Zhang, Songdou

AbstractThe severe Asiatic form of huanglongbing (HLB), caused by “Candidatus Liberibacter asiaticus” (CLas), threatens global citrus production via the citrus psyllid, Diaphorina citri. Culturing challenges of CLas necessitate reducing D. citri populations for disease management. CLas boosts the fecundity of CLas‐positive (CLas+) D. citri and fosters its own proliferation by modulating the insect host's juvenile hormone (JH), but the intricate endocrine regulatory mechanisms remain elusive. Here, it is reported that the D. citri ecdysis‐triggering hormone (DcETH) and its receptor DcETHR play pivotal roles in the reciprocal benefits between CLas and D. citri within the ovaries, influencing energy metabolism and reproductive development in host insects; miR‐210, negatively regulates DcETHR expression, contributing to this symbiotic interaction. CLas infection reduces 20‐hydroxyecdysone (20E) levels and stimulates DcETH release, elevating JH production via DcETHR, enhancing fecundity and CLas proliferation. Furthermore, circulating JH levels suppress 20E production in CLas+ ovaries. Collectively, the orchestrated functional interplay involving 20E, ETH, and JH increases energy metabolism and promotes the fecundity of CLas+ D. citri and CLas proliferation. These insights not only broaden the knowledge of how plant pathogens manipulate the reproductive behavior of insect hosts but also offer novel targets and strategies for combatting HLB and D. citri.

AbstractThe evolution of insect vector‐pathogen relationships has long been of interest in the field of molecular ecology. One system of special relevance, due to its economic impacts, is that between Diaphorina citri and ‘Candidatus Liberibacter asiaticus’ (CLas), the cause of the severe Asian form of huanglongbing. CLas‐positive D. citri are more fecund than their CLas‐negative counterparts, boosting opportunities for pathogens to acquire new vector hosts. The molecular mechanism behind this life‐history shift remains unclear. Here, we found that CLas promoted ovarian development and increased the expression of the vitellogenin receptor (DcVgR) in ovaries. DcVgR RNAi significantly decreased fecundity and CLas titer in ovaries, extended the preoviposition period, shortened the oviposition period and blocked ovarian development. Given their importance in gene regulation, we explored the role of miRNAs in shaping these phenotypes and their molecular triggers. Our results showed that one miRNA, miR‐275, suppressed DcVgR expression by binding to its 3' UTR. Overexpression of miR‐275 knocked down DcVgR expression and CLas titer in ovaries, causing reproductive defects that mimicked DcVgR knockdown phenotypes. We focused, further, on roles of the Juvenile Hormone (JH) pathway in shaping the observed fecundity phenotype, given its known impacts on ovarian development. After CLas infection, this pathway was upregulated, thereby increasing DcVgR expression. From these combined results, we conclude that CLas hijacks the JH signalling pathway and miR‐275, thereby targeting DcVgR to increase D. citri fecundity. These changes simultaneously increase CLas replication, suggesting a pathogen‐vector host mutualism, or a seemingly helpful, but cryptically costly life‐history manipulation.