Koop D et al. (2017), Nodal and BMP expression during the transition ...

ECB-ART-45192

BMC Dev Biol 2017 Feb 13;171:4. doi: 10.1186/s12861-017-0145-1.

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Nodal and BMP expression during the transition to pentamery in the sea urchin Heliocidaris erythrogramma: insights into patterning the enigmatic echinoderm body plan.

Koop D , Cisternas P , Morris VB , Strbenac D , Yang JY , Wray GA , Byrne M .

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BACKGROUND: The molecular mechanisms underlying the development of the unusual echinoderm pentameral body plan and their likeness to mechanisms underlying the development of the bilateral plans of other deuterostomes are of interest in tracing body plan evolution. In this first study of the spatial expression of genes associated with Nodal and BMP2/4 signalling during the transition to pentamery in sea urchins, we investigate Heliocidaris erythrogramma, a species that provides access to the developing adult rudiment within days of fertilization. RESULTS: BMP2/4, and the putative downstream genes, Six1/2, Eya, Tbx2/3 and Msx were expressed in the earliest morphological manifestation of pentamery during development, the five hydrocoele lobes. The formation of the vestibular ectoderm, the specialized region overlying the left coelom that forms adult ectoderm, involved the expression of putative Nodal target genes Chordin, Gsc and BMP2/4 and putative BMP2/4 target genes Dlx, Msx and Tbx. The expression of Nodal, Lefty and Pitx2 in the right ectoderm, and Pitx2 in the right coelom, was as previously observed in other sea urchins. CONCLUSION: That genes associated with Nodal and BMP2/4 signalling are expressed in the hydrocoele lobes, indicates that they have a role in the developmental transition to pentamery, contributing to our understanding of how the most unusual body plan in the Bilateria may have evolved. We suggest that the Nodal and BMP2/4 signalling cascades might have been duplicated or split during the evolution to pentamery.

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Species referenced: Echinodermata Heliocidaris erythrogramma
Genes referenced: bmp2 chrd dlxl eya1 gscl lefty1 LOC100887844 LOC115918707 msx1 nodall pitx2 six1 tbx2

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	Fig. 1. Confocal microscope sections of Heliocidaris erythrogramma from the gastrula to the rudiment stage larva. Orientation of larvae is with anterior to the top and posterior, the blastopore, to the base. The left coelom is either on the left (a–d), or the view is of the larval left side with the left coelom in frontal view (e–l). a–b Gastrulae with the archenteron and the left coelom. c–d Rudiment formation in the early larva begins with extension of the left and right coeloms posteriorly from the anterior coelom and the formation of the vestibular ectoderm. e–h Confocal sections through an advanced larva. Development of the anterior portion of the left coelom to form the hydrocoele lobes in the advanced larva. i–l Confocal sections through the same larva, the expansion of the hydrocoele lobes and the overlying vestibular ectoderm form the primary podia that are visible externally. The stone canal and vestibule are also evident. Ar, archenteron; Bp, blastopore; Lc, left coelom; Ac, anterior coelom; Rc, right coelom; Ve, vestibular ectoderm; Lpc, left posterior coelom; Hl, hydrocoele lobes; Pp, primary podia; V, vestibule; H, hydrocoele; Sc, stone canal; Hp, hydropore. Scale bar: 200 μm. See Morris [30] for a detailed assessment of coelomogenesis in H. erythrogramma though analysis of confocal sections
	Fig. 2. Expression of Nodal and BMP genes in Heliocidaris erythrogramma from gastrula to rudiment formation (24–40 hpf). Orientation of larvae is with anterior to the top and posterior, the blastopore, to the base. The left coelom is either on the left, or the view is of the larval left side with the left coelom in frontal view. a–d. Nodal was initially expressed in the right ectoderm extending approximately half way around the gastrula (a). This expression was reduced until only weak expression was detected along the right side and along the ciliated band of the 40 hpf larva (d). e–h. Lefty was also expressed in the right ectoderm extending halfway around the gastrula (e), (e insert, posterior view). Lefty was expressed in cells along the right ectoderm in a domain that was less extensive than Nodal, being reduced to a small domain at 40 hpf (f–h). i–l. BMP2/4 was expressed in the posterior half of the gastrula ectoderm (i) and at 32 hpf BMP2/4 was expressed in the presumptive vestibular ectoderm on the left side (j). A left-lateral view at 36 hpf (k) shows expression in the hydrocoele lobes with expression no longer detectable in the ectoderm. Left-lateral view of a 40 hpf larva (l) shows BMP2/4 expression in five clusters of cells at the bases of the primary podia. m–p Chordin was expressed in the left ectoderm in the 24 hpf gastrula (m) and at 32 hpf (n) extends halfway around the larva. This is followed by weak (36 hpf, o) expression of Chordin in posterior portion of the vestibule and then no evidence of expression in the 40 hpf larva (p). Ar, archenteron; H, hydrocoele; Lc, left coelom; Pp, primary podia; Cb, ciliated band; V, vestibule. Scale bar: 200 μm
	Fig. 3. Expression of downstream targets of Nodal and BMP in the left and right coeloms during rudiment formation. Orientation of larvae is with anterior to the top and posterior, the blastopore, to the base and the left coelom on the left. a–d Pitx2. The gastrula (a) shows Pitx2 expressed in the right side of the anterior archenteron where the right coelom is beginning to form and in the right posterior ectoderm. In the 32 hpf larva (b), Pitx2 was expressed in the right coelom and right lateral ectoderm (arrow) and at 36 hpf (c) was expressed throughout the right coelom (insert) extending to where the anterior coelom meets the right coelom. In the 40 hpf (d) Pitx2 was expressed in the right coelom and right ectoderm (arrow), with expression extending between the ciliated band and the lipid rich apical end of the larva. e–h. Six1/2. In the 24 hpf gastrula (e), Six1/2 was expressed in anterior half of the archenteron. At 32 hpf (f) Six1/2 was expressed in the anterior coelom at the head of the archenteron and in the anterior (top arrow) and posterior (bottom arrow) walls of the proximal left coelom. In the 36 hpf larva (g), Six1/2 was expressed in the anterior coelom and hydrocoele underlying the vestibular ectoderm. The 40 hpf larva (h), shows Six1/2 expression in the anterior coelom and hydrocoele. Expression is restricted to the central hydrocoele and does not extend into the lobes of the forming podia. i–l. In the 24 hpf gastrula (i), Eya was expressed in the mid region of the archenteron. In the 32 hpf larva (j), Eya was expressed at the head of the archenteron on the left side extending into the posterior wall of the proximal left coelom (arrow), as well as in the anterior coelom and the anterior wall of the proximal left coelom. In the 36 hpf larva (k), Eya was expressed in the anterior coelom and proximal hydrocoele. A lateral and frontal view of the adult rudiment in the 40 hpf larva (l) shows Eya expression in the anterior coelom, the hydrocoele and extending into the podia. Ar, archenteron; Lc, left coelom; Rc, right coelom; Ac, anterior coelom; Pp, primary podia; Ve, vestibular ectoderm; H, hydrocoele; V, vestibule. Scale bar: 200 μm
	Fig. 4. Expression in vestibular ectoderm and pentameral structures. Orientation of larvae is with anterior to the top and posterior, the blastopore, to the base. The left coelom is either on the left, or the view is of the larval left side with the left coelom in face view. a–c Gsc. At 24 hpf Gsc (a) was expressed in the posterior half of the gastrula ectoderm, extending halfway around as seen in the posterior view (insert). In the 32 hpf larva (b), Gsc was expressed on the left in the presumptive vestibular ectoderm. In the 36 and 40 hpf larvae (c) Gsc was expressed in the vestibular ectoderm. d–g Dlx. In the gastrula (24 hpf d), Dlx was expressed in the posterior ectoderm extending anteriorly to the head/tip/anterior of the archenteron. Expression extends halfway around the gastrula (insert). In the 32 hpf larva (e) Dlx expression was restricted to the vestibular ectoderm. At 36 hpf (f) expression was strong throughout the vestibular ectoderm with particularly strong staining around the rim of the vestibule (and insert). Additional expression was evident in the right and posterior ectoderm (arrows). In a lateral and frontal view of the adult rudiment in the 40 hpf larva (g), Dlx expression was in the ectoderm of the vestibule roof (insert shows a second plane of focus through vestibule) and in interambulacral regions of the vestibule floor ectoderm, as well as in the right ectoderm (arrow). h–k Tbx2/3. In the gastrula (h), Tbx2/3 was expressed in the posterior ectoderm, close to the margins of the blastopore (insert, posterior view). In the 32 hpf larva (i), Tbx2/3 was expressed in the vestibular ectoderm and at 36 hpf (j) was expressed in the hydrocoele lobes at the bases of the forming podia. A frontal and lateral view of the adult rudiment in the 40 hpf larva (k) shows Tbx2/3 expression in the hydrocoele at the bases of the primary podia. l–d Msx. In gastrulae (l), Msx was expressed broadly in posterior ectoderm with stronger expression on the left side as also in the 32 hpf larva (m). In a left side view (two focal planes) of a 36 hpf larva (n) Msx was expressed in the rim of the vestibule, particularly in the posterior portion and in the hydrocoele lobes with strongest expression at the base of the lobes. In the left side view of a 40 hpf larva (o), Msx expression was evident in the posterior rim of the vestibule wall and in the hydrocoele at the bases of the primary podia (arrow in insert). Ar, archenteron; Lc, left coelom; Ve, vestibular ectoderm; V, vestibule; Pp, primary podia; Scale bar: 200 μm
	Fig. 5. Diagrammatic representation of gene expression domains during the formation of the vestibular ectoderm and left coelom (a) at 32 hpf and the early rudiment (b) at 40 hpf. s. The left ectoderm adjacent to the left coelom thickens to form the vestibular ectoderm. The left and right coeloms have extended posteriorly, with the left coelom contacting the left ectoderm. The yellow asterisk indicates the location of Nodal expression to the right of the head of the archenteron in the developing right coelom of Heliocidaris erythrogramma (see [28]). This region may serve as an organizer analogous to that seen in vertebrates (see [3]). B. Sagittal view of the developing adult rudiment (region indicated in frontal view of the rudiment in insert). The hydrocoele and left posterior coelom (=somatocoele) are distinct and the hydrocoele lobes have extended to form the lumen of the primary podia. AC, anterior coelom; LC, left coelom; RC, right coelom; HC, hydrocoele; SC, somatocoele; VE, vestibular ectoderm; PP, Primary podia

References [+] :

Angerer, The evolution of nervous system patterning: insights from sea urchin development. 2011, Pubmed, Echinobase