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???displayArticle.abstract??? bicaudal-C (bicC) mRNA encodes a protein containing RNA-binding domains that is reported to be maternally present with deflection in the oocytes/eggs of some species. The translated protein plays a critical role in the regulation of cell fate specification along the body axis during early embryogenesis in flies and frogs. However, it is unclear how it functions in eggs in which bicC mRNA is uniformly distributed, for instance, sea urchin eggs. Here, we show the function of BicC in the formation of neurogenic ectoderm of the sea urchin embryo. Loss-of-function experiments reveal that BicC is required for serotonergic neurogenesis and for expression of ankAT-1 gene, which is essential for the formation of apical tuft cilia in the neurogenic ectoderm of the sea urchin embryo. In contrast, the expression of FoxQ2, the neurogenic ectoderm specification transcription factor, is invariant in BicC morphants. Because FoxQ2 is an upstream factor of serotonergic neurogenesis and ankAT-1 expression, these data indicate that BicC functions in regulating the events that are coordinated by FoxQ2 during sea urchin embryogenesis.
Figure 1. The expression pattern of bicC during sea urchin embryogenesis.Maternal bicC mRNA was detected at the unfertilized egg (A), 16-cell (B, C) and cleavage stages (D). Fluorescent in situ hybridization with DAPI staining was performed on a 16-cell embryo (C), cleavage stage (D), mesenchyme blastula (MBL; E), and early gastrula (eG; H). The signal was missing in MBL (E, F). bicC was expressed at the vegetal plate of eG (G, H), mid-gastrula (mG; I) and late gastrula (lG; J). In prism larva, bicC was expressed at the ciliary band and the tip of gut (K, L). The bar in (A) is 20 μm.
Figure 2. foxQ2 expression is spatially invariant without BicC.foxQ2 expression in BicC morphants (A, C, E, I) and glycerol-injected control embryos (B, D, F, J). The signals were detected at 7 hours (h; A, B), 9 h (C, D), 12 h (E, F), and 29 h (I, J). FoxQ2 protein was also detected in the BicC morphant (G) and in control (H) at 23 h. The inset of (A) shows a morphant injected with BicC-MO2 to confirm the specificity of the morpholinos. The expression of foxQ2 was weaker than that of the BicC-MO1 injected embryo, but the spatial pattern was invariant.
Figure 3. BicC is required for FoxQ2 function.The ankAT-1 gene and serotonin were not detected in BicC morphants (A, B) but were detected in the control (F, G). Inset in (A) showed no ankAT-1 gene expression in BicC-MO2 morphant to ensure the specificity of the morpholinos. (C) and (H) show a P4 antigen pattern detecting differentiated spicule cell lineage. The inset of (H) shows a P4 signal with DAPI staining in the body rod of a 48 h embryo because the P4 signal in the oral lobe at this stage is almost missing. (D) is a merged image of (B) and (C). (I) is a merged image of (G) and (H). (E) and (J) show the morphology of a BicC morphant and control, respectively, at 48 h. Double fluorescent in situ hybridization staining with foxQ2 (K, O) and lefty (L, P) in a BicC morphant (K–N) and control (O–R). (M) Merged image of (K) and (L). (Q) Merged image of (O) and (P). (N, R) DAPI staining shows the morphology with a merged image of (M) and (Q), respectively.
Figure 4. BicC is required for endoderm formation.The pmar1 gene was expressed in the BicC morphant (A) as it was in the control (B), but endo16 was not detected in BicC morphants (C, E) at the time that it was expressed in control embryos (D, F). In contrast, spatial control of foxA expression was almost invariant in the BicC morphant (G, I, K) and in the control (H, J, L).
Figure 5. univin expression is independent of BicC function.Double fluorescent in situ hybridization staining with univin (A, E) and foxA (B, F) in a BicC morphant (A–D) and control (E–H). (C, D) Merged image of (A) and (B). (G, H) Merged image of (E) and (F).
Figure 6. BicC mRNA injection does not affect the development of sea urchin embryos.The expression patterns of foxQ2, an animal plate marker (A, D), lefty, an oral ectoderm marker (B, E), and foxA, an endoderm and a mouthstomodeum marker at this stage (C, F) were observed in control (D–F) and BicC mRNA-injected embryos (A–C).
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