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Research Article
Development-specific transcriptomic profiling suggests new mechanisms for anoxic survival in the ventricle of overwintering turtles
Cornelia E. Fanter, Zhenguo Lin, Sarah W. Keenan, Fredric J. Janzen, Timothy S. Mitchell, Daniel E. Warren
Journal of Experimental Biology 2020 223: jeb213918 doi: 10.1242/jeb.213918 Published 17 February 2020
Cornelia E. Fanter
1Saint Louis University, Department of Biology, 3507 Laclede Avenue, St Louis, MO 63103, USA
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Zhenguo Lin
1Saint Louis University, Department of Biology, 3507 Laclede Avenue, St Louis, MO 63103, USA
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  • ORCID record for Zhenguo Lin
Sarah W. Keenan
2South Dakota School of Mines & Technology, Department of Geology and Geological Engineering, 501 East St Joseph Street, Rapid City, SD 57701, USA
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Fredric J. Janzen
3Iowa State University, Department of Ecology, Evolution and Organismal Biology, 251 Bessey Hall, Ames, IA 50011, USA
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Timothy S. Mitchell
4University of Minnesota, Department of Ecology, Evolution and Behavior, 1479 Gortner Avenue, Saint Paul, MN 55108, USA
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Daniel E. Warren
1Saint Louis University, Department of Biology, 3507 Laclede Avenue, St Louis, MO 63103, USA
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  • For correspondence: Daniel.Warren@slu.edu
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ABSTRACT

Oxygen deprivation swiftly damages tissues in most animals, yet some species show remarkable abilities to tolerate little or even no oxygen. Painted turtles exhibit a development-dependent tolerance that allows adults to survive anoxia approximately four times longer than hatchlings: adults survive ∼170 days and hatchlings survive ∼40 days at 3°C. We hypothesized that this difference is related to development-dependent differences in ventricular gene expression. Using a comparative ontogenetic approach, we examined whole transcriptomic changes before, during and 5 days after a 20-day bout of anoxic submergence at 3°C. Ontogeny accounted for more gene expression differences than treatment (anoxia or recovery): 1175 versus 237 genes, respectively. Of the 237 differences, 93 could confer protection against anoxia and reperfusion injury, 68 could be injurious and 20 may be constitutively protective. Most striking during anoxia was the main expression pattern of all 76 annotated ribosomal protein (R-protein) mRNAs, which decreased in anoxia-tolerant adults, but increased in anoxia-sensitive hatchlings, suggesting adult-specific regulation of translational suppression. These genes, along with 60 others that decreased their levels in adults and either increased or remained unchanged in hatchlings, implicate antagonistic pleiotropy as a mechanism to resolve the long-standing question about why hatchling painted turtles overwinter in terrestrial nests, rather than emerge and overwinter in water during their first year. In summary, developmental differences in the transcriptome of the turtle ventricle revealed potentially protective mechanisms that contribute to extraordinary adult-specific anoxia tolerance, and provide a unique perspective on differences between the anoxia-induced molecular responses of anoxia-tolerant and anoxia-sensitive phenotypes within a species.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: D.E.W.; Methodology: C.E.F., Z.L., D.E.W.; Formal analysis: C.E.F., Z.L.; Investigation: C.E.F., S.W.K., D.E.W.; Resources: F.J.J., T.S.M., D.E.W.; Writing - original draft: C.E.F., D.E.W.; Writing - review & editing: C.E.F., Z.L., S.W.K., F.J.J., T.S.M., D.E.W.; Visualization: C.E.F.; Supervision: D.E.W.; Project administration: C.E.F., S.W.K., D.E.W.; Funding acquisition: D.E.W.

  • Funding

    This work was supported by National Science Foundation CAREER grant 1253939 awarded to D.E.W.

  • Data availability

    Data can be accessed on the NCBI BioProject database at https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA526071.

  • Supplementary information

    Supplementary information available online at http://jeb.biologists.org/lookup/doi/10.1242/jeb.213918.supplemental

  • Received September 9, 2019.
  • Accepted December 18, 2019.
  • © 2020. Published by The Company of Biologists Ltd
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Keywords

  • Chrysemys picta
  • Comparative transcriptomics
  • Reptile
  • Ribosomal protein
  • RNA-seq

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Research Article
Development-specific transcriptomic profiling suggests new mechanisms for anoxic survival in the ventricle of overwintering turtles
Cornelia E. Fanter, Zhenguo Lin, Sarah W. Keenan, Fredric J. Janzen, Timothy S. Mitchell, Daniel E. Warren
Journal of Experimental Biology 2020 223: jeb213918 doi: 10.1242/jeb.213918 Published 17 February 2020
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Research Article
Development-specific transcriptomic profiling suggests new mechanisms for anoxic survival in the ventricle of overwintering turtles
Cornelia E. Fanter, Zhenguo Lin, Sarah W. Keenan, Fredric J. Janzen, Timothy S. Mitchell, Daniel E. Warren
Journal of Experimental Biology 2020 223: jeb213918 doi: 10.1242/jeb.213918 Published 17 February 2020

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