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.
Highlights
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
In the sea urchin larval skeletogenic GRN, Pmar[1] is one of the upstream key regulators, and we previously suggested that two Pmar1-related proteins, PhbA and PhbB, function as upstream regulators in the endomesoderm specification of starfish during e mbryogenesis[27]
To estimate the evolutionary modifications in the GRN associated with cooption of skeletogenesis, we examined the effects of the Vegf and target of rapamycin (TOR) signaling pathways on larval skeletogenesis in the sea urchin H. pulcherrimus, which belongs to the euechinoid group (Fig. 7)
Summary
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. In the larval skeletogenesis of sea urchins, the homeobox gene pmar[1] activates skeletogenic regulatory genes, but in starfish, localized expression of the pmar1related 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 genesystem during co-option of the skeletogenic GRN. Based on the comparison of data from P. pectinifera with data from the euechinoid Hemicentrotus pulcherrimus, we discuss evolutionary modifications that occurred during the co-option of the skeletogenic GRN in echinoderms
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