Regulatory circuit rewiring and functional divergence of the duplicate admp genes in dorsoventral axial patterning

Chang, Yi‐Cheng; Pai, Chih-Yu; Chen, Yi‐Chih; Ting, Hsiu-Chi; Martinez, Pedro; Telford, Maximilian J.; Yu, Jr-Kai; Su, Yi-Hsien

doi:10.1016/j.ydbio.2015.12.015

Cited by 18 publications

(13 citation statements)

References 54 publications

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“…6). Our present results and previous studies show that similar patterning mechanisms are used in echinoderm and hemichordate larvae (23,33,(36)(37)(38), suggesting that the common ancestor of Ambulacraria was an indirect developer with a larval stage. Moreover, because the ambulacrarian larval nervous system and the chordate CNS are similarly regulated (both repressed by BMP signaling), we propose that the deuterostome ancestor was also an indirect developer that metamorphosed into a worm-like, motile adult, similar to an indirect-developing enteropneust.…”

Section: Discussionsupporting

confidence: 86%

BMP controls dorsoventral and neural patterning in indirect-developing hemichordates providing insight into a possible origin of chordates

Chen

Ting

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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A defining feature of chordates is the unique presence of a dorsal hollow neural tube that forms by internalization of the ectodermal neural plate specified via inhibition of BMP signaling during gastrulation. While BMP controls dorsoventral (DV) patterning across diverse bilaterians, the BMP-active side is ventral in chordates and dorsal in many other bilaterians. How this phylum-specific DV inversion occurs and whether it is coupled to the emergence of the dorsal neural plate are unknown. Here we explore these questions by investigating an indirect-developing enteropneust from the hemichordate phylum, which together with echinoderms form a sister group of the chordates. We found that in the hemichordate larva, BMP signaling is required for DV patterning and is sufficient to repress neurogenesis. We also found that transient overactivation of BMP signaling during gastrulation concomitantly blocked mouth formation and centralized the nervous system to the ventral ectoderm in both hemichordate and sea urchin larvae. Moreover, this mouthless, neurogenic ventral ectoderm displayed a medial-to-lateral organization similar to that of the chordate neural plate. Thus, indirect-developing deuterostomes use BMP signaling in DV and neural patterning, and an elevated BMP level during gastrulation drives pronounced morphological changes reminiscent of a DV inversion. These findings provide a mechanistic basis to support the hypothesis that an inverse chordate body plan emerged from an indirect-developing ancestor by tinkering with BMP signaling.

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Section: Discussionsupporting

confidence: 86%

BMP controls dorsoventral and neural patterning in indirect-developing hemichordates providing insight into a possible origin of chordates

Chen

Ting

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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“…The expression of vasa , nanos , and piwi1 was also completely abolished in embryos treated with DMH1 immediately after fertilization (Figure 7a). Because dorsoventral polarity is disrupted in DMH1‐treated embryos (Chang et al, 2016; Su et al, 2019), it was possible that the disappearance of PGC marker expression could be a secondary effect resulting from the loss of the dorsal identity. Therefore, to assess the effects of BMP inhibition during stages that do not involve the initial dorsoventral patterning, we treated the embryos with DMH1 at different developmental periods and scored the number of Vasa‐positive cells at the tornaria stage (Figure 7b,c).…”

Section: Resultsmentioning

confidence: 99%

Evidence for BMP‐mediated specification of primordial germ cells in an indirect‐developing hemichordate

Lin

2020

Evolution and Development

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Primordial germ cells (PGCs) are specified during development by either one of two major mechanisms, the preformation mode or the inductive mode. Because the inductive mode is widely employed by many bilaterians and early branching metazoan lineages, it has been postulated as an ancestral mechanism. However, among the deuterostome species that have been studied, invertebrate chordates use the preformation mode, while many vertebrate and echinoderm species are known to utilize an inductive mechanism, thus leaving the evolutionary history of PGC specification in the deuterostome lineage unclear. Hemichordates are the sister phylum of echinoderms, and together they form a clade called Ambulacraria that represents the closest group to the chordates. Thus, research in hemichordates is highly informative for resolving this issue. In this study, we investigate the developmental process of PGCs in an indirect‐developing hemichordate, Ptychodera flava. We show that maternal transcripts of the conserved germline markers vasa, nanos, and piwi1 are ubiquitously distributed in early P. flava embryos, and these genes are coexpressed specifically in the dorsal hindgut starting from the gastrula stage. Immunostaining revealed that Vasa protein is concentrated toward the vegetal pole in early P. flava embryos, and it is restricted to cells in the dorsal hindgut of gastrulae and newly hatched larvae. The Vasa‐positive cells later contribute to the developing trunk coeloms of the larvae and eventually reside in the adult gonads. We further show that bone morphogenetic protein (BMP) signaling is required to activate expression of the germline determinants in the gastrula hindgut, suggesting that PGC specification is induced by BMP signaling in P. flava. Our data support the hypothesis that the inductive mode is a conserved mechanism in Ambulacraria, which might even trace back to the common ancestor of Deuterostomes.

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“…Injections and treatments mRNAs encoding Myc-HIFα, mutant forms of Myc-HIFα, mCherry-HIFα, Histone-GFP and HIFαODDD-GFP were in vitro transcribed using the mMESSAGE mMACHINE kit (Ambion) and injected into zygotes as previously described (Chang et al, 2016). For injection of the HRE-luciferase reporter (Addgene, 26731), the plasmid was linearized with BamHI and mixed with HindIII-digested sea urchin genomic DNA.…”

Section: Methodsmentioning

confidence: 99%

Asymmetric distribution of hypoxia-inducible factor α regulates dorsoventral axis establishment in the early sea urchin embryo

Chang

Lin

et al. 2017

Development

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Hypoxia signaling is an ancient pathway by which animals can respond to low oxygen. Malfunction of this pathway disturbs hypoxic acclimation and can result in various diseases, including cancers. The role of hypoxia signaling in early embryogenesis remains unclear. Here, we show that in the blastula of the sea urchin , hypoxia-inducible factor α (HIFα), the downstream transcription factor of the hypoxia pathway, is localized and transcriptionally active on the future dorsal side. This asymmetric distribution is attributable to its oxygen-sensing ability. Manipulations of the HIFα level entrained the dorsoventral axis, as the side with the higher level of HIFα tends to develop into the dorsal side. Gene expression analyses revealed that HIFα restricts the expression of to the ventral side and activates several genes encoding transcription factors on the dorsal side. We also observed that intrinsic hypoxic signals in the early embryos formed a gradient, which was disrupted under hypoxic conditions. Our results reveal an unprecedented role of the hypoxia pathway in animal development.

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Regulatory circuit rewiring and functional divergence of the duplicate admp genes in dorsoventral axial patterning

Cited by 18 publications

References 54 publications

BMP controls dorsoventral and neural patterning in indirect-developing hemichordates providing insight into a possible origin of chordates

BMP controls dorsoventral and neural patterning in indirect-developing hemichordates providing insight into a possible origin of chordates

Evidence for BMP‐mediated specification of primordial germ cells in an indirect‐developing hemichordate

Asymmetric distribution of hypoxia-inducible factor α regulates dorsoventral axis establishment in the early sea urchin embryo

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