Accelerated evolutionary rate of housekeeping genes in tunicates

Journal of Molecular Evolution

Volumn 71, Issue 2, 2010, Pages 153-167

  Tsagkogeorga, Georgia ^a   Turon, Xavier ^b   Galtier, Nicolas ^a   Douzery, Emmanuel J P ^a   Delsuc, Frédéric ^a  

^a UNIV MONTPELLIER   (France)

^b CENTRE D ESTUDIS AVANÇATS DE BLANES CEAB CSIC   (Spain)

Author keywords

454 sequencing; Chordates; Evolutionary rate; Microcosmus squamiger; Molecular evolution; Oikopleura dioica; Phylogenomics; Urochordates

Indexed keywords

AMINO ACID SUBSTITUTION; ANIMAL; ARTICLE; COMPARATIVE STUDY; GENE; GENE EXPRESSION PROFILING; GENETICS; MISSENSE MUTATION; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE HOMOLOGY; UROCHORDATA; VERTEBRATE;

AMINO ACID SUBSTITUTION; ANIMALS; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENES; MUTATION, MISSENSE; PHYLOGENY; SEQUENCE HOMOLOGY; UROCHORDATA; VERTEBRATES;

APLOUSOBRANCHIA; BILATERIA; CHORDATA; MICROCOSMUS SQUAMIGER; OIKOPLEURA DIOICA; UROCHORDATA; VERTEBRATA;

EID: 77956059445     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-010-9372-9     Document Type: Article

References (79)

1. SF Altschul W Gish W Miller EW Myers DJ Lipman 1990 Basic local alignment search tool J Mol Biol 215 403 410 2231712
2. M Ashburner CA Ball JA Blake D Botstein H Butler JM Cherry AP Davis K Dolinski SS Dwight JT Eppig MA Harris DP Hill L Issel-Tarver A Kasarskis S Lewis JC Matese JE Richardson M Ringwald GM Rubin G Sherlock 2000 Gene ontology: tool for the unification of biology. The Gene Ontology Consortium Nat Genet 25 25 29 10.1038/75556 10802651
3. Blaxter M, Thomas J (2004) A survey of genes expressed in the seasquirt Diplosoma listerianum. Unpublished
4. A Boorsma BC Foat D Vis F Klis HJ Bussemaker 2005 T-profiler: scoring the activity of predefined groups of genes using gene expression data Nucleic Acids Res 33 W592 W595 10.1093/nar/gki484 15980543
5. SJ Bourlat T Juliusdottir CJ Lowe R Freeman J Aronowicz M Kirschner ES Lander M Thorndyke H Nakano AB Kohn A Heyland LL Moroz RR Copley MJ Telford 2006 Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida Nature 444 85 88 10.1038/nature05241 17051155
6. SJ Bourlat C Nielsen AD Economou MJ Telford 2008 Testing the new animal phylogeny: a phylum level molecular analysis of the animal kingdom Mol Phylogenet Evol 49 23 31 10.1016/j.ympev.2008.07.008 18692145
7. CB Cameron JR Garey BJ Swalla 2000 Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla Proc Natl Acad Sci USA 97 4469 4474 10.1073/pnas.97.9.4469 10781046
8. C Cañestro JH Postlethwait 2007 Development of a chordate anterior-posterior axis without classical retinoic acid signaling Dev Biol 305 522 538 10.1016/j.ydbio.2007.02.032 17397819
9. C Cañestro S Bassham JH Postlethwait 2003 Seeing chordate evolution through the Ciona genome sequence Genome Biol 4 208 10.1186/gb-2003-4-3-208 12620098
10. J Castresana 2000 Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis Mol Biol Evol 17 540 552 10742046
11. B Charlesworth 2009 Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation Nat Rev Genet 10 195 205 10.1038/nrg2526 19204717
12. AC Cone RW Zeller 2005 Using ascidian embryos to study the evolution of developmental gene regulatory networks Can J Zool 83 75 89 10.1139/z04-165
13. B Davidson 2007 Ciona intestinalis as a model for cardiac development Semin Cell Dev Biol 18 16 26 10.1016/j.semcdb.2006.12.007 17223594
14. P Dehal JL Boore 2005 Two rounds of whole genome duplication in the ancestral vertebrate PLoS Biol 3 e314 10.1371/journal.pbio.0030314 16128622
15. P Dehal Y Satou RK Campbell J Chapman B Degnan A De Tomaso B Davidson A Di Gregorio M Gelpke DM Goodstein N Harafuji KE Hastings I Ho K Hotta W Huang T Kawashima P Lemaire D Martinez IA Meinertzhagen S Necula M Nonaka N Putnam S Rash H Saiga M Satake A Terry L Yamada HG Wang S Awazu K Azumi J Boore M Branno S Chin-Bow R DeSantis S Doyle P Francino DN Keys S Haga H Hayashi K Hino KS Imai K Inaba S Kano K Kobayashi M Kobayashi BI Lee KW Makabe C Manohar G Matassi M Medina Y Mochizuki S Mount T Morishita S Miura A Nakayama S Nishizaka H Nomoto F Ohta K Oishi I Rigoutsos M Sano A Sasaki Y Sasakura E Shoguchi T Shin-i A Spagnuolo D Stainier MM Suzuki O Tassy N Takatori M Tokuoka K Yagi F Yoshizaki S Wada C Zhang PD Hyatt F Larimer C Detter N Doggett T Glavina T Hawkins P Richardson S Lucas Y Kohara M Levine N Satoh DS Rokhsar 2002 The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins Science 298 2157 2167 10.1126/science.1080049 12481130
16. F Delsuc H Brinkmann D Chourrout H Philippe 2006 Tunicates and not cephalochordates are the closest living relatives of vertebrates Nature 439 965 968 10.1038/nature04336 16495997
17. F Delsuc G Tsagkogeorga N Lartillot H Philippe 2008 Additional molecular support for the new chordate phylogeny Genesis 46 592 604 10.1002/dvg.20450 19003928
18. N Donmez GA Bazykin M Brudno AS Kondrashov 2009 Polymorphism due to multiple amino acid substitutions at a codon site within Ciona savignyi Genetics 181 685 690 10.1534/genetics.108.097535 19087959
19. Douzery EJ, Snell EA, Bapteste E, Delsuc F, Philippe H (2004) The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils? Proc Natl Acad Sci USA 101:15386-15391
20. CW Dunn A Hejnol DQ Matus K Pang WE Browne SA Smith E Seaver GW Rouse M Obst GD Edgecombe MV Sorensen SH Haddock A Schmidt-Rhaesa A Okusu RM Kristensen WC Wheeler MQ Martindale G Giribet 2008 Broad phylogenomic sampling improves resolution of the animal tree of life Nature 452 745 749 10.1038/nature06614 18322464
21. RB Edvardsen E Lerat AD Maeland M Flat R Tewari MF Jensen H Lehrach R Reinhardt HC Seo D Chourrout 2004 Hypervariable and highly divergent intron-exon organizations in the chordate Oikopleura dioica J Mol Evol 59 448 457 10.1007/s00239-004-2636-5 15638456
22. J Felsenstein 1981 Evolutionary trees from DNA sequences: a maximum likelihood approach J Mol Evol 17 368 376 10.1007/BF01734359 7288891
23. Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) In: Department of genome sciences UoW (ed), Seattle
24. C Gissi G Pesole E Cattaneo M Tartari 2006 Huntingtin gene evolution in Chordata and its peculiar features in the ascidian Ciona genus BMC Genomics 7 288 10.1186/1471-2164-7-288 17092333
25. C Gissi F Iannelli G Pesole 2008 Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species Heredity 101 301 320 10.1038/hdy.2008.62 18612321
26. N Goldman Z Yang 1994 A codon-based model of nucleotide substitution for protein-coding DNA sequences Mol Biol Evol 11 725 736 7968486
27. JV Goldstone HM Goldstone AM Morrison A Tarrant SE Kern BR Woodin JJ Stegeman 2007 Cytochrome P450 1 genes in early deuterostomes (tunicates and sea urchins) and vertebrates (chicken and frog): origin and diversification of the CYP1 gene family Mol Biol Evol 24 2619 2631 10.1093/molbev/msm200 17916789
28. S Guindon O Gascuel 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood Syst Biol 52 696 704 10.1080/10635150390235520 14530136
29. F Gyoja Y Satou T Shin-i Y Kohara BJ Swalla N Satoh 2007 Analysis of large scale expression sequenced tags (ESTs) from the anural ascidian, Molgula tectiformis Dev Biol 307 460 482 10.1016/j.ydbio.2007.03.035 17540363
30. A Hejnol M Obst A Stamatakis M Ott GW Rouse GD Edgecombe P Martinez J Baguna X Bailly U Jondelius M Wiens WE Muller E Seaver WC Wheeler MQ Martindale G Giribet CW Dunn 2009 Assessing the root of bilaterian animals with scalable phylogenomic methods Proc Biol Sci 276 4261 4270 10.1098/rspb.2009.0896 19759036
31. LZ Holland JJ Gibson-Brown 2003 The Ciona intestinalis genome: when the constraints are off Bioessays 25 529 532 10.1002/bies.10302 12766941
32. X Huang A Madan 1999 CAP3: a DNA sequence assembly program Genome Res 9 868 877 10.1101/gr.9.9.868 10508846
33. T Ikuta N Yoshida N Satoh H Saiga 2004 Ciona intestinalis Hox gene cluster: its dispersed structure and residual colinear expression in development Proc Natl Acad Sci USA 101 15118 15123 10.1073/pnas.0401389101 15469921
34. KS Imai M Levine N Satoh Y Satou 2006 Regulatory blueprint for a chordate embryo Science 312 1183 1187 10.1126/science.1123404 16728634
35. G Jobb A von Haeseler K Strimmer 2004 TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics BMC Evol Biol 4 18 10.1186/1471-2148-4-18 15222900
36. K Katoh K Kuma H Toh T Miyata 2005 MAFFT version 5: improvement in accuracy of multiple sequence alignment Nucleic Acids Res 33 511 518 10.1093/nar/gki198 15661851
37. YO Kim HK Cho EM Park BH Nam YB Hur SJ Lee J Cheong 2008 Generation of expressed sequence tags for immune gene discovery and marker development in the sea squirt, Halocynthia roretzi J Microbiol Biotechnol 18 1510 1517 18852505
38. JH Kim MS Waterman LM Li 2007 Diploid genome reconstruction of Ciona intestinalis and comparative analysis with Ciona savignyi Genome Res 17 1101 1110 10.1101/gr.5894107 17567986
39. S Kimbacher I Gerstl B Velimirov S Hagemann 2009 Drosophila P transposons of the urochordata Ciona intestinalis Mol Genet Genomics 282 165 172 10.1007/s00438-009-0453-7 19424726
40. A Kowalevski 1868 Beiträge zur Entwicklungsgeschichte der Tunicaten Nachrichten Gesellschaft Wissenschaften Göttingen 19 401 415
41. S Kryazhimskiy JB Plotkin 2008 The population genetics of dN/dS PLoS Genet 4 e1000304 10.1371/journal.pgen.1000304 19081788
42. C Lambert 2005 Historical introduction, overview, and reproductive biology of the protochordates Can J Zool 83 1 7 10.1139/z04-160
43. N Lartillot H Philippe 2004 A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process Mol Biol Evol 21 1095 1109 10.1093/molbev/msh112 15014145
44. N Lartillot T Lepage S Blanquart 2009 PhyloBayes 3. A Bayesian software package for phylogenetic reconstruction and molecular dating Bioinformatics 25 2286 2288 10.1093/bioinformatics/btp368 19535536
45. SQ Le O Gascuel N Lartillot 2008 Empirical profile mixture models for phylogenetic reconstruction Bioinformatics 24 2317 2323 10.1093/bioinformatics/ btn445
46. J Mallatt CJ Winchell 2007 Ribosomal RNA genes and deuterostome phylogeny revisited: more cyclostomes, elasmobranchs, reptiles, and a brittle star Mol Phylogenet Evol 43 1005 1022 10.1016/j.ympev.2006.11.023 17276090
47. M Margulies M Egholm WE Altman S Attiya JS Bader LA Bemben J Berka MS Braverman YJ Chen Z Chen SB Dewell L Du JM Fierro XV Gomes BC Godwin W He S Helgesen CH Ho GP Irzyk SC Jando ML Alenquer TP Jarvie KB Jirage JB Kim JR Knight JR Lanza JH Leamon SM Lefkowitz M Lei J Li KL Lohman H Lu VB Makhijani KE McDade MP McKenna EW Myers E Nickerson JR Nobile R Plant BP Puc MT Ronan GT Roth GJ Sarkis JF Simons JW Simpson M Srinivasan KR Tartaro A Tomasz KA Vogt GA Volkmer SH Wang Y Wang MP Weiner P Yu RF Begley JM Rothberg 2005 Genome sequencing in microfabricated high-density picolitre reactors Nature 437 376 380 16056220
48. B Nabholz S Glemin N Galtier 2008 Strong variations of mitochondrial mutation rate across mammals-the longevity hypothesis Mol Biol Evol 25 120 130 10.1093/molbev/msm248 17998254
49. E Paradis J Claude K Strimmer 2004 APE: analyses of phylogenetics and evolution in R language Bioinformatics 20 289 290 10.1093/bioinformatics/btg412 14734327
50. R Perez-Portela JD Bishop AR Davis X Turon 2009 Phylogeny of the families Pyuridae and Styelidae (Stolidobranchiata, Ascidiacea) inferred from mitochondrial and nuclear DNA sequences Mol Phylogenet Evol 50 560 570 10.1016/j.ympev.2008.11.014 19059353
51. H Philippe U Sorhannus A Baroin R Perasso F Gasse A Adoutte 1994 Comparison of molecular and paleontological data in diatoms suggests a major gap in the fossil record J Evol Biol 7 247 265 10.1046/j.1420-9101.1994.7020247.x
52. NH Putnam T Butts DE Ferrier RF Furlong U Hellsten T Kawashima M Robinson-Rechavi E Shoguchi A Terry JK Yu EL Benito-Gutierrez I Dubchak J Garcia-Fernandez JJ Gibson-Brown IV Grigoriev AC Horton PJ de Jong J Jurka VV Kapitonov Y Kohara Y Kuroki E Lindquist S Lucas K Osoegawa LA Pennacchio AA Salamov Y Satou T Sauka-Spengler J Schmutz IT Shin A Toyoda M Bronner-Fraser A Fujiyama LZ Holland PW Holland N Satoh DS Rokhsar 2008 The amphioxus genome and the evolution of the chordate karyotype Nature 453 1064 1071 10.1038/nature06967 18563158
53. Rius M, Pascual M, Turon X (2008) Phylogeography of the widespread marine invader Microcosmus squamiger (Ascidiacea) reveals high genetic diversity of introduced populations and non-independent colonizations. Divers Distrib 14
54. M Rius X Turon DJ Marshall 2009 Non-lethal effects of an invasive species in the marine environment: the importance of early life-history stages Oecologia 159 873 882 10.1007/s00442-008-1256-y 19156442
55. N Satoh 2003 The ascidian tadpole larva: comparative molecular development and genomics Nat Rev Genet 4 285 295 10.1038/nrg1042 12671659
56. HC Seo M Kube RB Edvardsen MF Jensen A Beck E Spriet G Gorsky EM Thompson H Lehrach R Reinhardt D Chourrout 2001 Miniature genome in the marine chordate Oikopleura dioica Science 294 2506 10.1126/science.294.5551.2506 11752568
57. HC Seo RB Edvardsen AD Maeland M Bjordal MF Jensen A Hansen M Flaat J Weissenbach H Lehrach P Wincker R Reinhardt D Chourrout 2004 Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica Nature 431 67 71 10.1038/nature02709 15343333
58. J Shendure H Ji 2008 Next-generation DNA sequencing Nat Biotechnol 26 1135 1145 10.1038/nbt1486 18846087
59. N Sierro T Kusakabe KJ Park R Yamashita K Kinoshita K Nakai 2006 DBTGR: a database of tunicate promoters and their regulatory elements Nucleic Acids Res 34 D552 D555 10.1093/nar/gkj064 16381930
60. TR Singh G Tsagkogeorga F Delsuc S Blanquart N Shenkar Y Loya EJ Douzery D Huchon 2009 Tunicate mitogenomics and phylogenetics: peculiarities of the Herdmania momus mitochondrial genome and support for the new chordate phylogeny BMC Genomics 10 534 10.1186/1471-2164-10-534 19922605
61. KS Small M Brudno MM Hill A Sidow 2007 Extreme genomic variation in a natural population Proc Natl Acad Sci USA 104 5698 5703 10.1073/pnas.0700890104 17372217
62. KS Small M Brudno MM Hill A Sidow 2007 A haplome alignment and reference sequence of the highly polymorphic Ciona savignyi genome Genome Biol 8 R41 10.1186/gb-2007-8-3-r41 17374142
63. BJ Swalla J Xavier-Neto 2008 Chordate origins and evolution Genesis 46 575 579 10.1002/dvg.20477 19003925
64. BJ Swalla CB Cameron LS Corley JR Garey 2000 Urochordates are monophyletic within the deuterostomes Syst Biol 49 52 64 10.1080/ 10635150050207384 12116483
65. Swofford D (2002) PAUP. Phylogenetic analysis using parsimony (and other methods). Sinauer Associates Sunderland, Massachusetts
66. K Tamura J Dudley M Nei S Kumar 2007 MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0 Mol Biol Evol 24 1596 1599 10.1093/molbev/msm092 17488738
67. MJ Telford 2006 Animal phylogeny Curr Biol 16 R981 R985 10.1016/j.cub.2006.10.048 17141601
68. The R Development CoreTeam (2004) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
69. JL Thorne H Kishino IS Painter 1998 Estimating the rate of evolution of the rate of molecular evolution Mol Biol Evol 15 1647 1657 9866200
70. G Tsagkogeorga X Turon RR Hopcroft MK Tilak T Feldstein N Shenkar Y Loya D Huchon EJ Douzery F Delsuc 2009 An updated 18S rRNA phylogeny of tunicates based on mixture and secondary structure models BMC Evol Biol 9 187 10.1186/1471-2148-9-187 19656395
71. X Turon S Lopez-Legentil 2004 Ascidian molecular phylogeny inferred from mtDNA data with emphasis on the Aplousobranchiata Mol Phylogenet Evol 33 309 320 10.1016/j.ympev.2004.06.011 15336666
72. CJ Winchell J Sullivan CB Cameron BJ Swalla J Mallatt 2002 Evaluating hypotheses of deuterostome phylogeny and chordate evolution with new LSU and SSU ribosomal DNA data Mol Biol Evol 19 762 776 11961109
73. JB Wolf A Kunstner K Nam M Jakobsson H Ellegren 2009 Nonlinear dynamics of nonsynonymous (dN) and synonymous (dS) substitution rates affects inference of selection Genome Biol Evol 2009 308 319
74. M Yandell CJ Mungall C Smith S Prochnik J Kaminker G Hartzell S Lewis GM Rubin 2006 Large-scale trends in the evolution of gene structures within 11 animal genomes PLoS Comput Biol 2 e15 10.1371/journal.pcbi.0020015 16518452
75. Z Yang 2007 PAML 4: phylogenetic analysis by maximum likelihood Mol Biol Evol 24 1586 1591 10.1093/molbev/msm088 17483113
76. Z Yang R Nielsen N Goldman AM Pedersen 2000 Codon-substitution models for heterogeneous selection pressure at amino acid sites Genetics 155 431 449 10790415
77. S Yokobori A Kurabayashi BA Neilan T Maruyama E Hirose 2006 Multiple origins of the ascidian-Prochloron symbiosis: molecular phylogeny of photosymbiotic and non-symbiotic colonial ascidians inferred from 18S rDNA sequences Mol Phylogenet Evol 40 8 19 10.1016/j.ympev.2005.11.025 16531073
78. L Zeng B Swalla 2005 Molecular phylogeny of the protochordates: chordate evolution Can J Zool 83 24 33 10.1139/z05-010
79. L Zeng M Jacobs B Swalla 2006 Coloniality and sociality has evolved once in Stolidobranch ascidians Integr Comp Biol 46 255 268 10.1093/icb/icj035