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Research Article

Genomic basis for coral resilience to climate change

Daniel J. Barshis, Jason T. Ladner, Thomas A. Oliver, François O. Seneca, Nikki Traylor-Knowles, and Stephen R. Palumbi
  1. Department of Biology, Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950

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PNAS first published January 7, 2013; https://doi.org/10.1073/pnas.1210224110
Daniel J. Barshis
Department of Biology, Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950
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  • For correspondence: barshis@gmail.com
Jason T. Ladner
Department of Biology, Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950
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Thomas A. Oliver
Department of Biology, Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950
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François O. Seneca
Department of Biology, Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950
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Nikki Traylor-Knowles
Department of Biology, Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950
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Stephen R. Palumbi
Department of Biology, Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950
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  1. Edited by David M. Hillis, The University of Texas at Austin, Austin, TX, and approved November 30, 2012 (received for review June 15, 2012)

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Abstract

Recent advances in DNA-sequencing technologies now allow for in-depth characterization of the genomic stress responses of many organisms beyond model taxa. They are especially appropriate for organisms such as reef-building corals, for which dramatic declines in abundance are expected to worsen as anthropogenic climate change intensifies. Different corals differ substantially in physiological resilience to environmental stress, but the molecular mechanisms behind enhanced coral resilience remain unclear. Here, we compare transcriptome-wide gene expression (via RNA-Seq using Illumina sequencing) among conspecific thermally sensitive and thermally resilient corals to identify the molecular pathways contributing to coral resilience. Under simulated bleaching stress, sensitive and resilient corals change expression of hundreds of genes, but the resilient corals had higher expression under control conditions across 60 of these genes. These “frontloaded” transcripts were less up-regulated in resilient corals during heat stress and included thermal tolerance genes such as heat shock proteins and antioxidant enzymes, as well as a broad array of genes involved in apoptosis regulation, tumor suppression, innate immune response, and cell adhesion. We propose that constitutive frontloading enables an individual to maintain physiological resilience during frequently encountered environmental stress, an idea that has strong parallels in model systems such as yeast. Our study provides broad insight into the fundamental cellular processes responsible for enhanced stress tolerances that may enable some organisms to better persist into the future in an era of global climate change.

  • acquired stress tolerance
  • Acropora hyacinthus
  • thermal stress
  • transcriptomics
  • Cnidarian

Footnotes

  • ↵1Present address: Institute of Marine Science, NOAA Fisheries, University of California Santa Cruz, Santa Cruz, CA 95060.

  • ↵2To whom correspondence should be addressed. E-mail: barshis{at}gmail.com.
  • Author contributions: D.J.B., T.A.O., and S.R.P. designed research; D.J.B., J.T.L., and T.A.O. performed research; D.J.B. and J.T.L. contributed new reagents/analytic tools; D.J.B., J.T.L., T.A.O., F.O.S., N.T.-K., and S.R.P. analyzed data; and D.J.B., J.T.L., T.A.O., F.O.S., N.T.-K., and S.R.P. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited in the Transcriptome Shotgun Assembly database, www.ncbi.nlm.nih.gov/genbank/tsa (BioProject PRJNA177515), and the Dryad data repository (dx.doi.org/10.5061/dryad.bc0v0).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1210224110/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Transcriptomics of coral climate change resilience
Daniel J. Barshis, Jason T. Ladner, Thomas A. Oliver, François O. Seneca, Nikki Traylor-Knowles, Stephen R. Palumbi
Proceedings of the National Academy of Sciences Jan 2013, 201210224; DOI: 10.1073/pnas.1210224110

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Transcriptomics of coral climate change resilience
Daniel J. Barshis, Jason T. Ladner, Thomas A. Oliver, François O. Seneca, Nikki Traylor-Knowles, Stephen R. Palumbi
Proceedings of the National Academy of Sciences Jan 2013, 201210224; DOI: 10.1073/pnas.1210224110
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