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First published online July 2, 2004
Journal of Experimental Biology 207, i-a (2004)
Copyright © 2004 The Company of Biologists Limited
doi: 10.1242/jeb.01147
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Inside JEB |
SEEING RED
kathryn{at}biologists.com
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After the drabbest winter, it's always a relief to see the first bright blooms burst into flower. However, our bright world seen through insect eyes is probably a very different place. Some insects are sensitive to wavelengths well into the ultra-violet, while lacking photoreceptors sensitive to longer red wavelengths, yet others seem to have the best of both worlds, with photoreceptors covering the full spectrum, all the way from UV to red. Each photoreceptor is thought to be packed with photosensitive rhodopsins tuned to UV, blue, green or red wavelengths, and all four photoreceptors cluster together forming ommatidia, the individual visual units that comprise an insect's compound eye. But do all ommatidia contain the same combinations of photoreceptors? Kentaro Arikawa was curious to find out, and turned his attention to one of the world's less exotic butterflies, Pieris rapae crucivora (p. 2803).
Arikawa and his team painstakingly analysed the insect's ommatidia. Using a combination of light and electron microscopy, Arikawa could clearly see that the butterfly's eye was made up from three distinct classes of ommatidium, not one as he had originally thought, each with a unique distribution of photoreceptors. But more surprisingly, when the team began measuring each photoreceptor's spectral sensitivity, he realised that Pieris seemed to have at least six types of photoreceptor, not four; one tuned to short (UV) wavelengths, two to blue wavelengths, and three tuned to longer wavelengths at 560, 620 and 640 nm.
Focusing on the butterflies' long wave photoreceptors, Arikawa wondered whether the butterfly produced individual long wave tuned rhodopsins. Working with Motohiro Wakakuwa and Masumi Kurasawa, he began searching for opsin genes, but instead of finding three long wave opsin genes, they only found one. And when the team tried staining the insect's retina to identify the location of the long wave opsin in ommatidia, all three long wave photoreceptors lit up; they all carried the same rhodopsin. So how could three photoreceptors respond to light of such different wavelengths while containing the same photosensitive pigment?
Having carefully analysed the distribution of photoreceptors in the insect's eye, Arikawa knew that many of Pieris's photoreceptors also contained pale and dark red filter pigments. Could these filters shift the rhodopsin's spectral sensitivity? Biophysicist Doekele Stavenga flew to Yokohama from Groningen to join Arikawa's team. Calculating the rhodopsin's spectral sensitivity, Stavenga found that the protein was tuned to green wavelengths at 563 nm. Next he tested the filter hypothesis by combining his computational expertise with Arikawa's anatomical know-how and found that optical filter clusters surrounding the photoreceptors' rhabdom structure shifted the spectral sensitivity of the adjacent receptors, depending on the filter's shade. Pieris had gained three long wave photoreceptors for the price of one, by filtering the incident light.
Arikawa adds that although the chemical natures of Pieris's rhodopsin shifting pigments aren't known, the insects seem to have found a very effective way to make them see red.
References
Wakakuwa, M., Stavenga, D. G., Kurasawa, M. and Arikawa, K.
(2004). A unique visual pigment expressed in green, red and
deep-red receptors in the eye of the small white butterfly, Pieris rapae
crucivora. J. Exp. Biol.
207,2803
-2810.
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