Iroquois Complex Genes Induce Co-Expression of rhodopsins in Drosophila

Mazzoni, Esteban O.; Çelik, Arzu; Wernet, Mathias F.; Vasiliauskas, Daniel; Johnston, Robert J.; Cook, Tiffany; Pichaud, Franck; Desplan, Claude

doi:10.1371/journal.pbio.0060097

Cited by 106 publications

(116 citation statements)

References 47 publications

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“…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).…”

Section: Research Articlementioning

confidence: 99%

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

Schmeling

Wakakuwa

Tegtmeier

et al. 2014

Journal of Experimental Biology

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For compass orientation many insects rely on the pattern of sky polarization, but some species also exploit the sky chromatic contrast. Desert locusts, Schistocerca gregaria, detect polarized light through a specialized dorsal rim area (DRA) in their compound eye. To better understand retinal mechanisms underlying visual navigation, we compared opsin expression, spectral and polarization sensitivities and response-stimulus intensity functions in the DRA and main retina of the locust. In addition to previously characterized opsins of long-wavelength-absorbing (Lo1) and blue-absorbing visual pigments (Lo2), we identified an opsin of an ultraviolet-absorbing visual pigment (LoUV). DRA photoreceptors exclusively expressed Lo2, had peak spectral sensitivities at 441 nm and showed high polarization sensitivity (PS 1.3-31.7). In contrast, ommatidia in the main eye co-expressed Lo1 and Lo2 in five photoreceptors, expressed Lo1 in two proximal photoreceptors, and Lo2 or LoUV in one distal photoreceptor. Correspondingly, we found broadband blueand green-peaking spectral sensitivities in the main eye and one narrowly tuned UV peaking receptor. Polarization sensitivity in the main retina was low (PS 1.3-3.8). V-log I functions in the DRA were steeper than in the main retina, supporting a role in polarization vision. Desert locusts occur as two morphs, a day-active gregarious and a night-active solitarious form. In solitarious locusts, sensitivities in the main retina were generally shifted to longer wavelengths, particularly in ventral eye regions, supporting a nocturnal lifestyle at low light levels. The data support the role of the DRA in polarization vision and suggest trichromatic colour vision in the desert locust.

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Section: Research Articlementioning

confidence: 99%

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

Schmeling

Wakakuwa

Tegtmeier

et al. 2014

Journal of Experimental Biology

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“…The UV-sensitive cone of the salamander retina co-expresses three functional rhodopsins (Makino and Dodd, 1996). Examples in invertebrates include coexpression of rhodopsins in butterflies (Kitamoto et al, 2000;Arikawa et al, 2003;Sison-Mangus et al, 2006), co-expression of Rh3 and Rh4 UV-sensitive rhodopsins in Drosophila (Mazzoni et al, 2008), and co-expression of multiple long-wavelength rhodopsins in the horseshoe crab Limulus (Katti et al, 2010).…”

Section: I17mentioning

confidence: 99%

Rhodopsin coexpression in UV photoreceptors of Aedes aegypti and Anopheles gambiae mosquitoes

Leming

Whaley

et al. 2013

Journal of Experimental Biology

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Differential rhodopsin gene expression within specialized R7 photoreceptor cells divides the retinas of Aedes aegypti and Anopheles gambiae mosquitoes into distinct domains. The two species express the rhodopsin orthologs Aaop8 and Agop8, respectively, in a large subset of these R7 photoreceptors that function as ultraviolet receptors. We show here that a divergent subfamily of mosquito rhodopsins, Aaop10 and Agop10, is coexpressed in these R7 photoreceptors. The properties of the A. aegypti Aaop8 and Aaop10 rhodopsins were analyzed by creating transgenic Drosophila expressing these rhodopsins. Electroretinogram recordings, and spectral analysis of head extracts, obtained from the Aaop8 strain confirmed that Aaop8 is an ultravioletsensitive rhodopsin. Aaop10 was poorly expressed and capable of eliciting only small and slow light responses in Drosophila photoreceptors, and electroretinogram analysis suggested that it is a long-wavelength rhodopsin with a maximal sensitivity near 500 nm. Thus, coexpression of Aaop10 rhodopsin with Aaop8 rhodopsin has the potential to modify the spectral properties of mosquito ultraviolet receptors. Retention of Op10 rhodopsin family members in the genomes of Drosophila species suggests that this rhodopsin family may play a conserved role in insect vision.

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“…irxAa and irxBa are highly homologous to the mammalian IrxA and IrxB clusters (Dildrop and Rü ther, 2004). Genetic studies revealed that the Iroquois genes are required for patterning the dorsoventral axis of the eye imaginal discs at early stages (Dominguez and de Celis, 1998;Cavodeassi et al, 1999;Yang et al, 1999), and specification of the ommatidia at the dorsal rim (Tomlinson, 2003;Wernet et al, 2003) and the photoreceptor cells (Mazzoni et al, 2008) at later stages of eye development. It has been suggested that the architecture and major class of neurons as well as the neurogenesis events in the fish eye are reminiscent of the progression of the morphogenetic furrow in the Drosophila eye.…”

Section: Introductionmentioning

confidence: 99%

A cascade of irx1a and irx2a controls shh expression during retinogenesis

Choy

Cheng

Lee

et al. 2010

Developmental Dynamics

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In animal retina, hedgehog expression drives waves of neurogenesis, but genetic programs that control its expression during retinal neurogenesis are poorly elucidated. We have previously reported that irx1a is required for propagation of the sonic hedgehog (shh) expression waves in developing zebrafish retina. Here, we found that irx2a is expressed in the developing retina and that knockdown of irx2a results in a retinal phenotype strikingly similar to that of irx1a morphants. The expression of irx2a in retina ganglion cells was shown to be irx1a-and ath5-dependent suggesting that irx1a and ath5 are transcriptional regulators of irx2a. Furthermore, irx2a expression could rescue impaired propagation of shh waves in irx1a morphants. Together, these observations suggest that Irx2 functions downstream of irx1a to control shh expression in the retina. We proposed a novel transcriptional cascade of ath5-irx1a-irx2a in the regulation of hedgehog waves during vertebrate retinal development. Developmental Dynamics 239:3204-3214,

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Iroquois Complex Genes Induce Co-Expression of rhodopsins in Drosophila

Cited by 106 publications

References 47 publications

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

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

Rhodopsin coexpression in UV photoreceptors of Aedes aegypti and Anopheles gambiae mosquitoes

A cascade of irx1a and irx2a controls shh expression during retinogenesis

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