth and defense to drive HLB-associated fruit disorders.