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MBE Advance Access published online on July 28, 2003

Molecular Biology and Evolution, doi:10.1093/molbev/msg181
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2003; all rights reserved
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Accepted May 20, 2003
© 2003 Society for Molecular Biology and Evolution

Original Articles

The Cone Visual Pigments of an Australian Marsupial, the Tammar Wallaby (Macropus eugenii): Sequence, Spectral Tuning and Evolution

Samir S. Deeb 1*, Matthew J. Wakefield 2, Takashi Tada 3, Lauren Marotte 4, Shozo Yokoyama 3, and Jenny A. Marshall Graves 4

1 Department of Medicine, University of Washington, Seattle, WA
2 Research School of Biological Sciences, The Australian National University, Canberra, Australia; Centre for Bioinformation Science, JCSMR/SMS, The Australian National University, Canberra, Australia
3 Department of Biology, Syracuse University, Syracuse, NY
4 Research School of Biological Sciences, The Australian National University, Canberra, Australia

* To whom correspondence should be addressed. E-mail: sdeeb{at}u.washington.edu.


   Abstract

Studies on marsupial color vision have been limited to very few species. There is evidence from behavioral, electroretinographic (ERG) and microspectrophotometric (MSP) measurements for the existence of both dichromatic and trichromatic color vision. No studies have yet investigated the molecular mechanisms of spectral tuning in the visual pigments of marsupials. Our study is the first to determine the mRNA sequence, infer the amino acid sequence and determine, by in vitro expression, the spectra of the cone opsins of a marsupial, the tammar wallaby (Macropus eugenii). This yielded some information on mechanisms and evolution of spectral tuning of these pigments. The tammar wallaby retina contains only short-wavelength sensitive (SWS) and middle-wavelength sensitive (MWS) pigment mRNAs. This predicts dichromatic color vision, which is consistent with conclusions from previous behavioral studies (Hemmi 1999). We found that the wallaby has a SWS1 class pigment of 346 amino acids. Sequence comparison with eutherian SWS pigments predicts that this SWS1 pigment absorbs maximally ({lambda}max) at 424 nm and, therefore is a blue rather than a UV pigment. This ({lambda}max) is close to that of the in vitro-expressed wallaby SWS pigment ({lambda}max of 420 ±2 nm) and that determined behaviorally (420 nm) (Hemmi 1999). The difference from the mouse UV pigment ({lambda}max of 359 nm) is largely accounted for by the F86Y substitution, in agreement with in vitro results comparing a variety of other SWS pigments (Cowing et al. 2002; Fasick, Applebury, and Oprian 2002). This suggests that spectral tuning employing F86Y substitution most likely arose independently in the marsupials and ungulates as a result of convergent evolution. An apparently different mechanism of spectral tuning of the SWS1 pigments, involving 5 amino acid positions (Shi, Radlwimmer, and Yokoyama 2001) evolved in primates. The wallaby MWS pigment has 363 amino acids. Species comparisons at positions critical to spectral tuning predict a {lambda}max near 530 nm, which is close to that of the in vitro expressed pigment (529 ±1 nm), but quite different from the value of 539 nm determined by microspectrophotometry (Hemmi, Maddess, and Mark 2000). Introns interrupt the coding sequences of the wallaby, mouse and human MWS pigment sequences at the same corresponding nucleotide positions. However, the length of introns varies widely among these species.

Key Words: wallaby, visual pigments, cones, sequence


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