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

Shuonan He, Emma Rangel-Huerta, Eric Hill, Lacey Ellington, Shiyuan (Cynthia) Chen, Sofia Robb, Eva Majerová, Crawford Drury, Matthew C. Gibson
doi: https://doi.org/10.1101/2024.09.29.615694
Shuonan He
1Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
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Emma Rangel-Huerta
1Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
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Eric Hill
1Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
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Lacey Ellington
1Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
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Shiyuan (Cynthia) Chen
1Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
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Sofia Robb
1Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
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Eva Majerová
2Hawaiʻi Institute of Marine Biology, University of Hawaiʻi at Mānoa, Kāneʻohe, Hawaiʻi 96744, USA
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Crawford Drury
2Hawaiʻi Institute of Marine Biology, University of Hawaiʻi at Mānoa, Kāneʻohe, Hawaiʻi 96744, USA
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Matthew C. Gibson
1Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
3Department of Anatomy and Cell Biology, The University of Kansas School of Medicine, Kansas City, Kansas 66160, USA
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  • For correspondence: [email protected]
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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 anemone Nematostella 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 coral Montipora capitata. We first characterize the temporal sequence of segmentation in M. capitata juveniles and then combine transcriptomic profiling and in situ hybridization to identify three conserved homeobox-containing genes, McAnthox8, McAnthox6a.1 and McGbx, 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 their Nematostella homologs. 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.

Competing Interest Statement

The authors have declared no competing interest.

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Posted September 30, 2024.
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An evolutionarily conserved Hox-Gbx segmentation code in the rice coral Montipora capitata
Shuonan He, Emma Rangel-Huerta, Eric Hill, Lacey Ellington, Shiyuan (Cynthia) Chen, Sofia Robb, Eva Majerová, Crawford Drury, Matthew C. Gibson
bioRxiv 2024.09.29.615694; doi: https://doi.org/10.1101/2024.09.29.615694
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An evolutionarily conserved Hox-Gbx segmentation code in the rice coral Montipora capitata
Shuonan He, Emma Rangel-Huerta, Eric Hill, Lacey Ellington, Shiyuan (Cynthia) Chen, Sofia Robb, Eva Majerová, Crawford Drury, Matthew C. Gibson
bioRxiv 2024.09.29.615694; doi: https://doi.org/10.1101/2024.09.29.615694

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