Independent evolution of striated muscles in cnidarians and bilaterians

Journal name:
Nature
Volume:
487,
Pages:
231–234
Date published:
DOI:
doi:10.1038/nature11180
Received
Accepted
Published online

Striated muscles are present in bilaterian animals (for example, vertebrates, insects and annelids) and some non-bilaterian eumetazoans (that is, cnidarians and ctenophores). The considerable ultrastructural similarity of striated muscles between these animal groups is thought to reflect a common evolutionary origin1, 2. Here we show that a muscle protein core set, including a type II myosin heavy chain (MyHC) motor protein characteristic of striated muscles in vertebrates, was already present in unicellular organisms before the origin of multicellular animals. Furthermore, ‘striated muscle’ and ‘non-musclemyhc orthologues are expressed differentially in two sponges, compatible with a functional diversification before the origin of true muscles and the subsequent use of striated muscle MyHC in fast-contracting smooth and striated muscle. Cnidarians and ctenophores possess striated muscle myhc orthologues but lack crucial components of bilaterian striated muscles, such as genes that code for titin and the troponin complex, suggesting the convergent evolution of striated muscles. Consistently, jellyfish orthologues of a shared set of bilaterian Z-disc proteins are not associated with striated muscles, but are instead expressed elsewhere or ubiquitously. The independent evolution of eumetazoan striated muscles through the addition of new proteins to a pre-existing, ancestral contractile apparatus may serve as a model for the evolution of complex animal cell types.

At a glance

Figures

  1. Complex phylogenomic distribution of contractile machinery and Z-disc interactome components.
    Figure 1: Complex phylogenomic distribution of contractile machinery and Z-disc interactome components.

    a, b, Rows: gene names of vertebrate and/or D. melanogaster contractile machinery (a) or Z-disc complex components (b). Columns: species and their phylogenetic relationship29, 30. Only a preliminary assembly without gene predictions was available for M. leidyi (asterisk). Row labels in a denote the site of predominant gene expression; row labels in b show species with reported Z-disc localization of the gene product. Multifamily protein and orthologies are supported by further molecular phylogenetic and protein domain analyses (Supplementary Figs 2, 7 and 8). ess., essential; reg., regulatory.

  2. Ancient myhc gene duplication predated animal radiation.
    Figure 2: Ancient myhc gene duplication predated animal radiation.

    Maximum-likelihood phylogenetic tree of MyHC type II proteins with nodes collapsed if they diverged between neighbour-joining (NJ), maximum-likelihood (ML) or Bayesian inference. The nesting of protist MyHCs within the NM MyHC orthology group supports a myhc duplication event in the common ancestor of Metazoa, Choanoflagellata, Filasterea and Ichthyosporea, but also assumes secondary losses of ST myhc genes in protist phyla. Diagrams, MyHC domain structures. Final alignment length, 1,730 amino acids (a.a.). Scale bar, 0.2 changes per site. Coloured numbers represent positions of non-canonical coiled-coil domains. Sequence accession and protein model numbers are provided in Supplementary Table 1.

  3. Expression of ST myhc in a demosponge and in anthozoan and hydrozoan cnidarians.
    Figure 3: Expression of ST myhc in a demosponge and in anthozoan and hydrozoan cnidarians.

    aq, In situ hybridizations (a, dg, kn) and schematic representations (c, hj, oq) of ST myhc expression in the adult demosponge T. wilhelma (Tw; a, c), the anthozoan N. vectensis (Nv; dj) and the hydrozoan C. hemisphaerica (Ch; kq). Scanning electron microscopy image (b) and schematic representation (c) of a sectioned choanocyte chamber of T. wilhelma. T. wilhelma ST myhc-expressing multi-porous cells (b, white arrows, inlet; c, red) are probably involved in water flow (blue dotted arrows) regulation through choanocyte chambers (within dotted white lines). n, Velum of a young medusa was lifted. Developmental stages: d, e, h, i, 4-day-old planula; f, j, 9-day-old primary polyps; k, l, o, p, medusal buds; m, n, q, young medusae; ac, g, adults. a, g, Cross-sections of stained animals; dg, kn, whole-mount micrographs. Views: d, f, h, j, k, o, q, lateral; e, i, ln, p, oral. Aboral towards top (d, h, q) or right (f, j, k, o). Asterisks denote the mouth. In Clytia hemisphaerica, two identically expressed paralogues of ST myhc exist, ST myhc-a and -b. Ap, apopyle; cc, choanocyte chamber; exc, excurrent channel; inc, incurrent channel; mh, mesohyl; pp, prosopyle; rc, ring canal; rm, retractor muscle; su, subumbrella; tb, tentacle bulb; tm, tentacle muscle; v, velum. Scale bar, 10µm.

  4. Absence of Clytia hemisphaerica muscleLIM and ldb3 expression in striated muscles.
    Figure 4: Absence of Clytia hemisphaerica muscleLIM and ldb3 expression in striated muscles.

    In situ hybridization (ad) and schematic representation (e, f) of muscleLIM (a, b) and ldb3 (c, d) expression, mainly restricted to the developing radial canal endoderm (af). ST myhc-positive subumbrella striated muscle precursor cells (arrows, compare with Fig. 3l) do not show muscleLIM or ldb3 expression. a, c and e represent the medusal bud stage and b, d and f represent the young medusa stage. Views: oral (ae) and lateral (f).

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Author information

Affiliations

  1. Department for Molecular Evolution and Development, Centre for Organismal Systems Biology, University of Vienna, Althanstraße 14, A-1090 Vienna, Austria

    • Patrick R. H. Steinmetz,
    • Johanna E. M. Kraus &
    • Ulrich Technau
  2. Centre for Marine Science, School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia

    • Claire Larroux &
    • Bernard M. Degnan
  3. Department of Earth and Environmental Sciences, Palaeontology & Geobiology, Ludwig-Maximilians-Universität München, Richard-Wagner-Strasse 10, 80333 München, Germany

    • Claire Larroux &
    • Gert Wörheide
  4. Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universität Jena, Erbertstraße 1, D-07743 Jena, Germany

    • Jörg U. Hammel &
    • Michael Nickel
  5. Institute of Zoology, Technical University of Darmstadt, Schnittspahnstraße 10, 64287 Darmstadt, Germany

    • Annette Amon-Hassenzahl
  6. Université Pierre et Marie Curie and Centre National de la Recherche Scientifique, Biologie du Développement UMR 7009, 06230 Villefranche-sur-Mer, France

    • Evelyn Houliston
  7. GeoBio-Center, Ludwig-Maximilians-Universität München, Richard-Wagner-Strasse 10, 80333 München, Germany

    • Gert Wörheide &
    • Michael Nickel
  8. Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Strasse 10, 80333 München, Germany

    • Gert Wörheide

Contributions

P.R.H.S. and U.T. designed the study, analysed data and wrote the paper. P.R.H.S. performed the bioinformatic and phylogenetic analyses, most N. vectensis experiments and cloned two A. queenslandica myhc genes. J.E.M.K. performed and analysed all C. hemisphaerica experiments. C.L. cloned all T. wilhelma genes and performed all in situ hybridization experiments on T. wilhelma and A. queenslandica. J.U.H. and M.N. performed scanning electron microscopy and sectioning of T. wilhelma animals. A.A.-H. cloned the N. vectensis ST myhc gene and performed in situ hybridization and sectioning experiments of adult N. vectensis. G.W. and E.H. provided unpublished expressed sequence tag sequences and E.H. helped perform C. hemisphaerica experiments. M.N., C.L., G.W. and J.U.H. analysed the T. wilhelma data and C.L. and B.M.D. analysed the A. queenslandica data.

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The authors declare no competing financial interests.

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Supplementary information

PDF files

  1. Supplementary Information (16M)

    This file contains Supplementary Figures 1-11 comprising: the evolutionary origin of muscle components (Supplementary Figure 1); supporting molecular phylogenies (Supplementary Figures 2 and 7) and protein domain analyses of muscle components (Supplementary Figure 8); SEM pictures of T. wilhelma apopyle cells (Supplementary Figure 4) and additional myhc (Supplementary Figures 3, 5, 6) and z-disc gene orthologs expression data (Supplementary Figures 9-11). Supplementary References are also included.

Excel files

  1. Supplementary Table 1 (90K)

    This Excel file contains accession numbers, gene model names, fully spelled species names and the sequences of DNA oligonucleotides used to clone genes.

Additional data