Spatial transcriptomics reveals a conserved segment polarity program that governs muscle patterning inNematostella vectensis

Abstract

SummaryDuring early animal evolution, the emergence of axially-polarized segments was central to the diversification of complex bilaterian body plans. Nevertheless, precisely how and when segment polarity pathways arose remains obscure. Here we demonstrate the molecular basis for segment polarization in developing larvae of the pre-bilaterian sea anemoneNematostella vectensis. Utilizing spatial transcriptomics, we first constructed a 3-D gene expression atlas of developing larval segments. Capitalizing on accuratein silicopredictions, we identified Lbx and Uncx, conserved homeodomain-containing genes that occupy opposing subsegmental domains under the control of both BMP signaling and the Hox-Gbx cascade. Functionally,Lbxmutagenesis eliminated all molecular evidence of segment polarization at larval stage and caused an aberrant mirror-symmetric pattern of retractor muscles in primary polyps. These results demonstrate the molecular basis for segment polarity in a pre-bilaterian animal, suggesting that polarized metameric structures were present in the Cnidaria-Bilateria common ancestor over 600 million years ago.HighlightsNematostellaendomesodermal tissue forms metameric segments and displays a transcriptomic profile similar to that observed in bilaterian mesodermConstruction of a comprehensive 3-D gene expression atlas enables systematic dissection of segmental identity in endomesodermLbxandUncx, two conserved homeobox-containing genes, establish segment polarity inNematostellaThe Cnidarian-Bilaterian common ancestor likely possessed the genetic toolkit to generate polarized metameric structures