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      Molecular Characterization of the Gastrula in the Turtle Emys orbicularis: An Evolutionary Perspective on Gastrulation

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          Abstract

          Due to the presence of a blastopore as in amphibians, the turtle has been suggested to exemplify a transition form from an amphibian- to an avian-type gastrulation pattern. In order to test this hypothesis and gain insight into the emergence of the unique characteristics of amniotes during gastrulation, we have performed the first molecular characterization of the gastrula in a reptile, the turtle Emys orbicularis. The study of Brachyury, Lim1, Otx2 and Otx5 expression patterns points to a highly conserved dynamic of expression with amniote model organisms and makes it possible to identify the site of mesoderm internalization, which is a long-standing issue in reptiles. Analysis of Brachyury expression also highlights the presence of two distinct phases, less easily recognizable in model organisms and respectively characterized by an early ring-shaped and a later bilateral symmetrical territory. Systematic comparisons with tetrapod model organisms lead to new insights into the relationships of the blastopore/blastoporal plate system shared by all reptiles, with the blastopore of amphibians and the primitive streak of birds and mammals. The biphasic Brachyury expression pattern is also consistent with recent models of emergence of bilateral symmetry, which raises the question of its evolutionary significance.

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          Most cited references47

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          Expression pattern of the mouse T gene and its role in mesoderm formation.

          Formation of mesoderm is a crucial event in vertebrate development, establishing many of the important features of the body. Recent studies have implicated molecules that are similar to growth factors in mesoderm formation in Xenopus, but other gene products involved in this process have yet to be identified. Genetic evidence indicates that in the mouse the T gene (Brachyury) has a role in the formation and organization of mesoderm. Mice homozygous for mutant alleles of the T gene do not generate enough mesoderm, and show severe disruption in morphogenesis of mesoderm-derived structures, in particular the notochord. The cloning of the T gene has now allowed us to examine its expression pattern. We report that T-gene expression occurs in both early stage mesoderm and its epithelial progenitor, and then becomes restricted to the notochord. This expression pattern correlates with the tissues affected in the T-gene mutant, and indicates that the T gene has a direct role in the early events of mesoderm formation and in the morphogenesis of the notochord.
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            Neural induction: old problem, new findings, yet more questions.

            During neural induction, the embryonic neural plate is specified and set aside from other parts of the ectoderm. A popular molecular explanation is the 'default model' of neural induction, which proposes that ectodermal cells give rise to neural plate if they receive no signals at all, while BMP activity directs them to become epidermis. However, neural induction now appears to be more complex than once thought, and can no longer be fully explained by the default model alone. This review summarizes neural induction events in different species and highlights some unanswered questions about this important developmental process.
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              Requirement for Lim1 in head-organizer function.

              Lim1 is a homeobox gene expressed in the organizer region of mouse embryos. To investigate the role of Lim1 during embryogenesis, a targeted deletion of the Lim1 gene was generated in embryonic stem cells. Embryos homozygous for the null allele lacked anterior head structures but the remaining body axis developed normally. A partial secondary axis developed anteriorly in some mutant embryos. Lim1 is thus an essential regulator of the vertebrate head organizer.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2008
                16 July 2008
                : 3
                : 7
                : e2676
                Affiliations
                [1 ]Développement et Evolution des vertébrés, UMR 6218, CNRS et Université d'Orléans, Orleans, France
                [2 ]Institut Jacques Monod, UMR7592, CNRS et Université Pierre et Marie Curie-Paris6 and Paris7, Paris, France
                University of Maryland, United States of America
                Author notes

                Conceived and designed the experiments: MC SM. Performed the experiments: MC DN JLP AG TSS. Analyzed the data: MC AM SM. Contributed reagents/materials/analysis tools: CP. Wrote the paper: MC SM. Obtained turtles' embryos: CP.

                [¤a]

                Current address: Franconville, France,

                [¤b]

                Current address: Department of Biological Chemistry, University of California Los Angeles, Los Angeles, California, United States of America,

                [¤c]

                Current address: Howard Hughes Medical Institute, University of California Los Angeles, Los Angeles, California, United States of America,

                [¤d]

                Current address: Division of Biology, California Institute of Technology, Pasadena, California, United States of America

                Article
                08-PONE-RA-03730R1
                10.1371/journal.pone.0002676
                2442194
                18628985
                caecf6dc-decb-479d-9f59-27f68a5be861
                Coolen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 13 February 2008
                : 23 May 2008
                Page count
                Pages: 10
                Categories
                Research Article
                Developmental Biology/Developmental Evolution
                Evolutionary Biology/Developmental Evolution
                Evolutionary Biology/Developmental Molecular Mechanisms

                Uncategorized
                Uncategorized

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