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

Abstract

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.

Identification of distinct vascular mural cell populations during zebrafish embryonic development

“…Interestingly, the hypochord, floor plate, and notochord have been shown to be derived from the multipotent midline progenitor cells in the dorsal organizer or the tailbud 34,35 —a common origin which may, in part, explain how two structures that are dissimilar in function share this unique expression pattern. Furthermore, in the invertebrate Ciona , researchers show that a series of calponin/transgelin family genes ( tagln‐r.b , tagln‐r.c , tagln‐r.d , tagln‐r.e ) are expressed in the Ciona floor plate, notochord, and endodermal strand (the Ciona analog for the hypochord), indicating that Tagln expression in midline structures may have a conserved role in embryogenesis 49 . As Tagln is known primarily as an actin‐binding protein in contractile cells, the role of Tagln in these non‐contractile, non‐muscular, primitive midline structures remains unknown.…”

“…Furthermore, in the invertebrate Ciona, researchers show that a series of calponin/transgelin family genes (tagln-r.b, tagln-r.c, tagln-r. d, tagln-r.e) are expressed in the Ciona floor plate, notochord, and endodermal strand (the Ciona analog for the hypochord), indicating that Tagln expression in midline structures may have a conserved role in embryogenesis. 49 As Tagln is known primarily as an actin-binding protein in contractile cells, the role of Tagln in these noncontractile, non-muscular, primitive midline structures remains unknown.…”

Identification of overlapping and distinct mural cell populations during early embryonic development

“…The hypochord, floor plate, and notochord have been shown to be derived from the multipotent midline progenitor cells in the dorsal organizer or the tailbud (Row et al, 2016, Latimer andAppel, 2006)-a common origin which may, in part, explain how two structures that are dissimilar in function share this unique expression pattern. Furthermore, in the invertebrate Ciona, researchers show that a series of calponin/transgelin family genes (tagln-r.b, tagln-r.c, tagln-r.d, tagln-r.e) are expressed in the Ciona floor plate, notochord, and endodermal strand (the Ciona analogue for the hypochord), indicating that Tagln expression in midline structures may have a conserved role in embryogenesis (Oonuma et al, 2021). As Tagln is known primarily as an actinbinding protein in contractile cells, the role of Tagln in these non-contractile, nonmuscular, primitive midline structures remains unknown.…”

Evolution and function of calponin and transgelin

“…During larval-pupal metamorphosis of the cotton bollworm Helicoverpa armigera , calponin is expressed at a high level in the metamorphic epidermis and phosphorylated by protein kinase C ( Fu et al, 2009 ). In the embryonic stage, the sea squirt Ciona expresses a calponin-transgelin family gene that is crucial to nortocord development ( Oonuma et al, 2021 ). It was shown that non-phosphorylated calponin interacts with ultraspiracles protein to activate the juvenile hormone pathway and antagonize the 20-hydroxyecdysone pathway in initiating insect molting and metamorphosis ( Cai et al, 2014 ).…”