Functional evolution of Ets in echinoderms with focus on the evolution of echinoderm larval skeletons

Koga, Hisao; Matsubara, Mioko; Fujitani, Haruka; Miyamoto, Norio; Komatsu, Miéko; Kiyomoto, Masato; Akasaka, Koji; Wada, Hiroshi

doi:10.1007/s00427-010-0333-5

Cited by 35 publications

(51 citation statements)

References 32 publications

(46 reference statements)

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“…Our data also support previous notions about the origins of alx1 and ets1 functions -that these were obtained before diversification of the echinoid from holothuroids, a closely related echinoderm class (square and triangle in the phylogenetic tree in Fig. 7) (McCauley et al, 2012;Koga et al, 2010).…”

Section: Discussion the Distinction Of Mesenchyme Specification Mechasupporting

confidence: 90%

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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 Mechasupporting

confidence: 90%

“…For cloning of tbr and ets1, primer sets that have been described previously were used (Koga et al, 2010;Minemura et al, 2009). For the remaining the genes, the primers listed in supplementary material Table S2 were used.…”

Section: Isolation Of Genes From P Baculosamentioning

confidence: 99%

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

et al. 2014

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“…foxa , which is expressed in a torus above the central vegetal plate, likely marks the ring of future endoderm in sea cucumbers as it does in sea urchins and sea stars [33,38]. It has also previously been shown that the ets1 transcription factor is expressed in the vegetal pole of a closely-related species of sea cucumber [39]. Expression of sea star orthologs of these transcription factors has been reported [32-34,40].…”

Section: Resultsmentioning

confidence: 99%

Development of an embryonic skeletogenic mesenchyme lineage in a sea cucumber reveals the trajectory of change for the evolution of novel structures in echinoderms

McCauley

Wright

Exner

et al. 2012

EvoDevo

102

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BackgroundThe mechanisms by which the conserved genetic “toolkit” for development generates phenotypic disparity across metazoans is poorly understood. Echinoderm larvae provide a great resource for understanding how developmental novelty arises. The sea urchin pluteus larva is dramatically different from basal echinoderm larval types, which include the auricularia-type larva of its sister taxon, the sea cucumbers, and the sea star bipinnaria larva. In particular, the pluteus has a mesodermally-derived larval skeleton that is not present in sea star larvae or any outgroup taxa. To understand the evolutionary origin of this structure, we examined the molecular development of mesoderm in the sea cucumber, Parastichopus parvimensis.ResultsBy comparing gene expression in sea urchins, sea cucumbers and sea stars, we partially reconstructed the mesodermal regulatory state of the echinoderm ancestor. Surprisingly, we also identified expression of the transcription factor alx1 in a cryptic skeletogenic mesenchyme lineage in P. parvimensis. Orthologs of alx1 are expressed exclusively within the sea urchin skeletogenic mesenchyme, but are not expressed in the mesenchyme of the sea star, which suggests that alx1+ mesenchyme is a synapomorphy of at least sea urchins and sea cucumbers. Perturbation of Alx1 demonstrates that this protein is necessary for the formation of the sea cucumber spicule. Overexpression of the sea star alx1 ortholog in sea urchins is sufficient to induce additional skeleton, indicating that the Alx1 protein has not evolved a new function during the evolution of the larval skeleton.ConclusionsThe proposed echinoderm ancestral mesoderm state is highly conserved between the morphologically similar, but evolutionarily distant, auricularia and bipinnaria larvae. However, the auricularia, but not bipinnaria, also develops a simple skelotogenic cell lineage. Our data indicate that the first step in acquiring these novel cell fates was to re-specify the ancestral mesoderm into molecularly distinct territories. These new territories likely consisted of only a few cells with few regulatory differences from the ancestral state, thereby leaving the remaining mesoderm to retain its original function. The new territories were then free to take on a new fate. Partitioning of existing gene networks was a necessary pre-requisite to establish novelty in this system.

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“…PMCs arise from the large micromere lineage in response to the canonical Wnt signaling that leads to the activation of the transcriptional repressor Pmar1 (paired class homeodomain repressor) in the large micromeres (Oliveri et al, 2003). Activation of Pmar1 results in transcriptional inhibition of an ubiquitous transcriptional repressor HesC (Revilla-I-Domingo et al, 2007), leading to the activation of skeletogenic transcription factors which regulate various differentiation effector genes that are essential for PMC patterning and spicule formation (Damle and Davidson, 2011; Koga et al, 2010; Kurokawa et al, 1999; Sharma and Ettensohn, 2010, 2011; Wahl et al, 2009). Our data indicate that removal of miRNA regulation of β-catenin did not affect skeletogenesis of the sea urchin embryos (Fig.…”

Section: Discussionmentioning

confidence: 99%

microRNAs regulate β-catenin of the Wnt signaling pathway in early sea urchin development

Stepicheva

Nigam

Siddam

et al. 2015

Developmental Biology

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Development of complex multicellular organisms requires careful regulation at both transcriptional and post-transcriptional levels. Post-transcriptional gene regulation is in part mediated by a class of non-coding RNAs of 21–25 nucleotides in length known as microRNAs (miRNAs). β-catenin, regulated by the canonical Wnt signaling pathway, has a highly evolutionarily conserved function in patterning early metazoan embryos, in forming the Anterior-Posterior axis, and in establishing the endomesoderm. Using reporter constructs and site-directed mutagenesis, we identified at least three miRNA binding sites within the 3’ untranslated region (3’UTR) of the sea urchin β-catenin. Further, blocking these three miRNA binding sites within the β-catenin 3’UTR to prevent regulation of endogenous β-catenin by miRNAs resulted in a minor increase in β-catenin protein accumulation that is sufficient to induce aberrant gut morphology and circumesophageal musculature. These phenotypes are likely the result of increased transcript levels of Wnt responsive endomesodermal regulatory genes. This study demonstrates the importance of miRNA regulation of β-catenin in early development.

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Functional evolution of Ets in echinoderms with focus on the evolution of echinoderm larval skeletons

Cited by 35 publications

References 32 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

Development of an embryonic skeletogenic mesenchyme lineage in a sea cucumber reveals the trajectory of change for the evolution of novel structures in echinoderms

microRNAs regulate β-catenin of the Wnt signaling pathway in early sea urchin development

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