Byrne M et al. (2020), Transcriptomic analysis of sea star development...

ECB-ART-49848

DNA Res 2020 Feb 01;271:. doi: 10.1093/dnares/dsaa007.

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Transcriptomic analysis of sea star development through metamorphosis to the highly derived pentameral body plan with a focus on neural transcription factors.

Byrne M , Koop D , Strbenac D , Cisternas P , Balogh R , Yang JYH , Davidson PL , Wray G .

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The Echinodermata is characterized by a secondarily evolved pentameral body plan. While the evolutionary origin of this body plan has been the subject of debate, the molecular mechanisms underlying its development are poorly understood. We assembled a de novo developmental transcriptome from the embryo through metamorphosis in the sea star Parvulastra exigua. We use the asteroid model as it represents the basal-type echinoderm body architecture. Global variation in gene expression distinguished the gastrula profile and showed that metamorphic and juvenile stages were more similar to each other than to the pre-metamorphic stages, pointing to the marked changes that occur during metamorphosis. Differential expression and gene ontology (GO) analyses revealed dynamic changes in gene expression throughout development and the transition to pentamery. Many GO terms enriched during late metamorphosis were related to neurogenesis and signalling. Neural transcription factor genes exhibited clusters with distinct expression patterns. A suite of these genes was up-regulated during metamorphosis (e.g. Pax6, Eya, Hey, NeuroD, FoxD, Mbx, and Otp). In situ hybridization showed expression of neural genes in the CNS and sensory structures. Our results provide a foundation to understand the metamorphic transition in echinoderms and the genes involved in development and evolution of pentamery.

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	Figure 1. Echinoderm phylogeny showing class relationships, the Asterozoa (Asteroidea, Ophiuroidea), Echinozoa (Echinoidea, Holothuroidea), and basal Crinozoa and indicative relationship with the Hemichordata and Cephalochordata. Illustrations show adults and larvae. The Holothuroidea, Asteroidea, and Hemichordata have the ancestral-type feeding dipleurula larvae while the Echinoidea and Ophiuroidea have independently evolved the feeding pluteus larval form. The Crinoidea lack a feeding larva. Images provided: crinoid adult, A. Hoggett; crinoid larva H. Nakano; hemichordate images, B. Swalla, cephalochordate, P. Martinez.
	Figure 2. Parvulastra exigua (live images: AâE; confocal microscope sections: (FâI) including stages used for the developmental transcriptome. (A) Gastrula, one-day post fertilization (dpf) from the vegetal pole perspective to show the blastopore (bp) which subsequently closes. (B) Two early brachiolaria larvae (3 dpf). The left larva has hatched and the one on the right is emerging from the fertilization envelope (fe). b, brachia (C) Tripod brachiolaria (6 dpf) with well-developed brachia and adhesive disc (ad) that are used for attachment to the substratum. (D) Late metamorphosis (12 dpf) the attachment complex is being resorbed as the tube feet (tf) take over the role of benthic attachment. (E) Juvenile (20 dpf). (F) Section through the middle of a gastrula (1dpf) with the vegetal pole indicated by the blastopore at the bottom of the image and opening into the archenteron (ae). (G) Section through an unhatched early brachiolaria (3 dpf) with right and left coeloms evident on either side of the archenteron. (H and I) Mid-sections through tripod brachiolaria larvae at 6dpf (H) and 10 dpf (I) showing the developing hydrocoel (h) during metamorphosis (A, B, and DâH from 8, with permission). Scale bars = 100âÎ¼m.
	Figure 3. Principal component analysis of developmental gene expression across six stages of development in P. exigua. Most variation was between the pre-metamorphic stages (PC1â62%). Only 18% of variation is explained by differences in the metamorphic and post-metamorphic stages (PC2â18%). The PCA distinguishes the gastrula expression profile from all later developmental stages.
	Figure 4. Volcano plot of expression changes between (A) gastrula and hatched brachiolaria larva and (B) hatched brachiolaria and late metamorphosis stages. Genes with a log2 fold-change (FC) greater than or equal to 2 and supported by a false-discovery rate (FDR) less than 5% are coloured according to the stage at which they are significantly up-regulated: gastrula (green), hatched brachiolaria (pink), and late metamorphosis (blue).
	Figure 5. Multidimensional scaling plot of semantic similarity matrix generated from the top 30 enriched GO âBiological Processâ terms from genes significantly up-regulated during late metamorphosis relative to the hatched brachiolaria (larval) stage. GO term cluster representatives plotted as summarized by REVIGO. Bubble size reflects the frequency of the GO term in the Uniprot Gene Association Database and colour represents the log10 P-value of the GO term from the enrichment analyses. Genes up-regulated in the late metamorphosis stage are enriched for GO terms relating to neural development and signalling.
	Figure 6. Temporal expression profiles in P. exigua of putative neurogenic genes in three profiles, (A) Post-gastrula decrease, (B) up-regulation between gastrulation and the early larval stages followed by a decrease and an up-regulation at metamorphosis and juvenile stages, and (C) low expression in pre-metamorphic stages followed by an up-regulation during metamorphosis. The Fragments per kilobase of transcript per million mapped read (FPKM), log transformed, were plotted for the six developmental stages (see Supplementary Fig. 1).
	Figure 7. In situ hybridization of spatial expression of neurogenic genes in the developing juvenile P. exigua. (A) Otx expression in the oral nerve ring (NR) and the radial nerve cord (RNC). (B) Eya expression associated with the nervous system (arrow). (C) SoxB1 and (D) Pax6 expression in the developing juvenile tube feet (T) and eyespot (arrowhead). The specimen in C is an early metamorphosing juvenile and so lacks the mouth opening. M, mouth. Scale bars = 50âÎ¼m.

References [+] :

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