The origin of patterning systems in Bilateria-Insights from the Hox and ParaHox genes in acoelomorpha

Genomics, Proteomics and Bioinformatics

Volumn 9, Issue 3, 2011, Pages 65-76

  Moreno, Eduardo ^a   Permanyer, Jon ^a   Martinez, Pedro ^a,b  

^a UNIVERSITY OF BARCELONA   (Spain)

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

Author keywords

Acoelomorpha; Bilateria; Cluster; Hox code; Hox ParaHox; Transposon

Indexed keywords

ACOELOMORPHA; BILATERIA; CONSENSUS; GENE; GENE CLUSTER; GENE EXPRESSION; GENE FUNCTION; GENETIC COMPLEMENTATION; HOX GENE; INFORMATION; MOLECULAR EVOLUTION; MORPHOGENESIS; NONHUMAN; PARAHOX GENE; PHYLOGENETIC TREE; PHYLUM; REVIEW;

ANIMALS; EVOLUTION, MOLECULAR; GENES, HOMEOBOX; HOMEODOMAIN PROTEINS; HUMANS; PHYLOGENY; TURBELLARIA;

ACOELOMORPHA; ANIMALIA; BILATERIA; METAZOA;

EID: 79960739693     PISSN: 16720229     EISSN: 22103244     Source Type: Journal    
DOI: 10.1016/S1672-0229(11)60010-7     Document Type: Review

References (68)

1. McGinnis W., Krumlauf R. Homeobox genes and axial patterning. Cell 1992, 68:283-302.
2. Bürglin T.R. Homeodomain proteins. Encyclopedia of Molecular Biology and Molecular Medicine 1996, Vol.3:55-76. VCH Verlagsgesellschaft mbH, Weinheim, Germany. R.A. Meyers (Ed.).
3. Adoutte A., et al. The new animal phylogeny: reliability and implications. Proc. Natl. Acad. Sci. USA 2000, 97:4453-4456.
4. Chiori R., et al. Are Hox genes ancestrally involved in axial patterning? Evidence from the hydrozoan Clytia hemisphaerica (Cnidaria). PLoS One 2009, 4:e4231.
5. Quiquand M., et al. More constraint on ParaHox than Hox gene families in early metazoan evolution. Dev. Biol. 2009, 328:173-187.
6. Ryan J.F., et al. Pre-bilaterian origins of the Hox cluster and the Hox code: evidence from the sea anemone, Nematostella vectensis. PLoS One 2007, 2:e153.
7. Chourrout D., et al. Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements. Nature 2006, 442:684-687.
8. Kamm K., et al. Axial patterning and diversification in the Cnidaria predate the Hox system. Curr. Biol. 2006, 16:920-926.
9. Finnerty J.R., et al. Origins of bilateral symmetry: Hox and Dpp expression in a sea anemone. Science 2004, 304:1335-1337.
10. Gauchat D., et al. Evolution of Antpclass genes and differential expression of Hydra Hox/paraHox genes in anterior patterning. Proc. Natl. Acad. Sci. USA 2000, 97:4493-4498.
11. Gilbert S.F. Developmental Biology 2006, Sinauer Associates, Sunderland, USA. the eighth edition.
12. Arnone M.I., et al. Genetic organization and embryonic expression of the ParaHox genes in the sea urchin S. purpuratus: insights into the relationship between clustering and colinearity. Dev. Biol. 2006, 300:63-73.
13. Pearson J.C., et al. Modulating Hox gene functions during animal body patterning. Nat. Rev. Genet. 2005, 6:893-904.
14. Gegenbaur C. Grundzüge der Vergleichenden Anatomie 1859, W. Engelmann, Leipzig, Germany.
15. Ruiz-Trillo I., et al. Acoel flatworms: earliest extant bilaterian Metazoans, not members of Platyhelminthes. Science 1999, 283:1919-1923.
16. Hejnol A., et al. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc. Biol. Sci. 2009, 276:4261-4270.
17. Philippe H., et al. Acoel flatworms are not platyhelminthes: evidence from phylogenomics. PLoS One 2007, 2:e717.
18. De Mulder K., et al. Characterization of the stem cell system of the acoel Isodiametra pulchra. BMC Dev. Biol. 2009, 9:69.
19. Karling T.G. On the anatomy and affinities of the turbellarian orders. The Biology of the Turbellaria 1974, 1-16. McGraw-Hill, New York, USA. N.W. Riser, M.P. Morse (Eds.).
20. Keeble F. Plant-Animals: A Study in Symbiosis 1910, Cambridge University Press, London, UK.
21. Westblad E. On Meara stichopi (Bock) Westblad, a new representative of Turbellaria archoophora. Ark. Zool. 1949, 1:43-57.
22. Doe D.A. Comparative ultrastructure of the pharynx simplex in Turbellaria. Zoomorphology 1981, 97:133-193.
23. Cook C.E., et al. The Hox gene complement of acoel flatworms, a basal bilaterian clade. Evol. Dev. 2004, 6:154-163.
24. Moreno E., et al. Tracking the origins of the bilaterian Hox patterning system: insights from the acoel flatworm Symsagittifera roscoffensis. Evol. Dev. 2009, 11:574-581.
25. Moreno E., et al. Inferring the ancestral function of the posterior Hox gene within the Bilateria: controlling the maintenance of reproductive structures, the musculature and the nervous system in the acoel flatworm Isodiametra pulchra. Evol. Dev. 2010, 12:258-266.
26. Hejnol A., Martindale M.Q. Coordinated spatial and temporal expression of Hox genes during embryogenesis in the acoel Convolutriloba longifissura. BMC Biol. 2009, 7:65.
27. Sikes J.M., Bely A.E. Making heads from tails: development of a reversed anterior-posterior axis during budding in an acoel. Dev. Biol. 2010, 338:86-97.
28. Jiménez-Guri E., et al. Hox and ParaHox genes in Nemertodermatida, a basal bilaterian clade. Int. J. Dev. Biol. 2006, 50:675-679.
29. Balavoine G., et al. Hox clusters and bilaterian phylogeny. Mol. Phylogenet. Evol. 2002, 24:366-373.
30. Ogishima S., Tanaka H. Missing link in the evolution of Hox clusters. Gene 2007, 387:21-30.
31. Hejnol A., Martindale M.Q. Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature 2008, 456:382-386.
32. Wright C.V., et al. Xlhbox 8: a novel Xenopus homeo protein restricted to a narrow band of endoderm. Development 1988, 104:787-794.
33. Smith J.P.S., Tyler S. The acoel turbellarians: kingpins of metazoan evolution or a specialized offshoot?. The Origins and Relationships of Lower Invertebrates 1985, 123-142. Oxford University Press, Oxford, UK. S. Conway Morris (Ed.).
34. Duboule D. The rise and fall of Hox gene clusters. Development 2007, 134:2549-2560.
35. Garcia-Fernàndez J., Holland P.W. Amphioxus Hox genes: insights into evolution and development. Int. J. Dev. Biol. 1996, (Supp 1):71-72S.
36. Ferrier D.E., et al. The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14. Evol. Dev. 2000, 2:284-293.
37. Holland L.Z., et al. The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res. 2008, 18:1100-1111.
38. Ikuta T., et al. Ciona intestinalis Hox gene cluster: its dispersed structure and residual colinear expression in development. Proc. Natl. Acad. Sci. USA 2004, 101:15118-15123.
39. Aboobaker A.A., Blaxter M.L. Hox gene loss during dynamic evolution of the nematode cluster. Curr. Biol. 2003, 13:37-40.
40. Koziol U., et al. Hox genes in the parasitic platyhelminthes Mesocestoides corti, Echinococcus multilocularis, and Schistosoma mansoni: evidence for a reduced Hox complement. Biochem. Genet. 2009, 47:100-116.
41. Seo H.C., et al. Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 2004, 431:67-71.
42. Lim J.K., Simmons M.J. Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster. Bioessays 1994, 16:269-275.
43. Fried C., et al. Exclusion of repetitive DNA elements from gnathostome Hox clusters. J. Exp. Zool. B Mol. Dev. 2004, 302:165-173.
44. Minguillón C., Garcia-Fernández J. Genesis and evolution of the Evx and Mox genes and the extended Hox and ParaHox gene clusters. Genome Biol. 2003, 4:R12.
45. Cameron R.A., et al. Unusual gene order and organization of the sea urchin Hox cluster. J. Exp. Zool. B Mol. Dev. Evol. 2006, 306:45-58.
46. Tanzer A., et al. Evolution of microRNAs located within Hox gene clusters. J. Exp. Zool. B Mol. Dev. Evol. 2005, 304:75-85.
47. Yekta S., et al. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004, 304:594-596.
48. Monteiro A.S., Ferrier D.E.K. Hox genes are not always colinear. Int. J. Biol. Sci. 2006, 2:95-103.
49. Soshnikova N., Duboule D. Epigenetic temporal control of mouse Hox genes in vivo. Science 2009, 324:1320-1323.
50. Tarchini B., Duboule D. Control of Hoxd genes' collinearity during early limb development. Dev. Cell 2006, 10:93-103.
51. Tschopp P., et al. Uncoupling time and space in the collinear regulation of Hox genes. PLoS Genet. 2009, 5:e1000398.
52. Deutsch J., Le Guyader H. The neuronal zootype. An hypothesis. C. R. Acad. Sci. III 1998, 321:713-719.
53. Jakob W., Schierwater B. Changing hydrozoan bauplans by silencing Hox-like genes. PLoS One 2007, 2:e694.
54. Wu L.H., Lengyel J.A. Role of caudal in hindgut specification and gastrulation suggests homology between Drosophila amnioproctodeal invagination and vertebrate blastopore. Development 1998, 125:2433-2442.
55. James R., et al. Structure of the murine homeobox gene cdx-2. Expression in embryonic and adult intestinal epithelium. J. Biol. Chem. 1994, 269:15229-15237.
56. Brooke N.M., et al. The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster. Nature 1998, 392:920-922.
57. de Rosa R., et al. Caudal and even-skipped in the annelid Platynereis dumerilii and the ancestry of posterior growth. Evol. Dev. 2005, 7:574-587.
58. Ferrier D.E. Evolution of Hox complexes. Adv. Exp. Med. Biol. 2010, 689:91-100.
59. Lewis E.B. A gene complex controlling segmentation in Drosophila. Nature 1978, 276:565-570.
60. Gehring W.J., et al. Homeodomain proteins. Annu. Rev. Biochem. 1994, 63:487-526.
61. Schubert F.R., et al. The Antennapedia-type homeobox genes have evolved from three precursors separated early in metazoan evolution. Proc. Natl. Acad. Sci. USA 1993, 90:143-147.
62. Zhang J., Nei M. Evolution of Antennapedia-class homeobox genes. Genetics 1996, 142:295-303.
63. García-Fernández J. Hox, ParaHox, ProtoHox: facts and guesses. Heredity 2005, 94:145-152.
64. García-Fernández J. The genesis and evolution of homeobox gene clusters. Nat. Rev. Genet. 2005, 6:881-892.
65. Furlong R.F., et al. A degenerate ParaHox gene cluster in a degenerate vertebrate. Mol. Biol. Evol. 2007, 24:2681-2686.
66. Ruvkun G., Hobert O. The taxonomy of developmental control in Caenorhabditis elegans. Science 1998, 282:2033-2041.
67. Peterson K.J. Isolation of Hox and Parahox genes in the hemichordate Ptychodera flava and the evolution of deuterostome Hox genes. Mol. Phylogenet. Evol. 2004, 31:1208-1215.
68. Baguñà J., et al. Back in time: a new systematic proposal for the Bilateria. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2008, 363:1481-1491.