An evolutionarily conserved Hox-Gbx segmentation code in the rice coralMontipora capitata

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Abstract

Segmentation of the gastric cavity is a synapomorphic trait of cnidarians of the class Anthozoa (corals and sea anemones), with different clades forming distinct numbers of segments. In the starlet sea anemoneNematostella vectensis, for example, eight bilaterally positioned gastric segments are generated by the action of a group of Hox-Gbx genes in the developing larval endo-mesoderm. Still, given the range of segment numbers observed in different anthozoans, it remains unclear whether this Hox-Gbx module is evolutionarily conserved and how it might be deployed to generate different numbers of segments. Here, we systematically interrogate the role of Hox-Gbx genes during development of the rice coralMontipora capitata. We first characterize the temporal sequence of segmentation inM. capitatajuveniles and then combine transcriptomic profiling andin situhybridization to identify three conserved homeobox-containing genes,McAnthox8,McAnthox6a.1andMcGbx, which are collectively expressed in the developing endo-mesoderm prior to and during segment formation. The expression boundaries of these genes prefigure the positions of the first six segment boundaries, similar to theirNematostellahomologs. Further, we show that chemical inhibition of BMP activity at the planula stage abolishes the expression of Hox-Gbx genes, leading to the formation of an unsegmented gastric cavity. These findings demonstrate the existence of a functionally conserved Hox-Gbx module in evolutionarily divergent anthozoan species, suggesting that the last common ancestor of all anthozoans likely utilized a similar genetic toolkit to axially pattern the endo-mesoderm into metameric subunits.

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