Molluscan dorsal-ventral patterning relying on bmp2/4 and chordin provides insights into spiralian development and bilaterian evolution

Abstract

Although a conserved mechanism relying on bmp2/4 and chordin is suggested in animal dorsal-ventral (DV) patterning, this mechanism has not been reported in spiralians, one of the three major clades of bilaterians. Studies on limited spiralian representatives have suggested markedly diverse DV patterning mechanisms, a considerable amount of which no longer deploy BMP signaling. Here, we showed that bmp2/4 and chordin regulated DV patterning in the mollusk Lottia goshimai, which was predicted in spiralians but not reported before. In the context of the diverse reports in spiralians, it conversely represents a relatively unusual case. We then showed that bmp2/4 and chordin coordinated to mediate signaling from the D-quadrant organizer to induce the DV axis, among which chordin transferred breakdown-of-symmetry information. Further investigations on the L. goshimai embryos with influenced DV patterning suggested roles of BMP signaling in regulating the localization of the blastopore and the organization of the nervous system, indicating a cooption of DV patterning and the transition of these key characteristics at the origin of bilaterians. These findings provide insights into the evolution of animal DV patterning, the unique development mode of spiralians driven by the D-quadrant organizer, and the evolution of bilaterian body plans.