Mechanisms of evolutionary changes in timing, spatial expression, and mRNA processing in the msp130 gene in a direct-developing sea urchin, Heliocidaris erythrogramma

Abstract

Developmental processes associated with skeletogenesis differ in the direct-developing sea urchin Heliocidaris erythrogramma from that in Heliocidaris tuberculata and other indirect-developing species. In H. erythrogramma, the differences include ingression of a much higher number of mesenchyme cells, failure of the cells to form the typical ring pattern of cells prior to the onset of skeletogenesis, a significantly reduced larval skeleton, and a delay in timing of expression of the skeletogenic cell-restricted gene msp130. We report that the heterochronic change in msp130 expression is regulated at the level of transcription. By transient expression of reporter constructs containing msp130 promoter regions from direct- and indirect-developing species, we found that this evolutionary change in regulation is consistent with changes in the timing of action of trans-acting factors in skeletogenic mesenchyme cells. We further used these experiments to show that the H. erythrogramma promoter contains elements required for correct spatial expression in the primary mesenchyme cells of an indirect-developing host. We finally show that alternate processing of H. erythrogramma msp130 is thus far specific to this species and not an aspect of adult skeletogenesis.