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First published online September 19, 2008
Journal of Experimental Biology 211, 3077-3084 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.019950

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Effects of hypothermia on gene expression in zebrafish gills: upregulation in differentiation and function of ionocytes as compensatory responses

Ming-Yi Chou^1,2, Chung-Der Hsiao^1,3, Shyh-Chi Chen¹, I-Wen Chen¹, Sian-Tai Liu¹ and Pung-Pung Hwang^1,2,*

¹ Institute of Cellular and Organismic Biology, Academia Sinica, Taipei, 115 Taiwan
² Institute of Fishery Science, National Taiwan University, Taipei, 10617 Taiwan
³ Department of Bioscience Technology, Chung Yuan Christian University, Chung Li, 32023 Taiwan

^* Author for correspondence (e-mail: pphwang{at}gate.sinica.edu.tw)

Accepted 24 July 2008

Ectothermic vertebrates are different from mammals that are sensitive to hypothermia and have to maintain core temperature for survival. Why and how ectothermic animals survive, grow and reproduce in low temperature have been for a long time a scientifically challenging and important inquiry to biologists. We used a microarray to profile the gill transcriptome in zebrafish (Danio rerio) after exposure to low temperature. Adult zebrafish were acclimated to a low temperature of 12°C for 1 day and up to 30 days, and the gill transcriptome was compared with that of control fish in 28°C by oligonucleotide microarray hybridization. Results showed 11 and 22 transcripts were found to be upregulated, whereas 56 and 70 transcripts were downregulated by low-temperature treatment for 1 day and 30 days, respectively. The gill transcriptome profiles revealed that ionoregulation-related genes were highly upregulated in cold-acclimated zebrafish. This paved the way to investigate the role of ionoregulatory genes in zebrafish gills during cold acclimation. Cold acclimation caused upregulation of genes that are essential for ionocyte specification, differentiation, ionoregulation, acid–base balance and the number of cells expressing these genes increased. For instance, epithelial Ca²⁺ channel (EcaC; an ionoregulatory protein) mRNA increased in parallel with the level of Ca²⁺ influx, revealing a functional compensation after long-term acclimation to cold. Phosphohistone H3 and TUNEL staining showed that the cell turnover rate was retarded in cold-acclimated gills. Altogether, these results suggest that gills may sustain their functions by producing mature ionocytes from pre-existing undifferentiated progenitors in low-temperature environments.

Key words: acclimation, cold, differentiation, ionocyte, transcriptome, transporter

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