Coexpression of Spectrally Distinct Rhodopsins in Aedes aegypti R7 Photoreceptors

Abstract

The retina of the mosquito Aedes aegypti can be divided into four regions based on the non-overlapping expression of a UV sensitive Aaop8 rhodopsin and a long wavelength sensitive Aaop2 type rhodopsin in the R7 photoreceptors. We show here that another rhodopsin, Aaop9, is expressed in all R7 photoreceptors and a subset of R8 photoreceptors. In the dorsal region, Aaop9 is expressed in both the cell body and rhabdomere of R7 and R8 cells. In other retinal regions Aaop9 is expressed only in R7 cells, being localized to the R7 rhabdomere in the central and ventral regions and in both the cell body and rhabdomere within the ventral stripe. Within the dorsal-central transition area ommatidia do not show a strict pairing of R7–R8 cell types. Thus, Aaop9 is coexpressed in the two classes of R7 photoreceptors previously distinguished by the non-overlapping expression of Aaop8 and Aaop2 rhodopsins. Electroretinogram analysis of transgenic Drosophila shows that Aaop9 is a short wavelength rhodopsin with an optimal response to 400–450 nm light. The coexpressed Aaop2 rhodopsin has dual wavelength sensitivity of 500–550 nm and near 350 nm in the UV region. As predicted by the spectral properties of each rhodopsin, Drosophila photoreceptors expressing both Aaop9 and Aaop2 rhodopsins exhibit a uniform sensitivity across the broad 350–550 nm light range. We propose that rhodopsin coexpression is an adaptation within the R7 cells to improve visual function in the low-light environments in which Ae. aegypti is active.

Opsin expression, physiological characterization and identification of photoreceptor cells in the dorsal rim area and main retina of the desert locust,Schistocerca gregaria

“…Sison-Mangus et al, 2006;Awata et al, 2010), Diptera (e.g. Hu et al, 2011) and the two-spotted cricket (Henze et al, 2012), a dorsal-ventral gradient or regionalization was found with higher expression of longwavelength opsins in ventral eye regions.…”

“…Whereas in most cases two opsins of similar absorption spectra are co-expressed, combinations of UV and blue opsins have been reported in the mosquito Aedes and the butterfly Parnassius (Awata et al, 2010;Hu et al, 2011). The co-expression of blue and green opsins in five out of eight photoreceptors per ommatidium (which results in broad spectral sensitivity curves) may be an adaptation to low light conditions.…”

“…A trichromatic set of UV, blue and green receptors is the most common state in insects (Briscoe and Chittka, 2001), whereas receptors containing more than one opsin have been reported only recently (Kitamoto et al, 1998;Arikawa et al, 2003;Mazzoni et al, 2008;Awata et al, 2010;Hu et al, 2011;Ogawa et al, 2012). Whereas in most cases two opsins of similar absorption spectra are co-expressed, combinations of UV and blue opsins have been reported in the mosquito Aedes and the butterfly Parnassius (Awata et al, 2010;Hu et al, 2011).…”

Expression and light-triggered movement of rhodopsins in the larval visual system of mosquitoes

“…However, the Aaop7 transgenic fly retains high sensitivity to shorter wavelengths (400 and 350 nm) and does not exhibit the second peak response in the UV observed for Drosophila Rh1 (Fig. 4C,D) and Aaop2, the only other long-wavelength Aedes opsin that has been analyzed in this way (Hu et al, 2011).…”

“…Three of these groups are labeled as long-wavelength (>500 nm), short-wavelength (400-500 nm), and UV-sensitive rhodopsin (<400 nm), and two of these groups contain uncharacterized family members. We previously characterized the patterns of rhodopsin expression in the adult Aedes compound eye (Hu et al, 2009(Hu et al, , 2011(Hu et al, , 2012(Hu et al, , 2014. These studies revealed features of the visual system in Aedes that were not predicted from study of other invertebrate models.…”