Genetic Dissection Reveals Two Separate Retinal Substrates for Polarization Vision in Drosophila

Wernet, Mathias F.; Velez, Mariel M.; Clark, Damon A.; Baumann-Klausener, Franziska; Brown, Julian; Klovstad, Martha; Labhart, Thomas; Clandinin, Thomas R.

doi:10.1016/j.cub.2011.11.028

Cited by 109 publications

(158 citation statements)

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“…5E). Polarisation vision outside the DRA has been also demonstrated in the apposition eyes of the butterfly Papilio (Kelber et al, 2001;Kinoshita et al, 2011), backswimmer bugs, dragonflies and locusts to detect water (Schwind, 1983(Schwind, , 1985Wildermuth, 1998;Shashar et al, 2005), in horseflies to detect mammalian fur (Horvath et al, 2008), and in fruit flies (Wernet et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

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Extreme polarization sensitivity in the retina of the corn borer moth Ostrinia

Belušič

Šporar

Meglič

2017

Journal of Experimental Biology

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The visual system of the European corn borer (Ostrinia nubilalis) was analysed with microscopy and electrophysiological methods (electroretinograms and single-cell recordings). Ostrinia nubilalis has a pair of mainly ultraviolet-sensitive ocelli and a pair of compound eyes, maximally sensitive to green light. The ommatidia contain a tiered, fused rhabdom, consisting of the rhabdomeres of 9-12 photoreceptor cells with sensitivity peak wavelengths at 356, 413, 480 and 530 nm. The photoreceptors in a large dorsal rim area have straight rhabdomeres and high polarisation sensitivity (PS 1,2 =3.4, 14). Elsewhere, in the main retina, the majority of photoreceptors have non-aligned microvilli and negligible PS, but each ommatidium contains one or two blue-sensitive distal photoreceptors with straight microvilli parallel to the dorsoventral axis, yielding extremely high PS (PS 1,2,3 =56, 63, 316). Rhabdoms containing distal cells with potentially high PS have evolved at least twice: in moths (Crambidae, Noctuidae, Saturniidae), as well as in dung beetles (Scarabaeidae). The distal photoreceptors with high PS, sensitive to vertically polarised light, represent a monopolatic system, which is unsuitable for the proper analysis of electric field vector (e-vector) orientation. However, the distal photoreceptors might be used in conjunction with polarisationinsensitive photoreceptors to detect objects that reflect polarised light with stereotyped orientation.

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Section: Discussionmentioning

confidence: 99%

“…The probability of light absorption by the microvilli is highest when their long axis coincides with the direction of the electric field vector (e-vector) of incident light, and hence the PS of a photoreceptor can be inferred from the geometry of its rhabdomere (Meinecke and Langer, 1982;Wernet et al, 2012). In the main retina (i.e.…”

Section: Introductionmentioning

confidence: 99%

Extreme polarization sensitivity in the retina of the corn borer moth Ostrinia

Belušič

Šporar

Meglič

2017

Journal of Experimental Biology

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“…Hence, important similarities exist between the genes and pathways responsible for patterning of retinal mosaics in both flies and vertebrates. Understanding the transcriptional networks responsible for specification of individual retinal cell fates is therefore of general interest.The DRA is both necessary and sufficient for mediating orientation responses to polarized light perceived with the dorsal eye (Wernet et al, 2012). Here we have shown how factors expressed specifically in DRA R7 and R8 alter the transcriptional network of Drosophila ommatidia, resulting in a unique pattern specific to the DRA.…”

mentioning

confidence: 87%

“…A fourth ommatidial subtype is always found in the DRA, a narrow band along the dorsal head cuticle (Wada, 1974). The diameter of their inner photoreceptor rhabdomeres (light-gathering organelles) is enlarged, their rhabdomeric microvilli are untwisted, and their orientation in R7 is orthogonal to that of R8 microvilli (Wernet et al, 2012). As a result, DRA inner photoreceptors manifest high polarization sensitivity (Hardie, 1985).…”

Section: Introductionmentioning

confidence: 96%

Homothorax and Extradenticle alter the transcription factor network in Drosophila ommatidia at the dorsal rim of the retina

Wernet

Desplan

2014

Development

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A narrow band of ommatidia in the dorsal periphery of the Drosophila retina called the dorsal rim area (DRA) act as detectors for polarized light. The transcription factor Homothorax (Hth) is expressed in DRA inner photoreceptors R7 and R8 and is both necessary and sufficient to induce the DRA fate, including specialized morphology and unique Rhodopsin expression. Hth expression is the result of Wingless (Wg) pathway activity at the eye margins and restriction to the dorsal eye by the selector genes of the Iroquois complex (Iro-C). However, how the DRA is limited to exactly one or two ommatidial rows is not known. Although several factors regulating the Drosophila retinal mosaic are expressed in DRA ommatidia, the role of Hth in this transcriptional network is uncharacterized. Here we show that Hth functions together with its co-factor Extradenticle (Exd) to repress the R8-specific factor Senseless (Sens) in DRA R8 cells, allowing expression of an ultraviolet-sensitive R7 Rhodopsin (Rh3). Furthermore, Hth/Exd act in concert with the transcriptional activators Orthodenticle (Otd) and Spalt (Sal), to activate expression of Rh3 in the DRA. The resulting monochromatic coupling of Rh3 between R7 and R8 in DRA ommatidia is important for comparing celestial evector orientation rather than wavelengths. Finally, we show that Hth expression expands to many ommatidial rows in regulatory mutants of optomotorblind (omb), a transcription factor transducing Wg signaling at the dorsal and ventral eye poles. Therefore, locally restricted recruitment of the DRA-specific factor Hth alters the transcriptional network that regulates Rhodopsin expression across ommatidia. KEY WORDS: Drosophila, Retina, Patterning INTRODUCTIONThe ability of both vertebrates and invertebrates to detect the evector orientation of polarized light has been studied in great detail (for reviews, see Nilsson and Warrant, 1999;Wehner, 2001). The celestial pattern of polarized skylight provides an important orientation cue for navigating insects, such as honeybees, desert ants or monarch butterflies (reviewed by Rossel, 1993;Wehner, 2003). Ommatidia in the dorsal rim area (DRA) of the compound eye display important morphological specializations (Labhart and Meyer, 1999), making them potent polarization detectors (Hardie, 1985;Labhart et al., 1984;Stalleicken et al., 2006). The combination of behavioral experiments with molecular genetic tools in Drosophila confirmed that the DRA is both necessary and sufficient for polarization vision (Wehner and Strasser, 1985 et al., 2012). The retinal mosaic of Drosophila represents an excellent model for cell-fate specification in sensory epithelia (Johnston et al., 2011). However, although important progress has been made towards understanding the specification of DRA ommatidia (Tomlinson, 2003;Wernet et al., 2003), the network of transcription factors involved remains unclear.The Drosophila compound eye consists of ~800 unit eyes (ommatidia), each containing eight photoreceptor neurons (R1-8), pigment, cone, an...

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“…At the dorsal margin of the eye, the so-called dorsal rim area (DRA) ommatidia contain R7 and R8 PRs with enlarged rhabdomeres that both express Rh3 and mediate polarization vision Wernet et al, 2012). Furthermore, in the dorsal third of the eye y ommatidia are modified (located above the dotted line in Fig.…”

Section: Introductionmentioning

confidence: 99%

Establishing and maintaining gene expression patterns: insights from sensory receptor patterning

2013

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In visual and olfactory sensory systems with high discriminatory power, each sensory neuron typically expresses one, or very few, sensory receptor genes, excluding all others. Recent studies have provided insights into the mechanisms that generate and maintain sensory receptor expression patterns. Here, we review how this is achieved in the fly retina and compare it with the mechanisms controlling sensory receptor expression patterns in the mouse retina and in the mouse and fly olfactory systems.

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Genetic Dissection Reveals Two Separate Retinal Substrates for Polarization Vision in Drosophila

Cited by 109 publications

References 40 publications

Extreme polarization sensitivity in the retina of the corn borer moth Ostrinia

Extreme polarization sensitivity in the retina of the corn borer moth Ostrinia

Homothorax and Extradenticle alter the transcription factor network in Drosophila ommatidia at the dorsal rim of the retina

Establishing and maintaining gene expression patterns: insights from sensory receptor patterning

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