Molecular evidence of anteroposterior patterning in adult echinoderms
Molecular evidence of anteroposterior patterning in adult echinoderms
The origin of the pentaradial body plan of echinoderms from a bilateral ancestor is one of the most enduring zoological puzzles. Because echinoderms are defined by morphological novelty, even the most basic axial comparisons with their bilaterian relatives are problematic. To revisit this classical question, we used conserved anteroposterior axial molecular markers to determine whether the highly derived adult body plan of echinoderms masks underlying patterning similarities with other deuterostomes. We investigated the expression of a suite of conserved transcription factors with well-established roles in the establishment of anteroposterior polarity in deuterostomes and other bilaterians using RNA tomography and in situ hybridization in the sea star Patiria miniata. The relative spatial expression of these markers in P. miniata ambulacral ectoderm shows similarity with other deuterostomes, with the midline of each ray representing the most anterior territory and the most lateral parts exhibiting a more posterior identity. Strikingly, there is no ectodermal territory in the sea star that expresses the characteristic bilaterian trunk genetic patterning programme. This finding suggests that from the perspective of ectoderm patterning, echinoderms are mostly head-like animals and provides a developmental rationale for the re-evaluation of the events that led to the evolution of the derived adult body plan of echinoderms.
555-561
Formery, L.
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Peluso, P.
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Kohnle, I.
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Malnick, J.
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Thompson, J.R.
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Pitel, M.
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Uhlinger, K.R.
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Rokhsar, D.S.
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Rank, D.R.
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Lowe, C.J.
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16 November 2023
Formery, L.
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Peluso, P.
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Kohnle, I.
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Malnick, J.
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Thompson, J.R.
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Pitel, M.
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Uhlinger, K.R.
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Rokhsar, D.S.
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Rank, D.R.
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Lowe, C.J.
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Formery, L., Peluso, P., Kohnle, I., Malnick, J., Thompson, J.R., Pitel, M., Uhlinger, K.R., Rokhsar, D.S., Rank, D.R. and Lowe, C.J.
(2023)
Molecular evidence of anteroposterior patterning in adult echinoderms.
Nature, 623 (7987), .
(doi:10.1038/s41586-023-06669-2).
Abstract
The origin of the pentaradial body plan of echinoderms from a bilateral ancestor is one of the most enduring zoological puzzles. Because echinoderms are defined by morphological novelty, even the most basic axial comparisons with their bilaterian relatives are problematic. To revisit this classical question, we used conserved anteroposterior axial molecular markers to determine whether the highly derived adult body plan of echinoderms masks underlying patterning similarities with other deuterostomes. We investigated the expression of a suite of conserved transcription factors with well-established roles in the establishment of anteroposterior polarity in deuterostomes and other bilaterians using RNA tomography and in situ hybridization in the sea star Patiria miniata. The relative spatial expression of these markers in P. miniata ambulacral ectoderm shows similarity with other deuterostomes, with the midline of each ray representing the most anterior territory and the most lateral parts exhibiting a more posterior identity. Strikingly, there is no ectodermal territory in the sea star that expresses the characteristic bilaterian trunk genetic patterning programme. This finding suggests that from the perspective of ectoderm patterning, echinoderms are mostly head-like animals and provides a developmental rationale for the re-evaluation of the events that led to the evolution of the derived adult body plan of echinoderms.
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Formery_et_al_Author_Accepted_Merged
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More information
Accepted/In Press date: 22 September 2023
e-pub ahead of print date: 1 November 2023
Published date: 16 November 2023
Additional Information:
Funding Information:
We would like to thank F. Benedetti and R. Elahi for helping with RNA tomography analyses; A. Vailionis, P. Vyas and the Stanford Nano Shared Facility for helping with X-ray micro-CT; J. Grossman for the ambulacral-anterior model schematics; A. Formery for providing the 3D models of the RNA tomography sections; A. Rutledge for helping with animal husbandry; and V. Hinman for providing clones for preliminary analyses. We also thank G. A. Wray, T. Lacalli, R. Mooi, J. C. Croce and members of the Rokhsar and Lowe laboratories for discussions. This work was supported by a Leverhulme Trust Early Career Fellowship to J.R.T., a NASA grant to C.J.L. (NNX13AI68G), an NSF grant to C.J.L. (1656628) and Chan Zuckerberg BioHub funding to D.S.R. and C.J.L. For the purpose of open access, the author has applied a CC BY public copyright license to any Author Accepted Manuscript version arising from this submission.
Publisher Copyright:
© 2023, The Author(s), under exclusive licence to Springer Nature Limited.
Identifiers
Local EPrints ID: 484572
URI: http://eprints.soton.ac.uk/id/eprint/484572
ISSN: 0028-0836
PURE UUID: 63837de8-c4ec-47cc-8fa2-c33c42512b43
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Date deposited: 16 Nov 2023 18:07
Last modified: 18 Mar 2024 04:07
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Contributors
Author:
L. Formery
Author:
P. Peluso
Author:
I. Kohnle
Author:
J. Malnick
Author:
J.R. Thompson
Author:
M. Pitel
Author:
K.R. Uhlinger
Author:
D.S. Rokhsar
Author:
D.R. Rank
Author:
C.J. Lowe
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