Body-plan evolution in the Bilateria: Early antero-posterior patterning and the deuterostome-protostome dichotomy

Current Opinion in Genetics and Development

Volumn 10, Issue 4, 2000, Pages 434-442

  Holland, Linda Z ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBOSOME DNA;

EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; GASTRULATION; METAZOON; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 0033939644     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(00)00109-X     Document Type: Review

References (79)

1. Graham A. Animal phylogeny: root and branch surgery. Curr Biol. 10:2000;36-38. Phylogenies based on Hox genes and 18S rDNA both divide the Bilateria into lophotrochozoans, ecdysozoans, and deuterostomes. In this scheme, Caenorhabditis is no longer a basal protostome, but a (possibly degenerate) ecdysozoan.
2. Gilbert S.F. Developmental Biology. Fifth Edition:1997;Sinauer, Sunderland, Mass.
3. Miller J.R., Rowning B.A., Larabell C.A., Yang-Snyder J.A., Bates R.L., Moon R.T. Establishment of the dorsal-ventral axis in Xenopus embryos coincides with the dorsal enrichment of dishevelled that is dependent on cortical rotation. J Cell Biol. 146:1999;427-437.
4. De Robertis E.M., Sasai Y. A common plan for dorso-ventral patterning in Bilateria. Nature. 380:1996;37-40.
5. Nellen D., Burke R., Struhl G., Balser K. Direct and long range action of a DPP morphogen gradient. Cell. 85:1996;357-368.
6. Goldstein B., Hird S.N. Specification of the antero-posterior axis in Caenorhabditis elegans. Development. 122:1996;1467-1474.
7. Tamura K., Yonei-Tamura S., Belmonté J.C. Molecular basis of left-right asymmetry. Dev Growth Differentiation. 41:1999;645-656.
8. Shoguchi E., Satoh N., Maruyama Y.K. Pattern of Brachyury gene expression in starfish embryos resembles that of hemichordate embryos but not of sea urchin embryos. Mech Dev. 82:1999;185-189. Expression of Brachyury in a ring around the vegetal plate corresponding to the lips of the blastopore and later in the mouth invagination is similar to that of Brachyury in a hemichordate but different from that in a sea urchin. This emphasizes that starfish, which are basal to sea urchins, are probably the more appropriate echinoderm for evolutionary studies.
9. Tagawa K., Humphreys T., Satoh N. Novel pattern of Brachyury gene expression in hemichordate embryos. Mech Dev. 75:1998;139-143.
10. •] are the first to discuss developmental gene expression in hemichordates and demonstrate the value of this basal deuterostome group for studies on body-plan evolution. They show that Brachyury is expressed around the blastopore, which, taken together with similar expression in amphioxus and vertebrates, suggests that this is the ancestral deuterostome pattern. Brachyury is not expressed in the stomochord, casting doubt on the homology of stomochord and chordate notochord. Expression in the mouth invagination, a characteristic shared with starfish, may be a derived feature in echinoderms and hemichordates.
11. Holland P.W.H., Koschorz B., Holland L.Z., Herrmann B.G. Conservation of Brachyury (T) genes in amphioxus and vertebrates: developmental and evolutionary implications. Development. 121:1995;4283-4291.
12. Zhang S.C., Holland N.D., Holland L.Z. Topographic changes in nascent and early mesoderm in amphioxus embryo studies by Dil labeling and by in situ hybridization for a Brachyury gene. Dev Genes Evol. 206:1997;532-535.
13. Harada Y., Yasuo H., Satoh N. A sea urchin homologue of the chordate Brachyury (T) gene is expressed in the secondary mesenchyme founder cells. Development. 121:1995;2747-2754.
14. Hayata T., Eisaki A., Kuroda H., Asashima M. Expression of Brachyury-like T-box transcription factor, Xbra3 in Xenopus embryo. Dev Genes Evol. 209:1999;560-563.
15. Conlon F.L., Smith J.C. Interference with Brachyury function inhibits convergent extension, causes apoptosis, and reveals separate requirements in the FGF and activin signaling pathways. Dev Biol. 213:1999;85-100.
16. Peterson K.J., Harada Y., Cameron R.A., Davidson E.H. Expression pattern of Brachyury and Not in the sea urchin: comparative implications for the origins of mesoderm in the basal deuterostomes. Dev Biol. 207:1999;419-431.
17. Corbo J.C., Fujiwara S., Levine M., Di Gregorio A. Suppressor of hairless activates Brachyury expression in the Ciona embryo. Dev Biol. 203:1998;358-368.
18. •].
19. •], the first reports of germline mutants in ascidian tunicates, demonstrate the feasibility of using these marine organisms for genetic studies. The identification of several notochord mutants should facilitate an elucidation of the genes participating with Brachury in notochord development.
20. •].
21. •] report an alternative method to obtaining germline mutants for identifying downstream targets of ascidian Brachyury. The technique is to overexpress Brachyury by linking the Brachyury coding sequence to Forkhead regulatory sequences, electroporating the construct into large numbers of embryos and constructing a subtractive cDNA library of these embryos versus normal ones.
22. Takahashi H., Mitani Y., Satoh G., Satoh N. Evolutionary alterations of the minimal promoter for notochord-specific Brachyury expression in ascidian embryos. Development. 126:1999;3725-3734. Considerable differences in Brachyury regulation in two species of ascidian are demonstrated, detailing rapid evolutionary divergence of regulatory gene regions. Although a fusion construct of Halocynthia Brachyury with 289 bp of upstream sequence directs expression to the notochords of both Halocynthia and Ciona, a 250 bp reporter construct of the Ciona Brachyury upstream region, sufficient to direct expression to the Ciona notochord, does not direct expression to the notochord of Halocynthia - a 434 bp construct is required.
23. Taguchi Tagawa K., Humphryes T., Nishino A., Satoh N., Harada Y. Characterization of a hemichordate fork head/HNF-3 gene expression. Dev Genes Evol. 210:2000;11-17.
24. Harada Y., Akasaka K., Shimada H., Peterson K.J., Davidson E.H., Satoh N. Spatial expression of a forkhead homologue in the sea urchin embryo. Mech Dev. 60:1996;163-173.
25. Simauchi Y., Yasuo H., Satoh N. Automony of ascidian fork head/HNF-3 gene expression. Mech Dev. 69:1997;143-154.
26. Olsen C.L., Jeffery W.R. A forkhead gene related to HNF3-β is required for gastrulation and axis formation in the ascidian embryo. Development. 124:1997;23 609-23 616.
27. Shimeld S.M. Characterisation of amphioxus HNF-3 genes: conserved expression in the notochord and floor plate. Dev Biol. 183:1997;74-85.
28. Dufort D., Schwartz L., Harpal K., Rossant J. The transcription factor HNF3β is required in visceral endoderm for normal primitive streak morphogenesis. Development. 125:1998;3015-3025.
29. Ruiz I Altaba A., Preziosos V.R., Darnell J.E., Jessell T.M. Sequential expression of HNF-3-β and HNF-3-α by embryonic organizing centers: The dorsal lip/node, notochord and floor plate. Mech Dev. 44:1993;91-108.
30. Beck C.W., Slack J.M.W. Analysis of the developing Xenopus tail bud reveals separate phases of gene expression during determination and outgrowth. Mech Dev. 72:1998;41-52.
31. Katsuyama Y., Sato Y., Wada S., Saiga H. Ascidian tail formation requires caudal function. Dev Biol. 213:1999;257-268.
32. Brooke N.M., Garcia-Fernàndez J., Holland P.W.H. The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster. Nature. 392:1998;920-922.
33. Pillemer G., Epstein M., Blumberg B., Yisraeli J.K., De Robertis E.M., Steinbeisser H., Fainsod A. Nested expression and sequential downregulation of the Xenopus caudal genes along the anterior-posterior axis. Mech Dev. 71:1998;193-196.
34. Epstein M., Pillemer G., Yelijhn R., Yusraeli J.K., Fainsod A. Patterning of the embryo along the anterior-posterior axis: the role of the caudal genes. Development. 124:1997;3805-3814.
35. Sherwood D.R., McClay D.R. LvNotch signaling mediates secondary mesenchyme specification in the sea urchin embryo. Development. 126:1999;1703-1713. This reference and [36] show that Notch is initially expressed in all the cells of the blastula but subsequently downregulated in cells at the center of the vegetal plate - the future secondary mesenchyme cells. Overexpression of activated and dominant negative forms of Notch demonstrate that signaling by sea urchin Notch plays a critical role in specification of these cells and probably also plays a role in patterning of the endoderm, although it is not required for commitment of cells to an endodermal fate.
36. Sherwood D.R., McClay D.R. Identification and localization of a sea urchin Notch homologue: insights into vegetal plate regionalization and Notch receptor regulation. Development. 124:1997;3363-3374.
37. Sweet H.C., Hodor P.G., Ettensohn C.A. The role of micromere signaling in Notch activation and mesoderm specification during sea urchin embryogenesis. Development. 126:1999;5255-5265. The authors of this paper show that the vegetal-most cells of the blastula, the micromeres, play an important role in the induction of secondary mesenchyme cells, possibly by presenting a ligand for the Notch receptor.
38. Beck C.W., Slack J.M.W. A developmental pathway controlling outgrowth of the Xenopus tail bud. Development. 126:1999;1611-1620.
39. Hori S., Saitoh T., Matsumoto M., Makabe K.W., Nishida H. Notch homologue from Halocynthia roretzi is preferentially expressed in the central nervous system during ascidian embryogenesis. Dev Genes Evol. 207:1997;371-380.
40. Sasakura Y., Ogasawara M., Makabe K.W. HrWnt-5: a maternally expressed ascidian Wnt gene with a posterior localization in early embryos. Int J Dev Biol. 42:1998;573-579.
41. •,44] demonstrate that a vegetal-posterior identity is conferred on vegetal cells of the late sea urchin blastula by a Wnt-signaling pathway involving the localization of β-catenin to vegetal cells and the inhibition of the pathway in animal cells by GSK3. Nuclear accumulation of β-catenin in mesoderm and endoderm precursors in the vegetal plate is cell-autonomous. TCF mediates the activity of nuclear β-catenin. The long-known effect of lithium in switching cells in the animal hemisphere to a vegetal fate is shown to be caused by an activation of the pathway in animal cells by inhibition of GSK3. This pathway is like that involved in axial patterning in Xenopus, suggesting evolutionary conservation.
42. Emily-Fenouil F., Ghiglione C., Lhomond G., Lepage T., Gache C. GSK3β/shaggy mediates patterning along the animal-vegetal axis of the sea urchin embryo. Development. 125:1998;2489-2498.
43. •].
44. Wikramanayake A.H., Huang L., Klein W.H. β-catenin is essential for patterning the maternally specified animal-vegetal axis in the sea urchin embryo. Proc Natl Acad Sci USA. 95:1998;9343-9348.
45. Liu P., Wakamiya M., Shea M.J., Albrecht U., Behringer A., Bradley A. Requirement for Wnt3 in vertebrate axis formation. Nat Genet. 22:1999;361-365.
46. Shum A.S.W., Poon L.L.M., Tang W.W.T., Koide T., Chan B.W.H., Leung Y.C.G., Shiroishi T., Copp A.J. Retinoic acid induces down-regulation of Wnt-3a, apoptosis and diversion of tail bud cells to a neural fate in the mouse embryo. Mech Dev. 84:1999;17-30.
47. Niehrs C. Head in the WNT. The molecular nature of Spemann's head organizer. Trends Genet. 15:1999;314-319.
48. Fredieu J.R., Cui Y., Maier D., Danilchik M.V., Christian J.L. Xwnt-8 and lithium can act upon either dorsal mesodermal or neurectodermal cells to cause a loss of forebrain in Xenopus embryos. Dev Biol. 186:1997;100-114.
49. Bejsovec A. Signal transduction: wnt signaling shows its versatility. Curr Biol. 9:1999;R684-R687. Emphasizes differences between Wnt-signaling pathways in Drosophila and Caenorhabditis. The β-catenin-TCF interaction and the function of GSK-3 are fundamentally different in C. elegans on the one hand and Drosophila and vertebrates on the other.
50. Sokol S.Y. Wnt signaling and dorso-ventral axis specification in vertebrates. Curr Opin Genet Dev. 9:1999;405-410.
51. Martinez-Arias A., Brown A.M.C., Brennan K. Wnt signaling: pathway or network? Curr Opin Genet Dev. 9:1999;447-454.
52. Schneider S., Steinbeisser H., Warga R.M., Hausen P. β-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mech Dev. 57:1996;191-198.
53. Schubert M., Holland L.Z., Panopoulou G.D., Lehrach H., Holland N.D. Characterization of amphioxus AmphiWnt8: insights into the evolution of patterning of the embryonic dorso-ventral axis. Evolution Dev. 2:2000;85-92.
54. Holland L.Z., Holland N.D., Schubert M. Developmental expression of AmphiWnt1, an amphioxus gene in theWnt1/wingless subfamily. Dev Genes Evol. 210:2000;. in press.
55. Yoshida S., Marikawa Y., Satoh N. Regulation of the trunk-tail patterning in the ascidian embryo: a possible interaction of cascades between lithium/β-catenin and localized maternal factor pem. Dev Biol. 202:1998;264-279.
56. Wada S., Katsuyama Y., Saiga H. Antero-posterior patterning of the epidermis by inductive influences from the vegetal hemisphere cells in the ascidian embryo. Development. 126:1999;4955-4963.
57. Angerer L.M., Angerer R.C. Animal-vegetal axis patterning mechanism in the early sea urchin embryo. Development. 218:2000;1-12.
58. Angerer L.M., Oleksyn D.W., Logan C.Y., McClay D.R., Dale L., Angerer R.C. A BMP pathway regulates cell fate allocation along the sea urchin animal-vegetal embryonic axis. Development. 127:2000;1105-1114. BMP2/4 mRNA becomes localized to the presumptive ectoderm, where it is enriched on the oral side. BMP2/4 is involved in setting the ectoderm/endoderm boundary and influences the decision between epidermal and non-epidermal differentiation of ectoderm.
59. Panopoulou G.D., Clark M.D., Holland L.Z., Lehrach H., Holland N.D. AmphiBMP2/4, an amphioxus bone morphogenetic protein closely related to Drosophila decapentaplegic and vertebrate BMP2 and BMP4: insights into evolution of dorso-ventral axis specification. Dev Dyn. 213:1998;130-139.
60. Holland N.D., Panganiban G., Henyey E.L., Holland L.Z. Sequence and development expression of AmphiDII, an amphioxus Distal-less gene transcribed in the ectoderm, epidermis and nervous system: insights into evolution of craniate forebrain and neural crest. Development. 122:1996;2911-2920.
61. •,64] demonstrate conserved expression of several genes in both the hindgut and foregut primordium of Drosophila, suggesting that similar genetic mechanisms govern fore- and hindgut development. Expression of two of these genes (Fork head and Wingless) as well as of homologs of Brachyury and caudal, is also conserved between the hindgut of Drosophila and the blastopore of chordates, suggesting homology of the chordate blastopore and hindgut primordium of Drosophila.
62. •].
63. Schultz C., Schröder R., Hausdorf B., Wolff C., Tautz D. A caudal homologue in the short germ band beetle Tribolium shows similarities to both the Drosophila and the vertebrate caudal expression patterns. Dev Genes Evol. 208:1998;283-289.
64. Hoch M., Pankraz M.J. Control of gut development by fork head and cell signaling molecules in Drosophila. Mech Dev. 58:1996;3-14.
65. Shimeld S.M. The evolution of the hedgehog gene family in chordates: insights from amphioxus hedgehog. Dev Genes Evol. 1999:1999;40-47.
66. Voronov D.A., Panchin Y.V. Cell lineage in marine nematode Enoplus brevis. Development. 125:1998;143-150.
67. Hunter C.P., Harris J.M., Maloof J.N., Kenyon C. Hox gene expression in a single Caenorhabditis elegans cell is regulated by a caudal homolog and intercellular signals that inhibit Wnt signalling. Development. 126:1999;805-814.
68. Kalb J.M., Lau K.K., Goszczynski B., Fukushige T., Moons D., Okkema P.G., McGhee J.D. pha-4 is Ce-fkh-1, a fork head/HNF-3α,β,γ homolog that functions in organogenesis of the C. elegans pharynx. Development. 125:1998;2171-2180.
69. Nielsen C. Animal Evolution: Interrelationships of the Living Phyla. 1995;Oxford University Press, Oxford, New York.
70. Ruiz-Trillo I., Riutort M., Littlewood D.T.J., Herniou E.A., Baguña J. Acoel flatworms: earliest extant bilaterian metazoans, not members of platyhelminthes. Science. 283:1999;1919-1923.
71. Adoutte A., Balavoine G., Lartillot N., Lespinet O., Prud'homme B., de Rosa R. The new animal phylogeny: reliability and implications. Proc Natl Acad Sci. 97:2000;4453-4456.
72. Arendt D., Nübler-Jung K. Similarities in fate maps and gastrulation patterns in annelids, arthropods and chordates. Mech Dev. 61:1997;7-21.
73. Matsuda-Nakagawa L.M., Gröger H., Aerne B.L., Schmid V. The HOX like gene Cnox2-Pc is expressed at the anterior region in all life cycle stages of the jellyfish Podocoryne carnea. Dev Genes Evol. 210:2000;151-156. This paper shows that Hox gene expression in a cnidarian is perpendicular to the anterior-posterior axis, not parallel as would be predicted by the enterocoel theory. In hydrozoans, the planula larva settles on the substratum by its anterior end, and the posterior end then becomes the mouth/anus end of the sessile polyp. Cnox2-PC, related to vertebrate paralog group Hox 4 genes, is expressed across the anterior end of the planula. At settlement, however, expression switches to the opposite end around the mouth/anus.
74. Martindale M.Q., Henry J.Q. The development of radial and biradial symmetry: the evolution of bilaterality. Amer Zool. 38:1998;672-684.
75. Lacalli T. Dorso-ventral axis inversion: a phylogenetic perspective. Bioessays. 18:1996;251-254.
76. Technau U., Bode H. HyBra1, a Brachyury homologue, acts during head formation in Hydra. Development. 126:1999;999-1010.
77. Martinez D.E., Dirksen M-L., Bode P.M., Jamrich M., Steele R.E., Bode H.R. Budhead, a Fork Head/HNF-3 homologue, is expressed during axis formation and head specification in Hydra. Dev Biol. 192:1999;523-536.
78. Chitnis A.B. Control of neurogenesis-lessons from frogs, fish and flies. Curr Opin Neurobiol. 9:1999;18-25.
79. Bolker J.A. Model systems in developmental biology. Bioessays. 17:1995;451-455.