Developmental expression of transcription factor genes in a demosponge: Insights into the origin of metazoan multicellularity

Evolution and Development

Volumn 8, Issue 2, 2006, Pages 150-173

  Larroux, Claire ^a   Fahey, Bryony ^a   Liubicich, Danielle ^a,c   Hinman, Veronica F ^a,d   Gauthier, Marie ^a   Gongora, Milena ^a   Green, Kathryn ^a   Wörheide, Gert ^a,e   Leys, Sally P ^a,b   Degnan, Bernard M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF ALBERTA   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^e UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; LIGAND; TRANSCRIPTION FACTOR;

ANCESTRY; EMBRYONIC DEVELOPMENT; EVOLUTIONARY BIOLOGY; FERTILIZATION (REPRODUCTION); GENE EXPRESSION; PHYLOGENETICS;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BINDING SITE; BIOSYNTHESIS; CYTOLOGY; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; LARVA; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PRENATAL DEVELOPMENT; PROTEIN TERTIARY STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPONGE (PORIFERA);

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; DNA; EVOLUTION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LARVA; LIGANDS; MOLECULAR SEQUENCE DATA; PORIFERA; PROTEIN STRUCTURE, TERTIARY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS;

ANIMALIA; BILATERIA; EUMETAZOA; METAZOA; PORIFERA; RENIERA;

EID: 33646485296     PISSN: 1520541X     EISSN: 1525142X     Source Type: Journal    
DOI: 10.1111/j.1525-142X.2006.00086.x     Document Type: Article

References (82)

1. Adell T. Grebenjuk V. A. Wiens M. Muller W. E. G. 2003. Isolation and characterization of two T-box genes from sponges, the phylogenetically oldest metazoan taxon. Dev. Genes Evol. 213 421 434.
2. Adell T. Muller W. E. G. 2004. Isolation and characterization of five Fox (Forkhead) genes from the sponge Suberites domuncula. Gene 334 35 46.
3. Aguinaldo A. M. A. et al. 1997. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387 489 493.
4. Alvarez-Buylla E. R. et al. 2000. An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc. Natl. Acad. Sci. USA 97 5328 5333.
5. Auwerx J. et al. 1999. A unified nomenclature system for the nuclear receptor superfamily. Cell 97 161 163.
6. Banerjee-Basu S. Baxevanis A. D. 2001. Molecular evolution of the homeodoamin family of transcription factors. Nucleic Acids Res. 29 3258 3269.
7. Borchiellini C. Manuel M. Alivon E. Boury-Esnault N. Vacelet J. Le Parco Y. 2001. Sponge paraphyly and the origin of Metazoa. J. Evol. Biol. 14 171 179.
8. Bowles J. Schepers G. Koopman P. 2000. Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev. Biol. 227 239 255.
9. Carlsson P. Mahlapuu M. 2002. Forkhead transcription factors key players in development and metabolism. Dev. Biol. 250 1 23.
10. Carroll S. B. Grenier J. K. Weatherbee S. D. 2005. From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design. 2nd Ed. Blackwell Science Malden.
11. Castro L. F. C. Holland P. W. H. 2003. Chromosomal mapping of ANTP class homeobox genes in amphioxus piecing together ancestral genomes. Evol. Dev. 5 459 465.
12. Cavalier-Smith T. Chao E. E. Y. 2003. Phylogeny of choanozoa, apusozoa, and other protozoa and early eukaryote megaevolution. J. Mol. Evol. 56 540 563.
13. Collins A. G. 1998. Evaluating multiple alternative hypotheses for the origin of Bilateria an analysis of 18S rRNA molecular evidence. Proc. Natl. Acad. Sci. USA 95 15458 15463.
14. Coutinho C. C. Fonseca R. N. Mansure J. J. C. Borojevic R. 2003. Early steps in the evolution of multicellularity deep structural and functional homologies among homeobox genes in sponges and higher metazoans. Mech. Dev. 120 429 440.
15. Coutinho C. C. Vissers S. Van de Vyver G. 1994. Evidence of homeobox gene in the freshwater sponge Ephydatia fluviatilis. In Van Soest R. W. M. Van Kempen T. M. G. Braekman J. C. (eds.). Sponges in Time and Space. Balkema Press Rotterdam pp. 385 388.
16. Davidson E. H. 2001. Genomic Regulatory Systems. Development and Evolution. Academic Press San Diego.
17. Degnan B. M. Degnan S. M. Giusti A. F. Morse D. E. 1995. A hom/hox gene in sponges. Gene 155 175 177.
18. Degnan B. M. Degnan S. M. Naganuma T. Morse D. E. 1993. The ets multigene family is conserved throughout the Metazoa. Nucleic Acids Res. 21 3479 3484.
19. Degnan B. M. Leys S. P. Larroux C. 2005. Sponge development and antiquity of animal pattern formation. Integr. Comp. Biol. 45 335 341.
20. Degnan B. M. Morse D. E. 1993. Identification of eight homeobox-containing transcripts expressed during larval development and at metamorphosis in the gastropod mollusc Haliotis rufescens. Mol. Mar. Biol. Biotechnol. 2 1 9.
21. Degnan B. M. Rohde P. R. Lavin M. F. 1996. Normal development and embryonic gene activity of the ascidian Herdmania momus. Mar. Freshw. Res. 47 543 551.
22. Devine C. Hinman V. F. Degnan B. M. 2002. Evolution and developmental expression of nuclear receptor genes in the ascidian Herdmania curvata. Int. J. Dev. Biol. 46 687 692.
23. Felsenstein J. 2003. PHYLIP (Phylogeny Inference Package). Distributed by the author, Department of Genetics, University of Washington Seattle.
24. Finnerty J. R. Martindale M. Q. 1997. Homeoboxes in sea anemones (Cnidaria; Anthozoa) a PCR-based survey of Nematostella vectensis and Metridium senile. Biol. Bull. 193 62 76.
25. Garcia-Fernandez J. 2005. Hox, parahox, protohox facts and guesses. Heredity 94 145 152.
26. Gauchat D. et al. 2000. Evolution of Antp-class genes and differential expression of HydraHox/parahox genes in anterior patterning. Proc. Natl. Acad. Sci. USA 97 4493 4498.
27. Granadino B. Perez-Sanchez C. Rey-Campos J. 2000. Forkhead transcription factors. Curr. Genomics 1 353 382.
28. Hill A. Tetrault J. Hill M. 2004. Isolation and expression analysis of a poriferan Antp-class Bar-/Bsh-like homeobox gene. Dev. Genes Evol. 214 515 523.
29. Hinman V. F. Degnan B. M. 2000. Retinoic acid perturbs Otx gene expression in the ascidian pharynx. Dev. Genes Evol. 210 129 139.
30. Hobert O. Westphal H. 2000. Functions of LIM-homeobox genes. Trends Genet. 16 75 83.
31. Hoshiyama D. et al. 1998. Sponge Pax cdna related to Pax-2/5/8 and ancient gene duplications in the Pax family. J. Mol. Evol. 47 640 648.
32. Hyman L. H. 1940. The Invertebrates. McGraw-Hill New York.
33. Jackson D. Leys S. P. Hinman V. F. Woods R. Lavin M. F. Degnan B. M. 2002. Ecological regulation of development induction of marine invertebrate metamorphosis. Int. J. Dev. Biol. 46 679 686.
34. 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.
35. Kaestner K. H. Knochel W. Martinez D. E. 2000. Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 14 142 146.
36. Kortschak R. D. Samuel G. Saint R. Miller D. J. 2003. EST analysis of the Cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr. Biol. 13 2190 2195.
37. Kruse M. Leys S. P. Muller I. M. Muller W. E. G. 1998. Phylogenetic position of the Hexactinellida within the phylum Porifera based on the amino acid sequence of the protein kinase C from Rhabdocalyptus dawsoni. J. Mol. Evol. 46 721 728.
38. Lee S. E. Gates R. D. Jacobs D. K. 2003. Gene fishing the use of a simple protocol to isolate multiple homeodomain classes from diverse invertebrate taxa. J. Mol. Evol. 56 509 516.
39. Leys S. P. 2004. Gastrulation in sponges. In Stern C. (ed.). Gastrulation: from Cells to Embryos. Cold Spring Harbor Laboratory Press New York pp. 23 31.
40. Leys S. P. 2003a. Comparative study of spiculogenesis in demosponge and hexactinellid larvae. Microsc. Res. Tech. 62 300 311.
41. Leys S. P. 2003b. The significance of syncytial tissues for the position of the Hexactinellida in the Metazoa. Integr. Comp. Biol. 43 19.
42. Leys S. P. Cronin T. W. Degnan B. M. Marshall J. N. 2002. Spectral sensitivity in a sponge larva. J. Comp. Physiol. A Sens. Neural Behav. Physiol. 188 199 202.
43. Leys S. P. Degnan B. M. 2001. Cytological basis of photoresponsive behavior in a sponge larva. Biol. Bull. 201 323 338.
44. Leys S. P. Degnan B. M. 2002. Embryogenesis and metamorphosis in a haplosclerid demosponge gastrulation and transdifferentiation of larval ciliated cells to choanocytes. Invertebr. Biol. 121 171 189.
45. Leys S. P. Rokhsar D. S. Degnan B. M. 2005. Quick guide - sponges. Curr. Biol. 15 R114 R115.
46. Maldonado M. Durfort M. Mc Carthy D. A. Young C. M. 2003. The cellular basis of photobehavior in the tufted parenchymella larva of demosponges. Mar. Biol. 143 427 441.
47. Maldonado M. George S. B. Young C. M. Vaquerizo I. 1997. Depth regulation in parenchymella larvae of a demosponge relative roles of skeletogenesis, biochemical changes and behavior. Mar. Ecol. Prog. Ser. 148 115 124.
48. Manuel M. Borchiellini C. Alivon E. Le Parco Y. Vacelet J. Boury-Esnault N. 2003. Phylogeny and evolution of calcareous sponges monophyly of Calcinea and Calcaronea, high level of morphological homoplasy, and the primitive nature of axial symmetry. Syst. Biol. 52 311 333.
49. Manuel M. Le Parco Y. Borchiellini C. 2004. Comparative analysis of Brachyury T-domains, with the characterization of two new sponge sequences, from a hexactinellid and a calcisponge. Gene 340 291 301.
50. Martinez D. E. Dirksen M. L. Bode P. M. Jamrich M. Steele R. E. Bode H. R. 1997. Budhead, a fork head HNF-3 homologue, is expressed during axis formation and head specification in hydra. Dev. Biol. 192 523 536.
51. Mazet F. Yu J. K. Liberles D. A. Holland L. Z. Shimeld S. M. 2003. Phylogenetic relationships of the Fox (Forkhead) gene family in the Bilateria. Gene 316 79 89.
52. Medina M. Collins A. G. Silberman J. D. Sogin M. L. 2001. Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rrna. Proc. Natl. Acad. Sci. USA 98 9707 9712.
53. Miller D. J. et al. 2000. Pax gene diversity in the basal cnidarian Acropora millepora (Cnidaria, Anthozoa) implications for the evolution of the Pax gene family. Proc. Natl. Acad. Sci. USA 97 4475 4480.
54. Miyata T. Suga H. 2001. Divergence pattern of animal gene families and relationship with the Cambrian explosion. BioEssays 23 1018 1027.
55. Muller W. E. G. Muller I. M. Lukic L. Cetkovic H. Gamulin V. 1998. Monophyly of metazoa sponges as living fossils. Period Biol. 100 373 381.
56. Nam J. de Pamphilis C. W. Ma H. Nei M. 2003. Antiquity and evolution of the MADS-box gene family controlling flower development in plants. Mol. Biol. Evol. 20 1435 1447.
57. Nikoh N. et al. 1997. An estimate of divergence time of parazoa and eumetazoa and that of cephalochordata and vertebrata by aldolase and triose phosphate isomerase clocks. J. Mol. Evol. 45 97 106.
58. O'Brien E. K. Degnan B. M. 2000. Expression of POU, Sox, and Pax genes in the brain ganglia of the tropical abalone Haliotis asinina. Mar. Biotechnol. 2 545 557.
59. Pacifici M. Koyama E. Iwamoto M. Gentili C. 2000. Development of articular cartilage what do we know about it and how may it occur? Connect. Tissue Res. 41 175 184.
60. Papaioannou V. E. 2001. T-box genes in development from hydra to humans. Int. Rev. Cytol. 207 1 70.
61. Patterson K. D. Cleaver O. Gerber W. V. White F. G. Krieg P. A. 2000. Distinct expression patterns for two Xenopus Bar homeobox genes. Dev. Genes Evol. 210 140 144.
62. Perovic S. et al. 2003. Expression of one sponge Iroquois homeobox gene in primmorphs from Suberites domuncula during canal formation. Evol. Dev. 5 240 250.
63. Rambaut A. 1996. Se-Al: Sequence Alignment Editor. Available at
64. Richelle-Maurer E. Van de Vyver G. Vissers S. Coutinho C. C. 1998. Homeobox-containing genes in freshwater sponges characterization, expression, and phylogeny. In Muller W. E. G. (ed.). Progress in Molecular Subcell Biology. Springer-Verlag Berlin, Heidelberg pp. 158 175.
65. Rodrigo A. G. Bergquist P. R. Bergquist P. L. 1994. Inadequate support for an evolutionary link between the Metazoa and the Fungi. Syst. Biol. 43 578 584.
66. Ronquist F. Huelsenbeck J. P. 2003. Mrbayes 3 Bayesian phylogenetic inference under mixed models. Bioinformatics 19 1572 1574.
67. de Rosa R. et al. 1999. Hox genes in brachiopods and priapulids and protostome evolution. Nature 399 772 776.
68. Saba R. Nakatsuji N. Saito T. 2003. Mammalian barh1 confers commissural neuron identity on dorsal cells in the spinal cord. J. Neurosci. 23 1987 1991.
69. Seimiya M. Ishiguro H. Miura K. Watanabe Y. Kurosawa Y. 1994. Homeobox-containing genes in the most primitive Metazoa, the sponges. Eur. J. Biochem. 221 219 225.
70. Seimiya M. Watanabe Y. Kurosawa Y. 1997. Identification of POU-class homeobox genes in a freshwater sponge and the specific expression of these genes during differentiation. Eur. J. Biochem. 243 27 31.
71. Sharrocks A. D. 2001. The Ets-domain transcription factor family. Nat. Rev. Mol. Cell Biol. 2 827 837.
72. Spring J. Yanze N. Josch C. Middel A. M. Winninger B. Schmid V. 2002. Conservation of Brachyury, Mef2, and Snail in the myogenic lineage of jellyfish a connection to the mesoderm of bilateria. Dev. Biol. 244 372 384.
73. Sullivan J. Abdo Z. Joyce P. Swofford D. L. 2005. Evaluating the performance of a successive-approximations approach to parameter optimization in maximum-likelihood phylogeny estimation. Mol. Biol. Evol. 22 1386 1392.
74. Sun H. M. et al. 1997. Evolution of paired domains isolation and sequencing of jellyfish and hydra Pax genes related to Pax-5 and Pax-6. Proc. Natl. Acad. Sci. USA 94 5156 5161.
75. Takatori N. et al. 2004. T-box genes in the ascidian Ciona intestinalis characterization of cDNAs and spatial expression. Dev. Dyn. 230 743 753.
76. Technau U. Bode H. R. 1999. Hybra1, a Brachyury homologue, acts during head formation in Hydra. Development 126 999 1010.
77. Thompson J. D. Higgins D. G. Gibson T. J. 1994. Clustal W improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 4673 4680.
78. Tucker A. S. Matthews K. L. Sharpe P. T. 1998. Transformation of tooth type induced by inhibition of BMP signaling. Science 282 1136 1138.
79. Wiens M. Batel R. Korzhev M. Muller W. E. G. 2003a. Retinoid X receptor and retinoic acid response in the marine sponge Suberites domuncula. J. Exp. Biol. 206 3261 3271.
80. Wiens M. et al. 2003b. The molecular basis for the evolution of the metazoan bodyplan: extracellular matrix-mediated morphogenesis in marine demosponges. J. Mol. Evol. 57 S60 S75.
81. Wolpert L. 1994. The evolutionary origin of development - cycles, patterning, privilege and continuity. Development suppl. S 79 84.
82. Yang Z. 1997. Paml a program for package for phylogenetic analysis by maximum likelihood. CABIOS 15 555 556.