Cargando…

Evolution of Developmental Programs for the Midline Structures in Chordates: Insights From Gene Regulation in the Floor Plate and Hypochord Homologues of Ciona Embryos

In vertebrate embryos, dorsal midline tissues, including the notochord, the prechordal plate, and the floor plate, play important roles in patterning of the central nervous system, somites, and endodermal tissues by producing extracellular signaling molecules, such as Sonic hedgehog (Shh). In Ciona,...

Descripción completa

Detalles Bibliográficos
Autores principales: Oonuma, Kouhei, Yamamoto, Maho, Moritsugu, Naho, Okawa, Nanako, Mukai, Megumi, Sotani, Miku, Tsunemi, Shuto, Sugimoto, Haruka, Nakagome, Eri, Hasegawa, Yuichi, Shimai, Kotaro, Horie, Takeo, Kusakabe, Takehiro G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8256262/
https://www.ncbi.nlm.nih.gov/pubmed/34235159
http://dx.doi.org/10.3389/fcell.2021.704367
_version_ 1783718066972000256
author Oonuma, Kouhei
Yamamoto, Maho
Moritsugu, Naho
Okawa, Nanako
Mukai, Megumi
Sotani, Miku
Tsunemi, Shuto
Sugimoto, Haruka
Nakagome, Eri
Hasegawa, Yuichi
Shimai, Kotaro
Horie, Takeo
Kusakabe, Takehiro G.
author_facet Oonuma, Kouhei
Yamamoto, Maho
Moritsugu, Naho
Okawa, Nanako
Mukai, Megumi
Sotani, Miku
Tsunemi, Shuto
Sugimoto, Haruka
Nakagome, Eri
Hasegawa, Yuichi
Shimai, Kotaro
Horie, Takeo
Kusakabe, Takehiro G.
author_sort Oonuma, Kouhei
collection PubMed
description In vertebrate embryos, dorsal midline tissues, including the notochord, the prechordal plate, and the floor plate, play important roles in patterning of the central nervous system, somites, and endodermal tissues by producing extracellular signaling molecules, such as Sonic hedgehog (Shh). In Ciona, hedgehog.b, one of the two hedgehog genes, is expressed in the floor plate of the embryonic neural tube, while none of the hedgehog genes are expressed in the notochord. We have identified a cis-regulatory region of hedgehog.b that was sufficient to drive a reporter gene expression in the floor plate. The hedgehog.b cis-regulatory region also drove ectopic expression of the reporter gene in the endodermal strand, suggesting that the floor plate and the endodermal strand share a part of their gene regulatory programs. The endodermal strand occupies the same topographic position of the embryo as does the vertebrate hypochord, which consists of a row of single cells lined up immediately ventral to the notochord. The hypochord shares expression of several genes with the floor plate, including Shh and FoxA, and play a role in dorsal aorta development. Whole-embryo single-cell transcriptome analysis identified a number of genes specifically expressed in both the floor plate and the endodermal strand in Ciona tailbud embryos. A Ciona FoxA ortholog FoxA.a is shown to be a candidate transcriptional activator for the midline gene battery. The present findings suggest an ancient evolutionary origin of a common developmental program for the midline structures in Olfactores.
format Online
Article
Text
id pubmed-8256262
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-82562622021-07-06 Evolution of Developmental Programs for the Midline Structures in Chordates: Insights From Gene Regulation in the Floor Plate and Hypochord Homologues of Ciona Embryos Oonuma, Kouhei Yamamoto, Maho Moritsugu, Naho Okawa, Nanako Mukai, Megumi Sotani, Miku Tsunemi, Shuto Sugimoto, Haruka Nakagome, Eri Hasegawa, Yuichi Shimai, Kotaro Horie, Takeo Kusakabe, Takehiro G. Front Cell Dev Biol Cell and Developmental Biology In vertebrate embryos, dorsal midline tissues, including the notochord, the prechordal plate, and the floor plate, play important roles in patterning of the central nervous system, somites, and endodermal tissues by producing extracellular signaling molecules, such as Sonic hedgehog (Shh). In Ciona, hedgehog.b, one of the two hedgehog genes, is expressed in the floor plate of the embryonic neural tube, while none of the hedgehog genes are expressed in the notochord. We have identified a cis-regulatory region of hedgehog.b that was sufficient to drive a reporter gene expression in the floor plate. The hedgehog.b cis-regulatory region also drove ectopic expression of the reporter gene in the endodermal strand, suggesting that the floor plate and the endodermal strand share a part of their gene regulatory programs. The endodermal strand occupies the same topographic position of the embryo as does the vertebrate hypochord, which consists of a row of single cells lined up immediately ventral to the notochord. The hypochord shares expression of several genes with the floor plate, including Shh and FoxA, and play a role in dorsal aorta development. Whole-embryo single-cell transcriptome analysis identified a number of genes specifically expressed in both the floor plate and the endodermal strand in Ciona tailbud embryos. A Ciona FoxA ortholog FoxA.a is shown to be a candidate transcriptional activator for the midline gene battery. The present findings suggest an ancient evolutionary origin of a common developmental program for the midline structures in Olfactores. Frontiers Media S.A. 2021-06-21 /pmc/articles/PMC8256262/ /pubmed/34235159 http://dx.doi.org/10.3389/fcell.2021.704367 Text en Copyright © 2021 Oonuma, Yamamoto, Moritsugu, Okawa, Mukai, Sotani, Tsunemi, Sugimoto, Nakagome, Hasegawa, Shimai, Horie and Kusakabe. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Oonuma, Kouhei
Yamamoto, Maho
Moritsugu, Naho
Okawa, Nanako
Mukai, Megumi
Sotani, Miku
Tsunemi, Shuto
Sugimoto, Haruka
Nakagome, Eri
Hasegawa, Yuichi
Shimai, Kotaro
Horie, Takeo
Kusakabe, Takehiro G.
Evolution of Developmental Programs for the Midline Structures in Chordates: Insights From Gene Regulation in the Floor Plate and Hypochord Homologues of Ciona Embryos
title Evolution of Developmental Programs for the Midline Structures in Chordates: Insights From Gene Regulation in the Floor Plate and Hypochord Homologues of Ciona Embryos
title_full Evolution of Developmental Programs for the Midline Structures in Chordates: Insights From Gene Regulation in the Floor Plate and Hypochord Homologues of Ciona Embryos
title_fullStr Evolution of Developmental Programs for the Midline Structures in Chordates: Insights From Gene Regulation in the Floor Plate and Hypochord Homologues of Ciona Embryos
title_full_unstemmed Evolution of Developmental Programs for the Midline Structures in Chordates: Insights From Gene Regulation in the Floor Plate and Hypochord Homologues of Ciona Embryos
title_short Evolution of Developmental Programs for the Midline Structures in Chordates: Insights From Gene Regulation in the Floor Plate and Hypochord Homologues of Ciona Embryos
title_sort evolution of developmental programs for the midline structures in chordates: insights from gene regulation in the floor plate and hypochord homologues of ciona embryos
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8256262/
https://www.ncbi.nlm.nih.gov/pubmed/34235159
http://dx.doi.org/10.3389/fcell.2021.704367
work_keys_str_mv AT oonumakouhei evolutionofdevelopmentalprogramsforthemidlinestructuresinchordatesinsightsfromgeneregulationinthefloorplateandhypochordhomologuesofcionaembryos
AT yamamotomaho evolutionofdevelopmentalprogramsforthemidlinestructuresinchordatesinsightsfromgeneregulationinthefloorplateandhypochordhomologuesofcionaembryos
AT moritsugunaho evolutionofdevelopmentalprogramsforthemidlinestructuresinchordatesinsightsfromgeneregulationinthefloorplateandhypochordhomologuesofcionaembryos
AT okawananako evolutionofdevelopmentalprogramsforthemidlinestructuresinchordatesinsightsfromgeneregulationinthefloorplateandhypochordhomologuesofcionaembryos
AT mukaimegumi evolutionofdevelopmentalprogramsforthemidlinestructuresinchordatesinsightsfromgeneregulationinthefloorplateandhypochordhomologuesofcionaembryos
AT sotanimiku evolutionofdevelopmentalprogramsforthemidlinestructuresinchordatesinsightsfromgeneregulationinthefloorplateandhypochordhomologuesofcionaembryos
AT tsunemishuto evolutionofdevelopmentalprogramsforthemidlinestructuresinchordatesinsightsfromgeneregulationinthefloorplateandhypochordhomologuesofcionaembryos
AT sugimotoharuka evolutionofdevelopmentalprogramsforthemidlinestructuresinchordatesinsightsfromgeneregulationinthefloorplateandhypochordhomologuesofcionaembryos
AT nakagomeeri evolutionofdevelopmentalprogramsforthemidlinestructuresinchordatesinsightsfromgeneregulationinthefloorplateandhypochordhomologuesofcionaembryos
AT hasegawayuichi evolutionofdevelopmentalprogramsforthemidlinestructuresinchordatesinsightsfromgeneregulationinthefloorplateandhypochordhomologuesofcionaembryos
AT shimaikotaro evolutionofdevelopmentalprogramsforthemidlinestructuresinchordatesinsightsfromgeneregulationinthefloorplateandhypochordhomologuesofcionaembryos
AT horietakeo evolutionofdevelopmentalprogramsforthemidlinestructuresinchordatesinsightsfromgeneregulationinthefloorplateandhypochordhomologuesofcionaembryos
AT kusakabetakehirog evolutionofdevelopmentalprogramsforthemidlinestructuresinchordatesinsightsfromgeneregulationinthefloorplateandhypochordhomologuesofcionaembryos