Gene regulation of adult skeletogenesis in starfish and modifications during gene network co-option

Abstract

The larval skeleton of the echinoderm is believed to have been acquired through co-option of a pre-existing gene regulatory network (GRN); that is, the mechanism for adult skeleton formation in the echinoderm was deployed in early embryogenesis during echinoderm diversification. To explore the evolutionary changes that occurred during co-option, we examined the mechanism for adult skeletogenesis using the starfish Patiria pectinifera. Expression patterns of skeletogenesis-related genes (vegf, vegfr, ets1/2, erg, alx1, ca1, and clect) suggest that adult skeletogenic cells develop from the posterior coelom after the start of feeding. Treatment with inhibitors and gene knockout using transcription activator-like effector nucleases (TALENs) suggest that the feeding-nutrient sensing pathway activates Vegf signaling via target of rapamycin (TOR) activity, leading to the activation of skeletogenic regulatory genes in starfish. In the larval skeletogenesis of sea urchins, the homeobox gene pmar1 activates skeletogenic regulatory genes, but in starfish, localized expression of the pmar1-related genes phbA and phbB was not detected during the adult skeleton formation stage. Based on these data, we provide a model for the adult skeletogenic GRN in the echinoderm and propose that the upstream regulatory system changed from the feeding-TOR-Vegf pathway to a homeobox gene-system during co-option of the skeletogenic GRN.

An optimized Tet-On system for conditional control of gene expression in sea urchins

“…As the MAPK signaling pathway is activated cell-autonomously in the early embryo, possibly through the actions of localized maternal factors such as β-catenin (Fernandez-Serra et al, 2004; Röttinger et al, 2004), we proposed that the heterochronic shift in the deployment of the skeletogenic GRN that occurred during euechinoid evolution was achieved by an important evolutionary innovation that placed MAPK signaling under maternal control. We favor a model whereby current regulatory mechanisms that underlie late embryonic skeletal patterning and growth reflect an ancient heterochronic shift in VEGF3 expression by ectodermal cells (Morino et al, 2012; Yamazaki et al, 2021). We hypothesize that VEGF3 activates Ets1 through the MAPK signaling pathway at late embryonic stages, circuitry that is likely to be similar to the ancestral skeletogenic GRN found in the adult.…”

“…To establish the causal links required for the construction of experimental GRN models, functional perturbations of regulatory genes are usually performed, followed by observation of the effects on potential target genes. Although several approaches have been employed to successfully perturb gene function in sea urchin embryos, functional studies generally rely on microinjection of reagents such as morpholino antisense oligonucleotides (MOs) to block translation or splicing (Yaguchi, 2019), mRNAs encoding dominant-negative or constitutively active forms of proteins (Lepage and Gache, 2004), and targeted genome editing nucleases, such as transcription activator-like effector nucleases (TALENs) (Yamazaki et al, 2021) and CRISPR-Cas9 (Fleming et al, 2021; Lin et al, 2019; Wessel et al, 2020). These conventional approaches, however, face a common constraint.…”

Flower-like meristem conditions and spatial constraints shape architecture of floral pseudanthia in Apioideae

“…As components of a single GRN are interconnected, differences in spatio-temporal expression of particular regulatory gene can potentially affect its downstream effectors, allowing for their redeployment in the novel context. The examples of such evolutionary co-options are widespread in both animals [63][64][65] and plants [66][67][68]. As FUMs might evolve through heterochronic changes in FM genetic patterning, the co-option of multiple components of flower-specific GRN can tentatively explain the origin of some novelties associated with floral units, including formation of pseudanthia.…”

Detection of TALEN‐mediated genome cleavage during the early embryonic stage of the starfish Patiria pectinifera

“…2,3 Among echinoderms, starfish have been used to investigate various developmental phenomena such as whole-body regeneration, germline formation, and early specification. [4][5][6][7][8][9][10][11][12][13][14] For example, gene regulatory networks (GRNs) of early specification have been unraveled in starfish embryos and compared with other echinoderms to elucidate the evolutionary transition of GRN circuits. 5,6,[8][9][10][11][12]14 It is also revealed that starfish larval regeneration is regulated by an evolutionarily conserved machinery across the animal kingdom.…”

“…[4][5][6][7][8][9][10][11][12][13][14] For example, gene regulatory networks (GRNs) of early specification have been unraveled in starfish embryos and compared with other echinoderms to elucidate the evolutionary transition of GRN circuits. 5,6,[8][9][10][11][12]14 It is also revealed that starfish larval regeneration is regulated by an evolutionarily conserved machinery across the animal kingdom. 4 Overall, molecular study of starfish embryos has received considerable attention in recent years.…”