The Endosymbiotic Bacterium Wolbachia Selectively Kills Male Hosts by Targeting the Masculinizing Gene

• Published in: PLoS pathogens 2015-07, Vol.11 (7), p.e1005048-e1005048
• Main Authors: Fukui, Takahiro, Kawamoto, Munetaka, Shoji, Keisuke, Kiuchi, Takashi, Sugano, Sumio, Shimada, Toru, Suzuki, Yutaka, Katsuma, Susumu
• Format: Article
• Language: English
• Subjects: Animals; Butterflies & moths; Chromosomes; Compensation; Experiments; Female; Females; Genes; Genetic engineering; Male; Molecular Sequence Data; Moths - genetics; Moths - parasitology; Phylogenetics; Phylogeny; Proteins; Reverse Transcriptase Polymerase Chain Reaction; Transfection; Wolbachia; Zinc Fingers - genetics
• ISSN: 1553-7374; 1553-7366; 1553-7374
• DOI: 10.1371/journal.ppat.1005048

Pathogens are known to manipulate the reproduction and development of their hosts for their own benefit. Wolbachia is an endosymbiotic bacterium that infects a wide range of insect species. Wolbachia is known as an example of a parasite that manipulates the sex of its host's progeny. Infection of Ostrinia moths by Wolbachia causes the production of all-female progeny, however, the mechanism of how Wolbachia accomplishes this male-specific killing is unknown. Here we show for the first time that Wolbachia targets the host masculinizing gene of Ostrinia to accomplish male-killing. We found that Wolbachia-infected O. furnacalis embryos do not express the male-specific splice variant of doublesex, a gene which acts at the downstream end of the sex differentiation cascade, throughout embryonic development. Transcriptome analysis revealed that Wolbachia infection markedly reduces the mRNA level of Masc, a gene that encodes a protein required for both masculinization and dosage compensation in the silkworm Bombyx mori. Detailed bioinformatic analysis also elucidated that dosage compensation of Z-linked genes fails in Wolbachia-infected O. furnacalis embryos, a phenomenon that is extremely similar to that observed in Masc mRNA-depleted male embryos of B. mori. Finally, injection of in vitro transcribed Masc cRNA into Wolbachia-infected embryos rescued male progeny. Our results show that Wolbachia-induced male-killing is caused by a failure of dosage compensation via repression of the host masculinizing gene. Our study also shows a novel strategy by which a pathogen hijacks the host sex determination cascade.