Infection with 'Candidatus Liberibacter asiaticus' improves the fecundity of Diaphorina citri aiding its proliferation: a win-win strategy
<p>The coevolution between insect vectors and pathogens has long been of interest in molecular ecology and evolutionary biology, and <em>Diaphorina citri</em> is the main insect vector of the bacterium, ‘<em>Candidatus</em> Liberibacter asiaticus’ (<em>C</em>Las), the putative cause of the severe Asian form of huanglongbing. <em>C</em>Las-positive <em>D. citri</em> are more fecund than their <em>C</em>Las-negative counterparts; however, the molecular mechanism underlying of increased fecundity remains unclear. Here, we found that <em>C</em>Las promoted ovarian development and increased the expression of the <em>vitellogenin</em> <em>receptor</em> (<em>Dc</em><em>VgR</em>) in ovaries. <em>Dc</em><em>VgR</em> RNAi significantly decreased fecundity and <em>C</em>Las titer in ovaries, extended the preoviposition period, shortened the oviposition period, and blocked ovarian development. Combined <em>in vivo</em> and <em>in vitro</em> experiments showed that miR-275 suppressed <em>Dc</em><em>VgR</em> expression by binding to its 3’ untranslated region. Overexpression of miR-275 resulted in a decline of <em>Dc</em><em>VgR</em> expression and <em>C</em>Las titer in ovaries and caused reproductive defects that mimicked <em>Dc</em><em>VgR</em> knockdown phenotypes. After infection with <em>C</em>Las, the juvenile hormone (JH) signaling pathway was upregulated thereby increasing <em>Dc</em><em>VgR</em> expression via the JH receptor, <em>methoprene-tolerant</em> (Met), and downstream key transcription factor <em>Krüppel homolog 1</em>. As a result, <em>C</em>Las hijacks the JH signaling pathway and host miR-275 that targets <em>Dc</em><em>VgR</em> to improve <em>D. citri</em> fecundity, while simultaneously increasing the replication of <em>C</em>Las itself, suggesting a mutualistic interaction in <em>D. citri </em>ovaries with <em>C</em>Las.</p>
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