Antagonism between β-catenin and Gata.a sequentially segregates the germ layers of ascidian embryos

Imai, Kaoru S.; Hudson, C. S.; Oda-Ishii, Izumi; Yasuo, Hitoyoshi; Satou, Yutaka

doi:10.1242/dev.141481

Cited by 19 publications

(35 citation statements)

References 33 publications

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“…The enrichment of Tcf, which is an effector TF of the canonical Wnt signaling pathway, validating that the treatment indeed promoted this pathway. On the contrary, Gata motifs were found enriched in the set of less accessible peaks (Figure 2C), confirming the previously reported antagonism between Gata and Wnt in Ciona (Imai et al, 2016). The gene model is represented in blue.…”

Section: Anticipated Resultssupporting

confidence: 88%

Assaying Chromatin Accessibility Using ATAC-Seq in Invertebrate Chordate Embryos

Magri

Jiménez-Gancedo

Bertrand

et al. 2020

Front. Cell Dev. Biol.

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Cis-regulatory elements (CREs) are non-coding DNA regions involved in the spatiotemporal regulation of gene expression. Gene regulatory changes drive animal development and play major roles during evolution of animal body plans. Therefore, we believe that determining CREs at different developmental stages and across animal lineages is critical to understand how evolution operates through development. The Assay for Transposase-Accessible Chromatin followed by high-throughput sequencing (ATAC-seq) is a powerful technique for the study of CREs that takes advantage of Tn5 transposase activity. Starting from fewer than 10 5 cells, in a 1-day procedure, it is possible to detect, at a genome-wide level, CREs located in open chromatin regions with high resolution. Here, we describe a detailed step-by-step ATAC-seq protocol for invertebrate chordate marine embryos. We have successfully applied this technique to amphioxus and two species of tunicate embryos. We also show an easy workflow to analyze data generated with this technique. Moreover, we point out that this method and our bioinformatic pipeline are efficient to detect CREs associated with Wnt signaling pathway by simply using embryos treated with a drug that perturbs this pathway. This approach can be extended to other signaling pathways and also to embryo mutants for critical genes. Our results therefore demonstrate the power of ATAC-seq for the identification of CREs that play essential functions during animal development in a wide range of invertebrate or vertebrate animals.

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Section: Anticipated Resultssupporting

confidence: 88%

Assaying Chromatin Accessibility Using ATAC-Seq in Invertebrate Chordate Embryos

Magri

Jiménez-Gancedo

Bertrand

et al. 2020

Front. Cell Dev. Biol.

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“…First, Macho-1 is maternally expressed and localized in the posterior pole, and acts together with Tcf7/β-catenin to activate Tbx6-r.b in the muscle lineages (Nishida and Sawada, 2001;Oda-Ishii et al, 2016;Satou et al, 2002;Yagi et al, 2004). Zic-r.b is also activated in muscle lineages under the control of a maternal protein, Gata.a (Imai et al, 2016), probably in combination with Tbx6-r.b at the 32-cell stage (Yagi et al, 2005). Their protein products cooperatively activate Mrf, and then Tbx6-r.b is activated again by Zic-r.b and Mrf.…”

Section: Discussion the Genetic Program From Maternal Factors To Exprmentioning

confidence: 99%

“…S2). Zic-r.b is activated by Gata.a in the B7.4 lineage (Imai et al, 2016), probably in combination with Tbx6-r.b at the 32-cell stage (Yagi et al, 2005). Because Mrf expression does not begin at the 32cell stage (see Fig.…”

Section: Regulatory Interactions Among the Three Key Regulatory Factorsmentioning

confidence: 99%

“…In these somatic lineages, Tbx6-r.b is activated under the control of Macho-1 and β-catenin (Kugler et al, 2010;Oda-Ishii et al, 2016;Yagi et al, 2005). In addition, Zic-r.b (also known as Zic-L) is activated in these lineages (Imai et al, 2002;Wada and Saiga, 2002) by a maternal factor, Gata.a, the activity of which is initially weakened by β-catenin (Imai et al, 2016;Oda-Ishii et al, 2016). Subsequently, a myogenic factor gene, Mrf, is activated in the three lineages (Araki et al, 1994;Meedel et al, 1997) under the control of Tbx6-r.b and Zic-r.b (Imai et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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The regulatory pathway from genes directly activated by maternal factors to muscle structural genes in ascidian embryos

Oda-Ishii

Kubo

et al. 2019

Development

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Striated muscle cells in the tail of ascidian tadpole larvae differentiate cell-autonomously. Although several key regulatory factors have been identified, the genetic regulatory pathway is not fully understood; comprehensive understanding of the regulatory pathway is essential for accurate modeling in order to deduce principles for gene regulatory network dynamics, and for comparative analysis on how ascidians have evolved the cell-autonomous gene regulatory mechanism. Here, we reveal regulatory interactions among three key regulatory factors, Zic-r.b, Tbx6-r.b and Mrf, and elucidate the mechanism by which these factors activate muscle structural genes. We reveal a cross-regulatory circuit among these regulatory factors, which maintains the expression of Tbx6-r.b and Mrf during gastrulation. Although these two factors combinatorially activate muscle structural genes in late-stage embryos, muscle structural genes are activated mainly by Tbx6-r.b before gastrulation. Time points when expression of muscle structural genes become first detectable are strongly correlated with the degree of Tbx6r.b occupancy. Thus, the genetic pathway, starting with Tbx6-r.b and Zic-r.b, which are activated by maternal factors, and ending with expression of muscle structural genes, has been revealed.

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“…In the first specification event, nuclear localization of βcatenin in the vegetal cells is antagonistic to the ubiquitous expression of the maternal transcription factor Gata.a. Gata.a promotes the transcription of ectodermal specific genes in the animal cells (Rothbacher et al, 2007), while the nuclear localization of β-catenin both prevents the expression of ectodermal genes and promotes expression of mesendodermal genes in the vegetal cells (Imai et al, 2016). The second specification event in the following cell cycle also involves antagonism between vegetal β-catenin signaling and more broadly expressed Gata.a (Imai et al, 2016), where β-catenin promotes endodermal fate.…”

Section: Origin Of Germ Layersmentioning

confidence: 99%

Tunicate gastrulation

Winkley

Kourakis

DeTomaso

et al. 2020

Current Topics in Developmental Biology

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Tunicates are a diverse group of invertebrate marine chordates that includes the larvaceans, thaliaceans, and ascidians. Because of their unique evolutionary position as the sister group of the vertebrates, tunicates are invaluable as a comparative model and hold the promise of revealing both conserved and derived features of chordate gastrulation. Descriptive studies in a broad range of tunicates have revealed several important unifying traits that make them unique among the chordates, including invariant cell lineages through gastrula stages and an overall morphological simplicity. Gastrulation has only been studied in detail in ascidians such as Ciona and Phallusia, where it involves a simple cup-shaped gastrula driven primarily by endoderm invagination. This appears to differ significantly from vertebrate models, such as Xenopus, in which mesoderm convergent extension and epidermal epiboly are major contributors to involution. These differences may reflect the cellular simplicity of the ascidian embryo.Introduction: Tunicates: their place on the evolutionary tree and their contribution to our understanding of embryology Tunicates were among the earliest experimental models for embryology. Embryologists were attracted to the ascidian embryo, with its regular cleavage program and small, simple embryonic body plan. Laurent Chabry performed blastomere separation experiments in early embryos of the ascidian Ascidiella aspersa that are regarded as foundational to the discipline of experimental embryology (Chabry, 1887;Fischer, 1992). He found that isolated blastomeres showed predetermined fates, dividing as if they were still in the intact embryo.Although not obvious in their diverse adult forms, tunicates embryos are unmistakably chordate with a notochord and dorsal hollow nerve cord. The close evolutionary relationship of ascidians to vertebrates was well appreciated by this time (Darwin, 1871;Haeckel, 1874; Kowalevsky, 1866). Edwin G. Conklin (Conklin, 1905a) built on Chabry's work and mapped the complete lineage of cells through and beyond gastrulation, with illustrations by embryonic stage and a nomenclature still in use. Conklin's work included descriptions of cleavage planes, cell-cell contacts, nuclear positions, distribution of cytoplasmic determinants, cell fates, polar body location, and spindle dynamics, as well as comparisons of gastrulation and other aspects of embryogenesis between ascidians and other animals. Noriyuki Satoh's SEM studies of Halocynthia roretzi confirmed and expanded on these early descriptions of ascidian development, bolstering inferences concerning the coordination of

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Antagonism between β-catenin and Gata.a sequentially segregates the germ layers of ascidian embryos

Cited by 19 publications

References 33 publications

Assaying Chromatin Accessibility Using ATAC-Seq in Invertebrate Chordate Embryos

Assaying Chromatin Accessibility Using ATAC-Seq in Invertebrate Chordate Embryos

The regulatory pathway from genes directly activated by maternal factors to muscle structural genes in ascidian embryos

Tunicate gastrulation

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