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Independent evolution of striated muscles in cnidarians and bilaterians

Identifieur interne : 000E84 ( Ncbi/Merge ); précédent : 000E83; suivant : 000E85

Independent evolution of striated muscles in cnidarians and bilaterians

Auteurs : Patrick R. H. Steinmetz [Autriche] ; Johanna E. M. Kraus [Autriche] ; Claire Larroux [Australie, Allemagne] ; Jörg U. Hammel [Allemagne] ; Annette Amon-Hassenzahl [Allemagne] ; Evelyn Houliston [France] ; Gert Wörheide [Allemagne] ; Michael Nickel [Allemagne] ; Bernard M. Degnan [Australie] ; Ulrich Technau [Autriche]

Source :

RBID : PMC:3398149

Abstract

Striated muscles are present in bilaterian animals (e.g. vertebrates, insects, annelids) and some non-bilaterian eumetazoans (i.e. cnidarians and ctenophores). The striking 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 Myosin type II Heavy Chain motor protein characteristic of striated muscles in vertebrates (MyHC-st), was already present in unicellular organisms before the origin of multicellular animals. Furthermore, myhc-st and myhc-non-muscle (myhc-nm) orthologues are expressed differentially in two sponges, compatible with the functional diversification of myhc paralogues before the origin of true muscles and the subsequent deployment of MyHC-st in fast-contracting smooth and striated muscle. Cnidarians and ctenophores possess myhc-st orthologues but lack crucial components of bilaterian striated muscles, such as troponin complex and titin genes, 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 novel proteins to a pre-existing, ancestral contractile apparatus may serve as a paradigm for the evolution of complex animal cell types.


Url:
DOI: 10.1038/nature11180
PubMed: 22763458
PubMed Central: 3398149

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PMC:3398149

Le document en format XML

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<front>
<div type="abstract" xml:lang="en">
<p id="P1">Striated muscles are present in bilaterian animals (e.g. vertebrates, insects, annelids) and some non-bilaterian eumetazoans (i.e. cnidarians and ctenophores). The striking ultrastructural similarity of striated muscles between these animal groups is thought to reflect a common evolutionary origin
<sup>
<xref ref-type="bibr" rid="R1">1</xref>
,
<xref ref-type="bibr" rid="R2">2</xref>
</sup>
. Here we show that a muscle protein core set, including a Myosin type II Heavy Chain motor protein characteristic of striated muscles in vertebrates (MyHC-st), was already present in unicellular organisms before the origin of multicellular animals. Furthermore,
<italic>myhc-st</italic>
and
<italic>myhc-non-muscle (myhc-nm)</italic>
orthologues are expressed differentially in two sponges, compatible with the functional diversification of
<italic>myhc</italic>
paralogues before the origin of true muscles and the subsequent deployment of
<italic>MyHC-st</italic>
in fast-contracting smooth and striated muscle. Cnidarians and ctenophores possess
<italic>myhc-st</italic>
orthologues but lack crucial components of bilaterian striated muscles, such as
<italic>troponin</italic>
complex and
<italic>titin</italic>
genes, 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 novel proteins to a pre-existing, ancestral contractile apparatus may serve as a paradigm for the evolution of complex animal cell types.</p>
</div>
</front>
<back>
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</TEI>
<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<pmc-dir>properties manuscript</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-journal-id">0410462</journal-id>
<journal-id journal-id-type="pubmed-jr-id">6011</journal-id>
<journal-id journal-id-type="nlm-ta">Nature</journal-id>
<journal-id journal-id-type="iso-abbrev">Nature</journal-id>
<journal-title-group>
<journal-title>Nature</journal-title>
</journal-title-group>
<issn pub-type="ppub">0028-0836</issn>
<issn pub-type="epub">1476-4687</issn>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">22763458</article-id>
<article-id pub-id-type="pmc">3398149</article-id>
<article-id pub-id-type="doi">10.1038/nature11180</article-id>
<article-id pub-id-type="manuscript">UKMS48099</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Independent evolution of striated muscles in cnidarians and bilaterians</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Steinmetz</surname>
<given-names>Patrick R.H.</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kraus</surname>
<given-names>Johanna E.M.</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Larroux</surname>
<given-names>Claire</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
<xref ref-type="aff" rid="A3">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>U. Hammel</surname>
<given-names>Jörg</given-names>
</name>
<xref ref-type="aff" rid="A4">4</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Amon-Hassenzahl</surname>
<given-names>Annette</given-names>
</name>
<xref ref-type="aff" rid="A5">5</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Houliston</surname>
<given-names>Evelyn</given-names>
</name>
<xref ref-type="aff" rid="A6">6</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wörheide</surname>
<given-names>Gert</given-names>
</name>
<xref ref-type="aff" rid="A3">3</xref>
<xref ref-type="aff" rid="A7">7</xref>
<xref ref-type="aff" rid="A8">8</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Nickel</surname>
<given-names>Michael</given-names>
</name>
<xref ref-type="aff" rid="A4">4</xref>
<xref ref-type="aff" rid="A7">7</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Degnan</surname>
<given-names>Bernard M.</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Technau</surname>
<given-names>Ulrich</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="corresp" rid="CR1">#</xref>
</contrib>
</contrib-group>
<aff id="A1">
<label>1</label>
Department for Molecular Evolution and Development, Centre for Organismal Systems Biology, University of Vienna, Althanstraße 14, A-1090 Vienna, Austria</aff>
<aff id="A2">
<label>2</label>
Centre for Marine Science, School of Biological Sciences, The University of Queensland, Brisbane Queensland 4072, Australia</aff>
<aff id="A3">
<label>3</label>
Department of Earth and Environmental Sciences, Palaeontology & Geobiology, Ludwig-Maximilians-Universität München, Richard-Wagner-Str. 10, 80333 München, Germany</aff>
<aff id="A4">
<label>4</label>
Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universität Jena, Erbertstraße 1, D-07743 Jena, Germany</aff>
<aff id="A5">
<label>5</label>
Institute of Zoology, Technical University of Darmstadt, Schnittspahnstraße 10, 64287, Darmstadt, Germany</aff>
<aff id="A6">
<label>6</label>
Université Pierre et Marie Curie and CNRS, “Biologie du Développement” UMR 7009, 06230 Villefranche-sur-Mer, France</aff>
<aff id="A7">
<label>7</label>
GeoBio-Center, Ludwig-Maximilians-Universität München, Richard-Wagner-Str. 10, 80333 München, Germany</aff>
<aff id="A8">
<label>8</label>
Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Str. 10, 80333 München, Germany</aff>
<author-notes>
<corresp id="CR1">
<label>#</label>
Corresponding author:
<email>Ulrich.technau@univie.ac.at</email>
</corresp>
</author-notes>
<pub-date pub-type="nihms-submitted">
<day>21</day>
<month>5</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="ppub">
<day>12</day>
<month>7</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>12</day>
<month>1</month>
<year>2013</year>
</pub-date>
<volume>487</volume>
<issue>7406</issue>
<fpage>231</fpage>
<lpage>234</lpage>
<permissions>
<license>
<license-p>Users may view, print, copy, download and text and data- mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:
<uri xlink:type="simple" xlink:href="http://www.nature.com/authors/editorial_policies/license.html#terms">http://www.nature.com/authors/editorial_policies/license.html#terms</uri>
</license-p>
</license>
</permissions>
<abstract>
<p id="P1">Striated muscles are present in bilaterian animals (e.g. vertebrates, insects, annelids) and some non-bilaterian eumetazoans (i.e. cnidarians and ctenophores). The striking ultrastructural similarity of striated muscles between these animal groups is thought to reflect a common evolutionary origin
<sup>
<xref ref-type="bibr" rid="R1">1</xref>
,
<xref ref-type="bibr" rid="R2">2</xref>
</sup>
. Here we show that a muscle protein core set, including a Myosin type II Heavy Chain motor protein characteristic of striated muscles in vertebrates (MyHC-st), was already present in unicellular organisms before the origin of multicellular animals. Furthermore,
<italic>myhc-st</italic>
and
<italic>myhc-non-muscle (myhc-nm)</italic>
orthologues are expressed differentially in two sponges, compatible with the functional diversification of
<italic>myhc</italic>
paralogues before the origin of true muscles and the subsequent deployment of
<italic>MyHC-st</italic>
in fast-contracting smooth and striated muscle. Cnidarians and ctenophores possess
<italic>myhc-st</italic>
orthologues but lack crucial components of bilaterian striated muscles, such as
<italic>troponin</italic>
complex and
<italic>titin</italic>
genes, 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 novel proteins to a pre-existing, ancestral contractile apparatus may serve as a paradigm for the evolution of complex animal cell types.</p>
</abstract>
</article-meta>
</front>
<floats-group>
<fig id="F1" orientation="portrait" position="float">
<label>Figure 1</label>
<caption>
<title>Complex phylogenomic distribution of contractile machinery (a) and z-disc interactome (b) components</title>
<p>Rows: gene names of vertebrate and/or
<italic>D. melanogaster</italic>
contractile machinery (a) or z-disc complex (b) components. Columns: species and their phylogenetic relationship
<sup>
<xref ref-type="bibr" rid="R29">29</xref>
,
<xref ref-type="bibr" rid="R30">30</xref>
</sup>
. Asterisk: only a preliminary assembly without gene predictions was available for
<italic>M. leidyi</italic>
. Row labels in (a): site of predominant gene expression; in (b): species with reported z-disc localization of the gene product. Multifamily protein and uncertain orthologies supported by further molecular phylogenetic and protein domain analyses (
<xref ref-type="supplementary-material" rid="SD2">Supplementary Figs. 2</xref>
,
<xref ref-type="supplementary-material" rid="SD2">6</xref>
,
<xref ref-type="supplementary-material" rid="SD2">7</xref>
). All abbreviations in
<xref ref-type="supplementary-material" rid="SD3">Supplementary Table 1</xref>
.</p>
</caption>
<graphic xlink:href="ukmss-48099-f0001"></graphic>
</fig>
<fig id="F2" orientation="portrait" position="float">
<label>Figure 2</label>
<caption>
<title>Ancient
<italic>myhc</italic>
gene duplication predated animal radiation</title>
<p>Maximum likelihood phylogenetic tree of MyHC type II proteins with nodes collapsed if they diverged between neighbour-joining, maximum likelihood, or Bayesian inference. The nesting of protist MyHCs within the MyHC-nm orthology group supports a
<italic>myhc</italic>
duplication event in the common ancestor of Metazoa, Choanoflagellata, Filasterea and Ichthyosporea, but also assumes secondary losses of
<italic>myhc-st</italic>
genes in protist phyla. Diagrams: MyHC domain structures. Final alignment length: 1730 a.a. Scale bar: 0.2 changes per site. Coloured numbers: positions of non-canonical coiled-coil domains. a.a.: amino acid. Species abbreviations, sequence accession and protein model numbers in
<xref ref-type="supplementary-material" rid="SD3">Supplementary Table 1</xref>
.</p>
</caption>
<graphic xlink:href="ukmss-48099-f0002"></graphic>
</fig>
<fig id="F3" orientation="portrait" position="float">
<label>Figure 3</label>
<caption>
<title>Expression of
<italic>myhc-st</italic>
in a demosponge, and in anthozoan and hydrozoan cnidarians</title>
<p>
<italic>In situ</italic>
hybridisations (a, d-g, l-o) and schematic representations (c, h-k, p-r) of
<italic>myhc-st</italic>
expression in the adult demosponge
<italic>Tethya wilhelma</italic>
(a,c), the anthozoan
<italic>Nematostella vectensis</italic>
(d-k), and the hydrozoan
<italic>Clytia hemisphaerica</italic>
(l-r). Scanning electron microscopy image (b) and schematic representation (c) of a sectionned choanocyte chambers of
<italic>T. wilhelma. Tw-myhc-st</italic>
-expressing multi-porous cells (b, white arrows, inlet; c, red) are likely involved in water flow (blue dotted arrows) regulation through choanocyte chambers (within dotted white lines). (o) Velum of a young medusa was lifted. Developmental stages: (d-e, h-i) 4 days old planula; (f,k) 9 days old primary polyps; (l-m, p-q) medusal buds; (n-o, r) young medusae; (a-c, g) adults. (a,g) Cross-sections of stained animals; (d-g, l-o) whole-mount micrographs. Views: (d,f,h,k-l,p,r) lateral; (e,i, m-o,q) oral. Aboral towards top (d,h,r) or lower-right (f, k-l, p). Asterisk: mouth. 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.</p>
</caption>
<graphic xlink:href="ukmss-48099-f0003"></graphic>
</fig>
<fig id="F4" orientation="portrait" position="float">
<label>Figure 4</label>
<caption>
<title>Absence of
<italic>Clytia hemisphaerica muscleLim</italic>
and
<italic>Ch-ldb3/zasp</italic>
expression in striated muscles</title>
<p>
<italic>In situ</italic>
hybridisation (a-d) and schematic representation (e-f) of
<italic>Ch-muscleLim</italic>
(a, b),
<italic>Ch-ldb3/zasp</italic>
(c, d) expression mainly restricte to the developing radial canal endoderm (a-f).
<italic>Ch-myhc-st</italic>
-positive subumbrella striated muscle precursor cells (arrows, compare with
<xref ref-type="fig" rid="F3">Fig. 3m</xref>
) do not show
<italic>muscleLim</italic>
- or
<italic>ldb3/zasp</italic>
-expression. Stages: medusal bud (a,c,e), young medusa (b,d,f). All oral views.</p>
</caption>
<graphic xlink:href="ukmss-48099-f0004"></graphic>
</fig>
</floats-group>
</pmc>
<affiliations>
<list>
<country>
<li>Allemagne</li>
<li>Australie</li>
<li>Autriche</li>
<li>France</li>
</country>
<region>
<li>Bavière</li>
<li>District de Darmstadt</li>
<li>District de Haute-Bavière</li>
<li>Hesse (Land)</li>
</region>
<settlement>
<li>Darmstadt</li>
<li>Munich</li>
</settlement>
<orgName>
<li>Université Louis-et-Maximilien de Munich</li>
</orgName>
</list>
<tree>
<country name="Autriche">
<noRegion>
<name sortKey="Steinmetz, Patrick R H" sort="Steinmetz, Patrick R H" uniqKey="Steinmetz P" first="Patrick R. H." last="Steinmetz">Patrick R. H. Steinmetz</name>
</noRegion>
<name sortKey="Kraus, Johanna E M" sort="Kraus, Johanna E M" uniqKey="Kraus J" first="Johanna E. M." last="Kraus">Johanna E. M. Kraus</name>
<name sortKey="Technau, Ulrich" sort="Technau, Ulrich" uniqKey="Technau U" first="Ulrich" last="Technau">Ulrich Technau</name>
</country>
<country name="Australie">
<noRegion>
<name sortKey="Larroux, Claire" sort="Larroux, Claire" uniqKey="Larroux C" first="Claire" last="Larroux">Claire Larroux</name>
</noRegion>
<name sortKey="Degnan, Bernard M" sort="Degnan, Bernard M" uniqKey="Degnan B" first="Bernard M." last="Degnan">Bernard M. Degnan</name>
</country>
<country name="Allemagne">
<region name="Bavière">
<name sortKey="Larroux, Claire" sort="Larroux, Claire" uniqKey="Larroux C" first="Claire" last="Larroux">Claire Larroux</name>
</region>
<name sortKey="Amon Hassenzahl, Annette" sort="Amon Hassenzahl, Annette" uniqKey="Amon Hassenzahl A" first="Annette" last="Amon-Hassenzahl">Annette Amon-Hassenzahl</name>
<name sortKey="Nickel, Michael" sort="Nickel, Michael" uniqKey="Nickel M" first="Michael" last="Nickel">Michael Nickel</name>
<name sortKey="Nickel, Michael" sort="Nickel, Michael" uniqKey="Nickel M" first="Michael" last="Nickel">Michael Nickel</name>
<name sortKey="U Hammel, Jorg" sort="U Hammel, Jorg" uniqKey="U Hammel J" first="Jörg" last="U. Hammel">Jörg U. Hammel</name>
<name sortKey="Worheide, Gert" sort="Worheide, Gert" uniqKey="Worheide G" first="Gert" last="Wörheide">Gert Wörheide</name>
<name sortKey="Worheide, Gert" sort="Worheide, Gert" uniqKey="Worheide G" first="Gert" last="Wörheide">Gert Wörheide</name>
<name sortKey="Worheide, Gert" sort="Worheide, Gert" uniqKey="Worheide G" first="Gert" last="Wörheide">Gert Wörheide</name>
</country>
<country name="France">
<noRegion>
<name sortKey="Houliston, Evelyn" sort="Houliston, Evelyn" uniqKey="Houliston E" first="Evelyn" last="Houliston">Evelyn Houliston</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>

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