Abstract
BackgroundIn cephalochordates (amphioxus), the notochord runs along the dorsal to the anterior tip of the body. In contrast, the vertebrate head is formed anterior to the notochord, as a result of head organizer formation in anterior mesoderm during early development. A key gene for the vertebrate head organizer, goosecoid (gsc), is broadly expressed in the dorsal mesoderm of amphioxus gastrula. Amphioxus gsc expression subsequently becomes restricted to the posterior notochord from the early neurula. This has prompted the hypothesis that a change in expression patterns of gsc led to development of the vertebrate head during chordate evolution. However, molecular mechanisms of head organizer evolution involving gsc have never been elucidated.ResultsTo address this question, we compared cis-regulatory modules of vertebrate organizer genes between amphioxus, Branchiostoma japonicum, and frogs, Xenopus laevis and Xenopus tropicalis. Here we show conservation and diversification of gene regulatory mechanisms through cis-regulatory modules for gsc, lim1/lhx1, and chordin in Branchiostoma and Xenopus. Reporter analysis using Xenopus embryos demonstrates that activation of gsc by Nodal/FoxH1 signal through the 5′ upstream region, that of lim1 by Nodal/FoxH1 signal through the first intron, and that of chordin by Lim1 through the second intron, are conserved between amphioxus and Xenopus. However, activation of gsc by Lim1 and Otx through the 5′ upstream region in Xenopus are not conserved in amphioxus. Furthermore, the 5′ region of amphioxus gsc recapitulated the amphioxus-like posterior mesoderm expression of the reporter gene in transgenic Xenopus embryos.ConclusionsOn the basis of this study, we propose a model, in which the gsc gene acquired the cis-regulatory module bound with Lim1 and Otx at its 5′ upstream region to be activated persistently in anterior mesoderm, in the vertebrate lineage. Because Gsc globally represses trunk (notochord) genes in the vertebrate head organizer, this cooption of gsc in vertebrates appears to have resulted in inhibition of trunk genes and acquisition of the head organizer and its derivative prechordal plate.
Highlights
IntroductionIn cephalochordates (amphioxus), the notochord runs along the dorsal to the anterior tip of the body
In cephalochordates, the notochord runs along the dorsal to the anterior tip of the body
We focused on head organizer genes in vertebrates, otx2, lim1, goosecoid, and chordin, by comparing their gene regulatory networks (GRNs) during head formation in frogs (Xenopus) and amphioxus
Summary
In cephalochordates (amphioxus), the notochord runs along the dorsal to the anterior tip of the body. The vertebrate head is formed anterior to the notochord, as a result of head organizer formation in anterior mesoderm during early development. Amphioxus gsc expression subsequently becomes restricted to the posterior notochord from the early neurula This has prompted the hypothesis that a change in expression patterns of gsc led to development of the vertebrate head during chordate evolution. In the Vertebrata, the head is formed anterior to the notochord, suggesting evolutionary development of a “new head” in the space anterior to the notochord [1, 2]. This head includes two lobes of the telencephalon, paired eyes, placodes, and cranial neural crest cells, which are lacking in amphioxus [3, 4]. The definition of the vertebrate head remains problematic and involves many anatomical features, such as nerves, skeletal elements, and muscles, here we characterize the vertebrate head as the anteriorly enlarged central nervous system (forebrain) derived from anterior neuroectoderm, which is formed during gastrulation
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