Molecular evidence of anteroposterior patterning in adult echinoderms

Laurent Formery , Paul Peluso , I. Kohnle , J. Malnick , Mariya Pitel , K. R. Uhlinger , Daniel Rokhsar , David Rank , Christopher Lowe

Preprint posted on 5 February 2023 https://www.biorxiv.org/content/10.1101/2023.02.05.527185v1

Article now published in Nature at http://dx.doi.org/10.1038/s41586-023-06669-2

Spatial transcriptomics sheds light on the echinoderm body plan! The bilaterian antero- lateral axis shifts to medio-lateral in the ectoderm of adult echinoderms.

Selected by Rodrigo Senovilla-Ganzo

Categories: bioinformatics, cell biology, evolutionary biology, genetics, genomics, neuroscience, zoology

Updated 27 February 2024 with a postLight by Rodrigo Senovilla-Ganzo

The bioRxiv preprint highlighted here has now been peer-reviewed and published in Nature. This release has attracted both the attention of the general public (through several newspapers) as well as the scientific community (mostly through social media). Its reach was specifically increased by the outreach Nature Video produced by Shamini Bundell (https://www.nature.com/articles/d41586-023-03449-w) and the News&Views article written by Thurston Lacalli (https://www.nature.com/articles/d41586-023-03123-1?utm_medium=Social&utm_source=Twitter#Echobox=1698922903-2).

Comparing the preprint with the published paper reveals that no major modifications have been made in the figures and the overall manuscript. There is, however, a deeper discussion about the origin of the newly identified “ambulacral-anterior” patterning in the peer-reviewed paper. This discussion is focused on the origin of this new patterning mechanism as a recent co-option or ancestral modified form of antero-posterior patterning, highlighting the importance of homalozoan and helicoplacoid echinoderms to unravel this origin.

This group of echinoderms is thought to represent a transitional form between bilateral and pentaradial symmetry. Thus, “re-interpreting these fossils in light of new patterning datasets could allow us to discriminate between co-option with loss of the ancestral axial registry or descent with modification” (Formery et al., 2024). The existence of this transcriptomic evidence will enhance the comparative efforts across echinoderms and chordates. Unfortunately, I’m still missing an online resource with more accessible information for non-bioinformaticians in the evolutionary field.

Overall, the peer-reviewed published version of this bioRxiv preprint does provide improved figures and results, but the main improvement is found in the discussion section; specifically, when the evolutionary origins are addressed. Additionally, the disseminative works produced around this paper—including the mentioned outreach video and News&Views article—are of great value when reaching out to both scientific and non-scientific audiences.

Why I chose this preprint:

There are three main reasons to consider this paper as disruptive in the evolutionary biology field. Firstly, because of its novelty; spatial transcriptomics is a cutting-edge technology, which is finally reaching evolutionary biology to empower its research. Secondly, because this -omics data, at the same time, overthrows current theories about patterning in echinoderms and leaves the door open for a new paradigm in echinoderm body plan evolution. And last, but not least, due to the thought-provoking head-like theory. The segregation of posterior markers to the mesoderm, and anterior markers to the ectoderm is fascinating, although not unique. The separation between both anterior and posterior gene regulatory networks could have opened up doors for body plan evolution.

Background:

Living beings are extremely diverse, so to understand their evolutionary relationships, evolutionary developmental biologists have classified them by key features such as the order of appearance of mouth-anus (protostome/deuterostome) or the existence of bilateral symmetry (Cavalier-Smith, 2004). Although echinoderms, like sea urchins and starfish, display a non-bilateral pentaradial symmetry, they are included in the Bilateria clade. The reason behind this allocation is hidden in its larval development.

After gastrulation, the feeding larvae display a bilateral symmetry with several paired arms. However, subsequent metamorphosis leads to a reabsorption of anterior structures into a stacked shape with five not-paired rays (McEdward & Janies, 1993). From a developmental point of view, these early processes have been proven to be shared by sister group hemichordates and chordates. The gastrulation and early patterning of echinoderm bilaterian larvae are guided by Wnt, chordin and BMPs signalling – common pathways for all deuterostomes (Hinman & Burke, 2018; Holland & Anderson, 2015). However, after metamorphosis, the bilateral symmetry must be remodelled into radial symmetry, and the role of patterning genes in this process or even in the metamorphosed adult echinoderm remains a mystery (Figure 1a, b).

In order to explore the expression of these patterning genes in the larvae, the adult, and during metamorphosis, it is key to understand the evolution of radial echinoderms from a bilateral ancestor. Over time, several hypotheses have been proposed to explain adult divergence: bifurcation, circularization, duplication, and stacking (Adachi et al., 2018; Byrne et al., 2016; Luttrell et al., 2012; Peterson et al., 2000; Popodi, E., Andrews, M., & Raff, 1994; Rozhnov & Rozhnov, 2014; Smith, 2008). Bifurcation and circularization have been cast aside due to inconsistency with molecular data. However, duplication and stacking are still under consideration. In the duplication hypothesis (Byrne et al., 2016; Popodi, E., Andrews, M., & Raff, 1994), each of the five echinoderm rays is a copy of the ancestral AP axis, with the anterior ray displaying anterior markers and vice-versa for the posterior ray. In the stacking hypothesis (Adachi et al., 2018; Peterson et al., 2000; Smith, 2008), the oral-aboral axis of adult echinoderms is homologous to the bilaterian AP axis. Thus, the oral part would express anterior markers and the aboral posterior markers; or vice-versa. This hypothesis has been supported by Hox gene expression of the posterior mesoderm. However, broad bilaterian comparisons are normally based on ectodermal expression domains, as the authors of this preprint highlight.

Figure 1: Deployment of the antero-posterior patterning system in deuterostomes. a, Expression map of the conserved transcription factors and signalling ligands involved in ectoderm patterning along the AP axis, as observed in the hemichordate S. kowalveskii. b, Previous work in chordates and hemichordates has demonstrated extensive regulatory conservation in ectodermal AP patterning, establishing the ancestral regulatory characteristics of early deuterostomes. How this system is deployed in echinoderms remains unclear. c, Four hypotheses have been proposed for the deployment of the AP patterning system in establishing the echinoderm adult body plan: bifurcation, circularization, duplication and stacking. Extracted from Figure 1 (Formery et al., 2023).

Key findings:

The co-opted medio-lateral patterning. Antero-posterior patterning genes, which are responsible for regionalisation across deuterostomes, are expressed in an unexpected manner in echinoderm ectoderm. The markers defining anterior in deuterostomes are expressed in the midline of each array, while those marking posterior are expressed in the most lateral regions. The characterisation of evolutionary co-opted medio-lateral patterning is the major advancement described in this preprint (Figure 2).

Figure 2: Ambulacral-anterior model of echinoderm body plan evolution. a, Expression map of the conserved transcription factors and signalling ligands involved in ambulacral ectoderm patterning in P. miniata and organized from the midline of the ambulacrum (left) towards the interambulacrum (right). b, Diagram of the ambulacral-anterior model in a generalized asteroid with a cross-section through one of the arms. Only genes expressed in the ectoderm are shown. Extracted from Figure 4 (Formery et al., 2023).

Overthrown of current theories. These medial-lateral expression patterns do not match any of the mechanistical hypotheses out there (Formery et al., 2023). Thus, this finding overthrows all current theories about how echinoderm pentaradial symmetry evolved and leaves the door open for speculation.

Lack of trunk genetic markers on echinoderm ectoderm. In the echinoderm mesoderm, HOX genes are expressed in a stacked manner: anterior markers (Hox1-3) are expressed closer to the mouth and posterior genes (Hox11/13) closer to the anus. This patterning model favoured the stacked hypothesis, but now it conflicts with ectoderm expression, which displays a latero-medial expression of anterior (“head”) deuterostome markers. Thus, the mesoderm displays a “trunk” stacked patterning and the ectoderm shows a “head” latero-medial patterning.

Figure 3: Antero-posterior organization of anatomical elements at postmetamorphic stages (Mouth-anus distributed). Hox gene assignments in square brackets represent complementary data from other taxa. Vertical purple arrows represent the somatocoelar hox vectors. Other anatomical elements are indicated in the left scheme. Adapted from David & Mooi, 2014.

The authors of this preprint don’t dwell on this controversy, but they do highlight the concept of “head-like” animals. For Formery and co-authors, this “head-like” [sic] model is a sign of uncoupling between posterior and anterior programs, which seems common in other Echinodermata and Hemichordata (Lacalli, 2014). The decoupling between both tissues, quite unusual for chordates, could have allowed more evolutionary flexibility and could have driven its body plan evolution.

Transcriptomic tool. This article provides an extense transcriptomic resource for the community to consult markers and discuss about a new theory about echinoderm body plan evolution. A valuable contribution to open access science.

Future directions and questions for the authors (Answers below, at Author’s response)

What new theory is shaped by this data? Could you propose a new paradigm explaining pentaradial symmetry? Can the stacking theory still be plausible for mesoderm, but a new theory might be needed for ectoderm?

What are the patterning differences between larvae and adults? Is echinoderm adult patterning an exacerbation of the differences between echinoderm larvae and hemichordate?

Some of these antero-posterior genes (such as hedgehog, nkx2.1) are dorso-ventral in vertebrates. Did you already observe a different patterning in these vertebrate dorso-ventral genes? Is there a dorso-ventral patterning in echinoderms?

Bibliography.

Adachi, S., Niimi, I., Sakai, Y., Sato, F., Minokawa, T., Urata, M., Sehara-Fujisawa, A., Kobayashi, I., & Yamaguchi, M. (2018). Anteroposterior molecular registries in ectoderm of the echinus rudiment. Developmental Dynamics : An Official Publication of the American Association of Anatomists, 247(12), 1297–1307. https://doi.org/10.1002/DVDY.24686

Byrne, M., Martinez, P., & Morris, V. (2016). Evolution of a pentameral body plan was not linked to translocation of anterior Hox genes: the echinoderm HOX cluster revisited. Evolution & Development, 18(2), 137–143. https://doi.org/10.1111/EDE.12172

Cavalier-Smith, T. (2004). Only six kingdoms of life. Proceedings of the Royal Society B: Biological Sciences, 271(1545), 1251. https://doi.org/10.1098/RSPB.2004.2705

David, B., & Mooi, R. (2014). How Hox genes can shed light on the place of echinoderms among the deuterostomes. EvoDevo, 5(1), 1–19. https://doi.org/10.1186/2041-9139-5-22/FIGURES/6

Formery, L., Peluso, P., Kohnle, I., Malnick, J., Pitel, M., Uhlinger, K. R., Rokhsar, D. S., Rank, D. R., & Lowe, C. J. (2023). Molecular evidence of anteroposterior patterning in adult echinoderms. BioRxiv, 2023.02.05.527185. https://doi.org/10.1101/2023.02.05.527185

Hinman, V. F., & Burke, R. D. (2018). Embryonic neurogenesis in echinoderms. Wiley Interdisciplinary Reviews: Developmental Biology, 7(4), e316. https://doi.org/10.1002/WDEV.316

Holland, L. Z., & Anderson, P. A. V. (2015). Evolution of basal deuterostome nervous systems. Journal of Experimental Biology, 218(4), 637–645. https://doi.org/10.1242/JEB.109108

Lacalli, T. (2014). Echinoderm conundrums: Hox genes, heterochrony, and an excess of mouths. EvoDevo, 5(1), 1–4. https://doi.org/10.1186/2041-9139-5-46/FIGURES/1

Luttrell, S., Konikoff, C., Byrne, A., Bengtsson, B., & Swalla, B. J. (2012). Ptychoderid Hemichordate Neurulation without a Notochord. Integrative and Comparative Biology, 52(6), 829–834. https://doi.org/10.1093/ICB/ICS117

McEdward, L. R., & Janies, D. A. (1993). Life Cycle Evolution in Asteroids: What is a Larva? Https://Doi.Org/10.2307/1542444, 184(3), 255–268. https://doi.org/10.2307/1542444

Peterson, K. J., Arenas-Mena, C., & Davidson, E. H. (2000). The A/P axis in echinoderm ontogeny and evolution: evidence from fossils and molecules. Evolution & Development, 2(2), 93–101. https://doi.org/10.1046/J.1525-142X.2000.00042.X

Popodi, E., Andrews, M., & Raff, R. A. (1994). Evolution of body plans: using homeobox genes to examine the development of the radial CNS of echinoderms. Developmental Biology, 163, 540.

Rozhnov, S. V., & Rozhnov, S. V. (2014). Symmetry of echinoderms: From initial bilaterally-asymmetric metamerism to pentaradiality. Natural Science, 6(4), 171–183. https://doi.org/10.4236/NS.2014.64021

Smith, A. B. (2008). Deuterostomes in a twist: the origins of a radical new body plan. Evolution & Development, 10(4), 493–503. https://doi.org/10.1111/J.1525-142X.2008.00260.X

Tags: ambulacra, echinoderms, evolution, omics, patterning, spatialomics

Posted on: 3 May 2023 , updated on: 27 February 2024

doi: https://doi.org/10.1242/prelights.34443

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Author's response

Laurent Formery shared

I completely agree with your proposition that the stacking hypothesis might still be true in the mesoderm. The important nuance however, compared to what was proposed for instance by David and Mooi (2014) is that the ectoderm should not be considered the anterior-most of the stacked compartments. Instead, it has a patterning logic of its own, which is distinct from that of the mesoderm. As already proposed by Lacalli (2014) and Adachi et al. (2018), this suggests that in echinoderms the patterning of the different germ layers use completely different set of axial coordinates, whereas if you look for instance at a vertebrate, the anterior part of the ectoderm, endoderm and mesoderm are all on the same “side” of the animal.

When only looking at the ectoderm, the ambulacra of sea stars (and probably other echinoderm as well) appear to be an elaboration of an anterior territory which usescompletely different axial properties than what is used in the larva. We can’t demonstrate this yet, but this is probably the result of a signaling crosstalk between the mesoderm, which becomes pentaradial first and superimposes this symmetry onto the ectoderm. When considering a large comparative framework, this in fact makes a lot of sense. In hemichordates, the sister group of echinoderms, it has been demonstrated that the larva is a “head-larva” which is essentially anterior from an ectoderm patterning point of view (Gonzalez et al., 2017). During metamorphosis, hemichordate larvae add their trunk posteriorly by elongating a region that expresses hox genes. Echinoderm larvae are very similar to hemichordate larvae, and they are also “head-larvae” (Yankura et al., 2010), but in their case it seems that they have a very different way of making an adult body plan: instead of elongating a trunk, they make five ambulacra and reorganizes their body around these.

Importantly, our data do not predict anything about the nature of the pentaradial symmetry itself. Why the mesoderm in echinoderms becomes pentaradial, and how does this unusual symmetry propagates to the ectoderm later on is still completely unknown – and it is also unknown why there are 5 of them and not 4 or 6 for instance. What we can say is that the ambulacral ectoderm appears to be an outgrowth of an anterior-like territory.

What are the patterning differences between larvae and adults? Is echinoderm adult patterning an exacerbation of the differences between echinoderm larvae and hemichordate?

Echinoderm larvae and hemichordate larvae are very similar and they are both bilaterally symmetric for the most part, and as dicussed above they have both an anterior identity. The main difference is that for unknown reasons, the mesoderm on the left side of echinoderm larvae turn pentaradial, and then the rest of the larva reorganizes around this tissue while in hemichordates the development of the mesoderm remains bilateral. So I would say that they start very similar but then have completely different ways of making their adult body plan.

This is a very good question, in fact we have been looking at this but the data on the DV axis were not included in the preprint. A lot of markers of dorso-ventral patterning (also referred to as medio-lateral patterning, which is totally unrelated to the medio-lateral expression of AP markers that we show in Patiria) are expressed in the ambulacral area, such as hedgehog which is expressed at the midline of the ambulacra but also nkx2.2, nk6, foxA or msx. However, in other bilaterian most of these genes are involved in AP patterning as well. On the other hand, key players of DV axis specification like BMP2/4, ADMP or BMP1 were only detected in the hydrocoel, while other like chordin or nodal were not express at any time around the metamorphosis or even lost like pax3/7. This suggests that downstream components of DV specification might be used in patterning the ambulacra, but that there is no equivalent to a proper DV axis at this point of echinoderm ontogeny. There is a DV specification in the larva, but we think that this notion becomes irrelevant when the animal turn pentaradial.

I also would like to comment on the idea of co-option. In your pre-light, you mention “the co-opted medio-lateral patterning”. I suppose that this refers to the idea that the AP patterning system has been co-opted in the medio-lateral dimension of the sea star, but I would not necessary imply that this is the result of co-option. In hemichordates, the head-larva becomes the anterior part of the adult worm and this corresponds to the use of the anterior patterning framework to achieve a different anatomy, not to co-option. Similarly, although co-option can not be ruled out for sure in the case of echinoderms, we favor the idea that in this phylum as well the anterior identity of the larva just turns into an anatomically distinct anterior identity.

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