Erkenbrack EM and Thompson JR (2019), Cell type phylogenetics informs the evolutionar...

ECB-ART-49923

Commun Biol 2019 Jan 01;2:160. doi: 10.1038/s42003-019-0417-3.

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Cell type phylogenetics informs the evolutionary origin of echinoderm larval skeletogenic cell identity.

Erkenbrack EM , Thompson JR .

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The multiplicity of cell types comprising multicellular organisms begs the question as to how cell type identities evolve over time. Cell type phylogenetics informs this question by comparing gene expression of homologous cell types in distantly related taxa. We employ this approach to inform the identity of larval skeletogenic cells of echinoderms, a clade for which there are phylogenetically diverse datasets of spatial gene expression patterns. We determined ancestral spatial expression patterns of alx1, ets1, tbr, erg, and vegfr, key components of the skeletogenic gene regulatory network driving identity of the larval skeletogenic cell. Here we show ancestral state reconstructions of spatial gene expression of extant eleutherozoan echinoderms support homology and common ancestry of echinoderm larval skeletogenic cells. We propose larval skeletogenic cells arose in the stem lineage of eleutherozoans during a cell type duplication event that heterochronically activated adult skeletogenic cells in a topographically distinct tissue in early development.

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	Fig. 1. Gene regulatory network of the larval skeletogenic cell and spatial distribution of skeletogenic regulatory genes early in development of eleutherozoan echinoderms studied herein. a Gene regulatory network of the S. purpuratus larval skeletogenic cell type showing regulatory genes and their interactions. This study focuses on the evolution of the genes shown in the red dashed box, viz. alx1, erg, ets1, tbrain, and vegfr. The network is based on the GRN found at http://echinobase.org/endomes and various studies11,35. b Phylogeny of eleutherozoan echinoderms showing classes, typical indirect embryonic and larval developmental stages with skeletogenic cells and/or larval skeleton in blue, and typical adult forms. Aster, Asteroidea; Ophiur, Ophiuroidea; Holothur, Holothuroidea. Taxa in blue indicate presence of larval skeletogenic cells. c Spatial distribution of four transcription factors shown to be important for specification of euechinoid larval skeletogenic cells in early development of eleutherozoan echinoderms. Character states used for ancestral state reconstruction are shown at right along with examples of how states were scored. SM skeletogenic mesenchyme, NSM nonskeletogenic mesenchyme. Silhouette images in b were created individually or are in the public domain with the following exceptions: ophiuroid (credit Noah Shlottman, photo from Casey Dunn), clypeasteroid (credit Michelle Site), and camarodont echinoid (credit Frank FÃ¶rster based on a picture by Jerry Kirkhart; modified by T. Michael Keesey), all of which are used under license http://creativecommons.org/licenses/by-sa/3.0/. No changes were made to the images
	Fig. 2. Ancestral state reconstruction of spatial gene expression data using a single-rate Markov model42 across eleutherozoan echinoderms. Ancestral states of alx1, ets1, and tbrain, three transcription factors critical to euechinoid larval skeletogenic cell specification. Geological timescale shown at bottom. Nodes are represented by boxed numbers. For each extant character state, the probability that it occurs at the ancestral node was estimated. The pie charts at each node show the mean posterior probability for each spatial expression pattern of the genes shown at right. The colors represent the character states shown in Fig.Â 1c. Abbreviations in the geological timescale are as follows: Ordovi Ordovician, Silur Silurian, Carbonifer Carboniferous, Paleog Paleogene, Ne Neogene
	Fig. 3. Ancestral state reconstruction of spatial gene expression data for erg and vegfr using a single-rate Markov model42 across eleutherozoan echinoderms. a Ancestral state reconstruction of spatial expression patterns of the transcription factor erg. b Ancestral state reconstruction of spatial expression patterns of the signaling gene vegfr. Geological timescale shown at bottom. Nodes are represented by boxed numbers. For each extant character state, the probability that it occurs at the ancestral node was estimated. The pie charts at each node show the mean posterior probability for each spatial expression pattern of the genes shown at right. The colors represent the character states shown in Fig.Â 1c. Abbreviations in the geological timescale are as follows: Ordovi Ordovician, Silur Silurian, Carbonifer Carboniferous, Paleog Paleogene, Ne Neogene
	Fig. 4. Cell-type evolution of echinoderm larval skeletogenic cells. a A cell-type duplication event resulted in activation of the adult skeletogenic cell-type identity network in early development, and thus the presence of skeletogenic cells in ancestral embryonic mesodermal territories (Node 1). Alx1 and vegfr are components of a cell-type specific identity network of larval skeletogenic cells across all extant eleutherozoans. The combination of alx1, erg, ets1, and vegfr comprise the cell-type identity network of skeletogenic cells across this clade. After the duplication event, at least one transcription factor that was ancestrally expressed in embryonic mesoderm domains,Â tbrain, was subsequently integrated into the larval skeletogenic GRN (Node 2), giving rise to two sister cell types. The larval skeletogenic cell type was lost in asteroids after the divergence with ophiuroids (Node 3). In the lineage leading to extant camarodont euechinoids, tbrain was decoupled from and no longer participated in specification of non-skeletogenic mesodermal cell types through Erg-mediated repression. Different colors represent cell-type lineages. Adult skeletogenic cells, purple. Larval skeletogenic cells, red. b Two competing hypotheses for the origin of larval skeletogenic cells in eleutherozoan echinoderms. The common ancestry hypothesis suggests that all larval skeletogenic cells in eleutherozoans are the result of a cell-type duplication event in the stem lineage of eleutherozoans. These cells would be lost in the lineage leading to extant asteroids. The convergent evolution hypothesis posits that larval skeletogenic cells are the result of at least two evolutionary events, one in the stem lineage of echinozoans and one other in the stem lineage of ophiuroids. Our results support the common ancestry hypothesis

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Adomako-Ankomah, Growth factors and early mesoderm morphogenesis: insights from the sea urchin embryo. 2014, Pubmed, Echinobase