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The ascidian tadpole larva: comparative molecular development and genomics

Key Points

  • Ascidians are sessile marine invertebrate chordates that, because of their phylogenetic position, have been invaluable in addressing the question of chordate origins and evolution.

  • Ciona intestinalis is a useful model for studying chordate origins and evolution because its tadpole larva is believed to represent the closest living form to the ancestral chordate. C. intestinalis is also an excellent model for studying gene function and regulation, because of its unduplicated compact genome — the sequence of which has recently been published — and its short gene-regulatory regions.

  • Analysis of notochord and neural tube development in Ciona, and comparison with the development of these structures in vertebrates, provides valuable information on how the vertebrate form has evolved. Such comparisons involve the identification of orthologues, and the temporal and spatial analysis of their expression.

  • Comparative studies of gene expression have also been helpful in unravelling the basic mechanisms that underlie notochord and neural-tube development; for example, they have shown the central importance of the T-box transcription factor Brachyury in these processes.

  • The recent sequencing of the Ciona genome — the smallest of the experimentally accessible chordates — provides new opportunities for evolutionary genomic studies of chordates. For example, studying gene families, such as that of the nuclear receptors, shows which genes are ancient and which represent recent evolutionary innovations.

Abstract

Evolution is of interest not only to developmental biology but also to genetics and genomics. We are witnessing a new era in which evolution, development, genetics and genomics are merging to form a new discipline, a good example of which is the study of the origin and evolution of the chordates. Recent studies on the formation of the notochord and the dorsal neural tube in the increasingly famous Ciona intestinalis tadpole larva, and the availability of its draft genome, show how the combination of comparative molecular development and evolutionary genomics might help us to better understand our chordate ancestor.

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Figure 1: Tadpole-type larva of the ascidian Ciona intestinalis.
Figure 2: The evolution of the chordates.
Figure 3: A molecular phylogenetic tree of nuclear receptor (NR) proteins.

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Acknowledgements

I thank all my colleagues who have contributed to studies included in this review, and two anonymous referees for their helpful comments on the manuscript. The research of my laboratory is supported by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan, by Human Frontier Science Programme Research Grants and by the Core Research for Evolutional Science and Technology (CREST) project of the Japan Science and Technology Corporation (JST).

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DATABASES

LocusLink

Brachyury

prickle

FURTHER INFORMATION

Ghost Database

Glossary

CHORDATES

A phylum of animals (the Chordata) that is characterized by the possession of a notochord. It includes the urochordates (such as the ascidians), the cephalochordates (amphioxus) and the vertebrates.

DEUTEROSTOME

A bilaterian animal the mouth of which forms as a secondary opening that is separate from the blastopore. Deuterostomes include the chordates, the hemichordates and the echinoderms.

NOTOCHORD

A rod-like structure in the dorsal midline of the embryo that runs from the head to the tail beneath the future central nervous system.

CLADE

A lineage of organisms, or alleles, that comprises an ancestor and all of its descendants.

BLASTOMERE

An early embryonic cell that is derived from the cleavage of a fertilized egg.

MORPHOLINO

A chemically modified oligonucleotide that behaves as an antisense RNA analogue and is, therefore, used to interfere with gene function.

DIPLOBLAST

An animal with only two germ layers: the ectoderm and the endoderm. Diploblasts include the cnidarians, the ctenophorans and — according to some authors — the placozoans and the poriferans.

TRIPLOBLAST

An animal with three germ layers: the ectoderm, the mesoderm and the endoderm.

PROTOSTOME

A bilaterian animal, the mouth of which develops before the anus during embryogenesis. Protostomes include arthropods, molluscs and worms.

MONOPHYLETIC

A group that includes all of the descendants of a single common ancestor.

DIPLEURULA-TYPE LARVAE

A deuterostome larval type with a perforated ciliary band.

AURICULARIA LARVAE

A planktotrophic sea-cucumber larva with a continuous ciliary band.

TORNARIA LARVA

A hemichordate acorn-worm larva, with distinct ciliary bands.

PARAXIAL MESODERM

A subpopulation of the mesoderm that lies on both sides of the neural tube, which gives rise to the somites.

NEUROHYPOPHYSIS

A part of the hypophysis (along with the adenohypophysis), which is involved in neurohormone release.

APICAL ORGAN

The organ located at the anterior tip of the hemichordate tornaria larvae; a photoreceptor organ.

ARCHENTERON

The cavity formed inside the embryo when the endoderm and mesoderm invaginate during gastrulation, which forms the gut.

PRIMITIVE STREAK

A strip of cells that extends inwards from the posterior marginal zone. During gastrulation, cells move through the primitive streak into the interior of the blastoderm.

MARGINAL ZONE

The belt-like region surrounding the equator of the late blastula (found, in particular, in amphibians).

LIM DOMAIN

A repeat of 60 amino acids containing cysteine and histidine residues. It is thought to be involved in protein–protein interactions.

PLANAR-CELL POLARITY

The state in which epithelial cells are polarized in the apical–basolateral axis and in the horizontal plane of the epithelium.

CONVERGENT EXTENSION

The process by which a sheet of cells changes shape by extending in one direction and narrowing — converging —in a direction at right angles to the extension.

GASTRULATION

The process in animal embryos in which the endoderm and mesoderm move from the outer surface of the embryo to the inside, where they give rise to the internal organs.

NEURULATION

The process in which the ectoderm of the future brain and spinal cord develops folds and forms the neural tube.

NEIGHBOUR-JOINING METHOD

A distance-based molecular phylogenetic method that involves the sequential addition of taxa and the minimization of branch lengths, but does not assume a molecular clock.

BLASTOPORE

The slit-like or circular invagination on the surface of animal embryos, through which the mesoderm and endoderm move inside the embryo at gastrulation.

STOMODEUM

The invagination of the ectoderm that forms the mouth in animal embryos.

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Satoh, N. The ascidian tadpole larva: comparative molecular development and genomics. Nat Rev Genet 4, 285–295 (2003). https://doi.org/10.1038/nrg1042

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