The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage

Shaffer, H. Bradley, Minx, Patrick, Warren, Daniel E., Shedlock, Andrew M., Thomson, Robert C., Valenzuela, Nicole, Abramyan, John, Amemiya, Chris T., Badenhorst, Daleen, Biggar, Kyle K., Borchert, Glen M., Botka, Christopher W., Bowden, Rachel M., Braun, Edward L., Bronikowski, Anne M., Bruneau, Benoit G., Buck, Leslie T., Capel, Blanche, Castoe, Todd A., Czerwinski, Mike, Delehaunty, Kim D., Edwards, Scott V., Fronick, Catrina C., Fujita, Matthew K., Fulton, Lucinda, Graves, Tina A., Green, Richard E., Haerty, Wilfried ORCID: https://orcid.org/0000-0003-0111-191X, Hariharan, Ramkumar, Hernandez, Omar, Hillier, La Deana W., Holloway, Alisha K., Janes, Daniel, Janzen, Fredric J., Kandoth, Cyriac, Kong, Lesheng, de Koning, A. P.Jason, Li, Yang, Literman, Robert, McGaugh, Suzanne E., Mork, Lindsey, O'Laughlin, Michelle, Paitz, Ryan T., Pollock, David D., Ponting, Chris P., Radhakrishnan, Srihari, Raney, Brian J., Richman, Joy M., St John, John, Schwartz, Tonia, Sethuraman, Arun, Spinks, Phillip Q., Storey, Kenneth B., Thane, Nay, Vinar, Tomas, Zimmerman, Laura M., Warren, Wesley C., Mardis, Elaine R. and Wilson, Richard K. (2013) The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biology, 14 (3). ISSN 1474-760X

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Abstract

Background: We describe the genome of the western painted turtle, Chrysemys picta bellii, one of the most widespread, abundant, and well-studied turtles. We place the genome into a comparative evolutionary context, and focus on genomic features associated with tooth loss, immune function, longevity, sex differentiation and determination, and the species' physiological capacities to withstand extreme anoxia and tissue freezing.Results: Our phylogenetic analyses confirm that turtles are the sister group to living archosaurs, and demonstrate an extraordinarily slow rate of sequence evolution in the painted turtle. The ability of the painted turtle to withstand complete anoxia and partial freezing appears to be associated with common vertebrate gene networks, and we identify candidate genes for future functional analyses. Tooth loss shares a common pattern of pseudogenization and degradation of tooth-specific genes with birds, although the rate of accumulation of mutations is much slower in the painted turtle. Genes associated with sex differentiation generally reflect phylogeny rather than convergence in sex determination functionality. Among gene families that demonstrate exceptional expansions or show signatures of strong natural selection, immune function and musculoskeletal patterning genes are consistently over-represented.Conclusions: Our comparative genomic analyses indicate that common vertebrate regulatory networks, some of which have analogs in human diseases, are often involved in the western painted turtle's extraordinary physiological capacities. As these regulatory pathways are analyzed at the functional level, the painted turtle may offer important insights into the management of a number of human health disorders.

Item Type: Article
Additional Information: Funding Information: The sequencing of the western painted turtle genome was funded by the National Human Genome Research Institute (NHGRI). Further research support included grants to HBS (NSF DEB 0817042), NV (NSF IOS 0743284), NV & SVE (MCB 0815354), FJJ and AS (NSF DEB 0640932), KBS and LTB (NSERC), TV (FP7 IRG-224885, VEGA 1/1085/12), and SVE, CTA, and JRM (NSF IOS 0207870/0431717). Resources for exploring the sequence and annotation data are available on browser displays available at UCSC [118], Ensembl [119], NCBI [120], and MRC [105]. We thank Andrew Severin (Iowa State Genome Informatics Facility) for help with data analyses, Erik Larson (Illinois State) for contributing Glen Borchert’s time to the project, The Genome Institute members and Michael Montague for manuscript review, Louise Whitaker (UCLA) for bibliographic assistance, and Bronwen Aken (Wellcome Trust Sanger Institute) for displaying the genome annotation on ENSEMBL. During the development of this project we received input from Naoki Irie (RIKEN) and Guojie Zhang (BGI). We also thank the following members of The Genome Institute: Michael Montague for manuscript review, Chad Tomlinson for assembling cDNAs, Bob Fulton and Aye Wollam for finishing BACs used in assembly quality assessment.
Uncontrolled Keywords: amniote phylogeny,anoxia tolerance,chelonian,evolutionary rates,freeze tolerance,genomics,longevity,phylogenomics,physiology,turtle,ecology, evolution, behavior and systematics,genetics,cell biology,sdg 3 - good health and well-being ,/dk/atira/pure/subjectarea/asjc/1100/1105
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 15 Sep 2022 14:30
Last Modified: 26 Sep 2022 14:30
URI: https://ueaeprints.uea.ac.uk/id/eprint/88330
DOI: 10.1186/gb-2013-14-3-r28

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