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Hydrocoel morphogenesis forming the pentaradial body plan in a sea cucumber, Apostichopus japonicus.
Udagawa S
,
Ikeda T
,
Oguchi K
,
Kohtsuka H
,
Miura T
.
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Echinoderms constitute an animal phylum characterized by the pentaradial body plan. During the development from bilateral larvae to pentaradial adults, the formation of the multiple of five hydrocoel lobes, i.e., the buddings from the mesodermal coelom, is the firstly emerging pentameral character. The developmental mechanism underlying the hydrocoel-lobe formation should be revealed to understand the evolutionary process of this unique and highly derived body plan of echinoderms, although the morphogenetic mechanisms of hydrocoel lobes are largely uninvestigated. In this study, using the sea cucumber Apostichopus japonicus, in which hydrocoel is easily observable, the developmental process of hydrocoel lobes was described in detail, focusing on cell proliferation and rearrangement. Cell proliferation was not specifically distributed in the growing tips of the hydrocoel lobes, and inhibition of cell proliferation did not affect lobe formation. During lobe formation, the epithelium of the hydrocoel lobes was firstly thickened and then transformed into a simple epithelium, suggesting that tissue expansion via tissue remodeling contributes to the hydrocoel-lobe formation.
Figure 1. Normal development of the sea cucumber Apostichopus japonicus and schematic illustration of its hydrocoel. (a) The developmental process during auricularia larva and juvenile stages. Development proceeds from left to right. Auricularia, doliolaria, metamorphosis and pentactula are ventral views, anterior to the top, and juvenile is dorsal view, anterior to the top. (b) Schematic illustration of hydrocoel in each developmental stage. The orange part represents the hydrocoel or its derivative, i.e., the water vascular system. Auricularia and metamorphosing larvae are ventral views, and doliolaria, pentactula and juveniles are left lateral views, anterior to the top. The hydrocoel emerges on the left side of the archenteron in an auricularia, and 10 lobes are formed from the hydrocoel. After the lobe formation, the hydrocoel becomes horseshoe-like shaped to form a ring canal surrounding the digestive tract. Then, the larva metamorphoses into a doliolaria. Five of the lobes (IâV) extend anteriorly and become the water vascular canals of the tentacle of a juvenile, and another five lobes (iâv) are formed between the water vascular canals of the tentacle extend posteriorly and become radial canals. The numbering identities for hydrocoel lobes are based on the application of Lovenâs axis to sea cucumbers14.
Figure 2. Overall morphology of the developing hydrocoel lobes. (aâd) Whole embryos under the microscope (ventral view, anterior to the top) from phase 1 to phase 4. (aââdâ) show the hydrocoel of a-d. The dotted lines in (aâd) indicate the region shown in (aââdâ). The hydrocoel of the specimens stained with DAPI is shown in (aâââdâ: z-stack images) and (aââââdâââ: optical sections). In phase 1, the hydrocoel was spindle shaped and then extended up to 100 µm along the longitudinal axis in phase 2. The hydrocoel lobes started to form in phase 3, and the lobes extended in phase 4. During phases 1 and 4, no significant change in the overall morphology of entire larvae other than the change in the hydrocoel was observed.
Figure 3. The spatial distribution of cell proliferation in the hydrocoel during the hydrocoel lobe morphogenesis. Cell proliferation in the hydrocoel from phase 1 to phase 4 was detected using EdU after 3Â h of EdU treatment (aâd). The hydrocoel is indicated by the dotted lines. (aââdâ) show the optical sections of (aâc). The position of the hydrocoel lobe is indicated by arrowheads. The EdU signal was detected equally throughout the whole hydrocoel during phase 1 and phase 4, and specific localization was not observed.
Figure 4. Inhibition of cell proliferation by aphidicolin treatment during the hydrocoel lobe morphogenesis. (a) Experimental design for aphidicolin treatment. Auricularia larvae were treated with aphidicolin from phase 2, and the phenotype was observed at 20 h. (b) Phenotype caused by aphidicolin treatment. Hydrocoel lobes were formed in both aphidicolin-treated and DMSO-treated (control) larvae. The number or shape of hydrocoel lobes was not significantly affected by aphidicolin treatment compared to DMSO treatment. (c) Ratio of phase 3â4 larvae (lobe formed) to phase 2 larvae (lobe not formed) in the treated and control groups at 20 h after the initiation of treatment. There was no significant difference (two-sided Fisherâs exact test, p = 0.144). Graph represents the meanâ±âs.d. from 3 independent experiments.
Figure 5. The observed changes in cell shape and cell arrangement during the lobe formation in the hydrocoel. The cell membrane of larvae was stained with BODIPY FL C5-ceramide and observed using confocal laser scanning microscopy from phase 1 to phase 4. (aâf) Optical sections of the hydrocoel in each phase (ventral view, anterior to the top). The time course and stages are indicated in the figure. (aââfâ) show the magnification of the regions indicated in (aâf), respectively. Hydrocoel epithelium was a single cell layer in phase 1 and seemed to be multilayered in phase 2. In phase 3, the tissue became single layered again at the tip of the lobe (arrowhead in cââdâ) and then in the whole hydrocoel lobe.
Figure 6. Schematic illustration of the change in cell arrangement during the hydrocoel lobe morphogenesis. (a) represents an auricularia larva and (b) represents the development of its hydrocoel. The upper panel shows the overall shape of the hydrocoel, and the cell arrangement of the hydrocoel epithelium in dotted areas is shown in the lower panel. The hydrocoel at phase 1 consists of a single cell sheet, and it seemed to be multilayered at phase 2. As the formation of the hydrocoel lobe proceeded, the cell sheet became single layered again sequentially from the tip of the hydrocoel lobe (phase 3) to the proximal part of the lobe (phase 4).
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