Evolution of a pentameral body plan was not linked to translocation of anterior Hox genes: the echinoderm HOX cluster revisited

Abstract

Echinodermata is a large phylum of marine invertebrates characterized by an adult, pentameral body plan. This morphology is clearly derived as all members of Deuterostomia (the superphylum to which they belong) have a bilateral body plan. The origin of the pentameral plan has been the subject of intense debate. It is clear that the ancestor of Echinodermata had a bilateral plan but how this ancestor transformed its body "architecture" in such a drastic manner is not clear. Data from the fossil record and ontogeny are sparse and, so far, not very informative. The sequencing of the sea urchin genome a decade ago opened the possibility that the pentameral body plan was a consequence of a broken Hox cluster and a series of papers dwelt on the putative relationship between Hox gene arrangements in the chromosomes and the origin of pentamery. This relationship, sound as it was, is challenged by the revelation that the sea star HOX cluster is, in fact, intact, thus falsifying the hypothesis of a direct relationship between HOX cluster arrangement and the origin of the pentameral body plan. Here, we explore the relationship between Hox gene arrangements and echinoderm body "architecture," the expression of Hox genes in development and alternative scenarios for the origin of pentamery, with putative roles for signaling centers in generating multiple axes.

The sea cucumber genome provides insights into morphological evolution and visceral regeneration

“…purpuratus , whose anterior class genes ( Hox1 , Hox2 , and Hox3 ) were inverted and translocated to the end of the cluster because of genomic rearrangement (Fig 4) [32]. Thus, the present results are consistent with the opinion that translocation and inversion (TAI) of the Hox cluster was not a feature of the Echinozoa (sea urchins and sea cucumbers), and the pentameral body plan was not linked to Hox gene arrangements in echinoderms [34]. Hox4 and Hox6 were not found in the A .…”

“…filiformis , and F . serratissima were modified from Byrne et al 2016 [34]. Image credits: "Introduction to zoology; a guide to the study of animals, for the use of secondary schools" (1900) Macmillan; Freshwater and Marine Image Bank; Encyclopædia Britannica; Jerry Kirkhart; authors' own; public domain; Freshwater and Marine Image Bank; National Oceanic and Atmospheric Administration; Martin Cooper.…”

Expression of genes and proteins of the pax‐six‐eya‐dach network in the metamorphic sea urchin: Insights into development of the enigmatic echinoderm body plan and sensory structures

“…Overall, our results indicate that the PSEDN is deployed in development of the metamorphic sea urchin, and the expression of these genes indicates that they are involved in development of pentamery, the most derived deuterostome body plan (Arnone et al, ; Byrne et al, ). Interestingly, BMP2/4 signaling, through its control of Nodal , also appears to have a role in the development of pentamery (Koop et al, ).…”

The Link between Autotomy and CNS Regeneration: Echinoderms as Non‐Model Species for Regenerative Biology

“…Although echinoderms are not cephalized, they have a well‐developed CNS with features similar to that of the vertebrates . The nerve cord that runs along each primary body axis (ambulacrum or radius) ( Figure 3A,B,D,E) is considered to be homologous to the chordate nerve cord . In development, the nerve cords are formed in a manner similar to vertebrate neurulation .…”