Independent evolution of striated muscles in cnidarians and bilaterians

Nature

Volumn 487, Issue 7406, 2012, Pages 231-234

  Steinmetz, Patrick R H ^a   Kraus, Johanna E M ^a   Larroux, Claire ^b,c   Hammel, Jörg U ^d   Amon Hassenzahl, Annette ^e   Houliston, Evelyn ^f   Wörheide, Gert ^c,g   Nickel, Michael ^c,d   Degnan, Bernard M ^b   Technau, Ulrich ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF MUNICH   (Germany)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^e DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^f SORBONNE UNIVERSITÉ   (France)

^g BAYERISCHE STAATSSAMMLUNG FÜR PALÄONTOLOGIE UND GEOLOGIE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; CONNECTIN; LIM PROTEIN; MYOSIN HEAVY CHAIN; TROPONIN;

ANCESTRY; EVOLUTIONARY BIOLOGY; INVERTEBRATE; MUSCLE; PROTEIN; ULTRASTRUCTURE;

ARTICLE; BILATERIA; CNIDARIA; DROSOPHILA MELANOGASTER; EVOLUTION; JELLYFISH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SARCOMERE LENGTH; SKELETAL MUSCLE; SMOOTH MUSCLE;

ANIMALS; BIOLOGICAL EVOLUTION; CNIDARIA; GENE DUPLICATION; GENE EXPRESSION REGULATION; MUSCLE, STRIATED; MYOSIN HEAVY CHAINS; PHYLOGENY;

ANIMALIA; ANNELIDA; BILATERIA; CNIDARIA; CTENOPHORA (COELENTERATES); EUMETAZOA; HEXAPODA; METAZOA; SCYPHOZOA; VERTEBRATA;

EID: 84863655007     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature11180     Document Type: Article

References (67)

1. Seipel, K. & Schmid, V. Evolution of striated muscle: jellyfish and the origin of triploblasty. Dev. Biol. 282, 14-26 (2005).
2. Schuchert, P., Reber-Müller, S. & Schmid, V. Life stage specific expression of a myosin heavy chaininthe hydrozoan Podocorynecarnea. Differentiation 54, 11-18 (1993).
3. Chapman, D. M. in Coelenterate Biology (eds Muscatine, L. & Lenhoff, H. M.) Ch. 1 1-93 (Academic, 1974).
4. Burton, P. M. Inisghts from diploblasts; the evolution of mesoderm and muscle. J. Exp. Zool. 308B, 1-10 (2007).
5. Schmidt-Rhaesa, A. The Evolution of Organ Systems 1st edn (Oxford Univ. Press, 2007).
6. Mackie, G. O., Mills, C. E. & Singla, C. L. Structure and functionoftheprehensiletentilla of Euplokamis (Ctenophora, Cydippida). Zoomorphology 107, 319-337 (1988).
7. Boelsterli, U. An electron microscopic study of early developmental stages, myogenesis, oogenesis, andcnidogenesisinthe anthomedusa, Podocorynecarnea M. Sars. J. Morphol. 154, 259-289 (1977).
8. Squire, J. M., Al-Khayat, H. A., Knupp, C. & Luther, P. K. Molecular architecture in muscle contractile assemblies. Adv. Protein Chem. 71, 17-87 (2005).
9. Hooper, S. L., Hobbs, K. H. & Thuma, J. B. Invertebrate muscles: thin and thick filament structure; molecular basis of contraction and its regulation, catch and asynchronous muscle. Prog. Neurobiol. 86, 72-127 (2008).
10. Kamm, K. E. & Stull, J. T. Dedicated myosin light chain kinases with diverse cellular functions. J. Biol. Chem. 276, 4527-4530 (2001).
11. Korn, E. D. Coevolution of head, neck, and tail domains of myosin heavy chains. Proc. Natl Acad. Sci. USA 97, 12559-12564 (2000).
12. Oota, S. & Saitou, N. Phylogenetic relationship of muscle tissues deduced from superimposition of gene trees. Mol. Biol. Evol. 16, 856-867 (1999).
13. Goodson, H. V. & Spudich, J. A. Molecular evolution of the myosin family: relationships derived from comparisons ofamino acid sequences. Proc. Natl Acad. Sci. USA 90, 659-663 (1993).
14. Vicente-Manzanares, M., Ma, X., Adelstein, R. S. & Horwitz, A. R. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nature Rev. Mol. Cell Biol. 10, 778-790 (2009).
15. Hooper, S. L. & Thuma, J. B. Invertebrate muscles: muscle specific genes and proteins. Physiol. Rev. 85, 1001-1060 (2005).
16. Nickel, M., Scheer, C., Hammel, J. U., Herzen, J. & Beckmann, F. The contractile sponge epithelium sensu lato-body contraction of the demosponge Tethya wilhelma is mediated by the pinacoderm. J. Exp. Biol. 214, 1692-1698 (2011).
17. Hammel, J. U. Zur Funktion des Wasserleitungssystems und der Entwicklung von Knospen in Schwämmen. Morphologische Grundlagen einer reversen Genetik. PhD thesis, Friedrich Schiller Univ. Jena (2010).
18. Adamska, M. et al. Structure and expression of conserved Wnt pathway components in the demosponge Amphimedon queenslandica. Evol. Dev. 12, 494-518 (2010).
19. Renfer, E., Amon-Hassenzahl, A., Steinmetz, P. R. & Technau, U. A muscle-specific transgenic reporter line of the sea anemone, Nematostella vectensis. Proc. Natl Acad. Sci. USA 107, 104-108 (2010).
20. Rui, Y., Bai, J. & Perrimon, N. Sarcomere formation occurs by the assembly of multiple latent protein complexes. PLoS Genet. 6, e1001208 (2010).
21. Sanger, J. M. & Sanger, J. W. The dynamic Z bands of striated muscle cells. Sci. Signal. 1, pe37 (2008).
22. Clark, K. A., McElhinny, A. S., Beckerle, M. C. & Gregorio, C. C. Striated muscle cytoarchitecture: an intricate web of form and function. Annu. Rev. Cell Dev. Biol. 18, 637-706 (2002).
23. Frank, D., Kuhn, C., Katus, H. A. & Frey, N. The sarcomeric Z-disc: a nodal point in signalling and disease. J. Mol. Med. 84, 446-468 (2006).
24. Martindale, M. Q., Pang, K. & Finnerty, J. R. Investigating the origins of triploblasty: 'mesodermal' gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum Cnidaria; class Anthozoa). Development 131, 2463-2474 (2004).
25. Ayme-Southgate, A. J., Southgate, R. J., Philipp, R. A., Sotka, E. E. & Kramp, C. The myofibrillar protein, projectin, is highly conserved across insect evolution except for its PEVK domain. J. Mol. Evol. 67, 653-669 (2008).
26. Kenny, P. A., Liston, E. M. & Higgins, D. G. Molecular evolution of immunoglobulin and fibronectin domains in titin and related muscle proteins. Gene 232, 11-23 (1999).
27. Sutter, S. B., Raeker, M. O., Borisov, A. B. & Russell, M. W. Orthologous relationship of obscurin and Unc-89:phylogenyofanovel familyoftandem myosin light chain kinases. Dev. Genes Evol. 214, 352-359 (2004).
28. Craig, R. & Woodhead, J. L. Structure and function of myosin filaments. Curr. Opin. Struct. Biol. 16, 204-212 (2006).
29. Torruella, G. et al. Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single-copy protein domains. Mol. Biol. Evol. 29, 531-544 (2012).
30. Philippe, H. et al. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19, 706-712 (2009).
31. Fritzenwanker, J. H. & Technau, U. Induction of gametogenesis in the basal cnidarian Nematostella vectensis. Dev. Genes Evol. 212, 99-103 (2002).
32. Chevalier, S., Martin, A., Leclere, L., Amiel, A. & Houliston, E. Polarised expression of FoxBand FoxQ2genesduringdevelopmentofthehydrozoanClytiahemisphaerica. Dev. Genes Evol. 216, 709-720 (2006).
33. Leys, S. P. & Degnan, B. M. Cytological basis of photoresponsive behavior in a sponge larva. Biol. Bull. 201, 323-338 (2001).
34. Sarà, M., Sarà, A., Nickel, M. & Brümmer, F. Three new species of Tethya (Porifera: Demospongiae) from German aquaria. Stuttg. Beitr. Naturkd. A 631, 1-15 (2001).
35. Nickel, M. Kinetics and rhythmofbody contractionsinthe sponge Tethya wilhelma (Porifera: Demospongiae). J. Exp. Biol. 207, 4515-4524 (2004).
36. Putnam, N. H. et al. The amphioxus genome and the evolution of the chordate karyotype. Nature 453, 1064-1071 (2008).
37. Putnam, N. H. et al. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86-94 (2007).
38. Chapman, J. A. et al. The dynamic genomeofHydra. Nature 464, 592-596 (2010).
39. Ryan, J. F. et al. The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa. Evodevo 1, 9 (2010).
40. Srivastava, M. et al. The Trichoplax genome and the nature of placozoans. Nature 454, 955-960 (2008).
41. Srivastava, M. et al. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466, 720-726 (2010).
42. King, N. et al. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451, 783-788 (2008).
43. Ruiz-Trillo, I. et al. The origins of multicellularity: a multi-taxon genome initiative. Trends Genet. 23, 113-118 (2007).
44. Merchant, S. S. et al. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245-250 (2007).
45. Banks, J. A. et al. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332, 960-963 (2011).
46. Eichinger, L. et al. The genome of the social amoeba Dictyostelium discoideum. Nature 435, 43-57 (2005).
47. Fritz-Laylin, L. K. et al. The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140, 631-642 (2010).
48. Fernandez-Fueyo, E. et al. Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis. Proc. Natl Acad. Sci. USA 109, 5458-5463 (2012).
49. Wood, V. et al. The genome sequenceofSchizosaccharomyces pombe. Nature 415, 871-880 (2002).
50. Burge, C. & Karlin, S. Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 268, 78-94 (1997).
51. Shinzato, C. et al. Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476, 320-323 (2011).
52. Hunter, S. et al. InterPro: the integrative protein signature database. Nucleic Acids Res. 37, D211-D215 (2009).
53. Finn, R. D. et al. The Pfam protein families database. Nucleic Acids Res. 38, D211-D222 (2009).
54. Lupas, A., Van Dyke, M. & Stock, J. Predicting coiled coils from protein sequences. Science 252, 1162-1164 (1991).
55. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
56. Castresana, J. Selectionofconserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540-552 (2000).
57. Abascal, F., Zardoya, R. & Posada, D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105 (2005).
58. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. The Clustal-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882 (1997).
59. Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3. 0. Syst. Biol. 59, 307-321 (2010).
60. Altekar, G., Dwarkadas, S., Huelsenbeck, J. P. & Ronquist, F. Parallel Metropolis-coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20, 407-415 (2004).
61. Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574 (2003).
62. Genikhovich, G. & Technau, U. In situ hybridization of starlet sea anemone (Nematostella vectensis) embryos, larvae, and polyps. Cold Spring Harb. Protoc. 2009, pdb. prot5282 (2009).
63. Larroux, C. et al. Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. Evol. Dev. 8, 150-173 (2006).
64. Larroux, C. et al. Whole-mount In situ hybridization in Amphimedon. Cold Spring Harb. Protoc. 2008, pdb. prot5096 (2008).
65. Hammel, J. U., Herzen, J., Beckmann, F. & Nickel, M. Sponge budding is a spatiotemporal morphological patterning process: insights from synchrotron radiation-based X-ray microtomography into the asexual reproduction of Tethya wilhelma. Front. Zool. 6, 19 (2009).
66. Weissenfels, N. Scanning electron microscope histology of spongy Ephydatia fluviatilis. Microsc. Acta 85, 345-350 (1982).
67. Nickel, M., Donath, T., Schweikert, M. & Beckmann, F. Functional morphology of Tethya species (Porifera): 1. Quantitative 3D-analysis of Tethya wilhelma by synchrotron radiation based X-ray microtomography. Zoomorphology 125, 209-223 (2006).