Abstract
Formation of a dorsoventral axis is a key event in the early development of most animal embryos. It is well established that bone morphogenetic proteins (Bmps) and Wnts are key mediators of dorsoventral patterning in vertebrates. In the cephalochordate amphioxus, genes encoding Bmps and transcription factors downstream of Bmp signaling such as Vent are expressed in patterns reminiscent of those of their vertebrate orthologues. However, the key question is whether the conservation of expression patterns of network constituents implies conservation of functional network interactions, and if so, how an increased functional complexity can evolve. Using heterologous systems, namely by reporter gene assays in mammalian cell lines and by transgenesis in medaka fish, we have compared the gene regulatory network implicated in dorsoventral patterning of the basal chordate amphioxus and vertebrates. We found that Bmp but not canonical Wnt signaling regulates promoters of genes encoding homeodomain proteins AmphiVent1 and AmphiVent2. Furthermore, AmphiVent1 and AmphiVent2 promoters appear to be correctly regulated in the context of a vertebrate embryo. Finally, we show that AmphiVent1 is able to directly repress promoters of AmphiGoosecoid and AmphiChordin genes. Repression of genes encoding dorsal-specific signaling molecule Chordin and transcription factor Goosecoid by Xenopus and zebrafish Vent genes represents a key regulatory interaction during vertebrate axis formation. Our data indicate high evolutionary conservation of a core Bmp-triggered gene regulatory network for dorsoventral patterning in chordates and suggest that co-option of the canonical Wnt signaling pathway for dorsoventral patterning in vertebrates represents one of the innovations through which an increased morphological complexity of vertebrate embryo is achieved.
Highlights
Establishment of a dorsoventral (DV) axis is a key event in early development of any bilaterian animal embryo
Even though there appears to be a temporal difference between the ventral expression of AmphiVent1 and vertebrate Vent genes during early development, their dorsal expression is similar as exemplified by downregulation at the dorsal lip of the blastopore and neural plate [3]
We have focused on three main areas: the role of bone morphogenetic proteins (Bmps) and canonical Wnt signaling in AmphiVent1 gene regulation, functional properties of Vent proteins, and identification of direct targets of AmphiVent1 transcription factor
Summary
Establishment of a dorsoventral (DV) axis is a key event in early development of any bilaterian animal embryo. Amphioxus ventral-specific genes encoding Bmp signaling molecules, and Hex, Evx and Vent transcription factors demonstrate expression patterns homologous to their vertebrate counterparts [2,3]. The developmental expression of amphibian and teleost Vent genes during gastrula stages is most conspicuous in ventral mesoderm and is down-regulated in the regions of organizer, chordamesoderm and neural plate [5,7]. In the zebrafish embryo Wnt directly activates Vent and Vox genes through b-catenin [14] Both Xenopus Xvent-1 and Xvent-2 genes contain conserved Lef/Tcf binding sites in the promoter. We have focused on three main areas: the role of Bmp and canonical Wnt signaling in AmphiVent gene regulation, functional properties of Vent proteins, and identification of direct targets of AmphiVent transcription factor. The canonical Wnt signaling regulatory input for ventral-specific gene expression appears to be lacking in cephalochordates (this study) [17] and has likely been co-opted in vertebrates
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