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Biozentrum: flexible and redundant roles of Pax genes during early evolution of animals
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Published online 28 July 2010
A study in jellyfishes uncovers the diversity of the Pax transcription factors that are involved in a variety of developmental processes, including eye development. The authors propose that in the ancestral animal eye, which is likely to have evolved in the common ancestor of cnidarians and bilaterians, different classes of Pax genes were redundantly recruited and may then have been flexibly selected in distinct animal lineages for their roles in eye development.
An understanding of the function of Pax transcription factors is essential, since some Pax mutations are linked to certain inherited human diseases, such as the Waardenburg syndrome and Aniridia, both displaying anomalies in the development of the eye.
Pax genes (named for their conserved PAired boX domain) comprise a large family of developmental regulatory genes that encode nuclear transcription factors. They are normally expressed during embryogenesis and down regulated in adult stages. Their major roles in patterning, morphogenesis, and organogenesis as well as their occurrence in virtually all metazoans indicate that Pax genes are master control genes. Pax transcription factors are involved in various developmental processes in bilaterians (animals showing a bilateral body symmetry), including eye development, a role typically assigned to Pax-6. In the current online issue of PNAS, Hiroshi Suga and others from the labs of Walter J. Gehring and the late Volker Schmid now present data on Pax genes found in a jellyfish species with highly developed eyes.
Primitive jellyfishes with complex eyes
The fully aquatic phylum Cnidaria, represented by polyps such as sea anemones and corals, and by medusae such as jellyfish, consists of radially symmetrical, headless animals with a mouth surrounded by tentacles that bear the so-called cnidocytes, harpoon-like "nettle cells". Cnidaria is the earliest branching animal phylum containing species with multicellular eyes, which sometimes show complex structures such as lens, iris, pigmented and photosensitive cell layers. Since no true Pax-6 gene has been found in nonbilateral cnidarians to date other master control gene(s) than Pax-6 are expected to be responsible for eye development.
In the hydrozoan jellyfish Cladonema radiatum, which possesses elaborate eye structures, Suga et al. isolated and characterized three Pax genes (CrPax-A, CrPax-B, and CrPax-E). The authors found that CrPax-A is strongly expressed in the retina, whereas CrPax-B is required for the maturation of oocytes, and CrPax-E is predominantly expressed in the manubrium, the process that bears the mouth of a hydrozoan. By targeted expression experiments, they could show that CrPax-A was able to ectopically initiate eye development in Drosophila, whereas CrPax-B and CrPax-E were not. The ability of the Cladonema Pax-A paired domain to bind to the 5’ upstream regions of two eye-specific opsin genes suggests that CrPax-A directly regulates the expression of opsin genes during eye development. Their study uncovers the diversity of the Pax genes used for development and/or maintenance of animal eyes.
Common origin and molecular opportunism
The findings of Suga et al. stand in apparent contrast to the published data of the cubozoan jellyfish Tripedalia cystophora, another class of species with complex eyes, where Pax-B rather than Pax-A seems to be responsible for eye development. Although Pax-B for Cubozoa has been previously proposed to have diverged from Pax-6 by gene duplication in the bilaterian lineage after the separation from cnidarians, the authors' study showed that this gene duplication happened much earlier in the common ancestor of cnidarians and bilaterians.
The fact that the Pax family genes are always involved in eye development all along the animal evolution supports the hypothesis of a common ancestry of cnidarian and bilaterian eyes, conclude the authors. Moreover, the unexpected variety of Pax subfamilies that are used for animal eye development suggests a flexible recruitment and co-option of the gene family in animal evolution. After the divergence of bilaterians and cnidarians on one hand, and hydrozoans and cubozoans on the other hand, the three distinct animal lineages might have selected different classes of Pax genes for the roles in eye development. Such a molecular level opportunism has often been observed in evolution. If the model is correct, genes from different Pax subfamilies may still retain to some extent the ability to perform each other’s function redundantly, which in fact turned out to be the case. Multitasking and functional flexibility could be the apparent key to keep a “gene family business” ongoing.
Source article
Suga, H., Tschopp, P., Graziussi, D. F., Stierwald, M., Schmid, V., & Gehring, W. J. 2010. Flexibly deployed Pax genes in eye development at the early evolution of animals demonstrated by studies on a hydrozoan jellyfish. PNAS published ahead of print July 26, 2010, doi:10.1073/pnas.1008389107.
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Source: Biozentrum
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