The sea urchin and its Aristotle’s lantern shed light on mechanisms of genome evolution and embryo development

The researchers’ findings notably revealed the existence of opposing trends between sea urchins and vertebrates in the evolution of gene order within chromosomes, while suggesting strong conservation of gene regulatory modules between sea urchins and chordates.

Curious thinkers have been intrigued by sea urchins since antiquity, and one of them, the Greek philosopher and naturalist Aristotle, even gave his name to the animals' mouth apparatus, which he compared to a lantern: Aristotle's lantern. Prized by gourmets for the delicate taste of their gonads, sea urchins are also prized by developmental biologists for the breathtaking transparency of their eggs and embryos, and the abundance of their gametes. Sea urchins have been involved in major discoveries in developmental biology, such as discovery of the hereditary role of chromosomes by Boveri, research on the great plasticity of blastomeres and embryonic induction processes by Driesch and Hörstadius, and discovery of the role of cyclins in the cell cycle by Hunt.

Sea urchins belong to the echinoderm phylum, a sister group to the chordates and vertebrates in the evolutionary tree. Adult echinoderms are known for several remarkable characteristics, such as a calcium carbonate endoskeleton and a vascular system consisting of ambulacral feet driven by water circulating within a system of canals. During their development, sea urchin embryos, unlike other echinoderms, also possess a larval skeleton produced by a population of unique mesenchyme cells descending from a portion of the cells derived from the first cell divisions of the embryo (the micromeres) whose specification occurs very early in development.

To better understand the major trends in echinoderm genome evolution and the mechanisms underlying the appearance of these new structures in sea urchins, the researchers compared the genome architecture and gene expression program of the Mediterranean sea urchin Paracentrotus lividus with those of other urchin species and with chordates. Analyses carried out by the researchers reveal that the sea urchin genome is relatively stable compared with that of vertebrates. Like the genomes of cephalochordates, molluscs and cnidarians, but unlike vertebrates, the sea urchin genome seems to have preserved the ancestral chromosomes (or linkage groups) that have been present in animals for hundreds of millions of years.

Unexpectedly, however, the researchers discovered that, on a finer scale, the order of genes within chromosomes (microsynteny) has evolved very quickly between sea urchin species, resulting in very different gene orders between sea urchin species. Analysis of the gene content of the genome also reveals the existence of many duplicated genes whose localized expression in organs such as Aristotle's lantern, the aqueous vascular system or in the mesenchyme at the origin of the embryonic skeleton could be associated with the emergence of these structures.

Finally, comparison of temporal gene expression (RNA-seq technique) and cis-regulatory gene modules (ATAC-seq technique) between sea urchins and chordates suggests deep conservation of the mechanisms and regulatory logic controlling embryonic development. This study therefore highlights that very distinct trends occurred in the evolution of echinoderm and vertebrate genomes, despite strong conservation of the gene expression program during embryonic development.

 
© Thierry Lepage & Ferdinand Marletaz Figure. Bottom: comparison of chromosome structure between humans and mice, showing the existence of numerous inter-chromosomal reorganizations but also the presence of long collinear segments between the two species. Bottom, comparison of the chromosome 1 structure between two sea urchin species, revealing the absence of conservation of visible gene order within a pair of homologous chromosomes. Top: comparison of the temporal gene expression program (RNA-seq) and gene regulatory modules (ATAC-seq) between sea urchins and chordates, revealing significant conservation of the developmental program and en-cis gene regulatory modules.
 

More information

Ferdinand Marletaz, Arnaud Couloux, Julie Poulain, ..., Maria Ina Arnone, Christian Gache, Thierry Lepage. Analysis of the P. lividus sea urchin genome highlights contrasting trends of genomic and regulatory evolution in deuterostomes. Cell Genomics (2023).
DOI : https://doi.org/10.1016/j.xgen.2023.100295

Contact

Thierry Lepage, Directeur de Recherches CNRS - Thierry.LEPAGE@univ-cotedazur.fr - 04 89 15 08 30