Dopamine and its receptor <i>DcDop2</i> are involved in the coevolution between '<i>Candidatus</i> Liberibacter asiaticus' and <i>Diaphorina citri</i>.

Abstract

'<i>Candidatus</i> Liberibacter asiaticus' (<i>C</i>Las), the causal agent of citrus huanglongbing, is transmitted by the Asian citrus psyllid <i>Diaphorina citri</i>. While <i>C</i>Las-positive (<i>C</i>Las+) females exhibit increased fecundity and metabolic demands, their neuroendocrine regulation mechanisms remain unclear. We propose <i>C</i>Las manipulates dopamine (DA) signaling to enhance psyllid fecundity and <i>C</i>Las proliferation. Metabolomics revealed elevated DA in <i>C</i>Las+ females. Silencing DA synthesis genes and receptor <i>DcDop2</i> via RNAi reduced lipid reserves, fecundity, and ovarian <i>C</i>Las titers. Through combined <i>in vivo</i> and <i>in vitro</i> experiments, we demonstrated that the microRNA miR-31a suppresses <i>DcDop2</i> expression by binding to its 3' untranslated region. Overexpression of miR-31a resulted in decreased <i>DcDop2</i> expression and <i>C</i>Las titers in the ovaries, eliciting phenotypic defects akin to <i>DcDop2</i> knockdown. Furthermore, <i>DcDop2</i> knockdown and miR-31a overexpression reduced juvenile hormone (JH) levels and adipokinetic hormone (AKH) signaling in fat bodies and ovaries. Consequently, <i>C</i>Las regulates the DA-<i>DcDop2</i> signaling axis to improve <i>D. citri</i> lipid metabolism and fecundity, while simultaneously promoting its replication. These findings reveal a coevolution between <i>C</i>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.