Infection with ‘Candidatus Liberibacter asiaticus’ improves the fecundity of Diaphorina citri aiding its proliferation: A win‐win strategy

Abstract

The 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.

Adipokinetic hormone signaling mediates the enhanced fecundity of Diaphorina citri infected by ‘Candidatus Liberibacter asiaticus’

“…Although there is limited research on the mechanisms underlying vector-bacteria interactions. In D. citri-C Las interaction, C Las operates host hormone signaling and miRNA to mediate the mutualistic interaction between D. citri fecundity and its replication ( Nian et al, 2024 ). Singh and Linksvayer, 2020 found that Wolbachia -infected colonies of Monomorium pharaonis exhibited increased colony-level growth, accelerated colony reproduction, and shortened colony life cycles compared to uninfected colonies.…”

“…miRNAs play important roles in regulating cellular events at the post-transcriptional level during biological processes ( Bartel, 2018 ; Asgari, 2011 ; Asgari, 2014 ). For example, in D. citri-C Las interaction, C Las hijacks the JH signaling pathway and host miR-275 that targets the vitellogenin receptor ( DcVgR ) to improve D. citri fecundity, while simultaneously increasing the replication of C Las itself, suggesting a mutualistic interaction in D. citri ovaries with C Las ( Nian et al, 2024 ). In term of host-virus interactions, miR-8, and miR-429 target Broad isoform Z2 , the gene involved in the hormonal regulation of single nucleopolyhedrovirus (HaSNPV)-mediated climbing behavior in Helicoverpa armigera ( Zhang et al, 2018 ).…”

Adipokinetic hormone signaling mediates the enhanced fecundity ofDiaphorina citriinfected by ‘CandidatusLiberibacter asiaticus’

“…Although there is limited research on the mechanisms underlying vector-bacteria interactions. In D. citri - C Las interaction, C Las operates host hormone signaling and miRNA to mediate the mutualistic interactio between D. citri fecundity and its replication [35]. Singh and Linksvayer (2020) [41] found that Wolbachia -infected colonies of Monomorium pharaonis exhibited increased colony-level growth, accelerated colony reproduction, and shortened colony life cycles compared to uninfected colonies.…”

“…miRNAs play important roles in regulating cellular events at the post-transcriptional level during biological processes [32,33,34]. For example, in D. citri - C Las interaction, C Las hijacks the JH signaling pathway and host miR-275 that targets the vitellogenin receptor ( DcVgR ) to improve D. citri fecundity, while simultaneously increasing the replication of C Las itself, suggesting a mutualistic interaction in D. citri ovaries with C Las [35]. In term of host-virus interactions, miR-8 and miR-429 target Broad isoform Z2 , the gene involved in the hormonal regulation of single nucleopolyhedrovirus (HaSNPV)-mediated climbing behavior in Helicoverpa armigera [36].…”