Tracking the origins of the bilaterian Hox patterning system: Insights from the acoel flatworm Symsagittifera roscoffensis

Evolution and Development

Volumn 11, Issue 5, 2009, Pages 574-581

  Moreno, Eduardo ^a   Nadal, Marga ^b   Baguñà, Jaume ^a   Martínez, Pedro ^a,c  

^a UNIVERSITY OF BARCELONA   (Spain)

^b CATALAN INSTITUTE OF ONCOLOGY   (Spain)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN;

FLATWORM; GENE EXPRESSION; GENOMICS; HYBRIDIZATION; PHYLOGENY; RELATEDNESS; SYMMETRY;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; CLASSIFICATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MORPHOGENESIS; PHYLOGENY; PLATYHELMINTH; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; BODY PATTERNING; CHROMOSOMES, ARTIFICIAL, BACTERIAL; CLONING, MOLECULAR; EVOLUTION, MOLECULAR; HOMEODOMAIN PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLATYHELMINTHS; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA; BACTERIA (MICROORGANISMS); BILATERIA; DEUTEROSTOMIA; PLATYHELMINTHES; PROTOSTOMIA; SYMSAGITTIFERA;

EID: 70349138341     PISSN: 1520541X     EISSN: 1525142X     Source Type: Journal    
DOI: 10.1111/j.1525-142X.2009.00363.x     Document Type: Article

References (48)

1. Aboobaker, A. A. Blaxter, M. L. 2003. Hox gene loss during dynamic evolution of the nematode cluster. Curr. Biol. 13 : 37 40.
2. Adoutte, A., Balavoine, G., Lartillot, N. de Rosa, R. 1999. Animal evolution: the end of the intermediate taxa? Trends Genet. 15 : 104 108.
3. Adoutte, A., Balavoine, G., Lartillot, N., Lespinet, O., Prud'homme, B. de Rosa, R. 2000. The new animal phylogeny: reliability and implications. Proc. Natl. Acad. Sci. USA 97 : 4453 4456.
4. Amemiya, C. T. Wagner, G. P. 2006. Animal evolution: when did the 'Hox system' arise? Curr. Biol. 16 : R546 R548.
5. Arendt, D., Technau, U. Wittbrod, J. 2001. Evolution of the bilaterian larval foregut. Nature 409 : 81 85.
6. Ax, P. 1996. Multicellular Animals. A New Approach to the Phylogenetic Order in Nature. Vol. I. Springer, Berlin.
7. Baguñà, J., Martínez, P., Paps, J. Riutort, M. (2008). Back in time: a new proposal for the Bilateria. Phil. Trans. R. Soc. B. Biol. Sci. 363 : 1481 1491.
8. Baguñà, J. Riutort, M. 2004. The dawn of bilaterian animals. The case of acoelomorph flatworms. BioEssays 26 : 1046 1057.
9. Ball, E. E., de Jong, D. M., Schierwater, B., Shinzato, C., Hayward, D. C. Miller, D. J. (2007). Implications of cnidarian gene expression patterns for the origins of bilaterality - is the glass half full or half empty? Int. Comp. Biol. 47 : 701 711.
10. Budd, G. E. 2008. The earliest fossil record of the animals and its significance. Phil. Trans. R. Soc. B. 363 : 1425 1434.
11. Cameron, R. A., et al. 2006. Unusual gene order and organization of the sea urchin Hox cluster. J. Exp. Zool. (Mol. Dev. Evol.) 306B : 45 58.
12. 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 Scientific, Malden, Mass.
13. Chiori, R., et al. 2009. Are Hox genes ancestrally involved in axial patterning? Evidence fropm the hydrozoan Clytia hemispherica (Cnidaria). PloS ONE 4 : e423.
14. Chourrout, D., et al. 2006. Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements. Nature 442 : 684 687.
15. Cook, C. E., Jiménez, E., Akam, M. Saló, E. 2004. The Hox gene complement of acoel flatworms, a basal bilaterian clade. Evol. Dev. 6 : 154 163.
16. De Robertis, E. M. Sasai, Y. 1996. A unity of plan for dorsoventral patterning in the development of animal species. Nature 380 : 37 40.
17. de Rosa, R., et al. 1999. Hox genes in brachiopods and priapulids and protostome evolution. Nature 399 : 772 776.
18. Deutsch, J. S. 2008. Do acoels climb up the "Scale of Beings"? Evol. Dev. 10 : 135 140.
19. Duboule, D. 2007. The rise and fall of Hox gene clusters. Development 134 : 2549 2560.
20. Erwin, D. H., Valentine, J. W. Jablonski, D. 1997. The origin of animal body plans. Amer. Sci. 85 : 126 137.
21. Finnerty, J. R., Paulson, D., Burton, P., Pang, K. Martindale, M. Q. 2003. Early evolution of a homeobox gene: the parahox gene Gsx in the Cnidaria and the Bilateria. Evol. Dev. 5 : 331 345.
22. Fritzsch, G., et al. 2008. PCR survey of Xenoturbella bocki Hox genes. J. Exp. Zool. B (Mol. Dev. Evol). 310B : 278 284.
23. García-Fernàndez, J. 2005. The genesis and evolution of homeobox gene clusters. Nat. Rev Genet. 6 : 881 892.
24. Hejnol, A. Martindale, M. Q. 2008. Acoel development supports a simple planula-like urbilaterian. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 363 : 1493 1501.
25. Ikuta, T., Yoshida, N., Satoh, N. Saiga, H. 2004. Ciona intestinalis Hox gene cluster: its dispersed structure and residual colinear expression in development. Proc. Natl. Acad. Sci. USA 101 : 15118 15123.
26. In der Rieden, P. M., Mainguy, G., Woltering, J. M. Durston, A. J. 2004. Homeodomain to hexapeptide or PBC-interaction-domain distance: size apparently matters. Trends Genet. 20 : 76 79.
27. Jondelius, U., Ruiz-Trillo, I., Baguñà, J. Riutort, M. 2002. The Nemertodermatida are basal bilaterians and not members of the Platyhelminthes. Zool. Scr. 31 : 201 215.
28. Kamm, K., Schierwater, B., Jakob, W., Dellaporta, S. L. Miller, D. J. 2006. Axial patterning and diversification in the Cnidaria predate the Hox system. Curr. Biol. 16 : 1 7.
29. Koziol, U., Lalanne, A. I. Castillo, E. 2009. Hox genes in the parasitic platyhelminthes Mesocestoides corti, Echinococcus multilocularis, and Schistosoma mansoni: evidence for a reduced Hox complement. Biochem. Genet. 47 : 100 116.
30. Lemons, D. McGinnis, W. 2006. Genomic evolution of Hox gene clusters. Science 313 : 1918 1922.
31. Lim, J. K. Simmons, M. J. 1994. Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster. BioEssays 16 : 269 275.
32. McGinnis, W. Krumlauf, R. 1992. Homeobox genes and axial patterning. Cell 68 : 283 302.
33. Martindale, M. Q., Pang, K. Finnerty, J. R. 2004. Investigating the origins of triploblasty: 'mesodermal' gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131 : 2463 2474.
34. Martinez, P., Lee, J. C. Davidson, E. H. 1997. Complete sequence of SpHox8 and its linkage in the single Hox gene cluster of Strongylocentrotus purpuratus. J. Mol. Evol. 44 : 371 377.
35. Ogishima, S. Tanaka, H. 2007. Missing link in the evolution of Hox clusters. Gene 387 : 21 30.
36. Philippe, H., Brinkmann, H., Martinez, P., Riutort, M. Baguñà, J. 2007. Acoel flatworms are not platyhelminthes: evidence from phylogenomics. PLoS ONE 2 : e717.
37. Rieger, R. M., Tyler, S., Smith III., J. P. S. Rieger, G. E. 1991. Platyhelminthes: Turbellaria. In F. W. Harrison B. J. Bogitsh (eds.). Microscopic Anatomy of Invertebrates. Vol. 3. Platyhelminthes and Nemertinea. John Wiley & Sons, New York, pp. 7 140.
38. Ruiz-Trillo, I., et al. 2002. A phylogenetic analysis of myosin heavy chain type II sequences corroborate that Acoela and Nemertodermatida are basal bilaterians. Proc. Natl. Acad. Sci. USA 99 : 11246 11251.
39. Ruiz-Trillo, I., Riutort, M., Fourcade, H. M., Baguñà, J. Boore, J. L. 2004. Mitochondrial genome data support the basal position of Acoelomorpha and the polyphyly of the Platyhelminthes. Mol. Phylogenet. Evol. 33 : 321 332.
40. Ruiz-Trillo, I., Riutort, M., Littlewood, D. T. J., Herniou, E. A. Baguñà, J. 1999. Acoel flatworms: earliest extant bilaterian metazoans, not members of Platyhelminthes. Science 283 : 1919 1923.
41. Ryan, J. F., et al. 2007. Pre-bilaterian origins of the Hox cluster and the Hox code: evidence from the sea anemone, Nematostella vectensis. PLoS ONE 2 : e153.
42. Sempere, L. F., Martinez, P., Cole, C., Baguñà, J. Peterson, K. J. 2007. Phylogenetic distribution of microRNAs supports the basal position of acoel flatworms and the polyphyly of Platyhelminthes. Evol. Dev. 9 : 409 415.
43. Seo, H. C., et al. 2004. Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 431 : 67 71.
44. Telford, M. J. 2008. Xenoturbellida: the fourth Deuterostome phylum and the diet of worms. Genesis 46 : 580 586.
45. Telford, M. J., Lockyer, A. E., Cartwright-Finch, C. Littlewood, D. T. J. 2003. Combined large and small subunit ribosomal RNA phylogenies support a basal position of the acoelomorph flatworms. Proc. R. Soc. Lond. Biol. Sci. 270 : 1077 1083.
46. Valentine, J. W., Erwin, D. H. Jablonski, D. 1996. Developmental evolution of metazoan bodyplans: the fossil evidence. Dev. Biol. 173 : 373 381.
47. Wallberg, A., Curini-Galletti, M., Ahmadzadeh, A. Jondelius, U. 2007. Dismissal of Acoelomorpha: Acoela and Nemertodermatida are separate early bilaterian clades. Zool. Scr. 36 : 509 523.
48. Wheeler, B. M., et al. 2009. The deep evolution of Metazoan microRNA. Evol. Dev. 11 : 50 68.