Hostname: page-component-848d4c4894-p2v8j Total loading time: 0 Render date: 2024-05-07T15:22:13.524Z Has data issue: false hasContentIssue false
  • English
  • Français

The molecular control of spatial patterning in amphioxus

Published online by Cambridge University Press:  11 May 2009

P. W. H. Holland ,
J. Garcia-Fernàndez ,
L. Z. Holland ,
N. A. Williams  and
N. D. Holland
P. W. H. Holland
Affiliation:
Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS
J. Garcia-Fernàndez
Affiliation:
Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS
L. Z. Holland
Affiliation:
Scripps Institution of Oceanography, University of California, San Diego, CA 92093, USA
N. A. Williams
Affiliation:
Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS
N. D. Holland
Affiliation:
Scripps Institution of Oceanography, University of California, San Diego, CA 92093, USA
Get access Rights & Permissions [Opens in a new window]

Extract

The embryology of amphioxus (Chordata: Cephalochordata) has features in common with vertebrate embryology, reflecting a close phylogenetic relationship between the two taxa. Amphioxus differs from vertebrates, however, in having less complex organogenesis and cranial morphogenesis, and less specialization along the anteroposterior body axis. Here we illustrate this by describing the embryology of an amphioxus species, Branchiostoma floridae. To gain further insight into the origins, evolutionary divergence and comparative embryology of these taxa, we are comparing the molecular control of embryonic development in amphioxus and vertebrates. For these analyses, we are focusing on homeobox genes: a diverse multigene family implicated in developmental control in many Metazoa. We report the results of PCR-based experiments which reveal that the amphioxus genome has homeobox genes from several recognized gene classes. The PCR experiments also suggest that amphioxus has fewer ‘Hox’ and ‘Msx’ class homeobox genes than do vertebrates. We suggest, therefore, that amphioxus may be a living descendant from an intermediate stage in the evolution of homeobox gene family complexity, and the complexity of vertebrate developmental control. The pattern of gene expression during embryogenesis has been described for one amphioxus homeobox gene of the Hox class. This gene is primarily expressed in the presumptive neural tube of amphioxus neurulae, later embryos and larvae, in a spatially-restricted manner. The expression data lead us to suggest that Hox genes are involved in the control of spatial patterning in the neural tube of amphioxus; the data are also interpreted as giving insight into possible homology between the amphioxus and vertebrate body plans.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 74 , Issue 1 , February 1994 , pp. 49 - 60
Copyright
Copyright © Marine Biological Association of the United Kingdom 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Averof, M. & Akam, M., 1993. HOM/Hox genes of Artemia: implications for the origin of insect and crustacean body plans. Current Biology, 3, 73–78.CrossRefGoogle ScholarPubMed
Burglin, T., 1993. A comprehensive classification of homeobox genes. In A guidebook for homeobox genes (ed. D., Duboule), pp. 27–71. Oxford: Oxford University Press.Google Scholar
Conklin, E.G., 1932. The embryology of amphioxus. Journal of Morphology, 54, 69–151.CrossRefGoogle Scholar
Conway-Morris, S., 1993. The fossil record and the early evolution of the Metazoa. Nature, London, 361, 219–225.CrossRefGoogle Scholar
Frohman, M.A., Boyle, M. & Martin, G.R., 1990. Isolation of the mouse Hox-2·9 gene; analysis of embryonic expression suggests that positional information along the anterior-posterior axis is specified by mesoderm. Development, 110, 589–607.CrossRefGoogle ScholarPubMed
Gaunt, S.J., 1991. Expression patterns of mouse Hox genes: clues to an understanding of developmental and evolutionary strategies. BioEssays, 13, 505–513.CrossRefGoogle Scholar
Graham, A., 1992. Patterning the rostrocaudal axis of the hindbrain. Seminars in the Neurosciences, 4, 307–315.CrossRefGoogle Scholar
Hatschek, B., 1881. Studien über Entwicklung des Amphioxus. Arbeiten aus den Zoologischen Institute der Universität Wien und der Zoologischen Station in Triest, 4, 1–88.Google Scholar
Hirakow, R. & Kajita, N., 1990. An electron microscopic study of the development of amphioxus, Branchiostoma belcheri tsingtauense: cleavage. Journal of Morphology, 203, 331–344.CrossRefGoogle ScholarPubMed
Hirakow, R. & Kajita, N., 1991. Electron microscopic study of the development of amphioxus, Branchiostoma belcheri tsingtauense: the gastrula. Journal of Morphology, 207, 37–52.CrossRefGoogle ScholarPubMed
Holland, L.Z. & Holland, N.D., 1992. Early development in the lancelet (=amphioxus) Branchiostoma floridae from sperm entry through pronudear fusion: presence of vegetal pole plasm and lack of conspicuous ooplasmic segregation. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 182, 77–96.CrossRefGoogle ScholarPubMed
Holland, N.D. & Holland, L.Z., 1989. Fine structural study of the cortical reaction and formation of the egg coatsinalancelet(=amphioxus), Branchiostoma floridae (Phylum Chordata:SubphylumCephalochordata = Acrania). Biological Bulletin. Marine Biological Laboratory, Woods Hole, 176, 111–122.CrossRefGoogle Scholar
Holland, N.D. & Holland, L.Z., 1993. Embryos and larvae of invertebrate deuterostomes. In Essential developmental biology: a practical approach (ed. C.D., Stern and P.W.H., Holland). Oxford: IRL Press.Google Scholar
Holland, P.W.H., 1990. Homeobox genes and segmentation: co-option, co-evolution, and convergence. Seminars in Developmental Biology, 1, 135–145.Google Scholar
Holland, P.W.H., 1991. Cloning and evolutionary analysis of msh-like homeobox genes from mouse, zebrafish and ascidian. Gene, 98, 253–257.CrossRefGoogle ScholarPubMed
Holland, P.W.H., 1992. Homeobox genes in vertebrate evolution. BioEssays, 14, 267–273.CrossRefGoogle ScholarPubMed
Holland, P.W.H., 1993. Cloning genes using PCR. In Essential developmental biology: a practical approach (ed. C.D., Stern and P.W.H., Holland), pp. 243–255. Oxford: IRL Press.CrossRefGoogle Scholar
Holland, P.W.H. & Hogan, B.L.M., 1988. Expression of homeobox genes during mouse development: a review. Genes and Development, 2, 773–782.CrossRefGoogle ScholarPubMed
Holland, P.W.H., Holland, L.Z., Williams, N. A. & Holland, N.D., 1992a. An amphioxus homeobox gene: sequence conservation, spatial expression during development and insights into vertebrate evolution. Development, 116, 653–661.CrossRefGoogle ScholarPubMed
Holland, P.W.H., Ingham, P.W. & Krauss, S., 1992b. Development and evolution: mice and flies head to head. Nature, London, 358, 627–628.CrossRefGoogle ScholarPubMed
Holland, P.W.H. & Williams, N.A., 1990. Conservation of engrailed-like homeobox sequences during vertebrate evolution. FEBS Letters, 277, 250–252.CrossRefGoogle ScholarPubMed
Hunt, P., Gulisano, M., Cook, M., Sham, M.-H., Faiella, A., Wilkinson, D., Boncinelli, E. & Krumlauf, R., 1991. A distinct Hox code for the branchial region of the vertebrate head. Nature, London, 353, 861–864.CrossRefGoogle ScholarPubMed
Kappen, C., Schughart, K. & Ruddle, F.H., 1989. Two steps in the evolution of Antennapedia class vertebrate homeobox genes. Proceedings of the National Academy of Sciences of the United States of America, 86, 5459–5463.CrossRefGoogle ScholarPubMed
Lankester, E.R. & Willey, A., 1890. The development of the atrial chamber of amphioxus. Quarterly Journal of Microscopical Science, 31, 445–466.Google Scholar
Lumsden, A., 1990. The cellular basis of segmentation in the developing hindbrain. Trends in Neurosciences, 13, 329–335.CrossRefGoogle ScholarPubMed
McGinnis, W. & Krumlauf, R., 1992. Homeobox genes and axial patterning. Cell, 68, 283–302.CrossRefGoogle ScholarPubMed
Murtha, M.T., Leckman, J.F. & Ruddle, F.H., 1991. Detection of homeobox genes in development and evolution. Proceedings of the National Academy of Sciences of the United States of America, 88, 10711–10715.CrossRefGoogle ScholarPubMed
Northcutt, R.G. & Gans, C., 1983. The genesis of neural crest and epidermal placodes: a reinterpretation of vertebrate origins. Quarterly Review of Biology, 58, 1–28.CrossRefGoogle ScholarPubMed
Sham, M.-H., Hunt, P., Nonchev, S., Papalopulu, N., Graham, A., Boncinelli, E. & Krumlauf, R., 1992. Analysis of the murine Hox-2·7 gene: conserved alternative transcripts with differential distributions in the nervous system and the potential for shared regulatory regions. EMBO Journal, 11, 1825–1836.CrossRefGoogle ScholarPubMed
Slack, J.M.W., Holland, P.W.H. & Graham, C.F., 1993. The zootype and the phylotypic stage. Nature, London, 361, 490–492.CrossRefGoogle ScholarPubMed
Wedeen, C.J., Kostriken, R.G., Matsumura, I. & Weisblat, D.A., 1990. Evidence for a new family of evolutionarily conserved homeobox genes. Nucleic Acids Research, 18, 1908.CrossRefGoogle ScholarPubMed
Willey, A., 1894. Amphioxus and the ancestry of the vertebrates. New York: MacMillan.Google Scholar