Skip to main content
SpringerLink
Log in

Duplicated Clock genes with unique polyglutamine domains provide evidence for nonhomologous recombination in Chinook salmon (Oncorhynchus tshawytscha)

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Circadian rhythms underlie diverse life functions ranging from cellular activities to behavior. Multiple clock genes play a central role in the generation of these rhythms. We partially characterized two copies of the Clock gene from Chinook salmon (Oncorhynchus tshawytscha), OtsClock1a and OtsClock1b. The 6,460 bp OtsClock1a sequence contains 16 exons, 15 introns and encompasses three highly conserved domains indicating it is a novel member of the bHLH-PAS superfamily of transcription factors. The second copy, OtsClock1b, consists of five exons and five introns spanning 1,945 bp. A polyglutamine repeat motif (PolyQ), characteristic of a majority of CLOCK proteins, is present in both OTSCLOCK1a and OTSCLOCK1b. However, the Chinook PolyQ domains are uniquely positioned inside the gene. Interestingly, a 1,200 bp non-coding segment located downstream of the OtsClock1a PolyQ domain is absent from OtsClock1b. This insertion/deletion is 91% similar to the Salmo salar Transferrin gene. A phylogenetic analysis of 11 CLOCK proteins shows that OtsClock1a and OtsClock1b are paralogs which likely arose subsequent to the salmonid genome-wide duplication event. Ultimately, the Chinook salmon Clock genes are key components to our understanding the genetic mechanisms underlying temporally regulated life history traits in Pacific salmonids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allada R, White NE, So WV, Hall JC, Robash M (1998) A mutant Drosophila homolog of mammalian Clock disrupts circadian rhythms and transcription of period and timeless. Cell 93:791–804

    Article  PubMed  CAS  Google Scholar 

  • Allendorf FW, Thorgaard GH (1984) Tetraploidy and the evolution of salmonid fishes. In: Turner B (ed) Evolutionary genetics of fishes. Plenum Press, New York, pp 1–53

    Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Antoch MP, Song EJ, Chang AM, Vitaterna MH, Zhao Y, Wilsbacher LD, Sangoram AM, King DP, Pinto LH, Takanashi JS (1997) Functional identification of the mouse circadian Clock gene by transgenic BAC rescue. Cell 89:655–667

    Article  PubMed  CAS  Google Scholar 

  • Avivi A, Albrecht U, Oster H, Joel A, Beiles A, Nevo E (2001) Biological clock in total darkness: the Clock/MOP3 circadian system of the blind subterranean mole rat. Proc Natl Acad Sci U S A 98:13751–13756

    Article  PubMed  CAS  Google Scholar 

  • Bacolla A, Wells RD (2004) Non-B DNA conformations, genomic rearrangements, and human diseases. J Biol Chem 279:47411–47414

    Article  PubMed  CAS  Google Scholar 

  • Bailey GS, Poulter RT, Stockwell PA (1978) Gene duplication in tetraploid fish: model for gene silencing at unlinked duplicated loci. Proc Natl Acad Sci U S A 78:5575–5579

    Article  Google Scholar 

  • Chang DC, McWatters HG, Williams JA, Gotter AL, Levine JD, Reppert SM (2003) Constructing a feedback loop with circadian clock molecules from the silkmoth, Antheraea pernyi. J Biol Chem 278:38149–38158

    Article  PubMed  CAS  Google Scholar 

  • Chappell PE, White RS, Mellon PL (2003) Circadian gene expression regulates pulsatile gonadotropin-releasing hormone (GnRH) secretory patterns in the hypothalamic GnRH-secreting GT1–7 cell line. J Neuro 23:112022–11213

    Google Scholar 

  • Children’s Hospital Oakland Research Institute [http://bacpac.chori.org/highdensity.htm]

  • Cronn R, Cedroni M, Haselkorn T, Grover C, Wendel JF (2002) PCR-mediated recombination in amplification products derived from polyploidy cotton. Theor Appl Genet 104:482–489

    Article  PubMed  CAS  Google Scholar 

  • Darlington TK, Wager-Smith K, Ceriani MF, Staknis D, Gekakis N, Steeves TDL, Weitz CJ, Takahashi JS, Kay SA (1998) Closing the circadian loop: Clock-induced transcription of its own inhibitors per and tim. Science 280:1599–1603

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1991) PHYLIP: phylogeny inference package, version 3.4. Department of Genetics, SK-50, University of Washington, Seattle

    Google Scholar 

  • Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545

    PubMed  CAS  Google Scholar 

  • Gately KA (2000) Regulation of the Atlantic salmon (Salmo salar) transferrin gene and liver gene expression. Thesis (Ph.D.): National University of Ireland, Galway pp 197–224

  • Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP, Takahashi JS, Weitz CJ (1998) Role of the CLOCK protein in the mammalian circadian mechanism. Science 280:1564–1569

    Article  PubMed  CAS  Google Scholar 

  • Hall T (1997) BioEdit Sequence Alignment Editor. Ibis Therapeutics, Carlsbad, Ca

    Google Scholar 

  • He X, Zhang J (2006) Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169:1157–1164

    Article  Google Scholar 

  • Hirayama J, Kaneko M, Cardone L, Cahill G, Sassone-Corsi P (2005) Analysis of circadian rhythms in zebrafish. Methods Enzymol 393:186–204

    PubMed  CAS  Google Scholar 

  • Hughes A (1994) The evolution of functionally novel proteins after gene duplication. Proc R Soc Lon B 256:119–124

    Article  CAS  Google Scholar 

  • Jeffreys AJ, Neil DL, Neumann R (1998) Repeat instability at human minisatellites arising from meiotic recombination. EMBO J 17:4147–4157

    Article  PubMed  CAS  Google Scholar 

  • Kimura A, Ohta T (1974) On some principles governing molecular evolution. Proc Nat Acad Sci U S A 71:2848–2852

    Article  CAS  Google Scholar 

  • King DP, Zhao YL, Sangoram AM, Wilsbacher LD, Tanaka M, Antoch MP, Steeves TDL, Vitaterna MH, Kornhauser JM, Lowrey PL, Turek FW, Takahashi JS (1997) Positional cloning of the mouse circadian CLOCK gene. Cell 89:641–653

    Article  PubMed  CAS  Google Scholar 

  • Looby P, Loudon ASI (2005) Gene duplication and complex circadian clocks in mammals. Trends Genet 21:46–53

    Article  PubMed  CAS  Google Scholar 

  • Matsuo T, Yamaguchi S, Mitsui S, Emi A, Shimoda F, Okamura H (2003) Control mechanism for the circadian clock for timing of cell division in vivo. Science 202:255–259

    Article  CAS  Google Scholar 

  • Mazurais D, Le Drean G, Brierley I, Anglade I, Bromage N, Williams LM, Kah O (2000) Expression of clock gene in the brain of rainbow trout: comparison with the distribution of melatonin receptors. J Comp Neurol 422:612–620

    Article  PubMed  CAS  Google Scholar 

  • McNamara P et al (2001) Regulation of CLOCK and MOP4 by nuclear hormone receptors in the vasculature: a humoral mechanism to reset a peripheral clock. Cell 105:877–889

    Article  PubMed  CAS  Google Scholar 

  • Mitchell PJ, Tijian R (1989) Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science 245:371–378

    Article  PubMed  CAS  Google Scholar 

  • Near TJ, Parker SK, Detrich HW (2006) A genomic fossil reveals the key steps in hemoglobin loss by the Antarctic icefishes. Mol Biol Evol 23:2008–2016

    Article  PubMed  CAS  Google Scholar 

  • Ohno S, Wolf U, Atkin NB (1968) Evolution from fish to mammals by gene duplication. Hereditas 59:169–187

    Article  PubMed  CAS  Google Scholar 

  • Reppert SM, Weaver DJ (2002) Coordination of circadian timing in mammals. Nature 418:935–941

    Article  PubMed  CAS  Google Scholar 

  • Richard G-F, Paques E (2000) Myotonic dystrophy: RNA pathogenesis comes into focus. Am J Hum Genet 74:793–804

    Google Scholar 

  • Saleem Q, Anand A, Jain S, Brahmachari SK (2001) The polyglutamine motif is highly conserved at the Clock locus in various organisms and is not polymorphic in humans. Hum Genet 109:136–142

    Article  PubMed  CAS  Google Scholar 

  • Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A 95:5857–5864

    Article  PubMed  CAS  Google Scholar 

  • Schwassmann HO (1988) Biological rhythms. In: Hoar WS, Randall DJ (eds) Fish Physiology. Academic Press, New York, pp 371–416

    Google Scholar 

  • Steeves TDL, King DP, Zhao Y, Sangoram AM, Du F, Bowcock AM, Moore RY, Takahashi JS (1999) Molecular cloning and characterization of the human CLOCK gene: expression in the superchiasmatic nuclei. Genomics 57:189–200

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Verstrepen K, Jansen A, Lewitter F, Fink G (2005) Intragenic tandem repeats generate functional variability. Nat Genet 37:986–990

    Article  PubMed  CAS  Google Scholar 

  • Vitaterna MH, King DP, Chang AM, Kornhauser JM, Lowery PL, McDonald JD, Dove WF, Pinto LH, Turek FW, Takahashi JS (1994) Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. Science 264:719–725

    Article  PubMed  CAS  Google Scholar 

  • Whitmore D, Foulkes NS, Strahle U, Sassone-Corsi P (1998) Zebrafish Clock rhythmic expression reveals independent peripheral circadian oscillators. Nature Neurosci 1:701–707

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura T, Suzuki Y, Makino E, Suzuki T, Kuroiwa A, Matsuda Y, Namikawa T, Ebihara S (2000) Molecular analysis of avian clock genes. Mol Brain Res 78:207–215

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the California Department of Water Resources and the Mamie M. Markham Research Grant. We are grateful to M. Camara and G. Moyer for comments that considerably improved the manuscript and I. Meusnier for help with mRNA sampling and screening the BAC library. We thank B. Devlin of the Department of Fisheries and Oceans, British Columbia, Canada for providing reagents, laboratory equipment, and technical support to probe the Chinook salmon BAC library.

Author information

Authors and Affiliations

  1. Coastal Oregon Marine Experiment Station, Hatfield Marine Science Center, Department of Fisheries and Wildlife, Oregon State University, 2030 SE Marine Science Drive, Newport, OR, 97365, USA

    K. G. O’Malley & M. A. Banks

Authors
  1. K. G. O’Malley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. A. Banks
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. G. O’Malley.

Rights and permissions

Reprints and permissions

About this article

Cite this article

O’Malley, K.G., Banks, M.A. Duplicated Clock genes with unique polyglutamine domains provide evidence for nonhomologous recombination in Chinook salmon (Oncorhynchus tshawytscha). Genetica 132, 87–94 (2008). https://doi.org/10.1007/s10709-007-9151-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-007-9151-8

Keywords

Search

Navigation