Yamakawa S et al. (2019), Retinoic Acid Signaling Regulates the Metamorph...

ECB-ART-48684

Biomolecules 2019 Dec 25;101:. doi: 10.3390/biom10010037.

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Retinoic Acid Signaling Regulates the Metamorphosis of Feather Stars (Crinoidea, Echinodermata): Insight into the Evolution of the Animal Life Cycle.

Yamakawa S , Morino Y , Kohtsuka H , Wada H .

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Many marine invertebrates have a life cycle with planktonic larvae, although the evolution of this type of life cycle remains enigmatic. We recently proposed that the regulatory mechanism of life cycle transition is conserved between jellyfish (Cnidaria) and starfish (Echinoderm); retinoic acid (RA) signaling regulates strobilation and metamorphosis, respectively. However, the function of RA signaling in other animal groups is poorly understood in this context. Here, to determine the ancestral function of RA signaling in echinoderms, we investigated the role of RA signaling during the metamorphosis of the feather star, Antedon serrata (Crinoidea, Echinodermata). Although feather stars have different larval forms from starfish, we found that exogenous RA treatment on doliolaria larvae induced metamorphosis, like in starfish. Furthermore, blocking RA synthesis or binding to the RA receptor suppressed metamorphosis. These results suggested that RA signaling functions as a regulator of metamorphosis in the ancestor of echinoderms. Our data provides insight into the evolution of the animal life cycle from the viewpoint of RA signaling.

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	Figure 1. Development process and localization of ciliary bands in the feather star A. serrata. (A,D,G) show the living specimens of A. serrata larvae. Competent doliolaria larvae settle to the substrate with the apical tuft (A), then commence the metamorphosis process to transit to the csytidean larval phase (D, G; approximately two, four days after settlement, respectively). (D) shows the early cystidean larvae just after metamorphosis commenced. Calyx (ca), stalk (st) and adhesive plate (p) can be clearly observed in a few days after metamorphosis (G). (B,C,E,F,H,I) indicates the fixed embryos labeled with anti-acetylated tubulin antibody in doliolaria, early cystidean and late cystidean larvae, respectively (light field; B, E and H, observation of fluorescence; C, F and I). The specific fluorescence in ciliary bands (arrow heads) and apical tuft (asterisk) were observed in doliolaria larvae (C), whereas no specific fluorescence was observed in cystidean larvae (F,I). Scale bars: 250 µm (A,D,G), 100 µm (B,C,E,F,H,I).
	Figure 2. Effects of the presence or absence of substrates on settlement and metamorphosis. (A,B) indicate the doliolaria (arrowheads) or cystidean (dotted line circles) larvae incubated for six days with or without substrate, respectively. Scale bars: 1 mm. (C) shows the metamorphosis ratio for each treatment.
	Figure 3. Induction of metamorphosis by exogenous RA treatment. (A–I) respectively show the larvae treated for 96 h with DMSO, RA 0.1 µM and RA 1 µM. While almost all doliolaria larvae did not metamorphose to cystidean larvae (A), metamorphosis was induced by the treatment of RA 0.1 µM and RA 1 µM (D and G, respectively). The numbers in (A,D,G) refer to “the number of metamorphosed larvae” / “the number of treated larvae”. (B,C,E,F,H,I) indicate the fixed larvae labeled with anti-acetylated tubulin antibody after DMSO, RA 0.1 µM and RA 1 µM treatment, respectively (light field; B, E and H, observation of fluorescence; C, F and I). In RA treatment, metamorphosis was induced as the calyx (ca), stalk (st) and adhesive plate (p) can be clearly observed, whereas ciliary bands (arrowheads) and apical tuft (asterisk) did not disappear (E,F,H,I) like in doliolaria larvae with DMSO treatment (C). Scale bars: 250 µm (A), 125 µm (B,C).
	Figure 4. Effects of DEAB or RO treatment on settlement and metamorphosis. We treated doliolaria larvae with DMSO (control), DEAB 300 µM or RO 3 µM and examined the effects on settlement and metamorphosis. (A–C) show the settled larvae on substrates (natural sands from their adult habitat) in DMSO, DEAB and RO treatments. The ratio of settlement and metamorphosis is shown in (D) (dark gray; settlement ratio, light gray; metamorphosis ratio). Scale bars: 125 µm.
	Figure 5. RO treatment suppressed the induction of metamorphosis by RA. RA 0.1 µM treatment with doliolaria larvae induced the metamorphosis (A), while this induction was suppressed by adding RO 3 µM (B). ca; calyx, st; stalk and p; adhesive plate. Scale bar: 125 µm.
	Figure 6. Hypothetical regulatory mechanism for metamorphosis of feather stars. Black arrows indicate the developmental process of A. serrata. Competent doliolaria larvae settle to external substrate with reception of environmental cues to commence metamorphosis process. Finally, transition to sessile cystidean larvae is completed through the disappearance of ciliary bands and the development of calyx, stalk and adhesive plate. We hypothesized that RA signaling mediates the metamorphosis process such as the development of calyx upon the reception of environmental signals (shown in green).

References [+] :

Albalat, The retinoic acid machinery in invertebrates: ancestral elements and vertebrate innovations. 2009, Pubmed