Flexibly deployed Pax genes in eye development at the early evolution of animals demonstrated by studies on a hydrozoan jellyfish
Hiroshi Sugaa,1, Patrick Tschoppa,2, Daria F. Graziussia,3, Michael Stierwaldb,4, Volker Schmidb,5, and Walter J. Gehringa,6
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Author Affiliations
aDepartment of Cell Biology, Biozentrum, and
bInstitute of Zoology, Pharmazentrum, University of Basel, CH-4056 Basel, Switzerland
↵ 1Present address: Parc Cientifíc de Barcelona, Universitat de Barcelona, 08028 Barcelona, Spain.
↵ 2Present address: Department of Zoology and Animal Biology, Sciences III, University of Geneva, CH-1211 Geneva, Switzerland.
↵ 3Present address: Institut für Entwiklungsbiologie, Universität zu Köln, 50923 Köln, Germany.
↵ 4Present address: Patent Department, Novartis Pharma AG, 4056 Basel, Switzerland.
↵ 5Deceased April 1, 2008.
Contributed by Walter J. Gehring, June 14, 2010 (sent for review April 8, 2010)
Abstract
Pax transcription factors are involved in a variety of developmental processes in bilaterians, including eye development, a role typically assigned to Pax-6. Although no true Pax-6 gene has been found in nonbilateral animals, some jellyfish have eyes with complex structures. In the cubozoan jellyfish Tripedalia,Pax-B, an ortholog of vertebrate Pax-2/5/8, had been proposed as a regulator of eye development. Here we have isolated three Pax genes (Pax-A, Pax-B, and Pax-E) from Cladonema radiatum, a hydrozoan jellyfish with elaborate eyes. Cladonema Pax-A is strongly expressed in the retina, whereas Pax-B and Pax-Eare highly expressed in the manubrium, the feeding and reproductive organ. Misexpression of Cladonema Pax-A induces ectopic eyes in Drosophila imaginal discs, whereas Pax-B and Pax-E do not. Furthermore, Cladonema Pax-A paired domain protein directly binds to the 5′ upstream region of eye-specificCladonema opsin genes, whereas Pax-B does not. Our data suggest that Pax-A, but not Pax-B or Pax-E, is involved in eye development and/or maintenance inCladonema. Phylogenetic analysis indicates that Pax-6, Pax-B, and Pax-A belong to different Pax subfamilies, which diverged at the latest before the Cnidaria–Bilateria separation. We argue that our data, showing the involvement of Paxgenes in hydrozoan eye development as in bilaterians, supports the monophyletic evolutionary origin of all animal eyes. We then propose that during the early evolution of animals, distinct classes of Pax genes, which may have played redundant roles at that time, were flexibly deployed for eye development in different animal lineages.
biodiversity Cladonema radiatum Cnidaria evo-devo gene duplication
Footnotes
6To whom correspondence should be addressed. E-mail:walter.gehring@unibas.ch.
Author contributions: H.S., P.T., D.F.G., V.S., and W.J.G. designed research; H.S., P.T., D.F.G., and M.S. performed research; H.S., P.T., D.F.G., M.S., V.S., and W.J.G. analyzed data; and H.S. wrote the paper.
The authors declare no conflict of interest.
Data deposition:
Sequence data from this report have been deposited in the GenBank/European Molecular Biology Laboratory/DNA Data Base in Japan database under accession nos. AB379656–AB379659, AB332437, andAB439133.
Sequence data from this report have been deposited in the GenBank/European Molecular Biology Laboratory/DNA Data Base in Japan database under accession nos. AB379656–AB379659, AB332437, andAB439133.
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