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The Journal of Neuroscience, June 1, 2003, 23(11):4527-4532

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Coexpression of Two Visual Pigments in a Photoreceptor Causes an Abnormally Broad Spectral Sensitivity in the Eye of the Butterfly Papilio xuthus

Kentaro Arikawa,¹ Shin Mizuno,¹ Michiyo Kinoshita,¹ and Doekele G. Stavenga²

¹ Graduate School of Integrated Science, Yokohama City University, Yokohama 236-0027, Japan, and ² Department of Neurobiophysics, University of Groningen, 9747 AG, Groningen, The Netherlands

The compound eye of the butterfly Papilio xuthus consists of three different types of ommatidia, each containing nine photoreceptor cells (R1–R9). We have found previously that the R5–R8 photoreceptors of type II ommatidia coexpress two different mRNAs, encoding opsins of green- and orange-red-absorbing visual pigments (Kitamoto et al., 1998). Do these cells contain two functionally distinct visual pigments? First, we identified the sensitivity spectrum of these photoreceptors by using combined intracellular recording and dye injection. We thus found that the R5–R8 of type II ommatidia have a characteristic sensitivity spectrum extending over an excessively broad spectral range, from the violet to the red region; the photoreceptors are therefore termed broadband photoreceptors. The spectral shape was interpreted with a computational model for type II ommatidia, containing a UV visual pigment in cells R1 and R2, two green visual pigments in cells R3 and R4, a far-UV-absorbing screening pigment (3-hydroxyretinol) in the distal part of the ommatidium, and a red-screening pigment that surrounds the rhabdom. The modeling suggests that both visual pigments in the R5–R8 photoreceptors participate in phototransduction. This work provides the first compelling evidence that multiple visual pigments participate in phototransduction in single invertebrate photoreceptors.

Key words: vision; color; optical filters; insects; rhodopsin; signal transduction

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Received Oct. 15, 2002; revised Mar. 11, 2003; accepted Mar. 13, 2003.

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