Abstract
Cranial neurogenic placodes have been considered vertebrate innovations. However, anterior neural plate border (ANB) cells of ascidian embryos share many properties with vertebrate neurogenic placodes; therefore, it is now believed that the last common ancestor of vertebrates and ascidians had embryonic structures similar to neurogenic placodes of vertebrate embryos. Because BMP signaling is important for specifying the placode region in vertebrate embryos, we examined whether BMP signaling is also involved in gene expression in the ANB region of ascidian embryos. Our data indicated that Admp, a divergent BMP family member, is mainly responsible for BMP signaling in the ANB region, and that two BMP-antagonists, Noggin and Chordin, restrict the domain, in which BMP signaling is activated, to the ANB region, and prevent it from expanding to the neural plate. BMP signaling is required for expression of Foxg and Six1/2 at the late gastrula stage, and also for expression of Zf220, which encodes a zinc finger transcription factor in late neurula embryos. Because Zf220 negatively regulates Foxg, when we downregulated Zf220 by inhibiting BMP signaling, Foxg was upregulated, resulting in one large palp instead of three palps (adhesive organs derived from ANB cells). Functions of BMP signaling in specification of the ANB region give further support to the hypothesis that ascidian ANB cells share an evolutionary origin with vertebrate cranial placodes.
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Acknowledgements
We thank Reiji Masuda, Shinichi Tokuhiro, Chikako Imaizumi (Kyoto University), Manabu Yoshida (University of Tokyo), and other members working under the National BioResource Project for Ciona (MEXT, Japan) at Kyoto University. We also thank the University of Tokyo for providing experimental animals.
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This research was supported by grants from the Japan Society for the Promotion of Science under the grant numbers 21H02486 and 21H05239 to YS.
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BL and XR performed experiments. BL and YS drafted the original manuscript. BL, XR, and YS reviewed the manuscript draft, revised it, and approved the final version.
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Liu, B., Ren, X. & Satou, Y. BMP signaling is required to form the anterior neural plate border in ascidian embryos. Dev Genes Evol 233, 13–23 (2023). https://doi.org/10.1007/s00427-023-00702-0
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DOI: https://doi.org/10.1007/s00427-023-00702-0