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4 results on '"cidA"'

1. Paternal transmission of the Wolbachia CidB toxin underlies cytoplasmic incompatibility.

Author

Horard B, Terretaz K, Gosselin-Grenet AS, Sobry H, Sicard M, Landmann F, and Loppin B

Subjects
Animals, Cytoplasm, Cytosol, Drosophila, Male, Culex genetics, Wolbachia genetics
Abstract

Wolbachia are widespread endosymbiotic bacteria that manipulate the reproduction of arthropods through a diversity of cellular mechanisms. In cytoplasmic incompatibility (CI), a sterility syndrome originally discovered in the mosquito Culex pipiens, uninfected eggs fertilized by sperm from infected males are selectively killed during embryo development following the abortive segregation of paternal chromosomes in the zygote. Despite the recent discovery of Wolbachia CI factor (cif) genes, the mechanism by which they control the fate of paternal chromosomes at fertilization remains unknown. Here, we have analyzed the cytological distribution and cellular impact of CidA and CidB, a pair of Cif proteins from the Culex-infecting Wolbachia strain wPip. We show that expression of CidB in Drosophila S2R+ cells induces apoptosis unless CidA is co-expressed and associated with its partner. In transgenic Drosophila testes, both effectors colocalize in germ cells until the histone-to-protamine transition in which only CidB is retained in maturing spermatid nuclei. We further show that CidB is similarly targeted to maturing sperm of naturally infected Culex mosquitoes. At fertilization, CidB associates with paternal DNA regions exhibiting DNA replication stress, as a likely cause of incomplete replication of paternal chromosomes at the onset of the first mitosis. Importantly, we demonstrate that inactivation of the deubiquitylase activity of CidB does not abolish its cell toxicity or its ability to induce CI in Drosophila. Our study thus demonstrates that CI functions as a transgenerational toxin-antidote system and suggests that CidB acts by poisoning paternal DNA replication in incompatible crosses., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2022 Elsevier Inc. All rights reserved.)

Published
2022
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2. Variation in Wolbachia cidB gene, but not cidA, is associated with cytoplasmic incompatibility mod phenotype diversity in Culex pipiens.

Author

Bonneau M, Caputo B, Ligier A, Caparros R, Unal S, Perriat-Sanguinet M, Arnoldi D, Sicard M, and Weill M

Subjects
Animals, Animals, Genetically Modified genetics, Crosses, Genetic, Drosophila melanogaster genetics, Drosophila melanogaster microbiology, Female, Italy, Male, Phenotype, Reproduction genetics, Symbiosis genetics, Culex genetics, Culex microbiology, Cytoplasm genetics, Cytoplasm microbiology, Genes, Bacterial genetics, Wolbachia genetics
Abstract

Endosymbiotic Wolbachia bacteria are, to date, considered the most widespread symbionts in arthropods and are the cornerstone of major biological control strategies. Such a high prevalence is based on the ability of Wolbachia to manipulate their hosts' reproduction. One manipulation called cytoplasmic incompatibility (CI) is based on the death of the embryos generated by crosses between infected males and uninfected females or between individuals infected with incompatible Wolbachia strains. CI can be seen as a modification-rescue system (or mod-resc) in which paternal Wolbachia produce mod factors, inducing embryonic defects, unless the maternal Wolbachia produce compatible resc factors. Transgenic experiments in Drosophila melanogaster and Saccharomyces cerevisiae converged towards a model where the cidB Wolbachia gene is involved in the mod function while cidA is involved in the resc function. However, as cidA expression in Drosophila males was required to observe CI, it has been proposed that cidA could be involved in both resc and mod functions. A recent correlative study in natural Culex pipiens mosquito populations has revealed an association between specific cidA and cidB variations and changes in mod phenotype, also suggesting a role for both these genes in mod diversity. Here, by studying cidA and cidB genomic repertoires of individuals from newly sampled natural C. pipiens populations harbouring wPipIV strains from North Italy, we reinforce the link between cidB variation and mod phenotype variation fostering the involvement of cidB in the mod phenotype diversity. However, no association between any cidA variants or combination of cidA variants and mod phenotype variation was observed. Taken together our results in natural C. pipiens populations do not support the involvement of cidA in mod phenotype variation., (© 2019 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

Published
2019
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3. Paternal transmission of the Wolbachia CidB toxin underlies cytoplasmic incompatibility

Author

Béatrice Horard, Kevin Terretaz, Anne-Sophie Gosselin-Grenet, Hélène Sobry, Mathieu Sicard, Frédéric Landmann, Benjamin Loppin, Laboratoire de biologie et modélisation de la cellule (LBMC UMR 5239), École normale supérieure de Lyon (ENS de Lyon)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Centre de recherche en Biologie cellulaire de Montpellier (CRBM), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université de Montpellier (UM), Institut des Sciences de l'Evolution de Montpellier (UMR ISEM), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut de recherche pour le développement [IRD] : UR226-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), MUSE program of the University of MontpellierAAP17REC-FRS04-GENEWOL, SchlumbergerFSER202002011118, ANR-16-CE02-0006,CIAWOL,Bases moléculaire et cellulaire de la diversité phénotypique de l'incompatibilté cytoplasmique chez les insectes(2016), ANR-10-INBS-0004,France-BioImaging,Développment d'une infrastructure française distribuée coordonnée(2010), École normale supérieure - Lyon (ENS Lyon)-Université Claude Bernard Lyon 1 (UCBL), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École pratique des hautes études (EPHE), KARLI, Mélanie, Bases moléculaire et cellulaire de la diversité phénotypique de l'incompatibilté cytoplasmique chez les insectes - - CIAWOL2016 - ANR-16-CE02-0006 - AAPG2016 - VALID, and Développment d'une infrastructure française distribuée coordonnée - - France-BioImaging2010 - ANR-10-INBS-0004 - INBS - VALID

Subjects
toxin-antidote, Male, Cytoplasm, cytoplasmic incompatibility, [SDV]Life Sciences [q-bio], General Biochemistry, Genetics and Molecular Biology, DNA replication stress, spermiogenesis, [SDV] Life Sciences [q-bio], Culex, Cytosol, fertilization, Animals, Drosophila, General Agricultural and Biological Sciences, CidA, Wolbachia, CidB
Abstract

International audience; Wolbachia are widespread endosymbiotic bacteria that manipulate the reproduction of arthropods through a diversity of cellular mechanisms. In cytoplasmic incompatibility (CI), a sterility syndrome originally discovered in the mosquito Culex pipiens, uninfected eggs fertilized by sperm from infected males are selectively killed during embryo development following the abortive segregation of paternal chromosomes in the zygote. Despite the recent discovery of Wolbachia CI factor (cif) genes, the mechanism by which they control the fate of paternal chromosomes at fertilization remains unknown. Here, we have analyzed the cytological distribution and cellular impact of CidA and CidB, a pair of Cif proteins from the Culex-infecting Wolbachia strain wPip. We show that expression of CidB in Drosophila S2R+ cells induces apoptosis unless CidA is co-expressed and associated with its partner. In transgenic Drosophila testes, both effectors colocalize in germ cells until the histone-to-protamine transition in which only CidB is retained in maturing spermatid nuclei. We further show that CidB is similarly targeted to maturing sperm of naturally infected Culex mosquitoes. At fertilization, CidB associates with paternal DNA regions exhibiting DNA replication stress, as a likely cause of incomplete replication of paternal chromosomes at the onset of the first mitosis. Importantly, we demonstrate that inactivation of the deubiquitylase activity of CidB does not abolish its cell toxicity or its ability to induce CI in Drosophila. Our study thus demonstrates that CI functions as a transgenerational toxin-antidote system and suggests that CidB acts by poisoning paternal DNA replication in incompatible crosses.

Published
2021
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4. Variation in Wolbachia cidB gene, but not cidA, is associated with cytoplasmic incompatibility mod phenotype diversity in Culex pipiens

Author

Aude Ligier, Daniele Arnoldi, Sandra Unal, Rudy Caparros, Marco Perriat-Sanguinet, Beniamino Caputo, Mathieu Sicard, Mylène Weill, Manon Bonneau, Institut des Sciences de l'Evolution de Montpellier (UMR ISEM), École pratique des hautes études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Université de Montpellier (UM)-Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Centre National de la Recherche Scientifique (CNRS)-Institut de recherche pour le développement [IRD] : UR226, Instituto Gulbenkian de Ciência [Oeiras] (IGC), Fundação Calouste Gulbenkian, Institut Pasteur, Fondation Cenci Bolognetti - Istituto Pasteur Italia, Fondazione Cenci Bolognetti, Réseau International des Instituts Pasteur (RIIP), Université de Liège, Centro Ricerca e Innovazione - Research and Innovation Centre [FEM - Italie], Fondazione Edmund Mach - Edmund Mach Foundation [Italie] (FEM), This work was funded by the French ANR (project 'CIAWOL' ANR‐16‐ CE02‐0006‐01)., We would like to thank Bertrand Lelièvre for his help with mosquito sampling and Dr Nicole Pasteur for helpful comments on the manuscript. We thank Fabienne Justy for her help in RNA extraction and Dr Laurent Marivaux for the use of the stereomicroscope funded by PALASIAFRICA ANR/ERC. We also thank Dr Philippe Clair for his help with the real‐time quantitative PCR experiments performed at the technical facility of the qPCR Haut Debit (qPHD) Montpellier génomiX platform. Sequencing data were generated on the GENSEQ platform of the technical facilities of the LabEX Centre Méditerranéen de l'Environnement et de la Biodiversité. The CI status of crosses was determined with help of the CytoEvol facilities of UMR ISEM ‐ CBGP of the LabEx CeMEB., ANR-16-CE02-0006,CIAWOL,Bases moléculaire et cellulaire de la diversité phénotypique de l'incompatibilté cytoplasmique chez les insectes(2016), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE), and Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Université de Montpellier (UM)-Institut de recherche pour le développement [IRD] : UR226-Centre National de la Recherche Scientifique (CNRS)

Subjects
0106 biological sciences, 0301 basic medicine, Male, Cytoplasm, wolbachia, vector control, cytoplasmic incompatibility, aedes, mosquito, diseases, Transgene, Population and Conservation Genetics, cidA, 010603 evolutionary biology, 01 natural sciences, cidB, Animals, Genetically Modified, 03 medical and health sciences, [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], parasitic diseases, Culex pipiens, Genetics, Animals, Symbiosis, Gene, Ecology, Evolution, Behavior and Systematics, Crosses, Genetic, Settore BIO/11 - BIOLOGIA MOLECOLARE, biology, Reproduction, biology.organism_classification, Phenotype, [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology, Culex, 030104 developmental biology, Drosophila melanogaster, Italy, Genes, Bacterial, Wolbachia, Original Article, Female, ORIGINAL ARTICLES, Function (biology), Cytoplasmic incompatibility, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

International audience; Endosymbiotic Wolbachia bacteria are, to date, considered the most widespread symbionts in arthropods and are the cornerstone of major biological control strategies. Such a high prevalence is based on the ability of Wolbachia to manipulate their hosts' reproduction. One manipulation called cytoplasmic incompatibility (CI) is based on the death of the embryos generated by crosses between infected males and uninfected females or between individuals infected with incompatible Wolbachia strains. CI can be seen as a modification-rescue system (or mod-resc) in which paternal Wolbachia produce mod factors, inducing embryonic defects, unless the maternal Wolbachia produce compatible resc factors. Transgenic experiments in Drosophila melanogaster and Saccharomyces cerevisiae converged towards a model where the cidB Wolbachia gene is involved in the mod function while cidA is involved in the resc function. However, as cidA expression in Drosophila males was required to observe CI, it has been proposed that cidA could be involved in both resc and mod functions. A recent correlative study in natural Culex pipiens mosquito populations has revealed an association between specific cidA and cidB variations and changes in mod phenotype, also suggesting a role for both these genes in mod diversity. Here, by studying cidA and cidB genomic repertoires of individuals from newly sampled natural C. pipiens populations harbouring wPipIV strains from North Italy, we reinforce the link between cidB variation and mod phenotype variation fostering the involvement of cidB in the mod phenotype diversity. However, no association between any cidA variants or combination of cidA variants and mod phenotype variation was observed. Taken together our results in natural C. pipiens populations do not support the involvement of cidA in mod phenotype variation.

Published
2019
Full Text
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