Coping with cold: An integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate.
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 (approximately 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.
Gracey
Andrew Y
AY
School of Biological Sciences, University of Liverpool, Biosciences Building, Crown Street, Liverpool L39 7ZB, United Kindgom. agracey@stanford.edu
Fraser
E Jane
EJ
Li
Weizhong
W
Fang
Yongxiang
Y
Taylor
Ruth R
RR
Rogers
Jane
J
Brass
Andrew
A
Cossins
Andrew R
AR
D000222:Adaptation, Physiological / Q000235:genetics*; D000818:Animals; D002347:Carps / Q000235:genetics / Q000502:physiology*; D003080:Cold Temperature; D015342:DNA Probes; D018076:DNA, Complementary; D020869:Gene Expression Profiling; D008969:Molecular Sequence Data; D020411:Oligonucleotide Array Sequence Analysis; D012333:RNA, Messenger / Q000235:genetics*
D015342:DNA Probes; D018076:DNA, Complementary; D012333:RNA, Messenger