Developmental expression of homeobox genes in the ctenophore Mnemiopsis leidyi

Development Genes and Evolution

Volumn 218, Issue 6, 2008, Pages 307-319

  Pang, Kevin ^a   Martindale, Mark Q ^a  

^a UNIVERSITY OF HAWAII   (United States)

Author keywords

Ctenophore; Homeobox; Metazoan evolution

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR M1BAR; TRANSCRIPTION FACTOR M1BSH; TRANSCRIPTION FACTOR M1NKL1; TRANSCRIPTION FACTOR M1PRD1; TRANSCRIPTION FACTOR M1PRD2; TRANSCRIPTION FACTOR M1PRD3; TRANSCRIPTION FACTOR M1T1X LIKE;

ARTICLE; CELL MATURATION; CELL SPECIFICITY; DEVELOPMENTAL GENE; DEVELOPMENTAL GENETICS; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; GASTRULATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE ISOLATION; GENE SEQUENCE; HOMEOBOX; MARINE SPECIES; METAZOON; MNEMIOPSIS LEIDYI; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AMINO ACID SEQUENCE; ANIMALS; CLONING, MOLECULAR; CTENOPHORA; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, DEVELOPMENTAL; GENES, HOMEOBOX; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA; CTENOPHORA (COELENTERATES); FUNGI; METAZOA; MNEMIOPSIS LEIDYI; PLACOZOA;

EID: 44649187827     PISSN: 0949944X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00427-008-0222-3     Document Type: Article

References (46)

1. Ax P (1996) Multicellular animals: A new approach to the phylogenetic order in nature. Springer, Berlin Heidelberg New York
2. Banerjee-Basu S, Baxevanis AD (2001) Molecular evolution of the homeodomain family of transcription factors. Nucleic Acids Res 29:3258-3269
3. Bumann D, Puls G (1997) The ctenophore Mnemiopsis leidyi has a flow-through system for digestion with three consecutive phases of extracellular digestion. Physiol Zool 70:1-6
4. Chun C (1880) Die Ctenophoren des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. In: Fauna und Flora des Golfes Neapel, vol 1. Engelmann, Leipzig, pp 1-311
5. Cremona M, Colombo E, Andreazzoli M, Cossu G, Broccoli V (2004) Bsx, an evolutionary conserved Brain Specific homeoboX gene expressed in the septum, epiphysis, mammillary bodies and arcuate nucleus. Gene Expr Patterns 4:47-51
6. Derelle R, Manuel M (2007) Ancient connection between NKL genes and the mesoderm? Insights from Tlx expression in a ctenophore. Dev Genes Evol 217:253-261
7. Derelle R, Lopez P, Le Guyader H, Manuel M (2007) Homeodomain proteins belong to the ancestral molecular toolkit of eukaryotes. Evol Dev 9:212-219
8. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sorensen MV, Haddock SHD, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745-749
9. Galliot B, de Vargas C, Miller D (1999) Evolution of homeobox genes: Q50 paired-like genes founded the paired class. Dev Genes Evol 209:186-197
10. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696-704
11. Hernandez-Nicaise M-L (1991) Ctenophora. In: Harrison FW, Westfall JA (eds) Microscopic anatomy of invertebrates: Placozoa, Porifera, Cnidaria and Ctenophora. vol. 2. Wiley-Liss, New York, pp 359-418
12. Higashijima S, Kojima T, Michiue T, Ishimaru S, Emori Y, Saigo K (1992a) Dual Bar homeobox genes of Drosophila are required in two photoreceptor cells, R1 and R6, and primary pigment cells for normal eye development. Genes Dev 6:50-60
13. Higashijima S, Michiue T, Emori Y, Saigo K (1992b) Subtype determination of Drosophila embryonic external sensory organs by redundant homeobox genes BarH1 and BarH2. Genes Dev 6:1005-1018
14. Hoshiyama D, Iwabe N, Miyata T (2007) Evolution of the gene families forming the Pax/Six regulatory network: Isolation of genes from primitive animals and molecular phylogenetic analyses. FEBS Lett 581:1639-1643
15. Hyman LH (1940) The invertebrates: Protozoa through Ctenophora. McGraw-Hill, New York
16. Jager M, Queinnec E, Houliston E, Manuel M (2006) Expansion of the SOX gene family predate the emergence of the Bilateria. Mol Phylogenet Evol 39:842-854
17. Jakob W, Sagasser S, Dellaporta S, Holland P, Kuhn K, Schierwater B (2004) The Trox-2 Hox/ParaHox gene of the Trichoplax (Placozoa) marks an epithelial boundary. Dev Genes Evol 214:170-175
18. Jones B, McGinnis W (1993) A new Drosophila homeobox gene, bsh, is expressed in a subset of brain cells during embryogenesis. Development 117:793-806
19. Jones FS, Kioussi C, Copertino DW, Kallunki P, Holst BD, Edelman GM (1997) Barx2, a new homeobox gene of the Bar class, is expressed in neural and craniofacial structures during development. Proc Natl Acad Sci USA 94:2632-2637
20. Kusserow A, Pang K, Sturm C, Hrouda M, Lentfer J, Schmidt HA, Technau U, von Haeseler A, Hobmayer B, Martindale MQ, Holstein TW (2005) Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433:156-160
21. Larroux C, Fahey B, Liubicich D, Hinman VF, Gauthier M, Gongora M, Green K, Wörheide G, Leys SP, Degnan B (2006) Developmental expression of transcription factor genes in a demosponge: Insights into the origin of metazoan multicellularity. Evol Dev 8:150-173
22. Larroux C, Fahey B, Degnan SM, Adamski M, Rohksar DS, Degnan BM (2007) The NK homeobox gene cluster predates the origin of Hox genes. Curr Biol 17:706-710
23. Larroux C, Luke GN, Koopman P, Rokhsar DS, Shimeld SM, Degnan BM (2008) Genesis and expansion of metazoan transcription factor gene classes. Mol Biol Evol 25:980-996
24. Magie CR, Pang K, Martindale MQ (2005) Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis. Dev Genes Evol 215:618-630
25. Martindale MQ, Henry JQ (1999) 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 214:243-257
26. Martinelli C, Spring J (2005) T-box and homeobox genes from the ctenophore Pleurobrachia pileus: Comparison of Brachyury, Tbx2/3 and Tlx in basal metazoans and bilaterians. FEBS Lett 579:5024-5028
27. Metschnikoff E (1885) Vergleichend-embryologische Studien. IV. Ueber die gastrulation und mesodermbildung der Ctenophoren. Z Wiss Zool 42:648-656
28. Monteiro AS, Schierwater B, Dellaporta SL, Holland PWH (2006) A low diversity of ANTP class homeobox genes in Placozoa. Evol Dev 8:779-794
29. Panganiban G, Rubenstein JLF (2002) Developmental functions of the Distal-less/Dlx homeobox genes. Development 129:4371-4386
30. Patterson KD, Cleaver O, Gerber WV, White FG, Krieg PA (2000) Distinct expression patterns for two Xenopus Bar homeobox genes. Dev Genes Evol 210:140-144
31. Peterson KJ, Eernisse DJ (2001) Animal phylogeny and the ancestry of bilaterians: Inferences from morphology and 18S rDNA gene sequences. Evol Dev 3:170-205
32. Peterson KJ, Sperling EA (2007) Poriferan ANTP genes: Primitively simple or secondarily reduced? Evol Dev 9:405-408
33. Podar M, Haddock SHD, Sogin ML, Harbison GR (2001) A molecular phylogenetic framework for the phylum Ctenophora using 18S rRNA genes. Mol Phylogenet Evol 21:218-230
34. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, Jurka J, Genikhovich G, Grigoriev IV, Lucas SM, Steele RE, Finnerty JR, Technau U, Martindale MQ, Rokhsar DS (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86-94
35. Reig G, Cabrejos ME, Concha ML (2007) Functions of BarH transcription factors during embryonic development. Dev Biol 302:367-375
36. Reverberi G, Ortolani G (1965) The development of the ctenophores egg. Riv Biol 58:113-137
37. Rohnquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574
38. Ryan JF, Burton PM, Mazza ME, Kwong GK, Mullikan JC, Finnerty JR (2006) The Cnidarian-Bilaterian ancestor possessed at least 56 homeoboxes. Evidence from the starlet sea anemone, Nematostella vectensis. Genome Biol 7:R54
39. Ryan JF, Mazza ME, Pang K, Matus DQ, Baxevanis AD, Martindale MQ, Finnerty JR (2007) Pre-bilaterian origins of the Hox cluster and the Hox code: Evidence from the sea anemone Nematostella vectensis. PloS ONE 2:e153
40. Shu D-G, Morris SC, Han J, Li Y, Zhang X-L, Hua H, Zhang Z-F, Liu J-N, Guo J-F, Yao Y, Yasui K (2006) Lower Cambrian vendobionts from China and early diploblast evolution. Science 312:731-734
41. Siminionato E, Ledent V, Richards G, Thomas-Chollier M, Kerner P, Coornaert D, Degnan BM, Vervoort M (2007) Origin and diversification of the basic helix-loop-helix gene family in metazoans: Insights from comparative genomics. BMC Evol Biol 7:33
42. Tamm SL, Tamm S (2002) Novel bridge of axon-like processes of epithelial cells in the aboral sense organ of ctenophores. J Morphol 254:99-120
43. Tissier-Seta J-P, Mucchielli M-L, Mark M, Mattei M-G, Goridis C, Brunet J-F (1995) Barx1, a new mouse homeodomain transcription factor expressed in cranio-facial ectomesenchyme and the stomach. Mech Dev 51:3-15
44. Wallberg A, Thollesson M, Farris JS, Jondelius U (2004) The phylogenetic position of the comb jellies (Ctenophora) and the importance of taxonomic sampling. Cladistics 20:558-578
45. Yamada A, Martindale MQ (2002) Expression of the ctenophore Brain Factor 1 forkhead gene ortholog (ctenoBF-1) mRNA is restricted to the presumptive mouth and feeding apparatus: Implications for axial organization in the Metazoa. Dev Genes Evol 212:338-348
46. Yamada A, Pang K, Martindale MQ, Tochinai S (2007) Surprisingly complex T-box gene complement in diploblastic metazoans. Evol Dev 9:220-230