Diaphorina citri
serves as the primary vector for ‘
Candidatus
Liberibacter asiaticus’ (
C
Las), the bacterium associated with the severe Asian form of huanglongbing.
C
Las-positive
D. citri
are more fecund than their
C
Las-negative counterparts and require extra energy expenditure. Therefore, understanding the molecular mechanisms linking metabolism and reproduction is of particular importance. In this study, we found adipokinetic hormone (
DcAKH
) and its receptor (
DcAKHR
) were essential for increasing lipid metabolism and fecundity in response to
C
Las infection in
D. citri.
Knockdown of
DcAKH
and
DcAKHR
not only resulted in the accumulation of triacylglycerol and a decline of glycogen, but also significantly decreased fecundity and
C
Las titer in ovaries. Combined
in vivo
and
in vitro
experiments showed that miR-34 suppresses
DcAKHR
expression by binding to its 3’ untranslated region, whilst overexpression of miR-34 resulted in a decline of
DcAKHR
expression and
C
Las titer in ovaries and caused defects that mimicked
DcAKHR
knockdown phenotypes. Additionally, knockdown of
DcAKH
and
DcAKHR
significantly reduced juvenile hormone (JH) titer and JH signaling pathway genes in fat bodies and ovaries, including the JH receptor,
methoprene-tolerant
(
DcMet
), and the transcription factor,
Krüppel homolog 1 (DcKr-h1)
, that acts downstream of it, as well as the egg development related genes
vitellogenin 1-like
(
DcVg-1-like
),
vitellogenin A1-like
(
DcVg-A1-like
) and the vitellogenin receptor (
DcVgR
). As a result,
C
Las hijacks AKH/AKHR-miR-34-JH signaling to improve
D. citri
lipid metabolism and fecundity, while simultaneously increasing the replication of
C
Las, suggesting a mutualistic interaction between
C
Las and
D. citri
ovaries.