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Cleavage pattern, gastrulation, and neurulation in the appendicularian, Oikopleura dioica

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Abstract

The appendicularian, Oikopleura dioica is a chordate. Its life cycle is extremely short—approximately 5 days—and its tadpole shape with a beating tail is retained throughout entire life. The tadpole hatches after 3 h of development at 20°C. Here, we describe the cleavage pattern and morphogenetic cell movements during gastrulation and neurulation. Cleavage showed an invariant pattern. It is basically bilateral but also shows various minor left–right asymmetries starting from the four-cell stage. We observed two rounds of unequal cleavage of the posterior-vegetal B-line cells at the posterior pole. The nature of the unequal cleavages is reminiscent of those in ascidian embryos and suggests the presence of a centrosome-attracting body, a special subcellular structure at the posterior pole. The representation of the cell division pattern in this report will aid the identification of each cell, a prerequisite for clarifying the gene expression patterns in early embryos. Gastrulation started as early as the 32-cell stage and progressed in three phases. By the end of the second phase at the 64-cell stage, every vegetal cell had ingressed into the embryo, and animal cells had covered the entire embryo by epiboly. There was no archenteron formation. In the anterior region, eight A-line cells were aligned as a 2 × 4 array along the anterior–posterior axis and become internalized during the 64-cell stage. This process was considered to correspond to neurulation. The simple and accelerated development of Oikopleura, nevertheless giving rise to a conserved chordate body plan, is advantageous for studying developmental mechanisms using molecular and genetic approaches and makes this animal the simplest model organism in the phylum Chordata.

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Acknowledgments

We thank Dr. D. Chourrout for inviting HN to their lab and teaching us how to culture Oikopleura. Thanks are also due to the members of the Misaki Marine Biological Station and the Seto Marine Biological Laboratory for help in collecting Oikopleura to start our culture. We are grateful to Dr. T. Stach and his colleagues for sharing their unpublished results. We also thank Dr. A. Nishino (Osaka University) for critical reading of the manuscript. This work was supported by Grants in Aid from Ministry of Education, Culture, Sports, Science and Technology (17657073).

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Correspondence to Hiroki Nishida.

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Communicated by N. Satoh

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Supplemental Movie S1

Embryogenesis of Oikopleura dioica, from egg to tadpole larva. Larvae hatched at 6 h of development at 13°C. (MOV 6.30 KB)

Supplemental Movie S2

Two rounds of unequal cell division of B-line blastomeres at the posterior pole; the vegetal pole is at the upper left. Posterior view, the video starts at the eight-cell stage and ends during gastrulation. The B blastomere pair of the eight-cell embryo divides unequally twice–generating the smaller B1 of the 16-cell embryo and B11 of the 32-cell embryo. (AVI 4.42 KB)

Supplemental Movie S3

Gastrulation movements, vegetal view; anterior is up. The video starts at the four-cell stage and finishes at the end of the second phase of gastrulation. Neurulation is also visible in the anterior region. This video corresponds to Fig. 4. (MOV 449 KB)

Supplemental Movie S4

Neurulation; anterior is at bottom left. Vegetal pole is at the upper right. Four cells of A1 descendants in the anterior region divide once along the anterior–posterior axis and are then internalized. This video corresponds to Fig. 6. (AVI 1.83 KB)

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Fujii, S., Nishio, T. & Nishida, H. Cleavage pattern, gastrulation, and neurulation in the appendicularian, Oikopleura dioica . Dev Genes Evol 218, 69–79 (2008). https://doi.org/10.1007/s00427-008-0205-4

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  • DOI: https://doi.org/10.1007/s00427-008-0205-4

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