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You are here: Home / Teams / Epigenetics and Zygote Formation - B. Loppin / Publications / Paternal transmission of the Wolbachia CidB toxin underlies cytoplasmic incompatibility.

Paternal transmission of the Wolbachia CidB toxin underlies cytoplasmic incompatibility.

Béatrice Horard, Kevin Terretaz, Anne-Sophie Gosselin-Grenet, Hélène Sobry, Mathieu Sicard, Frédéric Landmann, and Benjamin Loppin (2022)

Curr Biol, 32:1319-1331.

Wolbachia are widespread endosymbiotic bacteria that manipulate the reproduction ofarthropods through a diversity of cellular mechanisms. In cytoplasmicincompatibility (CI), a sterility syndrome originally discovered in the mosquitoCulex pipiens, uninfected eggs fertilized by sperm from infected males areselectively killed during embryo development following the abortive segregation ofpaternal chromosomes in the zygote. Despite the recent discovery of Wolbachia CIfactor (cif) genes, the mechanism by which they control the fate of paternalchromosomes at fertilization remains unknown. Here, we have analyzed the cytologicaldistribution and cellular impact of CidA and CidB, a pair of Cif proteins from theCulex-infecting Wolbachia strain wPip. We show that expression of CidB in DrosophilaS2R+ cells induces apoptosis unless CidA is co-expressed and associated with itspartner. In transgenic Drosophila testes, both effectors colocalize in germ cellsuntil the histone-to-protamine transition in which only CidB is retained in maturingspermatid nuclei. We further show that CidB is similarly targeted to maturing spermof naturally infected Culex mosquitoes. At fertilization, CidB associates withpaternal DNA regions exhibiting DNA replication stress, as a likely cause ofincomplete replication of paternal chromosomes at the onset of the first mitosis.Importantly, we demonstrate that inactivation of the deubiquitylase activity of CidBdoes not abolish its cell toxicity or its ability to induce CI in Drosophila. Ourstudy thus demonstrates that CI functions as a transgenerational toxin-antidotesystem and suggests that CidB acts by poisoning paternal DNA replication inincompatible crosses.

intergenerational epigentics, Germline, Wolbachia, germline
automatic medline import

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