Wolbachia-induced paternal defect in Drosophila is likely by interaction with the juvenile hormone pathway.
Wolbachia are endosymbionts that infect many insect species. They can manipulate the host's reproduction to increase their own maternal transmission. Cytoplasmic incompatibility (CI) is one such manipulation, which is expressed as embryonic lethality when Wolbachia-infected males mate with uninfected females. However, matings between males and females carrying the same Wolbachia strain result in viable progeny. The molecular mechanisms of CI are currently not clear. We have previously reported that the gene Juvenile hormone-inducible protein 26 (JhI-26) exhibited the highest upregulation in the 3rd instar larval testes of Drosophila melanogaster when infected by Wolbachia. This is reminiscent of an interaction between Wolbachia and juvenile hormone (JH) pathway in flies. Considering that Jhamt gene encodes JH acid methyltransferase, a key regulatory enzyme of JH biosynthesis, and that methoprene-tolerant (Met) has been regarded as the best JH receptor candidate, we first compared the expression of Jhamt and Met between Wolbachia-infected and uninfected fly testes to investigate whether Wolbachia infection influence the JH signaling pathway. We found that the expressions of Jhamt and Met were significantly increased in the presence of Wolbachia, suggesting an interaction of Wolbachia with the JH signaling pathway. Then, we found that overexpression of JhI-26 in Wolbachia-free transgenic male flies caused paternal-effect lethality that mimics the defects associated with CI. JhI-26 overexpressing males resulted in significantly decrease in hatch rate. Surprisingly, Wolbachia-infected females could rescue the egg hatch. In addition, we showed that overexpression of JhI-26 caused upregulation of the male accessory gland protein (Acp) gene CG10433, but not vice versa. This result suggests that JhI-26 may function at the upstream of CG10433. Likewise, overexpression of CG10433 also resulted in paternal-effect lethality. Both JhI-26 and CG10433 overexpressing males resulted in nuclear division defects in the early embryos. Finally, we found that Wolbachia-infected males decreased the propensity of the mated females to remating, a phenotype also caused by both JhI-26 and CG10433 overexpressing males. Taken together, our results provide a working hypothesis whereby Wolbachia induce paternal defects in Drosophila probably by interaction with the JH pathway via JH response genes JhI-26 and CG10433.
Hubei Key Laboratory of Genetic Regulation and Integrative Biology, College of Life Science, Central China Normal University, Wuhan 430079, PR China.
Chen
C
Liu
Hubei Key Laboratory of Genetic Regulation and Integrative Biology, College of Life Science, Central China Normal University, Wuhan 430079, PR China.
Jia-Lin
JL
Wang
Hubei Key Laboratory of Genetic Regulation and Integrative Biology, College of Life Science, Central China Normal University, Wuhan 430079, PR China.
Ya
Y
Zheng
Hubei Key Laboratory of Genetic Regulation and Integrative Biology, College of Life Science, Central China Normal University, Wuhan 430079, PR China.
En-Juan
EJ
Xiong
Hubei Key Laboratory of Genetic Regulation and Integrative Biology, College of Life Science, Central China Normal University, Wuhan 430079, PR China.
Jing-Jing
JJ
Li
Hubei Key Laboratory of Genetic Regulation and Integrative Biology, College of Life Science, Central China Normal University, Wuhan 430079, PR China.
Lin-Ling
LL
Yuan
Hubei Key Laboratory of Genetic Regulation and Integrative Biology, College of Life Science, Central China Normal University, Wuhan 430079, PR China; School of Biological Sciences, University of Missouri-Kansas City, MO 64110, USA.
Xiao-Qiang
XQ
Yu
Hubei Key Laboratory of Genetic Regulation and Integrative Biology, College of Life Science, Central China Normal University, Wuhan 430079, PR China. Electronic address: yfengw@mail.ccnu.edu.cn.
Yu-Feng
YF
Wang
D000818:Animals; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D004331:Drosophila melanogaster / Q000196:embryology / Q000235:genetics* / Q000378:metabolism / Q000382:microbiology*; D005260:Female; D007605:Juvenile Hormones / Q000378:metabolism*; D008297:Male; D010063:Ovum / Q000378:metabolism / Q000382:microbiology; D015398:Signal Transduction; D013045:Species Specificity; D013737:Testis / Q000378:metabolism / Q000382:microbiology; D020577:Wolbachia / Q000502:physiology*
C000593727:CG10433 protein, Drosophila; D029721:Drosophila Proteins; C000593726:JhI-26 protein, Drosophila; D007605:Juvenile Hormones
CG10433; Drosophila melanogaster; JhI-26; Juvenile hormone; Paternal defects; Wolbachia