A Sea Cucumber Homolog of the Mouse<i>T-Brain-1</i>is Expressed in the Invaginated Cells of the Early Gastrula in Holothuria leucospilota

Maruyama, Yoshihiko K.

doi:10.2108/jsz.17.383

Cited by 15 publications

(10 citation statements)

References 41 publications

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“…But tel and tbr are in the upstream region of the GRN and are under control of the double-negative gate. We know nothing of evolutionary significance for this story about tel, but tbr provides an explicit case of cooption, because this gene is expressed in endomesoderm in other echinoderms, including sea stars (20,21), where it is obligatory for endomesoderm specification (21); in echinoids, tbr is expressed only in the skeletogenic micromere lineage. We may conclude that, perhaps typically, following the linkage of the pleisiomorphic skeletogenic regulatory apparatus into the micromere GRN, additional regulatory gene cooptions took place in the echinoid lineage.…”

Section: Discussionmentioning

confidence: 99%

Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution

Gao

Davidson

2008

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

159

200

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Of the five echinoderm classes, only the modern sea urchins (euechinoids) generate a precociously specified embryonic micromere lineage that ingresses before gastrulation and then secretes the biomineral embryonic skeleton. The gene regulatory network (GRN) underlying the specification and differentiation of this lineage is now known. Many of the same differentiation genes as are used in the biomineralization of the embryo skeleton are also used to make the similar biomineral of the spines and test plates of the adult body. Here, we determine the components of the regulatory state upstream of these differentiation genes that are shared between embryonic and adult skeletogenesis. An abrupt ''break point'' in the micromere GRN is thus revealed, on one side of which most of the regulatory genes are used in both, and on the other side of which the regulatory apparatus is entirely micromerespecific. This reveals the specific linkages of the micromere GRN forged in the evolutionary process by which the skeletogenic gene batteries were caused to be activated in the embryonic micromere lineage. We also show, by comparison with adult skeletogenesis in the sea star, a distant echinoderm outgroup, that the regulatory apparatus responsible for driving the skeletogenic differentiation gene batteries is an ancient pleisiomorphic aspect of the echinoderm-specific regulatory heritage.embryonic and adult skeletogenesis ͉ gene network evolution ͉ sea urchin ͉ sea star

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Section: Discussionmentioning

confidence: 99%

Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution

Gao

Davidson

2008

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

159

200

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“…Expression is maintained in these cells during involution of the archenteron, but it is downregulated by the end of gastrulation. Transient expression is also reported in the animal hemisphere on one side of the blastula wall in starfish (Shoguchi et al, 2000) and sea cucumbers (Maruyama, 2000), but not sea urchins (Croce et al, 2001; confirmed by K. Akasaka, personal communication), however the precise fate of these cells is not clear. In hemichordates, the gene is also expressed in mesendoderm cells during gastrulation, but in addition signal is seen in apical ectoderm cells of the gastrula, where the eyespots of the tornaria larva form.…”

mentioning

confidence: 81%

“…Hemichordates clearly express the gene in the apical sensory organ, suggesting that the last common ancestor of hemichordates and vertebrates possessed an Eomes/Tbr1/Tbx21 gene, and used it to specify anterior neural structures (Tagawa et al, 2000). Since echinoderms plus hemichordates form the sister clade to chordates (Wada and Satoh, '94;Cameron et al, 2000), the transient expression detected on one side of the blastula wall in the animal hemispheres of starfish (Shoguchi et al, 2000) and sea cucumbers (Maruyama, 2000) may mark the development of neural precursors, although the precise fate of these cells remains to be determined. Interestingly, we detected no anterior neural expression at any stage of development in amphioxus, suggesting that this expression domain has been secondarily lost in cephalochordates.…”

Section: Amphieomes/tbr1/tbx21mentioning

confidence: 99%

“…Previous studies have identified a single invertebrate gene orthologous to the vertebrate Eomesodermin, Tbr1, and Tbx21 genes in basal deuterostomes, including echinoderms (Maruyama, 2000;Shoguchi et al, 2000;Croce et al, 2001), hemichordates (Tagawa et al, 2000), and urochordates (Takada et al,'98). In echinoderms, the gene is first expressed at the blastula stage in the vegetal (posterior) pole in presumptive mesendoderm cells.…”

mentioning

confidence: 99%

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Evolution of developmental functions by the Eomesodermin, T‐brain‐1, Tbx21 subfamily of T‐box genes: insights from amphioxus

Horton

Gibson‐Brown

2002

J. Exp. Zool.

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We have identified an amphioxus T-box gene that is orthologous to the Eomesodermin, T-brain-1, and Tbx21 genes of vertebrates, and we have characterized its expression pattern during embryonic and larval development. AmphiEomes/Tbr1/Tbx21 is maternally expressed in oocytes and cleavage stage embryos. After the onset of zygotic transcription at the blastula stage, it is expressed in invaginating mesendoderm cells during gastrulation, but it is downregulated in presumptive ectoderm and neurectoderm. Expression is seen in both axial and paraxial mesendoderm in neurulae and early larvae, but it is not detected in differentiated endoderm, somites, or notochord. Expression persists in mesendoderm cells of the tail bud in early larvae, but it disappears between 1 to 1.5 days post fertilization. Unlike orthologous genes in basal deuterostomes or vertebrates, no anterior neural expression domain is detected at any stage of development. Integrating phylogenetic and developmental data, we have reconstructed the evolutionary history of the Eomesodermin/Tbr1/Tbx21 subfamily of T-box genes from a single ancestral locus that originated very early in metazoan evolution, before the evolution of triploblasts from their diploblast ancestor.

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“…However, no anterior central nervous system expression similar to that of vertebrates was detected in amphioxus. In indirectly developing deuterostomes, T-brain homologs are also expressed during gastrulation; this is the case in starfish (Shoguchi et al, 2000), sea cucumber (Maruyama, 2000), and hemichordate embryos (Tagawa et al, 2000). In sea urchins, a T-brain homolog is expressed in primary mesenchyme mesoderm, where it controls instructive signals required for proper gastrulation (Fuchikami et al, 2002).…”

mentioning

confidence: 99%

The transcription factors HeBlimp and HeT‐brain of an indirectly developing polychaete suggest ancestral endodermal, gastrulation, and sensory cell‐type specification roles

Arenas-Mena

2008

J Exp Zool Pt B

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The expression of Blimp and T-brain was characterized during embryogenesis of the indirectly developing polychaete Hydroides elegans. The expression of both genes in the vegetal blastomeres of this lophotrochozoan is restricted to the lateral and oral regions of the blastopore. Both transcription factors also have expression patterns consistent with ancestral neural functions. HeBlimp is expressed in a couple of animal cap cells and exhibits a marked left bias that correlates with earlier development of the left eye in H. elegans. HeT-brain is expressed in animal cap blastomeres and eventually becomes restricted to apical tuft cells of early trochophore stages. The expression of Blimp and T-brain among directly and indirectly developing bilaterians suggests ancestral sensory cell-type specification, gastrulation by invagination, endoderm specification, mesoderm specification, and/or tripartite gut subdivision. These characterizations add to the long-term goal of understanding the regulatory evolution functions that underlies complex life cycles in metazoans.

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A Sea Cucumber Homolog of the MouseT-Brain-1is Expressed in the Invaginated Cells of the Early Gastrula in Holothuria leucospilota

Cited by 15 publications

References 41 publications

Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution

Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution

Evolution of developmental functions by the Eomesodermin, T‐brain‐1, Tbx21 subfamily of T‐box genes: insights from amphioxus

The transcription factors HeBlimp and HeT‐brain of an indirectly developing polychaete suggest ancestral endodermal, gastrulation, and sensory cell‐type specification roles

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