Visual Neuroscience

Research Article

Cone visual pigments of monotremes: Filling the phylogenetic gap

MATTHEW J. WAKEFIELDa1, MARK ANDERSONa2, ELLEN CHANGa2, KE-JUN WEIa3, RAJINDER KAULa4, JENNIFER A. MARSHALL GRAVESa3, FRANK GRÜTZNERa5 and SAMIR S. DEEBa2 c1

a1 ARC, Centre for Kangaroo Genomics, Bioinformatics, The Walter and Eliza Hall Institute, Parkville, Australia

a2 Departments of Medicine and Genome Sciences, University of Washington, Seattle, Washington

a3 ARC, Centre for Kangaroo Genomics, Research School of Biological Science, The Australian National University, Canberra, Australia

a4 Genome Centre, University of Washington, Seattle, Washington

a5 School of Molecular and Biomedical Science, The University of Adelaide, Adelaide, Australia

Abstract

We have determined the sequence and genomic organization of the genes encoding the cone visual pigment of the platypus (Ornithorhynchus anatinus) and the echidna (Tachyglossus aculeatus), and inferred their spectral properties and evolutionary pathways. We prepared platypus and echidna retinal RNA and used primers of the middle-wave-sensitive (MWS), long-wave-sensitive (LWS), and short-wave sensitive (SWS1) pigments corresponding to coding sequences that are highly conserved among mammals; to PCR amplify the corresponding pigment sequences. Amplification from the retinal RNA revealed the expression of LWS pigment mRNA that is homologous in sequence and spectral properties to the primate LWS visual pigments. However, we were unable to amplify the mammalian SWS1 pigment from these two species, indicating this gene was lost prior to the echidna-platypus divergence (xs223C21 MYA). Subsequently, when the platypus genome sequence became available, we found an LWS pigment gene in a conserved genomic arrangement that resembles the primate pigment, but, surprisingly we found an adjacent (xs223C20 kb) SWS2 pigment gene within this conserved genomic arrangement. We obtained the same result after sequencing the echidna genes. The encoded SWS2 pigment is predicted to have a wavelength of maximal absorption of about 440 nm, and is paralogous to SWS pigments typically found in reptiles, birds, and fish but not in mammals. This study suggests the locus control region (LCR) has played an important role in the conservation of photo receptor gene arrays and the control of their spatial and temporal expression in the retina in all mammals. In conclusion, a duplication event of an ancestral cone visual pigment gene, followed by sequence divergence and selection gave rise to the LWS and SWS2 visual pigments. So far, the echidna and platypus are the only mammals that share the gene structure of the LWS-SWS2 pigment gene complex with reptiles, birds and fishes.

(Received September 30 2007)

(Accepted January 20 2008)

Correspondence:

c1 Address correspondence and reprint requests to: Samir S. Deeb, Departments of Medicine and Genome Sciences, University of Washington, Seattle, WA 98195. E-mail: sdeeb@u.washington.edu