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PMID: 24337300 Published · ppublish English Journal Article Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution.

Science (New York, N.Y.) ·Vol. 342 ·No. 6164 ·2013-12-13 ·Pages 1242592

Ryan JF, Pang K, Schnitzler CE, Nguyen AD, Moreland RT, Simmons DK, Koch BJ, Francis WR, Havlak P, NISC Comparative Sequencing Program, Smith SA, Putnam NH, Haddock SH, Dunn CW, Wolfsberg TG, Mullikin JC, Martindale MQ, Baxevanis AD

Abstract

An understanding of ctenophore biology is critical for reconstructing events that occurred early in animal evolution. Toward this goal, we have sequenced, assembled, and annotated the genome of the ctenophore Mnemiopsis leidyi. Our phylogenomic analyses of both amino acid positions and gene content suggest that ctenophores rather than sponges are the sister lineage to all other animals. Mnemiopsis lacks many of the genes found in bilaterian mesodermal cell types, suggesting that these cell types evolved independently. The set of neural genes in Mnemiopsis is similar to that of sponges, indicating that sponges may have lost a nervous system. These results present a newly supported view of early animal evolution that accounts for major losses and/or gains of sophisticated cell types, including nerve and muscle cells.

MeSH Terms
Animals Base Sequence Biological Evolution Cell Lineage/genetics Ctenophora/classification,cytology,genetics Genome Mesoderm/cytology Molecular Sequence Data Muscle Development/genetics Neurogenesis/genetics Phylogeny
Authors & Affiliations
18 authors, click to expand affiliations / ORCID
Ryan Joseph F
Genome Technology Branch, Division of Intramural Research, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD 20892, USA.
Pang Kevin
Schnitzler Christine E
Nguyen Anh-Dao
Moreland R Travis
Simmons David K
Koch Bernard J
Francis Warren R
Havlak Paul
NISC Comparative Sequencing Program
Smith Stephen A
Putnam Nicholas H
Haddock Steven H D
Dunn Casey W
Wolfsberg Tyra G
Mullikin James C
Martindale Mark Q
Baxevanis Andreas D
References (46)
46 references, click to expand
  1. CONSEL: for assessing the confidence of phylogenetic tree selection.
    Bioinformatics. 2001 Dec;17(12):1246-7 PMID: 11751242
  2. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization.
    Science. 2007 Jul 6;317(5834):86-94 PMID: 17615350
  3. Broad phylogenomic sampling improves resolution of the animal tree of life.
    Nature. 2008 Apr 10;452(7188):745-9 PMID: 18322464
  4. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating.
    Bioinformatics. 2009 Sep 1;25(17):2286-8 PMID: 19535536
  5. New insights on ctenophore neural anatomy: immunofluorescence study in Pleurobrachia pileus (Müller, 1776).
    J Exp Zool B Mol Dev Evol. 2011 May 15;316B(3):171-87 PMID: 21462312
  6. Intracellular fate mapping in a basal metazoan, the ctenophore Mnemiopsis leidyi, reveals the origins of mesoderm and the existence of indeterminate cell lineages.
    Dev Biol. 1999 Oct 15;214(2):243-57 PMID: 10525332
  7. Lim homeobox genes in the Ctenophore Mnemiopsis leidyi: the evolution of neural cell type specification.
    Evodevo. 2012 Jan 13;3(1):2 PMID: 22239757
  8. Evolution of the TGF-β signaling pathway and its potential role in the ctenophore, Mnemiopsis leidyi.
    PLoS One. 2011;6(9):e24152 PMID: 21931657
  9. Genomic insights into Wnt signaling in an early diverging metazoan, the ctenophore Mnemiopsis leidyi.
    Evodevo. 2010 Oct 04;1(1):10 PMID: 20920349
  10. Deep metazoan phylogeny: when different genes tell different stories.
    Mol Phylogenet Evol. 2013 Apr;67(1):223-33 PMID: 23353073
  11. The Trichoplax genome and the nature of placozoans.
    Nature. 2008 Aug 21;454(7207):955-60 PMID: 18719581
  12. The phusion assembler.
    Genome Res. 2003 Jan;13(1):81-90 PMID: 12529309
  13. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation.
    Nat Biotechnol. 2010 May;28(5):511-5 PMID: 20436464
  14. Nuclear receptors from the ctenophore Mnemiopsis leidyi lack a zinc-finger DNA-binding domain: lineage-specific loss or ancestral condition in the emergence of the nuclear receptor superfamily?
    Evodevo. 2011 Feb 03;2(1):3 PMID: 21291545
  15. Full-length transcriptome assembly from RNA-Seq data without a reference genome.
    Nat Biotechnol. 2011 May 15;29(7):644-52 PMID: 21572440
  16. The nervous system of ctenophores. III. Ultrastructure of synapses.
    J Neurocytol. 1973 Sep;2(3):249-63 PMID: 9224490
  17. The evolution of signalling pathways in animal development.
    Nat Rev Genet. 2003 Jan;4(1):39-49 PMID: 12509752
  18. Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes.
    BMC Biol. 2012 Dec 21;10:107 PMID: 23259493
  19. Evolution of sodium channels predates the origin of nervous systems in animals.
    Proc Natl Acad Sci U S A. 2011 May 31;108(22):9154-9 PMID: 21576472
  20. The dynamic genome of Hydra.
    Nature. 2010 Mar 25;464(7288):592-6 PMID: 20228792
  21. Concatenated analysis sheds light on early metazoan evolution and fuels a modern "urmetazoon" hypothesis.
    PLoS Biol. 2009 Jan 27;7(1):e20 PMID: 19175291
  22. The Radiata and the evolutionary origins of the bilaterian body plan.
    Mol Phylogenet Evol. 2002 Sep;24(3):358-65 PMID: 12220977
  23. Rapid evolution of the compact and unusual mitochondrial genome in the ctenophore, Pleurobrachia bachei.
    Mol Phylogenet Evol. 2012 Apr;63(1):203-7 PMID: 22201557
  24. Mnemiopsis leidyi Spawning and Embryo Collection.
    CSH Protoc. 2008 Nov 01;2008:pdb.prot5085 PMID: 21356725
  25. Regulation and regeneration in the ctenophore Mnemiopsis leidyi.
    Dev Biol. 2000 Nov 15;227(2):720-33 PMID: 11071786
  26. OrthoMCL: identification of ortholog groups for eukaryotic genomes.
    Genome Res. 2003 Sep;13(9):2178-89 PMID: 12952885
  27. Near intron pairs and the metazoan tree.
    Mol Phylogenet Evol. 2013 Mar;66(3):811-23 PMID: 23201572
  28. Phylogenomics revives traditional views on deep animal relationships.
    Curr Biol. 2009 Apr 28;19(8):706-12 PMID: 19345102
  29. The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa.
    Evodevo. 2010 Oct 04;1(1):9 PMID: 20920347
  30. A receptor tyrosine kinase from choanoflagellates: molecular insights into early animal evolution.
    Proc Natl Acad Sci U S A. 2001 Dec 18;98(26):15032-7 PMID: 11752452
  31. Expression and phylogenetic analysis of the zic gene family in the evolution and development of metazoans.
    Evodevo. 2010 Nov 05;1(1):12 PMID: 21054859
  32. The evolution of the serotonergic nervous system.
    Proc Biol Sci. 2000 Jun 7;267(1448):1071-9 PMID: 10885511
  33. The Amphimedon queenslandica genome and the evolution of animal complexity.
    Nature. 2010 Aug 5;466(7307):720-6 PMID: 20686567
  34. Reassessing embryogenesis in the Ctenophora: the inductive role of e1 micromeres in organizing ctene row formation in the 'mosaic' embryo, Mnemiopsis leidyi.
    Development. 1997 May;124(10):1999-2006 PMID: 9169846
  35. Independent evolution of striated muscles in cnidarians and bilaterians.
    Nature. 2012 Jul 12;487(7406):231-4 PMID: 22763458
  36. Assessing the root of bilaterian animals with scalable phylogenomic methods.
    Proc Biol Sci. 2009 Dec 22;276(1677):4261-70 PMID: 19759036
  37. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.
    Bioinformatics. 2006 Nov 1;22(21):2688-90 PMID: 16928733
  38. Extreme mitochondrial evolution in the ctenophore Mnemiopsis leidyi: Insight from mtDNA and the nuclear genome.
    Mitochondrial DNA. 2011 Aug;22(4):130-42 PMID: 21985407
  39. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments.
    Genome Biol. 2008 Jan 11;9(1):R7 PMID: 18190707
  40. Ancient origin of the integrin-mediated adhesion and signaling machinery.
    Proc Natl Acad Sci U S A. 2010 Jun 1;107(22):10142-7 PMID: 20479219
  41. My favorite animal, Trichoplax adhaerens.
    Bioessays. 2005 Dec;27(12):1294-302 PMID: 16299758
  42. The development of bioluminescence in the ctenophore Mnemiopsis leidyi.
    Dev Biol. 1973 Mar;31(1):61-100 PMID: 4150750
  43. A post-synaptic scaffold at the origin of the animal kingdom.
    PLoS One. 2007 Jun 06;2(6):e506 PMID: 17551586
  44. Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships.
    Mol Biol Evol. 2010 Sep;27(9):1983-7 PMID: 20378579
  45. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans.
    Nature. 2008 Feb 14;451(7180):783-8 PMID: 18273011
  46. Developmental expression of homeobox genes in the ctenophore Mnemiopsis leidyi.
    Dev Genes Evol. 2008 Jun;218(6):307-19 PMID: 18504608
Article Info
Journal
Science (New York, N.Y.)
Abbr.
Science
ISSN
1095-9203
Published
2013-12-13
Pages
1242592
Language
English
Region
United States
NLM ID
0404511
PMCID
PMC3920664
Subset
IM
Grants
Intramural NIH HHS · ZIA HG000140-13 · United States
Intramural NIH HHS · ZIA HG000140-14 · United States
Intramural NIH HHS · ZIA HG000140-15 · United States
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GENBANK
AGCP00000000
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