Coping with cold: An integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate

November 18, 2004
101 (48) 16970-16975

Abstract

How do organisms respond adaptively to environmental stress? Although some gene-specific responses have been explored, others remain to be identified, and there is a very poor understanding of the system-wide integration of response, particularly in complex, multitissue animals. Here, we adopt a transcript screening approach to explore the mechanisms underpinning a major, whole-body phenotypic transition in a vertebrate animal that naturally experiences extreme environmental stress. Carp were exposed to increasing levels of cold, and responses across seven tissues were assessed by using a microarray composed of 13,440 cDNA probes. A large set of unique cDNAs (≈3,400) were affected by cold. These cDNAs included an expression signature common to all tissues of 252 up-regulated genes involved in RNA processing, translation initiation, mitochondrial metabolism, proteasomal function, and modification of higher-order structures of lipid membranes and chromosomes. Also identified were large numbers of transcripts with highly tissue-specific patterns of regulation. By unbiased profiling of gene ontologies, we have identified the distinctive functional features of each tissue's response and integrate them into a comprehensive view of the whole-body transition from one strongly adaptive phenotype to another. This approach revealed an expression signature suggestive of atrophy in cooled skeletal muscle. This environmental genomics approach by using a well studied but nongenomic species has identified a range of candidate genes endowing thermotolerance and reveals a previously unrecognized scale and complexity of responses that impacts at the level of cellular and tissue function.

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Acknowledgments

We thank G. Govan and M. Hughes for expert technical assistance. This work was supported by the Natural Environment Research Council (Swindon, U.K.).

Supporting Information

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 101 | No. 48
November 30, 2004
PubMed: 15550548

Classifications

Submission history

Received: May 24, 2004
Accepted: October 19, 2004
Published online: November 18, 2004
Published in issue: November 30, 2004

Keywords

  1. fish
  2. microarray
  3. stress

Acknowledgments

We thank G. Govan and M. Hughes for expert technical assistance. This work was supported by the Natural Environment Research Council (Swindon, U.K.).

Authors

Affiliations

Andrew Y. Gracey
School of Biological Sciences, University of Liverpool, Biosciences Building, Crown Street, Liverpool L39 7ZB, United Kindgom; Department of Computer Science and School of Biological Science, University of Manchester, Manchester M13 9PL, United Kingdom; and Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom
E. Jane Fraser
School of Biological Sciences, University of Liverpool, Biosciences Building, Crown Street, Liverpool L39 7ZB, United Kindgom; Department of Computer Science and School of Biological Science, University of Manchester, Manchester M13 9PL, United Kingdom; and Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom
Weizhong Li
School of Biological Sciences, University of Liverpool, Biosciences Building, Crown Street, Liverpool L39 7ZB, United Kindgom; Department of Computer Science and School of Biological Science, University of Manchester, Manchester M13 9PL, United Kingdom; and Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom
Yongxiang Fang
School of Biological Sciences, University of Liverpool, Biosciences Building, Crown Street, Liverpool L39 7ZB, United Kindgom; Department of Computer Science and School of Biological Science, University of Manchester, Manchester M13 9PL, United Kingdom; and Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom
Ruth R. Taylor
School of Biological Sciences, University of Liverpool, Biosciences Building, Crown Street, Liverpool L39 7ZB, United Kindgom; Department of Computer Science and School of Biological Science, University of Manchester, Manchester M13 9PL, United Kingdom; and Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom
Jane Rogers
School of Biological Sciences, University of Liverpool, Biosciences Building, Crown Street, Liverpool L39 7ZB, United Kindgom; Department of Computer Science and School of Biological Science, University of Manchester, Manchester M13 9PL, United Kingdom; and Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom
Andrew Brass
School of Biological Sciences, University of Liverpool, Biosciences Building, Crown Street, Liverpool L39 7ZB, United Kindgom; Department of Computer Science and School of Biological Science, University of Manchester, Manchester M13 9PL, United Kingdom; and Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom
Andrew R. Cossins
School of Biological Sciences, University of Liverpool, Biosciences Building, Crown Street, Liverpool L39 7ZB, United Kindgom; Department of Computer Science and School of Biological Science, University of Manchester, Manchester M13 9PL, United Kingdom; and Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom

Notes

To whom correspondence should be sent at the present address: Hopkins Marine Station of Stanford University, Ocean View Boulevard, Pacific Grove, CA 93950. E-mail: [email protected].
Edited by Patrick O. Brown, Stanford University School of Medicine, Stanford, CA

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    Coping with cold: An integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate
    Proceedings of the National Academy of Sciences
    • Vol. 101
    • No. 48
    • pp. 16709-16982

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