The impact of mitochondrial genome analyses on the understanding of deuterostome phylogeny

Molecular Phylogenetics and Evolution

Volumn 66, Issue 3, 2013, Pages 898-905

  Perseke, Marleen ^a,c   Golombek, Anja ^b,d   Schlegel, Martin ^a   Struck, Torsten H ^b,d  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY OF OSNABRÜCK   (Germany)

^c SOUTH CHINA SEA INSTITUTE OF OCEANOLOGY   (China)

^d ZOOLOGISCHES FORSCHUNGSMUSEUM ALEXANDER KOENIG   (Germany)

Author keywords

Ambulacraria; Chordata; Echinodermata; Mitochondrial genomes; Tunicata; Xenoturbella

Indexed keywords

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BIOLOGY; CHORDATA; CLASSIFICATION; ECHINODERM; GENETIC CODE; GENETICS; METHODOLOGY; MITOCHONDRIAL GENOME; PHYLOGENY; STATISTICAL MODEL;

ANIMALS; CHORDATA; CLASSIFICATION; COMPUTATIONAL BIOLOGY; ECHINODERMATA; GENETIC CODE; GENOME, MITOCHONDRIAL; LIKELIHOOD FUNCTIONS; MODELS, GENETIC; PHYLOGENY;

ANIMALIA; ASCIDIACEA; ASTEROIDEA; BILATERIA; CHORDATA; DEUTEROSTOMIA; ECHINODERMATA; ECHINOIDEA; OPHIUROIDEA; PTEROBRANCHIA; UROCHORDATA; VERTEBRATA; XENOTURBELLA;

EID: 84873107359     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2012.11.019     Document Type: Article

References (78)

1. Adoutte A., Balavoine G., Lartillot N., Lespinet O., Prud'homme B., de Rosa R. The new animal phylogeny: reliability and implications. Proc. Natl. Acad. Sci. USA 2000, 97:4453-4456.
2. Asakawa S., Himeno H., Miura K., Watanabe K. Nucleotide sequence and gene organization of the starfish Asterina pectinifera mitochondrial genome. Genetics 1995, 140:1047-1060.
3. Barnes R.D. Invertebrate Zoology 1968, WB Saunders Co., Philadelphia, PA.
4. Benito J., Pardos F. Hemichordata. Microscopic Anatomy of Invertebrates 1997, 15-101. Wiley Liss, New York. M.A. Harrison (Ed.).
5. Bernt M., Merkle D., Ramsch K., Fritzsch G., Perserke M., Bernhard D., Schlegel M., Stadler P., Middendorf M. CREx: inferring genomic rearrangements based on common intervals. Bioinformatics 2007, 23:2957-2958.
6. Bernt M., Bleidorn C., Braband A., Dambach J., Donath A., Fritzsch G., Golombek A., Hadrys H., Jühling F., Meusemann K., Middendorf M., Misof B., Perseke M., Podsiadlowski L., von Reumont B., Schierwater B., Schlegel M., Schrödl M., Simon S., Stadler P.F., Stöger I., Struck T.H. A comprehensive analysis of metazoan mitochondrial genomes and animal phylogeny. Mol. Phylogenet. Evol. 2013, 9:90-99. (in this special issue).
7. Bleidorn C., Eeckhaut I., Podsiadlowski L., Schult N., McHugh D., Halanych K.M., Milinkovitch M.C., Tiedemann R. Mitochondrial genome and nuclear sequence data support Myzostomida as part of the annelid radiation. Mol. Biol. Evol. 2007, 24:1690-1701.
8. Boore J.L. Animal mitochondrial genomes. Nucl. Acids Res. 1999, 27:1767-1780.
9. Bourlat S.J., Nielsen C., Lockyer A.E., Littlewood D.T.J., Telford M.J. Xenoturbella is a deuterostome that eats molluscs. Nature 2003, 424:925-928.
10. Bourlat S.J., Juliusdottir T., Lowe C.J., Freeman R., Aronowicz J., Kirschner M., Lander E.S., Thorndyke M., Nakano H., Kohn A.B., Heyland A., Moroz L.L., Copley R.R., Telford M.J. Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 2006, 444:85-88.
11. Bourlat S.J., Rota-Stabelli O., Lanfear R., Telford M.J. The mitochondrial genome structure of Xenoturbella bocki (phylum Xenoturbellida) is ancestral within the deuterostomes. BMC Evol. Biol. 2009, 9:107.
12. Brusca R.C., Brusca G.J. Invertebrates 1990, Sinauer Associates, Inc., Sunderland, Massachusetts. first ed.
13. Cameron C.B., Garey J.R., Swalla B.J. Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Proc. Natl. Acad. Sci. USA 2000, 97:4469-4474.
14. Cannon J.T., Rychel A.L., Eccleston H., Halanych K.M., Swalla B.J. Molecular phylogeny of hemichordata, with updated status of deep-sea enteropneusts. Mol. Phylogenet. Evol. 2009, 52:17-24.
15. Cantatore P., Roberti M., Loguercio Polosa P., Mustich A., Gadalet M.A. Mapping and characterization of Paracentrotus lividus mitochondrial transcripts: multiple and overlapping transcription units. Curr. Genet. 1990, 17:235-245.
16. Castresana J., Feldmaier-Fuchs G., Paabo S. Codon reassignment and amino acid composition in hemichordate mitochondria. Proc. Natl. Acad. Sci. USA 1998, 95:3703-3707.
17. Castresana J., Feldmaier-Fuchs G., Yokobori S.-i., Satoh N., Paabo S. The mitochondrial genome of the hemichordate Balanoglossus carnosus and the evolution of deuterostome mitochondria. Genetics 1998, 150:1115-1123.
18. Delsuc F., Brinkmann H., Chourrout D., Philippe H. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 2006, 439:965-968.
19. Drees A.W.M., Flamm C., Fritzsch G., Grünewald S., Kruspe M., Prohaska S.J., Stadler P.F. Noisy: identification of problematic columns in multiple sequence alignments. Algorithms Mol. Biol. 2008, 3:7.
20. Ehlers U., Sopott-Ehlers B. Ultrastructure of the subepidermal musculature of Xenoturbella bocki, the adelphotaxon of the Bilateria. Zoomorphology 1997, 117:71-79.
21. Fernandez-Silva P., Enriquez J.A., Montoya J. Replication and transcription of mammalian mitochondrial DNA. Exp. Physiol. 2003, 88:41-56.
22. Fritzsch G., Böhme M.U., Thorndyke M., Nakano H., Israelsson O., Stach T., Schlegel M., Hankeln T., Stadler P.F. PCR survey of Xenoturbella bocki Hox genes. J. Exp. Zool. (Mol Dev Evol) 2008, 310B:278-284.
23. Garstang W. The morphology of the Tunicata and its bearing on the phylogeny of the Chordata. Q. J. Microsc. Sci. 1928, 72:51-187.
24. Gilbert S.F. Developmental Biology 2000, Sinauer Associates, Sunderland, MA.
25. Gissi C., Pesole G., Mastrototaro F., Iannelli F., Guida V., Griggio F. Hypervariability of ascidian mitochondrial gene order: exposing the myth of deuterostome organelle genome stability. Mol. Biol. Evol. 2010, 27:211-215.
26. Halanych K.M. The phylogenetic position of the pterobranch hemichordates based on 18S rDNAsequence data. Mol. Phylogenet. Evol. 1995, 4:72-76.
27. Halanych K.M. The new view of animal phylogeny. Annu. Rev. Ecol. Evol. Syst. 2004, 35:229-256.
28. Hejnol A., Obst M., Stamatakis A., Ott M., Rouse G.W., Edgecombe G.D., Martinez P., Baguñà J., Bailly X., Jondelius U., Wiens M., Müller W.E.G., Seaver E., Wheeler W.C., Martindale M.Q., Giribet G., Dunn C.W. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc. Roy. Soc. B: Biol. Sci. 2009, 276:4261-4270.
29. Helfenbein K.G., Fourcade H.M., Vanjani R.G., Boore J.L. The mitochondrial genome of Paraspadella gotoi is highly reduced and reveals that chaetognaths are a sister group to protostomes. Proc. Natl. Acad. Sci. USA 2004, 101:10639-10643.
30. Israelsson O. and molluscan embryogenesis. Nature 1997, 390:32.
31. Ivanov V., Beniaminov A., Mikheyev A., Minyat E. A mechanism for stop codon recognition by the ribosome: a bioinformatic approach. RNA 2001, 7:1683-1692.
32. Janies D. Phylogenetic relationships of extant echinoderm classes. Can. J. Zool. 2001, 79:1232-1250.
33. Jeffrey W.R. Migratory neural crest-like cells form body pigmentation in a urochordate embryo. Nature 2004, 431:696-699.
34. Katoh K., Kuma K.-i., Toh H., Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucl. Acids Res. 2005, 33:511-518.
35. Kon T., Nohara M., Yamamoue Y., Fujiwara Y., Nishida M., Nishikawa T. Phylogenetic position of a whale-fall lancelet (Cephalochordata) inferred from whole mitochondrial genome sequences. BMC Evol. Biol. 2007, 7:127.
36. Kondow A., Suzuki T., Yokobori S.-i., Ueda T., Watanabe K. An extra tRNAGly(U*CU) found in ascidian mitochondria responsible for decoding non-universal codons AGA/AGG as glycine. Nucl. Acids Res. 1999, 27:2554-2559.
37. Lane N. Mitochondrial disease: powerhouse of disease. Nature 2006, 440:600-602.
38. Lavrov D.V., Lang B.F. Poriferan mtDNA and animal phylogeny based on mitochondrial gene arrangements. Syst. Biol. 2005, 54:651-659.
39. Littlewood D.T.J., Smith A.B., Clough K.A., Emson R.H. The interrelationships of the echinoderm classes: morphological and molecular evidence. Biol. J. Linn. Soc. Lond. 1997, 61:409-438.
40. Mallatt J., Winchell C.J. Ribosomal RNA genes and deuterostome phylogeny revisited: more cyclostomes, elasmobranchs, reptiles, and a brittle star. Mol. Phylogenet. Evol. 2007, 43:1005-1022.
41. Marletaz F., Martin E., Perez Y., Papillon D., Caubit X., Lowe C.J., Freeman B., Fasano L., Dossat C., Wincker P. Chaetognath phylogenomics: a protostome with deuterostome-like development. Curr. Biol. 2006, 16:R577-R578.
42. Matus D.Q., Copley R.R., Dunn C.W., Hejnol A., Eccleston H., Halanych K.M., Martindale M.Q., Telford M.J. Broad taxon and gene sampling indicate that chaetognaths are protostomes. Curr. Biol. 2006, 16:R575-R576.
43. Mayhook A.G., Rinaldi A.M., Jacobs H.T. Replication origins and pause sites in sea urchin mitochondrial DNA. Proc. Roy. Soc. Lond. B 1992, 248:85-94.
44. Metschnikoff V.E. über die systematische Stellung von Balanoglossus. Zool. Anz. 1881, 4:139-157.
45. Mwinyi A., Bailly X., Bourlat S.J., Jondelius U., Littlewood D.T.J., Podsiadlowski L. The phylogenetic position of Acoela as revealed by the complete mitochondrial geneome of Symsagittifera roscoffensis. BMC Evol. Biol. 2010, 10:309.
46. Nielsen C. After all: Xenoturbella is an acoelomorph!. Evol. Dev. 2010, 12:241-243.
47. Nohara M., Nishida M., Miya M.U., Nishikawa T. Evolution of the mitochondrial genome in cephalochordata as inferred from complete nucleotide sequences from two Epigonichthys species. J. Mol. Evol. 2005, 60:526-537.
48. Osawa S., Jukes S.T., Watanabe K., Muto A. Recent evidence for evolution of the genetic code. Microbiol. Rev. 1992, 56:229-264.
49. Perseke M., Hankeln T., Weich B., Fritzsch G., Stadler P., Israelsson O., Bernhard D., Schlegel M. The mitochondrial DNA of Xenoturbella bocki: genomic architecture and phylogenetic analysis. Theory Biosci. 2007, 126:35-42.
50. Perseke M., Bernhard D., Fritzsch G., Brümmer F., Stadler P.F., Schlegel M. Mitochondrial genome evolution in Ophiuroidea, Echinoidea, and Holothuroidea: insights in phylogenetic relationships of Echinodermata. Mol. Phylogenet. Evol. 2010, 56:201-211.
51. Perseke M., Hetmank J., Bernt M., Stadler P.F., Schlegel M., Bernhard D. The enigmatic mitochondrial genome of Rhabdopleura compacta (Pterobranchia) reveals insights into selection of an efficient tRNA system and supports monophyly of Ambulacraria. BMC Evol. Biol. 2011, 9:90-99.
52. Philippe H., Brinkmann H., Copley R.R., Moroz L.L., Nakano H., Poustka A.J., Wallberg A., Peterson K.J., Telford M.J. Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 2011, 470:255-258.
53. Putnam N.H., Butts T., Ferrier D.E.K., Furlong R.F., Hellsten U., Kawashima T., Robinson-Rechavi M., Shoguchi E., Terry A., Yu J.-K., Benito-Gutierrez E., Dubchak I., Garcia-Fernandez J., Gibson-Brown J.J., Grigoriev I.V., Horton A.C., de Jong P.J., Jurka J., Kapitonov V.V., Kohara Y., Kuroki Y., Lindquist E., Lucas S., Osoegawa K., Pennacchio L.A., Salamov A.A., Satou Y., Sauka-Spengler T., Schmutz J., Shin-I T., Toyoda A., Bronner-Fraser M., Fujiyama A., Holland L.Z., Holland P.W.H., Satoh N., Rokhsar D.S. The amphioxus genome and the evolution of the chordate karyotype. Nature 2008, 453:1064-1071.
54. Reisinger E. Was ist Xenoturbella?. Z. Wiss. Zool. 1960, 164:188-198.
55. Ruiz-Trillo I., Riutort M., Fourcade H.M., Baguna J., Boore J.L. Mitochondrial genome data support the basal position of Acoelomorpha and the polyphyly of the Platyhelminthes. Mol. Phylogenet. Evol. 2004, 33:321-332.
56. Schaeffer B. Deuterostome monophyly and phylogeny. Evol. Biol. 1987, 21:179-235.
57. Scouras A., Smith J.M. The complete mitochondrial genomes of the sea lily Gymnocrinus richeri and the feather star Phanogenia gracilis: signature nucleotide bias and unique nad4L gene rearrangement within crinoids. Mol. Phylogenet. Evol. 2006, 39:323-334.
58. Scouras A., Beckenbach K., Arndt A., Smith J.M. Complete mitochondrial genome DNA sequence for two ophiuroids and a holothuroid: the utility of protein gene sequence and gene maps in the analyses of deep deuterostome phylogeny. Mol. Phylogenet. Evol. 2004, 31:50-65.
59. Singh T.R., Tsagkogeorga G., Delsuc F., Blanquart S., Shenkar N., Loya Y., Douzery E.J.P., Huchon D. Tunicate mitogenomics and phylogenetics: peculiarities of the Herdmania momus mitochondrial genome and support for the new chordate phylogeny. BMC Genomics 2009, 10:534.
60. Sodergren E., Weinstock G.M., Davidson E.H., Cameron R.A., Gibbs R.A., Angerer R.C., Angerer L.M., Arnone M.I., Burgess D.R., Burke R.D., Coffman J.A., Dean M., Elphick M.R., Ettensohn C.A., Foltz K.R., Hamdoun A., Hynes R.O., Klein W.H., Marzluff W., McClay D.R., Morris R.L., Mushegian A., Rast J.P., Smith L.C., Thorndyke M.C., Vacquier V.D., Wessel G.M., Wray G., Zhang L., Elsik C.G., Ermolaeva O., Hlavina W., Hofmann G., Kitts P., Landrum M.J., Mackey A.J., Maglott D., Panopoulou G., Poustka A.J., Pruitt K., Sapojnikov V., Song X., Souvorov A., Solovyev V., Wei Z., Whittaker C.A., Worley K., Durbin K.J., Shen Y., Fedrigo O., Garfield D., Haygood R., Primus A., Satija R., Severson T., Gonzalez-Garay M.L., Jackson A.R., Milosavljevic A., Tong M., Killian C.E., Livingston B.T., Wilt F.H., Adams N., Bellé R., Carbonneau S., Cheung R., Cormier P., Cosson B., Croce J., Fernandez-Guerra A., Genevière A.-M., Goel M., Kelkar H., Morales J., Mulner-Lorillon O., Robertson A.J., Goldstone J.V., Cole B., Epel D., Gold B., Hahn M.E., Howard-Ashby M., Scally M., Stegeman J.J., Allgood E.L., Cool J., Judkins K.M., McCafferty S.S., Musante A.M., Obar R.A., Rawson A.P., Rossetti B.J., Gibbons I.R., Hoffman M.P., Leone A., Istrail S., Materna S.C., Samanta M.P., Stolc V., Tongprasit W., Tu Q., Bergeron K.-F., Brandhorst B.P., Whittle J., Berney K., Bottjer D.J., Calestani C., Peterson K., Chow E., Yuan Q.A., Elhaik E., Graur D., Reese J.T., Bosdet I., Heesun S., Marra M.A., Schein J., Anderson M.K., Brockton V., Buckley K.M., Cohen A.H., Fugmann S.D., Hibino T., Loza-Coll M., Majeske A.J., Messier C., Nair S.V., Pancer Z., Terwilliger D.P., Agca C., Arboleda E., Chen N., Churcher A.M., Hallböök F., Humphrey G.W., Idris M.M., Kiyama T., Liang S., Mellott D., Mu X., Murray G., Olinski R.P., Raible F., Rowe M., Taylor J.S., Tessmar-Raible K., Wang D., Wilson K.H., Yaguchi S., Gaasterland T., Galindo B.E., Gunaratne H.J., Juliano C., Kinukawa M., Moy G.W., Neill A.T., Nomura M., Raisch M., Reade A., Roux M.M., Song J.L., Su Y.-H., Townley I.K., Voronina E., Wong J.L., Amore G., Branno M., Brown E.R., Cavalieri V., Duboc V., Duloquin L., Flytzanis C., Gache C., Lapraz F., Lepage T., Locascio A., Martinez P., Matassi G., Matranga V., Range R., Rizzo F., Röttinger E., Beane W., Bradham C., Byrum C., Glenn T., Hussain S., Manning G., Miranda E., Thomason R., Walton K., Wikramanayke A., Wu S.-Y., Xu R., Brown C.T., Chen L., Gray R.F., Lee P.Y., Nam J., Oliveri P., Smith J., Muzny D., Bell S., Chacko J., Cree A., Curry S., Davis C., Dinh H., Dugan-Rocha S., Fowler J., Gill R., Hamilton C., Hernandez J., Hines S., Hume J., Jackson L., Jolivet A., Kovar C., Lee S., Lewis L., Miner G., Morgan M., Nazareth L.V., Okwuonu G., Parker D., Pu L.-L., Thorn R., Wright R. The genome of the sea urchin Strongylocentrotus purpuratus. Science 2006, 314:941-952.
61. Stach T. Chordate phylogeny and evolution: a not so simple three-taxon problem. J. Zool. 2008, 276:117-141.
62. Stach T. Anatomy of the trunk mesoderm in tunicates: homology considerations and phylogenetic interpretation. Zoomorphology 2009, 128:97-109.
63. Stach T., Kirbach A. Larval convergence in a colonial tunicate: the organization of the sarcotubular complex in Ecteinascidia turbinata (Perophoridae, Phlebobranchiata, Tunicata, Chordata). Zoomorphology 2009, 128:1-11.
64. Stach T., Turbeville J.M. Phylogeny of Tunicata inferred from molecular and morphological characters. Mol. Phylogenet. Evol. 2002, 25:408-428.
65. Stach T., Dupont S., Israelsson O., Fauville G., Nakano H., Kånneby T., Horndyke M. Nerve cells of Xenoturbella bocki (phylum uncertain) and Harrimania kupfferi (Enteropneusta) are positively immunireactive to antibodies raised against echinoderm neuropeptids. J. Mar. Biol. Assoc. UK 2005, 85:1519-1524.
66. Stach T., Braband A., Podsiadlowski L. Erosion of phylogenetic signal in tunicate mitochondrial genomes on different levels of analysis. Mol. Phylogenet. Evol. 2010, 55:860-870.
67. Stamatakis A., Hoover P., Rougemont J. A rapid bootstrap algorithm for the RAxML web-servers. Syst. Biol. 2008, 75:758-771.
68. Stechmann A., Schlegel M. Analysis of the complete mitochondrial DNA sequence of the brachiopod Terebratulina retusa places Brachiopoda within the protostomes. Proc. Roy. Soc. B: Biol. Sci. 1999, 266:1-10.
69. Swalla B.J. Building divergent body plans with similar genetic pathways. Heredity 2006, 97:235-243.
70. Swalla B.J., Smith A.B. Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Philos. Trans. Roy. Soc. Lond. B. Biol. Sci. 2008, 363:1557-1568.
71. Swalla B.J., Cameron C.B., Corley L.S., Garey J.R. Urochordates are monophyletic within the deuterostomes. Syst. Biol. 2000, 49:52-64.
72. Tsagkogeorga G., Turon X., Hopcroft R., Tilak M.-K., Feldstein T., Shenkar N., Loya Y., Huchon D., Douzery E., Delsuc F. An updated 18S rRNA phylogeny of tunicates based on mixture and secondary structure models. BMC Evol. Biol. 2009, 9:187.
73. Tsagkogeorga G., Turon X., Galtier N., Douzery E., Delsuc F. Accelerated evolutionary rate of housekeeping genes in tunicates. J. Mol. Evol. 2010, 71:153-167.
74. Watterson W.A., Ewens W.J., Hall T.E., Morgan A. The chromosome inversion problem, J. Theor. Biol. 1982, 99:1-7.
75. Westblad E. Xenoturbella bocki n.g, n.sp, a peculiar, primitive turbellarian type. Ark. Zool. 1949, 1:3-29.
76. Winchell C.J., Sullivan J., Cameron C.B., Swalla B.J., Mallatt J. Evaluating hypotheses of deuterostome phylogeny and chordate evolution with new LSU and SSU ribosomal DNA data. Mol. Biol. Evol. 2002, 19:762-776.
77. Zeng L., Jacobs M.W., Swalla B.J. Coloniality has evolved once in stolidobranch ascidians. Integr. Comp. Biol. 2006, 46:255-268.
78. Zimmer R.L. Morphological and developmental affinities of the lophophorates. Living and Fossil Bryozoa 1973, 593-599. Academic Press, New York. G.P. Larwood (Ed.).