Pathogen promotes insect ovarian development by inducing a dual role of host ATPSyn-β

Candidatus Liberibacter asiaticus (CLas), a pathogenic bacterium causing citrus Huanglongbing, forms a mutualistic relationship with the Asian citrus psyllid, Diaphorina citri. However, the underlying molecular mechanisms remain unclear. We find that CLas enhances the development of testes, ovaries, and mating behavior in D. citri. Transcriptome analysis of ovaries reveals that CLas infection upregulates ATP synthesis genes, increasing ATP levels in D. citri. Silencing the ATPSyn-β gene expression reduces ATP content in the ovary and triglyceride and glycogen content in the fat body, thus decreasing ovarian development, mating, and oviposition. ATPSyn-β localizes to the oocyte cell membrane interacts with vitellogenin (Vg), suggesting that it facilitates Vg entry into ovaries. In conclusion, CLas promotes ovarian development in D. citri by upregulating ATPSyn-β, which supports energy production and nutrient supply. This study provides valuable insights into CLas and may inform novel strategies to control citrus Huanglongbing by reducing D. citri populations.