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Independent innexin radiation shaped signaling in ctenophores

Jennifer Ortiz, View ORCID ProfileYuriy V. Bobkov, View ORCID ProfileMelissa B. DeBiasse, View ORCID ProfileDorothy G Mitchell, View ORCID ProfileAllison Edgar, View ORCID ProfileMark Q. Martindale, View ORCID ProfileAnthony G. Moss, View ORCID ProfileLeslie S. Babonis, View ORCID ProfileJoseph F. Ryan
doi: https://doi.org/10.1101/2022.10.11.511657
Jennifer Ortiz
1Whitney Laboratory for Marine Bioscience, University of Florida, St Augustine, FL 32080, USA
2Department of Biology, University of Washington, Seattle, WA 98105, USA
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Yuriy V. Bobkov
1Whitney Laboratory for Marine Bioscience, University of Florida, St Augustine, FL 32080, USA
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Melissa B. DeBiasse
1Whitney Laboratory for Marine Bioscience, University of Florida, St Augustine, FL 32080, USA
3School of Natural Sciences, University of California Merced, Merced CA 95343, USA
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Dorothy G Mitchell
1Whitney Laboratory for Marine Bioscience, University of Florida, St Augustine, FL 32080, USA
4Department of Biology, University of Florida, Gainesville, FL 32611, USA
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Allison Edgar
1Whitney Laboratory for Marine Bioscience, University of Florida, St Augustine, FL 32080, USA
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Mark Q. Martindale
1Whitney Laboratory for Marine Bioscience, University of Florida, St Augustine, FL 32080, USA
4Department of Biology, University of Florida, Gainesville, FL 32611, USA
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Anthony G. Moss
5Biological Sciences Department, Auburn University, AL 36849, USA
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Leslie S. Babonis
1Whitney Laboratory for Marine Bioscience, University of Florida, St Augustine, FL 32080, USA
6Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853, USA
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Joseph F. Ryan
1Whitney Laboratory for Marine Bioscience, University of Florida, St Augustine, FL 32080, USA
4Department of Biology, University of Florida, Gainesville, FL 32611, USA
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  • For correspondence: joseph.ryan@whitney.ufl.edu
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ABSTRACT

Innexins facilitate cell-cell communication by forming gap junctions or non-junctional hemichannels, which play important roles in metabolic, chemical, ionic, and electrical coupling. The lack of knowledge regarding the evolution and role of these channels in ctenophores (comb jellies), the likely sister group to the rest of animals, represents a substantial gap in our understanding of the evolution of intercellular communication in animals. Here we identify and phylogenetically characterize the complete set of innexins of four ctenophores: Mnemiopsis leidyi, Hormiphora californensis, Pleurobrachia bachei, and Beroe ovata. Our phylogenetic analyses suggest that ctenophore innexins diversified independently from those of other animals and were established early in the emergence of ctenophores. We identified a four-innexin genomic cluster, which was present in the last common ancestor of these four species and has been largely maintained in these lineages. Evidence from correlated spatial and temporal gene expression of the M. leidyi innexin cluster suggest that this cluster has been maintained due to constraints related to gene regulation. We describe basic electrophysiological properties of putative ctenophore hemichannels from muscle cells using intracellular recording techniques, showing substantial overlap with the properties of bilaterian innexin channels. Together, our results suggest that the last common ancestor of animals had gap junctional channels also capable of forming functional innexin hemichannels, and that innexin genes have independently evolved in major lineages throughout Metazoa.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted October 14, 2022.
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Independent innexin radiation shaped signaling in ctenophores
Jennifer Ortiz, Yuriy V. Bobkov, Melissa B. DeBiasse, Dorothy G Mitchell, Allison Edgar, Mark Q. Martindale, Anthony G. Moss, Leslie S. Babonis, Joseph F. Ryan
bioRxiv 2022.10.11.511657; doi: https://doi.org/10.1101/2022.10.11.511657
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Independent innexin radiation shaped signaling in ctenophores
Jennifer Ortiz, Yuriy V. Bobkov, Melissa B. DeBiasse, Dorothy G Mitchell, Allison Edgar, Mark Q. Martindale, Anthony G. Moss, Leslie S. Babonis, Joseph F. Ryan
bioRxiv 2022.10.11.511657; doi: https://doi.org/10.1101/2022.10.11.511657

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