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Research Article

Transcriptomic resilience to global warming in the seagrass Zostera marina, a marine foundation species

Susanne U. Franssen, Jenny Gu, Nina Bergmann, Gidon Winters, Ulrich C. Klostermeier, Philip Rosenstiel, Erich Bornberg-Bauer, and Thorsten B. H. Reusch
PNAS first published November 14, 2011; https://doi.org/10.1073/pnas.1107680108
Susanne U. Franssen
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Jenny Gu
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Nina Bergmann
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Gidon Winters
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Ulrich C. Klostermeier
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Philip Rosenstiel
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Erich Bornberg-Bauer
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Thorsten B. H. Reusch
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  • For correspondence: treusch@ifm-geomar.de
  1. Edited by Edward F. DeLong, Massachusetts Institute of Technology, Cambridge, MA, and approved July 18, 2011 (received for review May 17, 2011)

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Abstract

Large-scale transcription profiling via direct cDNA sequencing provides important insights as to how foundation species cope with increasing climatic extremes predicted under global warming. Species distributed along a thermal cline, such as the ecologically important seagrass Zostera marina, provide an opportunity to assess temperature effects on gene expression as a function of their long-term adaptation to heat stress. We exposed a southern and northern European population of Zostera marina from contrasting thermal environments to a realistic heat wave in a common-stress garden. In a fully crossed experiment, eight cDNA libraries, each comprising ∼125 000 reads, were obtained during and after a simulated heat wave, along with nonstressed control treatments. Although gene-expression patterns during stress were similar in both populations and were dominated by classical heat-shock proteins, transcription profiles diverged after the heat wave. Gene-expression patterns in southern genotypes returned to control values immediately, but genotypes from the northern site failed to recover and revealed the induction of genes involved in protein degradation, indicating failed metabolic compensation to high sea-surface temperature. We conclude that the return of gene-expression patterns during recovery provides critical information on thermal adaptation in aquatic habitats under climatic stress. As a unifying concept for ecological genomics, we propose transcriptomic resilience, analogous to ecological resilience, as an important measure to predict the tolerance of individuals and hence the fate of local populations in the face of global warming.

  • EST-library
  • extreme event
  • thermal tolerance

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: treusch{at}ifm-geomar.de.
  • Author contributions: T.B.H.R. designed research; S.U.F., N.B., G.W., U.C.K., and T.B.H.R. performed research; J.G., U.C.K., and P.R. contributed new reagents/analytic tools; S.U.F., J.G., P.R., and E.B.-B. analyzed data; and S.U.F., P.R., E.B.-B., and T.B.H.R. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: Raw sequence data for the eight generated libraries have been deposited at the Sequence Read Archive (http://trace.ncbi.nlm.nih.gov/Traces/sra/?study=SRP007220, accession no. SRP007220). ESTs for the third assembly came from a single clone (National Center for Biotechnology Information Sequence Read Archive, http://trace.ncbi.nlm.nih.gov/Traces/sra/?study=SRP002573, accession no. SRA002573).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1107680108/-/DCSupplemental.

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Transcriptomic resilience to global warming in the seagrass Zostera marina, a marine foundation species
Susanne U. Franssen, Jenny Gu, Nina Bergmann, Gidon Winters, Ulrich C. Klostermeier, Philip Rosenstiel, Erich Bornberg-Bauer, Thorsten B. H. Reusch
Proceedings of the National Academy of Sciences Nov 2011, 201107680; DOI: 10.1073/pnas.1107680108

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Transcriptomic resilience to global warming in the seagrass Zostera marina, a marine foundation species
Susanne U. Franssen, Jenny Gu, Nina Bergmann, Gidon Winters, Ulrich C. Klostermeier, Philip Rosenstiel, Erich Bornberg-Bauer, Thorsten B. H. Reusch
Proceedings of the National Academy of Sciences Nov 2011, 201107680; DOI: 10.1073/pnas.1107680108
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