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Molecular evidence of anteroposterior patterning in adult echinoderms

Nature volume 623, pages 555–561 (2023)Cite this article

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Abstract

The origin of the pentaradial body plan of echinoderms from a bilateral ancestor is one of the most enduring zoological puzzles1,2. 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 deuterostomes3,4,5 and other bilaterians6,7,8 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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Fig. 1: Deployment of the anteroposterior patterning system in deuterostomes.
Fig. 2: RNA tomography reveals the mediolateral dimension of the arms as the main driver of A–P patterning system deployment in P. miniata.
Fig. 3: Gene expression data reveal the deployment of the A–P patterning system in P. miniata ambulacral ectoderm.
Fig. 4: The ambulacral-anterior model of echinoderm body plan evolution.

Data availability

Specimens used for micro-CT analyses are registered at the Natural History Museum (London, UK) under registration no. NHMUK 2023.263. The segmented scans and reconstructed mesh files are available in Morphosource under project no. 000529415. Genome haplotypes are available at DDBJ/ENA/GenBank under accession nos. JAPJSQ000000000 and JAPJSR000000000. Sequence read archives for RNA sequencing are available at DDBJ/ENA/GenBank under Bioproject PRJNA873766. RNA tomography dataset is available at Zenodo: https://doi.org/10.5281/zenodo.8327479. Source data are provided with this paper.

Code availability

Custom code used for RNA tomography analyses is available at Zenodo: https://doi.org/10.5281/zenodo.8327479.

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Acknowledgements

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.

Author information

Author notes

  1. These authors contributed equally: D. S. Rokhsar, D. R. Rank, C. J. Lowe

Authors and Affiliations

  1. Department of Biology, Hopkins Marine Station, Stanford University, Pacific Grove, CA, USA

    L. Formery, I. Kohnle, J. Malnick, K. R. Uhlinger & C. J. Lowe

  2. Department of Molecular and Cell Biology, University of California Berkeley, Berkeley, CA, USA

    L. Formery & D. S. Rokhsar

  3. Pacific Biosciences, Menlo Park, CA, USA

    P. Peluso & D. R. Rank

  4. School of Biological Sciences, University of Southampton, Southampton, UK

    J. R. Thompson

  5. School of Ocean and Earth Science, University of Southampton, Southampton, UK

    J. R. Thompson

  6. Columbia Equine Hospital, Gresham, OR, USA

    M. Pitel

  7. Chan Zuckerberg BioHub, San Francisco, CA, USA

    D. S. Rokhsar & C. J. Lowe

  8. Molecular Genetics Unit, Okinawa Institute of Science and Technology, Onna, Okinawa, Japan

    D. S. Rokhsar

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Contributions

Experiments were designed by L.F., P.P., D.R.R. and C.J.L. Preliminary data were acquired by I.K., J.M. and K.R.U. Genome sequencing was done by P.P. and D.R.R. RNA tomography sectioning and sequencing were done by P.P., M.P., D.R.R. and C.J.L. RNA tomography analyses were performed by L.F. and D.S.R. Micro-CT preparation was done by L.F. and segmentation of the scans was done by J.R.T. Immunofluorescence, HCRs and imaging were performed by L.F. Data were analysed by L.F., D.S.R. and C.J.L. The manuscript was written by L.F., D.S.R. and C.J.L. with input from all authors.

Corresponding authors

Correspondence to L. Formery or C. J. Lowe.

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Competing interests

P.P. and D.R.R. are employees and shareholders of Pacific Biosciences. The remaining authors declare no competing interests.

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Nature thanks Andreas Hejnol and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data figures and tables

Extended Data Fig. 1 Patiria miniata anatomy is reflected by RNA tomography.

a, Phylogenetic position of P. miniata within deuterostomes, the grey box highlights the echinoderm phylum. b, Young adult P. miniata, viewed from the aboral side. c,d, Reconstructions of a young juvenile P. miniata scanned by micro-CT and segmented to highlight the main anatomical features of the animal, including the endoskeleton (grey), the digestive tract (yellow), the main body muscles (red), the water vascular system (WVS; purple) and the central nervous system (CNS; blue). c, Lateral views showing virtual sections of the micro-CT reconstruction along the proximodistal (P–D), oral–aboral (O–A) and mediolateral (M–L) dimensions used in the RNA tomography. Scale bar, 1 mm. d, Details of the different anatomical features shown in aboral or lateral views. The different panels are shown at the same scale. TAM: transverse ambulacral muscle; LTAM: lateral transverse ambulacral muscle; Long. M: longitudinal muscle; RNC: radial nerve cord; CNR: circumoral nerve ring. e, Principal component analysis of the RNA tomography sections. For each dimension the sections are colour-coded according to the geometry of the animal. f, Spearman correlations between the sections of the RNA tomography in each of the three dimensions. Epi: epidermis; Amb: ambulacrum. g, Expression profiles along the three dimensions of the RNA tomography for tissue marker genes known based on published literature to be expressed in the endoskeleton (grey), digestive tract (yellow), muscles (red), WVS (purple) and in the nervous system (blue) are consistent with the anatomy of the animal. Note that in the case of digestive tract markers, there is a left shift of expression in the M–L dimension that we assume resulted from displacement of the pyloric caeca during the dissection of the arm.

Source Data

Extended Data Fig. 2 Dorsoventral and appendage patterning in Patiria miniate.

a, Schematic representation of D–V patterning in bilaterians. b, Expression profile of D–V specification and patterning genes along the P–D, O–A and M–L dimensions of the RNA tomography. For the M–L dimension, the dotted line indicates the midline. c-v,y-α, HCRs of P. miniata brachiolariae (c,h,m), early metamorphosis (d,i,n), late metamorphosis (e,j,o) and postmetamorphic juveniles (f,g,k,l,p-v,y-α) imaged from the oral side. In c-q,t,u,y-α, specimens are counterstained with DAPI (blue). g,l,q,r,s,v, Magnification of a single ambulacrum. c-v, Expression patterns of genes involved in D–V axis specification and patterning. w, Schematic representation of limb proximodistal patterning in bilaterians. x, Expression profile of limb proximodistal patterning genes along the P–D dimension of the RNA tomography. y-α, Expression patterns of genes involved in limb proximodistal patterning. Scale bars, 100 µm.

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Supplementary Figs. 1–10 and Tables 1–7.

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Supplementary Video

Virtual sectioning of P. miniata juvenile. Animation showing a reconstruction of a young juvenile P. miniata scanned by micro-CT and segmented to highlight the main anatomical features of the animal, including the endoskeleton (grey), the digestive tract (yellow), the main body muscles (red), the water vascular system (purple) and the central nervous system (radial nerve cords and nerve ring; blue). Cut-away views of the model show virtual sectioning along the O–A, M–L and P–D dimensions.

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Formery, L., Peluso, P., Kohnle, I. et al. Molecular evidence of anteroposterior patterning in adult echinoderms. Nature 623, 555–561 (2023). https://doi.org/10.1038/s41586-023-06669-2

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