Dopamine and its receptor DcDop2 are involved in the coevolution between ‘ Candidatus Liberibacter asiaticus’ and Diaphorina citri

‘ Candidatus Liberibacter asiaticus’ (CLas), the causal agent of citrus huanglongbing, is transmitted by the Asian citrus psyllid Diaphorina citri . While C Las-positive ( C Las+) females exhibit increased fecundity and metabolic demands, their neuroendocrine regulation mechanisms remain unclear. We propose C Las manipulates dopamine (DA) signaling to enhance psyllid fecundity and C Las proliferation. Metabolomics revealed elevated DA in C Las+ females. Silencing DA synthesis genes and receptor DcDop2 via RNAi reduced lipid reserves, fecundity, and ovarian C Las titers. Through combined in vivo and in vitro experiments, we demonstrated that the microRNA miR-31a suppresses DcDop2 expression by binding to its 3’ untranslated region. Overexpression of miR-31a resulted in decreased DcDop2 expression and C Las titers in the ovaries, eliciting phenotypic defects akin to DcDop2 knockdown. Furthermore, DcDop2 knockdown and miR-31a overexpression reduced juvenile hormone (JH) levels and adipokinetic hormone (AKH) signaling in fat bodies and ovaries. Consequently, C Las regulates the DA- DcDop2 signaling axis to improve D. citri lipid metabolism and fecundity, while simultaneously promoting its replication. These findings reveal a coevolution between C Las proliferation and ovarian development in the insect host. This discovery enhances our understanding of the molecular interplay between plant pathogens and vector insects and offers novel targets and strategies for HLB field management.