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Independent evolution of striated muscles in cnidarians and bilaterians

Abstract

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.

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Figure 1: Complex phylogenomic distribution of contractile machinery and Z-disc interactome components.
Figure 2: Ancient myhc gene duplication predated animal radiation.
Figure 3: Expression of ST myhc in a demosponge and in anthozoan and hydrozoan cnidarians.
Figure 4: Absence of Clytia hemisphaerica muscleLIM and ldb3 expression in striated muscles.

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Acknowledgements

For access and use of publicly available, unpublished genome sequences, we thank the Origins of Multicellularity Sequencing Project, Broad Institute of Harvard and MIT (http://www.broadinstitute.org/), the Joint Genome Institute as well as A. Baxevanis and J. Ryan. We thank M. Adamska for providing Amphimedon total RNA, M. Kube for T. wilhelma transcriptome 454 sequencing, D. Fredman and T. Momose for the C. hemisphaerica and T. Nosenko for T. wilhelma transcriptome assemblies, H. Schmidt for advice on phylogeny, B. Weiss for technical assistance with T. wilhelma sections, Genoscope for C. hemisphaerica sequencing projects and the members of the Technau laboratory for discussion. The research was funded by fellowships of the Austrian Science Fund P21108-B17 and the ITN EVONET (project 215781) to U.T., the Australian Research Council to B.M.D., the Alexander von Humboldt Foundation to C.L., ANR grant DiploDevo to E.H. and the German Science Foundation through the Priority Program 1174 Deep Metazoan Phylogeny (project Wo896/6) to G.W.

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Authors and Affiliations

Authors

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.

Corresponding author

Correspondence to Ulrich Technau.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

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. (PDF 16393 kb)

Supplementary Table 1

This Excel file contains accession numbers, gene model names, fully spelled species names and the sequences of DNA oligonucleotides used to clone genes. (XLS 90 kb)

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Steinmetz, P., Kraus, J., Larroux, C. et al. Independent evolution of striated muscles in cnidarians and bilaterians. Nature 487, 231–234 (2012). https://doi.org/10.1038/nature11180

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