Abstract
Background Wolbachia are obligate endosymbiotic bacteria that infect numerous species of arthropods and nematodes. Wolbachia can induce several reproductive phenotypes in their insect hosts including feminization, male-killing, parthenogenesis and cytoplasmic incompatibility (CI). CI is the most common phenotype and occurs when Wolbachia-infected males mate with uninfected females resulting in no or very low numbers of viable offspring. However, matings between males and females infected with the same strain of Wolbachia result in viable progeny. Despite substantial scientific effort, the molecular mechanisms underlying CI are currently unknown.Methodology/Principal FindingsGene expression studies were undertaken in Drosophila melanogaster and D. simulans which display differential levels of CI using quantitative RT-PCR. We show that Hira expression is correlated with the induction of CI and occurs in a sex-specific manner. Hira expression is significantly lower in males which induce strong CI when compared to males inducing no CI or Wolbachia-uninfected males. A reduction in Hira expression is also observed in 1-day-old males that induce stronger CI compared to 5-day-old males that induce weak or no CI. In addition, Hira mutated D. melanogaster males mated to uninfected females result in significantly decreased hatch rates comparing with uninfected crosses. Interestingly, wMel-infected females may rescue the hatch rates. An obvious CI phenotype with chromatin bridges are observed in the early embryo resulting from Hira mutant fertilization, which strongly mimics the defects associated with CI.Conclusions/SignificanceOur results suggest Wolbachia-induced CI in Drosophila occurs due to a reduction in Hira expression in Wolbachia-infected males leading to detrimental effects on sperm fertility resulting in embryo lethality. These results may help determine the underlying mechanism of CI and provide further insight in to the important role Hira plays in the interaction of Wolbachia and its insect host.
Highlights
Wolbachia are endosymbiotic bacteria that infect many species of arthropods and filarial nematode [1,2]
To determine whether Hira expression is involved in cytoplasmic incompatibility (CI) level in D. melanogaster males, a quantitative reverse transcriptase (RT)-PCR assay was performed on 1-day-old male flies
In order to determine if the correlation between CI level and Hira expression occurs in additional combinations of Wolbachia and their hosts, we examined Hira expression in D. simulans infected with Drosophila simulans infected with wRi (wRi) and Drosophila simulans infected with wAu (wAu)
Summary
Wolbachia are endosymbiotic bacteria that infect many species of arthropods and filarial nematode [1,2]. The molecular mechanism of CI has not been elucidated, several studies suggest that sperm is modified by Wolbachia during spermatogenesis This modification prevents the paternal chromosomes from entering the anaphase of the first division, leading to a defect in embryogenesis except that the same Wolbachia strain is present in the egg and rescue of CI occurs resulting in hatched embryos [3,4,5]. In the parasitic wasp Nasonia vitripennis, Wolbachia are found only in around 28% of developing sperm, but induce almost complete CI with nearly 100% embryo mortality [7,8] This is probably because Wolbachia may produce an unknown diffusible CIinducing factor that can spread from infected to uninfected cells throughout the testis [7]. The molecular mechanisms underlying CI are currently unknown
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