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Transcriptome Profiling of Selectively Bred Pacific Oyster Crassostrea gigas Families that Differ in Tolerance of Heat Shock

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Abstract

Sessile inhabitants of marine intertidal environments commonly face heat stress, an important component of summer mortality syndrome in the Pacific oyster Crassostrea gigas. Marker-aided selection programs would be useful for developing oyster strains that resist summer mortality; however, there is currently a need to identify candidate genes associated with stress tolerance and to develop molecular markers associated with those genes. To identify candidate genes for further study, we used cDNA microarrays to test the hypothesis that oyster families that had high (>64%) or low (<29%) survival of heat shock (43°C, 1 h) differ in their transcriptional responses to stress. Based upon data generated by the microarray and by real-time quantitative PCR, we found that transcription after heat shock increased for genes putatively encoding heat shock proteins and genes for proteins that synthesize lipids, protect against bacterial infection, and regulate spawning, whereas transcription decreased for genes for proteins that mobilize lipids and detoxify reactive oxygen species. RNAs putatively identified as heat shock protein 27, collagen, peroxinectin, S-crystallin, and two genes with no match in Genbank had higher transcript concentrations in low-surviving families than in high-surviving families, whereas concentration of putative cystatin B mRNA was greater in high-surviving families. These ESTs should be studied further for use in marker-aided selection programs. Low survival of heat shock could result from a complex interaction of cell damage, opportunistic infection, and metabolic exhaustion.

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Acknowledgements

Funding for this research was provided by the Oyster Disease Research Program, NOAA agreement no. NA16RG1039, Sea Grant Project SAQ-08-NSI. Additional funding was provided by the Lylian Brucefield Scholarship and the Mamie Markham Award. We thank A. Barton, F. Evans, D. Mosher, and D. Stick for rearing the oyster families used during this experiment and for assistance during the heat-shocking experiments. We thank Oregon Oyster Farms, Newport, Oregon for the generous use of their facilities. We thank R. Chapman, Y. A. Chen, M. Cook, P. Cupit, P. Gross, M. Lundqvist, D. MacKillan, A. Mancia, N. Taris, H. Trent, and G. Warr for technical assistance and support during the hybridization of the microarrays and during data analysis. We thank W. Huber and W. Zhong for their advice during data analysis using vsn and SSClust, respectively. We thank A. Huvet, N. Taris, and two anonymous reviewers for thoughtful review of this manuscript. Any use of trade, firm, or corporation names in this publication is for the information and convenience of the reader. Such use does not constitute an official endorsement or approval by the United States Department of Agriculture or the Agricultural Research Service of any product or service to the exclusion of others that may be suitable.

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Authors and Affiliations

  1. Department of Fisheries and Wildlife, Coastal Oregon Marine Experiment Station, Hatfield Marine Science Center, Oregon State University, Newport, OR, 97365, USA

    R. Paul Lang & Christopher J. Langdon

  2. Department of Entomology, Louisiana State University Agricultural Center, 404 Life Sciences Building, Baton Rouge, LA, 70803, USA

    R. Paul Lang

  3. Department of Zoology, Oregon State University, Corvallis, OR, 97331, USA

    Christopher J. Bayne

  4. United States Department of Agriculture, Agricultural Research Service, Hatfield Marine Science Center, Newport, OR, 97365, USA

    Mark D. Camara

  5. Department of Biology, University of New Mexico, Albuquerque, NM, 87131, USA

    Charles Cunningham

  6. Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA, 02543, USA

    Matthew J. Jenny

Authors
  1. R. Paul Lang
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  2. Christopher J. Bayne
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  3. Mark D. Camara
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  4. Charles Cunningham
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  5. Matthew J. Jenny
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  6. Christopher J. Langdon
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Corresponding author

Correspondence to R. Paul Lang.

Electronic Supplementary Material

Below is the image is a link to a high resolution version.

Supplementary Figure 1

Raw output for 95% confidence intervals for ESTs in which transcription level differed among sampling times in gill of heat-shocked (40°C, 1 h) oysters before and at 1, 3, 6, and 24 h after heat shock. Data were clustered using the program SSClust. The vsn-transformed data for each sampling time are presented relative to the average for all sampling times for a given EST. (GIF 129 kb)

High resolution image file (TIF 8.96 MB)

Supplementary Figure 2

Average vsn-transformed signal (±SEM) for ESTs that were not studied using real-time quantitative PCR. Gill samples were collected before and at 1, 3, 6, and 24 h after heat shock (40°C, 1 h), and RNAs from those samples were hybridized to cDNA microarrays. In each plot, families with low survival (<29%) after heat shock are represented by hatched bars and those with high survival (>64%) are represented by white bars. Each bar represents nine individuals from each of two individual families of the specified survival type. (JPG 2.67 MB)

Supplementary Figure 3

Average vsn-transformed signal (±SEM) for ESTs that were not studied using real-time quantitative PCR. Gill samples were collected before and at 1, 3, 6, and 24 h after heat shock (40°C, 1 h), and RNAs from those samples were hybridized to cDNA microarrays. In each plot, families with low survival (<29%) after heat shock are represented by hatched bars and those with high survival (>64%) are represented by white bars. Each bar represents nine individuals from each of two individual families of the specified survival type. (JPG 2.52 MB)

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Lang, R.P., Bayne, C.J., Camara, M.D. et al. Transcriptome Profiling of Selectively Bred Pacific Oyster Crassostrea gigas Families that Differ in Tolerance of Heat Shock. Mar Biotechnol 11, 650–668 (2009). https://doi.org/10.1007/s10126-009-9181-6

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  • DOI: https://doi.org/10.1007/s10126-009-9181-6

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