Over 99% of modern animals are members of the evolutionary lineage Bilateria. The evolutionary success of Bilateria is credited partly to the origin of bilateral symmetry. Although animals of the phylum Cnidaria are not within the Bilateria, some representatives, such as the sea anemone Nematostella vectensis , exhibit bilateral symmetry. We show that Nematostella uses homologous genes to achieve bilateral symmetry: Multiple Hox genes are expressed in a staggered fashion along its primary body axis, and the transforming growth factor–β gene decapentaplegic ( dpp ) is expressed in an asymmetric fashion about its secondary body axis. These data suggest that bilateral symmetry arose before the evolutionary split of Cnidaria and Bilateria.

https://science.sciencemag.org/content/sci/304/5675/1335.full.pdf

Origins of Bilateral Symmetry: Hox and Dpp Expression in a Sea Anemone

The Hox gene cluster has a crucial function in body patterning during animal development. How and when this gene cluster originated is being clarified by recent data from Cnidaria, a basal animal phylum. The characterization of Hox-like genes from Hydra, sea anemones and jellyfish has revealed that a Hox gene cluster is extremely ancient, having originated even before the divergence of these basal animals.

Ancient origin of the Hox gene cluster.

National Science Foundation and the National Atmospheric and Space Administration (DEB519727244, IBN-0212773) NASA (NAG2-1374, NAG2-1519s); Intramural Research Program of the National Human Genome Research Institute; National Institutes of Health; Boston University Women's Guild

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Pre-bilaterian origins of the Hox cluster and the Hox code: evidence from the sea anemone, Nematostella vectensis.

The conservation of developmental functions exerted by Antp-class homeoproteins in protostomes and deuterostomes suggested that homologs with related functions are present in diploblastic animals. Our phylogenetic analyses showed that Antp-class homeodomains belong either to non-Hox or to Hox/paraHox families. Among the 13 non-Hox families, 9 have diploblastic homologs, Msx, Emx, Barx, Evx, Tlx, NK-2, and Prh/Hex, Not, and Dlx, reported here. Among the Hox/paraHox, poriferan sequences were not found, and the cnidarian sequences formed at least five distinct cnox families. Two are significantly related to the paraHox Gsx (cnox-2) and the mox (cnox-5) sequences, whereas three display some relatedness to the Hox paralog groups 1 (cnox-1), 9/10 (cnox-3) and the paraHox cdx (cnox-4). Intermediate Hox/paraHox genes (PG 3 to 8 and lox) did not have clear cnidarian counterparts. In Hydra, cnox-1, cnox-2, and cnox-3 were not found chromosomally linked within a 150-kb range and displayed specific expression patterns in the adult head. During regeneration, cnox-1 was expressed as an early gene whatever the polarity, whereas cnox-2 was up-regulated later during head but not foot regeneration. Finally, cnox-3 expression was reestablished in the adult head once it was fully formed. These results suggest that the Hydra genes related to anterior Hox/paraHox genes are involved at different stages of apical differentiation. However, the positional information defining the oral/aboral axis in Hydra cannot be correlated strictly to that characterizing the anterior–posterior axis in vertebrates or arthropods.

https://www.pnas.org/content/pnas/97/9/4493.full.pdf

Evolution of Antp-class genes and differential expression of Hydra Hox/paraHox genes in anterior patterning

Organisms develop through a series of stages leading to sexually mature adults. In a few cases ontogeny reversal is possible, but it does not occur typically after the onset of sexual reproduction. All stages of the medusa Turritopsis nutricula, from newly liberated to fully mature individuals, can transform back into colonial hydroids, either directly or through a resting period, thus escaping death and achieving potential immortality. This is the first metazoan known to revert to a colonial, juvenile morph after having achieved sexual maturity in a solitary stage. Selective excision experiments show that the transformation of medusae into polyps occurs only if differentiated cells of the exumbrellar epidermis and part of the gastrovascular system are present, revealing a transformation potential unparalleled in the animal kingdom.

Reversing the Life Cycle: Medusae Transforming into Polyps and Cell Transdifferentiation in Turritopsis nutricula (Cnidaria, Hydrozoa)

The marine jellyfish Podocoryne carnea (Cnidaria, Hydrozoa) has a metagenic life cycle consisting of a larva, a colonial polyp and a free-swimming jellyfish (medusa). To study the function of HOX genes in primitive diploblastic animals we screened a library of P. carnea cDNA using PCR primers derived from the most conserved regions in helix 1 and helix 3 of the homeobox. A novel gene, Cnox2-Pc, has been isolated and characterized. Cnox2-Pc is a HOX cluster-like gene, and its homeodomain shows similarity to the Deformed subfamily of HOM-C/HOX genes. In situ hybridization revealed that Cnox2-Pc is expressed in the anterior region of the larva, the polyp head, and the most apical ectoderm of the differentiating bud during medusa development. In adult medusa expression is restricted to the gastrovascular entoderm. The results suggest that Cnox2-Pc is involved in establishment of an anterior-posterior axis during development in primitive metazoans.

Birgit L. Aerne

Papers

The HOX-like gene Cnox2-Pc is expressed at the anterior region in all life cycle stages of the jellyfish Podocoryne carnea.

Life stage and tissue-specific expression of the homeobox gene cnox1-Pc of the hydrozoan Podocoryne carnea.

The polyp and its medusa: a molecular approach

Actin-encoding genes of the hydrozoan Podocoryne carnea.

The sequence of a cDNA encoding ribosomal protein S14 from the hydrozoan Podocoryne carnea reveals high evolutionary conservation.