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In several model animals, the earliest phases of embryogenesis are regulated by lineage-specific genes, such as Drosophila bicoid. Sea urchin (echinoid) embryogenesis is initiated by zygotic expression of pmar1, a paired-class homeobox gene that has been considered to be present only in the lineage of modern urchins (euechinoids). In euechinoids, Pmar1 promotes endomesoderm specification by repressing the hairy and enhancer of split C (hesC) gene. Here, we identified the basal echinoid (cidaroid) pmar1 gene, which also promotes endomesoderm specification but not by repressing hesC. A further search for related genes demonstrated that other echinoderms have pmar1-related genes named phb. Functional analyses of starfish Phb proteins indicated that similar to cidaroid Pmar1, they promote activation of endomesoderm regulatory gene orthologs via an unknown repressor that is not HesC. Based on these results, we propose that Pmar1 may have recapitulated the regulatory function of Phb during the early diversification of echinoids and that the additional repressor HesC was placed under the control of Pmar1 in the euechinoid lineage. This case provides an exceptional model for understanding how early developmental processes diverge.

Pmar1/phb homeobox genes and the evolution of the double-negative gate for endomesoderm specification in echinoderms