Conserved early expression patterns of micromere specification genes in two echinoid species belonging to the orders clypeasteroida and echinoida

Yamazaki, Atsuko; Furuzawa, Yousuke; Yamaguchi, Masatoshi

doi:10.1002/dvdy.22476

Cited by 19 publications

(33 citation statements)

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“…7). We have previously shown that the DNG-characteristic gene expression pattern is also observed in the euechinoid S. mirabilis, the ancestor of which had been separated from the camarodonta (the group including S. purpuratus) approximately 200 million years ago (Yamazaki et al, 2010) (Fig. 7), indicating that the euechinoid ancestor had obtained DNG.…”

Section: Discussion the Distinction Of Mesenchyme Specification Mechamentioning

confidence: 81%

“…The collection of adult P. baculosa, S. mirabilis and H. pulcherrimus, and the handling of gametes and embryos were performed according to a previously described method (Yamazaki et al, 2010(Yamazaki et al, , 2012. To estimate the transition of total cell numbers during the early stages of development in P. baculosa embryos, the number of nuclei per embryo were counted after staining with propidium iodide (Nacalai Tesque), as described previously (Stickland et al, 2004) (supplementary material Table S1).…”

Section: Animals and Embryosmentioning

confidence: 99%

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Larval mesenchyme cell specification in the primitive echinoid occurs independently of the double-negative gate

et al. 2014

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Echinoids (sea urchins) are divided into two major groups -cidaroids (a 'primitive' group) and euechinoids (a 'derived' group). The cidaroids are a promising model species for understanding the ancestral developmental mechanisms in echinoids, but little is known about the molecular mechanisms of cidaroid development. In euechinoids, skeletogenic mesenchyme cell specification is regulated by the double-negative gate (DNG), in which hesC represses the transcription of the downstream mesenchyme specification genes (alx1, tbr and ets1), thereby defining the prospective mesenchyme region. To estimate the ancestral mechanism of larval mesenchyme cell specification in echinoids, the expression patterns and roles of mesenchyme specification genes in the cidaroid Prionocidaris baculosa were examined. The present study reveals that the expression pattern and function of hesC in P. baculosa were inconsistent with the DNG model, suggesting that the euechinoidtype DNG is not utilized during cidaroid mesenchyme specification. In contrast with hesC, the expression patterns and functions of alx1, tbr and ets1 were similar between P. baculosa and euechinoids. Based on these results, we propose that the roles of alx1, tbr and ets1 in mesenchyme specification were established in the common ancestor of echinoids, and that the DNG system was acquired in the euechinoid lineage after divergence from the cidaroid ancestor. The evolutionary timing of the establishment of the DNG suggests that the DNG was originally related to micromere and/or primary mesenchyme cell formation but not to skeletogenic cell differentiation.

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Section: Discussion the Distinction Of Mesenchyme Specification Mechamentioning

confidence: 81%

Section: Animals and Embryosmentioning

confidence: 99%

Larval mesenchyme cell specification in the primitive echinoid occurs independently of the double-negative gate

et al. 2014

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“…The now-classic experiment in which ectopic overexpression of pmar1 converts all embryonic cells to a skeletogenic fate (26) has been duplicated in numerous camaradont euechinoids, including Hemicentrotus pulcherrimus (29), Paracentrotus lividus (30), and Lytechinus variegatus (31), suggesting that DNG function and circuitry are conserved in these taxa. Furthermore, whole-mount in situ hybridization data from the camarodonts H. pulcherrimus (32) and L. variegatus (33) reveal spatial distributions of hesc and its downstream targets that are consistent with the existence of the DNG in these euechinoids.…”

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confidence: 74%

“…It also has been shown that the DNG appears to be present in a number of euechinoid echinoid taxa outside the camaradonts (28,32). Micro1, a pmar1 ortholog, localizes to the 16-cell-stage micromeres of the clypeasteroid sand dollar Scaphechinus mirabilis (32) and the spatangoid heart urchin Echinocardium cordatum (28).…”

mentioning

confidence: 99%

“…Micro1, a pmar1 ortholog, localizes to the 16-cell-stage micromeres of the clypeasteroid sand dollar Scaphechinus mirabilis (32) and the spatangoid heart urchin Echinocardium cordatum (28). Furthermore, hesc shows complementary yet nonoverlapping expression patterns with alx1, ets1, and delta at the 10th cleavage stage in S. mirabilis (32), and roughly complementary expression with alx1, tbr, and ets1 at the blastula stage in E. cordatum and the stomopneustoid Glyptocidaris crenularis (28).…”

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confidence: 99%

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Paleogenomics of echinoids reveals an ancient origin for the double-negative specification of micromeres in sea urchins

Thompson

Erkenbrack

Hinman

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Establishing a timeline for the evolution of novelties is a common, unifying goal at the intersection of evolutionary and developmental biology. Analyses of gene regulatory networks (GRNs) provide the ability to understand the underlying genetic and developmental mechanisms responsible for the origin of morphological structures both in the development of an individual and across entire evolutionary lineages. Accurately dating GRN novelties, thereby establishing a timeline for GRN evolution, is necessary to answer questions about the rate at which GRNs and their subcircuits evolve, and to tie their evolution to paleoenvironmental and paleoecological changes. Paleogenomics unites the fossil record and all aspects of deep time, with modern genomics and developmental biology to understand the evolution of genomes in evolutionary time. Recent work on the regulatory genomic basis of development in cidaroid echinoids, sand dollars, heart urchins, and other nonmodel echinoderms provides an ideal dataset with which to explore GRN evolution in a comparative framework. Using divergence time estimation and ancestral state reconstructions, we have determined the age of the double-negative gate (DNG), the subcircuit which specifies micromeres and skeletogenic cells in Strongylocentrotus purpuratus. We have determined that the DNG has likely been used for euechinoid echinoid micromere specification since at least the Late Triassic. The innovation of the DNG thus predates the burst of post-Paleozoic echinoid morphological diversification that began in the Early Jurassic. Paleogenomics has wide applicability for the integration of deep time and molecular developmental data, and has wide utility in rigorously establishing timelines for GRN evolution.evolution | evo-devo | euechinoid | cidaroid | gene regulatory networks

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Selective accumulation of germ‐line associated gene products in early development of the sea star and distinct differences from germ‐line development in the sea urchin

Fresques

Zazueta-Novoa

Reich

et al. 2013

Developmental Dynamics

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Background Echinodermata is a diverse Phylum, a sister group to chordates, and contains diverse organisms that may be useful to understand varied mechanisms of germ-line specification. Results We tested 23 genes in development of the sea star Patiria miniata that fall into five categories: 1) Conserved germ-line factors; 2) Genes involved in the inductive mechanism of germ-line specification; 3) Germ-line associated genes; 4) Molecules involved in left-right asymmetry; and 5) Genes involved in regulation and maintenance of the genome during early embryogenesis. Overall, our results support the contention that the posterior enterocoel is a source of the germ line in the sea star P. miniata. Conclusion The germ line in this organism appears to be specified late in embryogenesis, and in a pattern more consistent with inductive interactions amongst cells. This is distinct from the mechanism seen in sea urchins, a close relative of the sea star clad. We propose that P. miniata may serve as a valuable model to study inductive mechanisms of germ-cell specification and when compared to germ-line formation in the sea urchin S. purpuratus may reveal developmental transitions that occur in the evolution of inherited and inductive mechanisms of germ-line specification.

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Conserved early expression patterns of micromere specification genes in two echinoid species belonging to the orders clypeasteroida and echinoida

Cited by 19 publications

References 131 publications

Larval mesenchyme cell specification in the primitive echinoid occurs independently of the double-negative gate

Larval mesenchyme cell specification in the primitive echinoid occurs independently of the double-negative gate

Paleogenomics of echinoids reveals an ancient origin for the double-negative specification of micromeres in sea urchins

Selective accumulation of germ‐line associated gene products in early development of the sea star and distinct differences from germ‐line development in the sea urchin

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