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Genomic Evidence for a Simpler Clotting Scheme in Jawless Vertebrates

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Abstract

Mammalian blood clotting involves numerous components, most of which are the result of gene duplications that occurred early in vertebrate evolution and after the divergence of protochordates. As such, the genomes of the jawless fish (hagfish and lamprey) offer the best possibility for finding systems that might have a reduced set of the many clotting factors observed in higher vertebrates. The most straightforward way of inventorying these factors may be through whole genome sequencing. In this regard, the NCBI Trace database (http://www.ncbi.nlm.nih.gov/Traces/trace.cgi) for the lamprey (Petromyzon marinus) contains more than 18 million raw DNA sequences determined by whole-genome shotgun methodology. The data are estimated to be about sixfold redundant, indicating that coverage is sufficiently complete to permit judgments about the presence or absence of particular genes. A search for 20 proteins whose sequences were determined prior to the trace database study found all 20. A subsequent search for specified coagulation factors revealed a lamprey system with a smaller number of components than is found in other vertebrates in that factors V and VIII seem to be represented by a single gene, and factor IX, which is ordinarily a cofactor of factor VIII, is not present. Fortuitously, after the completion of the survey of the Trace database, a draft assembly based on the same database was posted. The draft assembly allowed many of the identified Trace fragments to be linked into longer sequences that fully support the conclusion that lampreys have a simpler clotting scheme compared with other vertebrates. The data are also consistent with the hypothesis that a whole-genome duplication or other large scale block duplication occurred after the divergence of jawless fish from other vertebrates and allowed the simultaneous appearance of a second set of two functionally paired proteins in the vertebrate clotting scheme.

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Notes

  1. The search of the factor V B domain actually detected a large number of almost-perfect tandem 27-nt repeats in the lamprey Trace database. Although both human and mouse factor V have 30 imperfect copies of these tandem nine-amino acid repeats, none occurs in the factor V sequences of chicken or puffer fish; this coincidental but perhaps chance similarity does not bear directly on the problem at hand.

  2. One of the Trace sequences (G52 in Fig. 2; Trace ID 1446326143) exhibited a remarkable 77% identity to a 34-residue segment of human factor VIII (26 identities among the 34 residues) and may be a contaminant. The corresponding region from puffer fish is only 44% identical to the human segment. The same region from chicken is coincidentally 77% identical to the human sequence, but the eight differences are not the same as observed in the lamprey sequence.

  3. Initially we reported that there were 19 GLA domains in the puffer fish (Jiang and Doolittle 2003), but some redundant sequences have apparently been removed from updated versions of that database, and we now count 16.

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Acknowledgments

This work was supported in part by National Institutes of Health Grant HL-81553. We thank Steve Culbertson for assistance in identifying mate-pairs. We are also are grateful to Jonathan Gitlin (Washington University, St. Louis) for sharing his unpublished findings on lamprey ceruloplasmin and to Steve Sommer (City of Hope) for unpublished cDNA sequences of two vitamin K-dependent proteases from lamprey.

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Author notes

  1. Yong Jiang

    Present address: Moores Cancer Center, University of California, San Diego, La Jolla, CA, 92093, USA

Authors and Affiliations

  1. Department of Chemistry & Biochemistry, University of California, San Diego, La Jolla, CA, 92093-0314, USA

    Russell F. Doolittle, Yong Jiang & Justin Nand

  2. Department of Molecular Biology, University of California, San Diego, La Jolla, CA, 92093-0314, USA

    Russell F. Doolittle, Yong Jiang & Justin Nand

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  1. Russell F. Doolittle
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Correspondence to Russell F. Doolittle.

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Doolittle, R.F., Jiang, Y. & Nand, J. Genomic Evidence for a Simpler Clotting Scheme in Jawless Vertebrates. J Mol Evol 66, 185–196 (2008). https://doi.org/10.1007/s00239-008-9074-8

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