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

Author:

Li Jiayun,Holford Paul,Beattie George Andrew Charles,Wu Shujie,He Jielan,Tan Shijian,Wang Desen,He Yurong,Cen Yijing,Nian XiaogeORCID

Abstract

AbstractDiaphorina citriis the primary vector of the bacterium, ‘CandidatusLiberibacter asiaticus’ (CLas) associated with the severe Asian form of huanglongbing.CLas-positiveD. citriare more fecund than theirCLas-negative counterparts and require extra energy expenditure. Therefore, understanding the molecular mechanisms linking metabolism and reproduction is of particular importance. In this present study, we found adipokinetic hormone (DcAKH) and its receptor (DcAKHR) were essential for increased lipid metabolism and fecundity in response toCLas infection inD. citri.Knockdown ofDcAKHandDcAKHRnot only resulted in triacylglycerol accumulation and a decline of glycogen, but also significantly decreased fecundity andCLas titer in ovaries. Combinedin vivoandin vitroexperiments showed that miR-34 suppressesDcAKHRexpression by binding to its 3’ untranslated region, whilst overexpression of miR-34 resulted in a decline ofDcAKHRexpression andCLas titer in ovaries and caused defects that mimickedDcAKHRknockdown phenotypes. In addition, knockdown ofDcAKHandDcAKHRsignificantly 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 genesvitellogenin 1-like(DcVg-1-like),vitellogenin A1-like(DcVg-A1-like) and the vitellogenin receptor (DcVgR). As a result,CLas hijacks AKH/AKHR-miR-34-JH signaling to improveD. citrilipid metabolism and fecundity, while simultaneously increasing the replication ofCLas, suggesting a mutualistic interaction inD. citriovaries withCLas.

Publisher

Cold Spring Harbor Laboratory

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