Early evolution of animal cell signaling and adhesion genes

  1. Scott A. Nichols*,
  2. William Dirks,
  3. John S. Pearse, and
  4. Nicole King*,,§,
  1. Departments of *Molecular and Cell Biology and
  2. §Integrative Biology and
  3. Center for Integrative Genomics, University of California, Berkeley, CA 94720; and
  4. Joseph M. Long Marine Laboratory, University of California, Santa Cruz, CA 95060
  1. Edited by James W. Valentine, University of California, Berkeley, CA, and approved June 28, 2006 (received for review May 17, 2006)

Abstract

In stark contrast to the rapid morphological radiation of eumetazoans during the Cambrian explosion, the simple body plan of sponges (Phylum Porifera) emerged from the Cambrian relatively unchanged. Although the genetic and developmental underpinnings of these disparate evolutionary outcomes are unknown, comparisons between modern sponges and eumetazoans promise to reveal the extent to which critical genetic factors were present in their common ancestors. Two particularly interesting classes of genes in this respect are those involved in cell signaling and adhesion. These genes help guide development and morphogenesis in modern eumetazoans, but the timing and sequence of their origins is unknown. Here, we demonstrate that the sponge Oscarella carmela, one of the earliest branching animals, expresses core components of the Wnt, transforming growth factor β, receptor tyrosine kinase, Notch, Hedgehog, and Jak/Stat signaling pathways. Furthermore, we identify sponge homologs of nearly every major eumetazoan cell-adhesion gene family, including those that encode cell-surface receptors, cytoplasmic linkers, and extracellular-matrix proteins. From these data, we infer that key signaling and adhesion genes were in place early in animal evolution, before the divergence of sponge and eumetazoan lineages.

Footnotes

  • To whom correspondence should be addressed. E-mail: nking{at}berkeley.edu
  • Author contributions: S.A.N. and N.K. designed research; S.A.N. performed research; W.D. and J.S.P. contributed new reagents/analytic tools; S.A.N. analyzed data; and S.A.N. and N.K. wrote the paper.

  • Conflict of interest statement: No conflicts declared.

  • This paper was submitted directly (Track II) to the PNAS office.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. EB741367EB741549 and EC366551EC377543).

  • Abbreviations:

    Abbreviations

    GO,
    Gene Ontology;
    NCBI,
    National Center for Biotechnology Information;
    nr,
    nonredundant.
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