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One prophage WO gene rescues cytoplasmic incompatibility in Drosophila melanogaster

View ORCID ProfileJ. Dylan Shropshire, Jungmin On, Emily M. Layton, Helen Zhou, View ORCID ProfileSeth R. Bordenstein
doi: https://doi.org/10.1101/300269
J. Dylan Shropshire
1Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA
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  • For correspondence: dylan.shropshire@vanderbilt.edu s.bordenstein@vanderbilt.edu
Jungmin On
1Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA
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Emily M. Layton
1Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA
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Helen Zhou
1Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA
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Seth R. Bordenstein
1Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA
2Department of Pathology, Microbiology, and Immunology, Vanderbilt University, Nashville, TN 37235, USA
3Vanderbilt Genetics Institute, Vanderbilt University, Nashville, TN 37235, USA
4Vanderbilt Institute of Infection, Immunology and Inflammation, Vanderbilt University, Nashville, TN 37235, USA
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  • For correspondence: dylan.shropshire@vanderbilt.edu s.bordenstein@vanderbilt.edu
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Abstract

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 cifA 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 new ‘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.

Significance Statement The World Health Organization recommended pilot deployment of Wolbachia-infected mosquitoes to curb viral transmission to humans. Releases of mosquitoes are underway worldwide because Wolbachia can block replication of these pathogenic viruses and deterministically spread by a drive system termed cytoplasmic incompatibility (CI). Despite extensive research, the underlying genetic basis of CI remains only half-solved. We recently reported that two prophage WO genes recapitulate the modification component of CI in a released strain for vector control. Here we show that one of these genes underpins rescue of CI. Together, our results reveal the complete genetic basis of this selfish trait and pave the way for future studies exploring WO prophage genes as adjuncts or alternatives to current control efforts.

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Posted April 13, 2018.
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One prophage WO gene rescues cytoplasmic incompatibility in Drosophila melanogaster
J. Dylan Shropshire, Jungmin On, Emily M. Layton, Helen Zhou, Seth R. Bordenstein
bioRxiv 300269; doi: https://doi.org/10.1101/300269
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One prophage WO gene rescues cytoplasmic incompatibility in Drosophila melanogaster
J. Dylan Shropshire, Jungmin On, Emily M. Layton, Helen Zhou, Seth R. Bordenstein
bioRxiv 300269; doi: https://doi.org/10.1101/300269

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