Advertisement
JOURNAL ARTICLES
Tail formation as a continuation of gastrulation: the multiple cell populations of the Xenopus tailbud derive from the late blastopore lip
L.K. Gont, H. Steinbeisser, B. Blumberg, E.M. de Robertis
Development 1993 119: 991-1004;

Summary

Three lines of evidence suggest that tail formation in Xenopus is a direct continuation of events initiated during gastrulation. First, the expression of two gene markers, Xbra and Xnot2, can be followed from the blastopore lip into distinct cell populations of the developing tailbud. Second, the tip of the tail retains Spemann's tail organizer activity until late stages of development. Third, lineage studies with the tracer DiI indicate that the cells of the late blastopore are fated to form specific tissues of the tailbud, and that intercalation of dorsal cells continues during tail elongation. In particular, the fate map shows that the tip of the tail is a direct descendant of the late dorsal blastopore lip. Thus, the tailbud is not an undifferentiated blastema as previously thought, but rather consists of distinct cell populations which arise during gastrulation.

REFERENCES

    1. Blumberg B.,
    2. Mangelsdorf D. J.,
    3. Dyck J. A.,
    4. Bittner D. A.,
    5. Evans R. M.,
    6. De Robertis E. M.
    (1992). Multiple retinoid-responsive receptors in a single cell: Families of retinoid ‘X’ receptors and retinoic acid receptors in the Xenopus egg. Proc. Natl. Acad. Sci. USA 89, 2321–2325
    OpenUrlAbstract/FREE Full Text
    1. Burglin T. R.,
    2. Finney M.,
    3. Coulson A.,
    4. Ruvkun G.
    (1989). Caenorhabditis elegans has scores of homeobox-containing genes. Nature 341, 239–243
    OpenUrlCrossRefPubMed
    1. Cho K. W. Y.,
    2. Blumberg B.,
    3. Steinbeisser H.,
    4. De Robertis E. M.
    (1991). Molecular nature of Spemann's organizer:the role of the Xenopus homeobox gene goosecoid. Cell 67, 1111–1120
    OpenUrlCrossRefPubMedWeb of Science
    1. Cho K. W. Y.,
    2. Morita E. A.,
    3. Wright C. V. E.,
    4. De Robertis E. M.
    (1991). Overexpression of a homeodomain protein confers axis-forming activity to uncommitted Xenopus embryonic cells. Cell 65, 55–64
    OpenUrlCrossRefPubMedWeb of Science
    1. Cunliffe V.,
    2. Smith J. C.
    (1992). Ectopic mesoderm formation in Xenopus embryos caused by widespread expression of a Brachyury homologue. Nature 358, 427–430
    OpenUrlCrossRefPubMed
    1. Devereux J.,
    2. Haeverli P.,
    3. Smithies O.
    (1984). A comprehensive set of sequence analysis programs for the VAX. Nuc. Acids Res 12, 387–395
    OpenUrlAbstract/FREE Full Text
    1. Dixon J. E.,
    2. Kintner C. R.
    (1989). Cellular contacts required for neural induction in Xenopus embryos: evidence for two signals. Development 106, 749–757
    OpenUrlAbstract/FREE Full Text
    1. Dobrovolskaia-Zavadskaia N.
    (1927). Sur la mortification spontanee de la queue chez la souris nouveau-nee et sur l'existence d'un caractere heriditaire ‘non-viable’. C. R. Soc. Biol 97, 114–116
    OpenUrlWeb of Science
    1. Doniach T.,
    2. Phillips C. R.,
    3. Gerhart J. C.
    (1992). Planar induction of anteroposterior pattern in the developing central nervous system of Xenopus laevis. Science 257, 542–545
    OpenUrlAbstract/FREE Full Text
    1. Elsdale T.,
    2. Davidson D.
    (1983). Somitogenesis in amphibia IV. The dynamics of tail development. J. Embryol. Exp. Morph 76, 157–176
    OpenUrlPubMed
    1. Gimlich R.,
    2. Braun J.
    (1985). Improved fluorescent compounds for tracing cell lineage. Dev. Biol 109, 509–514
    OpenUrlCrossRefPubMedWeb of Science
    1. Gluecksohn-Schoenheimer S.
    (1938). The development of two tailless mutants in the house mouse. Genetics 23, 573–584
    OpenUrlFREE Full Text
    1. Green B. A.,
    2. New H.,
    3. Smith J. C.
    (1992). Responses of embryonic Xenopus cells to activin and FGF are separated by multiple dose thresholds and correspond to distinct axes of the mesoderm. Cell 71, 731–739
    OpenUrlCrossRefPubMedWeb of Science
    1. Griffith C. M.,
    2. Wiley M. J.,
    3. Sanders E. J.
    (1992). The vertebrate tail bud: three germ layers from one tissue. Anat. Embryol 185, 101–113
    OpenUrlPubMed
    1. Gurdon J. B.
    (1976). Injected nuclei in frog oocytes: fate, enlargement and chromatin dispersal. J. Embryol. Exp. Morph 36, 523–540
    OpenUrlPubMedWeb of Science
    1. Harland R. M.
    (1991). In situ hybridization: An improved whole-mount method for Xenopus embryos. Meth. Cell Biol 36, 685–695
    OpenUrlCrossRefPubMedWeb of Science
    1. Herrmann B. G.
    (1991). Expression pattern of the Brachyury gene in whole-mount T wis/ T wismutant embryos. Development 113, 913–917
    OpenUrlAbstract
    1. Holmdahl D. E.
    (1925). Experimentelle Untersuchungen uber die Lage der Grenze zwischen primärer und sekundärer Körperentwicklung beim Huhn. Anat. Anz 59, 393–396
    OpenUrl
    1. Isaacs H. V.,
    2. Tannahill D.,
    3. Slack J. M. W.
    (1992). Expression of a novel FGF in the Xenopus embryo. A new candidate inducing factor for mesoderm formation and anteroposterior specification. Development 114, 711–720
    OpenUrlAbstract
    1. Izpisúa Belmonte J. C.,
    2. De Robertis E. M.,
    3. Storey K. G.,
    4. Stern C. D.
    (1993). The homeobox gene goosecoid and the origin of organizer cells in the early chick blastoderm. Cell 76, 645–659
    OpenUrl
    1. Keller R. E.
    (1976). Vital dye mapping of the gastrula and neurula of Xenopus II. Prospective areas and morphogenic movements of the deep layer. Dev. Biol 51, 118–137
    OpenUrlCrossRefPubMedWeb of Science
    1. Keller R.,
    2. Danilchik M.
    (1988). Regional expression, pattern and timing of convergence and extension during gastrulation of Xenopus laevis. Development 103, 193–209
    OpenUrlAbstract
    1. Kimelman D.,
    2. Christian J. L.,
    3. Moon R. T.
    (1992). Synergistic principles of development:overlapping patterning systems in Xenopus mesoderm induction. Development 116, 1–9
    OpenUrlAbstract
    1. Kingsbury B. F.
    (1932). The ‘law’ of cephalocaudal differential growth in its application to the nervous system. J. Comp. Neur 56, 431–463
    OpenUrlCrossRef
    1. Mackenzie I. R. A.,
    2. Gilbert J. J.
    (1991). Cysts of the neuraxis of endodermal origin. J. Neurology, Neurosurgery and Psychiatry 54, 572–575
    OpenUrlAbstract/FREE Full Text
    1. Niehrs C.,
    2. De Robertis E. M.
    (1991). Ectopic expression of a homeobox gene changes cell fate in Xenopus embryos in a position-specific manner. EMBO J 10, 3621–3629
    OpenUrlPubMed
    1. Niehrs C.,
    2. Keller R.,
    3. Cho K. W. Y.,
    4. De Robertis E. M.
    (1993). The homeobox gene goosecoid controls cell migration in Xenopus embryos. Cell 72, 491–503
    OpenUrlCrossRefPubMedWeb of Science
    1. Pasteels J.
    (1943). Proliferations et croissance dans la gastrulation et la formation de la queue des Vertebres. Archives de Biologie 54, 1–51
    OpenUrl
    1. Rhaney H.,
    2. Barclay G. P. T.
    (1959). Enterogenous cysts and congenital diverticula of the alimentary canal with abnormalities of the vertebral column and spinal cord. J. Pathol. Bacteriol 77, 457–471
    OpenUrlCrossRefPubMedWeb of Science
    1. Ruiz i Altaba A.
    (1992). Planar and vertical signals in the induction and patterning of the Xenopus nervous system. Development 116, 67–80
    OpenUrlAbstract
    1. Ruiz i Altaba A.,
    2. Melton D. A.
    (1989). Interaction between peptide growth factors and homeobox genes in the establishment of anteroposterior polarity in frog embryos. Nature 341, 33–38
    OpenUrlCrossRefPubMedWeb of Science
    1. Schulte-Merker S.,
    2. Ho R. K.,
    3. Herrmann B. G.,
    4. Nusslein-Volhard C.
    (1992). The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo. Development 116, 1021–1032
    OpenUrlAbstract/FREE Full Text
    1. Selleck M. A. J.,
    2. Stern C. D.
    (1991). Fate mapping and cell lineage analysis of Hensen's node in the chick embryo. Development 112, 615–626
    OpenUrlAbstract
    1. Shih J.,
    2. Keller R.
    (1992). Cell motility driving mediolateral intercalation in explants of Xenopus laevis. Development 116, 901–914
    OpenUrlAbstract/FREE Full Text
    1. Sive H. L.
    (1993). The frog prince-ss: A molecular formula for dorsoventral patterning in Xenopus. Genes Dev 7, 1–12
    OpenUrlFREE Full Text
    1. Smith J. C.,
    2. Price B. M. J.,
    3. Green J. B. A.,
    4. Weigel D.,
    5. Herrmann B. G.
    (1991). Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 67, 79–87
    OpenUrlCrossRefPubMedWeb of Science
    1. Smith J. C.,
    2. Slack J. M. W.
    (1983). Dorsalization and neural induction: properties of the organizer in Xenopus laevis. J. Embryol. Exp. Morph 78, 299–317
    OpenUrlPubMedWeb of Science
    1. Spemann H.
    (1931). Über den Anteil von Implantat und Wirtskeim an der Orientierung und Beschaffenheit der induzierten Embryonalanlage. Wilhelm Roux' Arch. EntwMech. Org 123, 389–517
    OpenUrl
    1. Spofford W.
    (1948). Observations on the posterior part of the neural plate in amblystoma. J. Exp. Zool 107, 123–163
    OpenUrlCrossRefPubMed
    1. Spratt N. T. Jr.
    (1955). Analysis of the organizer center in the early chick embryo. I. Localization of prospective notochord and somite cells. J. Exp. Zool 128, 121–163
    OpenUrlCrossRef
    1. von Dassow G.,
    2. Schmidt J. E.,
    3. Kimelman D.
    (1993). Induction of1004the Xenopus organizer: expression and regulation of Xnot, a novel FGF and activin-regulated homeobox gene. Genes Dev 7, 355–366
    OpenUrlAbstract/FREE Full Text
    1. Whittaker C. A.,
    2. DeSimone D. W.
    (1993). Integrin a subunit mRNAs are differentially expressed in early Xenopus embryos. Development 117, 1239–1249
    OpenUrlAbstract
    1. Winklbauer R.
    (1990). Mesodermal cell migration during Xenopus gastrulation. Dev. Biol 142, 155–168
    OpenUrlCrossRefPubMedWeb of Science
    1. Wolda S. L.,
    2. Moody C. J.,
    3. Moon R. T.
    (1993). Overlappingexpression of Xwnt-3A and Xwnt-1 in neural tissue of Xenopus laevis embryos. Dev. Biol 155, 46–57
    OpenUrlCrossRefPubMedWeb of Science
    1. Yntema C. L.
    (1968). A series of stages in the embryonic development of Cheldra serpentina. J. Morph 125, 219–252
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Tail formation as a continuation of gastrulation: the multiple cell populations of the Xenopus tailbud derive from the late blastopore lip
L.K. Gont, H. Steinbeisser, B. Blumberg, E.M. de Robertis
Development 1993 119: 991-1004;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

The people behind the papers – George Britton and Aryeh Warmflash

George and Aryeh

First author George Britton and his supervisor Aryeh Warmflash discuss their new Development paper in which they apply advanced in vitro culturing techniques to investigate embryonic ectoderm patterning.

Travelling Fellowship – New imaging approach unveils a bigger picture

Highlights from Travelling Fellowship trips

Find out how Pamela Imperadore’s Travelling Fellowship grant from The Company of Biologists took her to Germany, where she used new imaging techniques to investigate the cellular machinery underlying octopus arm regeneration. Don’t miss the next application deadline for 2020 travel, coming up on 29 November. Where will your research take you?

Protein function can be controlled by light using optogenetic techniques. In their new Primer, Stefano De Renzis and his colleagues in Heidelberg provide an overview of the most commonly used optogenetic tools and their application in developmental biology.

preLights – Self-organised symmetry breaking in zebrafish reveals feedback from morphogenesis to pattern formation

Sundar Naganathan

preLighter Sundar Naganathan explains his selected preprint by Vikas Trivedi, Benjamin Steventon and their co-workers on pescoids, a new in vitro model system to study early zebrafish embryogenesis.

Spotlight – Can laboratory model systems instruct human limb regeneration?

An extract from a schematic demonstrating the possible pipeline for how discovery in lab model systems can influence applications for regenerative therapies.

One of the most challenging objectives of tissue regeneration research is regrowth of a lost or amputated limb. Here, Ben Cox, Maximina Yun and Kenneth Poss outline the research avenues yet to be explored to move closer to this capstone achievement.

Articles of interest in our sister journals

Tox4 modulates cell fate reprogramming

Lotte Vanheer, Juan Song, Natalie De Geest, Adrian Janiszewski, Irene Talon, Caterina Provenzano, Taeho Oh, Joel Chappell, Vincent Pasque
Journal of Cell Science

Drosophila melanogaster: a simple system for understanding complexity

Stephanie E. Mohr, Norbert Perrimon
Disease Models & Mechanisms