Adipokinetic hormone signaling mediates the enhanced fecundity of Diaphorina citri infected by ‘Candidatus Liberibacter asiaticus’
Jiayun Li,
Paul Holford,
George Andrew Charles Beattie,
Shujie Wu,
Jielan He,
Shijian Tan,
Desen Wang,
Yurong He,
Yijing Cen,
Xiaoge Nian
Affiliations
Jiayun Li
National Key Laboratory of Green Pesticide, Department of Entomology, College of Plant Protection, South China Agricultural University, Guangzhou, China
Paul Holford
School of Science, Western Sydney University, Penrith, Australia
George Andrew Charles Beattie
School of Science, Western Sydney University, Penrith, Australia
Shujie Wu
National Key Laboratory of Green Pesticide, Department of Entomology, College of Plant Protection, South China Agricultural University, Guangzhou, China
Jielan He
National Key Laboratory of Green Pesticide, Department of Entomology, College of Plant Protection, South China Agricultural University, Guangzhou, China
Shijian Tan
National Key Laboratory of Green Pesticide, Department of Entomology, College of Plant Protection, South China Agricultural University, Guangzhou, China
Desen Wang
National Key Laboratory of Green Pesticide, Department of Entomology, College of Plant Protection, South China Agricultural University, Guangzhou, China
Yurong He
National Key Laboratory of Green Pesticide, Department of Entomology, College of Plant Protection, South China Agricultural University, Guangzhou, China
Yijing Cen
National Key Laboratory of Green Pesticide, Department of Entomology, College of Plant Protection, South China Agricultural University, Guangzhou, China
National Key Laboratory of Green Pesticide, Department of Entomology, College of Plant Protection, South China Agricultural University, Guangzhou, China; Henry Fok School of Biology and Agriculture, Shaoguan University, Shaoguan, China
Diaphorina citri serves as the primary vector for ‘Candidatus Liberibacter asiaticus (CLas),’ the bacterium associated with the severe Asian form of huanglongbing. CLas-positive D. citri are more fecund than their CLas-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 CLas 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 CLas 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 CLas 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, CLas hijacks AKH/AKHR-miR-34-JH signaling to improve D. citri lipid metabolism and fecundity, while simultaneously increasing the replication of CLas, suggesting a mutualistic interaction between CLas and D. citri ovaries.
