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One prophage WO gene rescues cytoplasmic incompatibility in Drosophila melanogaster

Wolbachia are maternally inherited, intracellular bacteria at the forefront of vector control efforts to curb arbovirus transmission. In international field trials, the cytoplasmic incompatibility (CI) drive system of wMel Wolbachia is deployed to replace target vector populations, whereby a Wolbach...

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Autores principales: Shropshire, J. Dylan, On, Jungmin, Layton, Emily M., Zhou, Helen, Bordenstein, Seth R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5948995/
https://www.ncbi.nlm.nih.gov/pubmed/29686091
http://dx.doi.org/10.1073/pnas.1800650115
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author Shropshire, J. Dylan
On, Jungmin
Layton, Emily M.
Zhou, Helen
Bordenstein, Seth R.
author_facet Shropshire, J. Dylan
On, Jungmin
Layton, Emily M.
Zhou, Helen
Bordenstein, Seth R.
author_sort Shropshire, J. Dylan
collection PubMed
description Wolbachia are maternally inherited, intracellular bacteria at the forefront of vector control efforts to curb arbovirus transmission. In international field trials, the cytoplasmic incompatibility (CI) drive system of wMel Wolbachia is deployed to replace target vector populations, whereby a Wolbachia-induced modification of the sperm genome kills embryos. However, Wolbachia in the embryo rescue the sperm genome impairment, and therefore CI results in a strong fitness advantage for infected females that transmit the bacteria to offspring. The two genes responsible for the wMel-induced sperm modification of CI, cifA and cifB, were recently identified in the eukaryotic association module of prophage WO, but the genetic basis of rescue is unresolved. Here we use transgenic and cytological approaches to demonstrate that maternal cifA expression independently rescues CI and nullifies embryonic death caused by wMel Wolbachia in Drosophila melanogaster. Discovery of cifA as the rescue gene and previously one of two CI induction genes establishes a “Two-by-One” model that underpins the genetic basis of CI. Results highlight the central role of prophage WO in shaping Wolbachia phenotypes that are significant to arthropod evolution and vector control.
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spelling pubmed-59489952018-05-14 One prophage WO gene rescues cytoplasmic incompatibility in Drosophila melanogaster Shropshire, J. Dylan On, Jungmin Layton, Emily M. Zhou, Helen Bordenstein, Seth R. Proc Natl Acad Sci U S A Biological Sciences Wolbachia are maternally inherited, intracellular bacteria at the forefront of vector control efforts to curb arbovirus transmission. In international field trials, the cytoplasmic incompatibility (CI) drive system of wMel Wolbachia is deployed to replace target vector populations, whereby a Wolbachia-induced modification of the sperm genome kills embryos. However, Wolbachia in the embryo rescue the sperm genome impairment, and therefore CI results in a strong fitness advantage for infected females that transmit the bacteria to offspring. The two genes responsible for the wMel-induced sperm modification of CI, cifA and cifB, were recently identified in the eukaryotic association module of prophage WO, but the genetic basis of rescue is unresolved. Here we use transgenic and cytological approaches to demonstrate that maternal cifA expression independently rescues CI and nullifies embryonic death caused by wMel Wolbachia in Drosophila melanogaster. Discovery of cifA as the rescue gene and previously one of two CI induction genes establishes a “Two-by-One” model that underpins the genetic basis of CI. Results highlight the central role of prophage WO in shaping Wolbachia phenotypes that are significant to arthropod evolution and vector control. National Academy of Sciences 2018-05-08 2018-04-23 /pmc/articles/PMC5948995/ /pubmed/29686091 http://dx.doi.org/10.1073/pnas.1800650115 Text en Copyright © 2018 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Shropshire, J. Dylan
On, Jungmin
Layton, Emily M.
Zhou, Helen
Bordenstein, Seth R.
One prophage WO gene rescues cytoplasmic incompatibility in Drosophila melanogaster
title One prophage WO gene rescues cytoplasmic incompatibility in Drosophila melanogaster
title_full One prophage WO gene rescues cytoplasmic incompatibility in Drosophila melanogaster
title_fullStr One prophage WO gene rescues cytoplasmic incompatibility in Drosophila melanogaster
title_full_unstemmed One prophage WO gene rescues cytoplasmic incompatibility in Drosophila melanogaster
title_short One prophage WO gene rescues cytoplasmic incompatibility in Drosophila melanogaster
title_sort one prophage wo gene rescues cytoplasmic incompatibility in drosophila melanogaster
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5948995/
https://www.ncbi.nlm.nih.gov/pubmed/29686091
http://dx.doi.org/10.1073/pnas.1800650115
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