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. 2008 Jul 24;454(7203):533-7.
doi: 10.1038/nature07062. Epub 2008 Jun 25.

Switch of Rhodopsin Expression in Terminally Differentiated Drosophila Sensory Neurons

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Free PMC article

Switch of Rhodopsin Expression in Terminally Differentiated Drosophila Sensory Neurons

Simon G Sprecher et al. Nature. .
Free PMC article

Abstract

Specificity of sensory neurons requires restricted expression of one sensory receptor gene and the exclusion of all others within a given cell. In the Drosophila retina, functional identity of photoreceptors depends on light-sensitive Rhodopsins (Rhs). The much simpler larval eye (Bolwig organ) is composed of about 12 photoreceptors, eight of which are green-sensitive (Rh6) and four blue-sensitive (Rh5). The larval eye becomes the adult extraretinal 'eyelet' composed of four green-sensitive (Rh6) photoreceptors. Here we show that, during metamorphosis, all Rh6 photoreceptors die, whereas the Rh5 photoreceptors switch fate by turning off Rh5 and then turning on Rh6 expression. This switch occurs without apparent changes in the programme of transcription factors that specify larval photoreceptor subtypes. We also show that the transcription factor Senseless (Sens) mediates the very different cellular behaviours of Rh5 and Rh6 photoreceptors. Sens is restricted to Rh5 photoreceptors and must be excluded from Rh6 photoreceptors to allow them to die at metamorphosis. Finally, we show that Ecdysone receptor (EcR) functions autonomously both for the death of larval Rh6 photoreceptors and for the sensory switch of Rh5 photoreceptors to express Rh6. This fate switch of functioning, terminally differentiated neurons provides a novel, unexpected example of hard-wired sensory plasticity.

Figures

Figure 1
Figure 1. Transformation of the larval eye into the adult eyelet
a, b, The eyelet locates between the optic ganglia (anti-Elav, red; La, lamina; Me, medulla) and retina (anti-Chp, blue; rPR, retinal photoreceptors). b, The eyelet only expresses Rh6 (green). c, Larval photoreceptors express Rh6 (green) or Rh5 (blue), nuclei in red (GMR > H2B::YFP). d, Rh6 photoreceptors (green) degenerate during prepupation (arrow), Rh5 photoreceptors (rh5 > GFP, blue) remain, nuclei in red (anti-Elav). e, High magnification of eyelet photoreceptors expressing Rh6 (green) not Rh5 (blue), nuclei in red (GMR > H2B::YFP). f, Transformation of larval photoreceptors: Rh6 photoreceptors degenerate, Rh5 photoreceptors remain at prepupation stages but express Rh6 in the eyelet. gi, Rh5 photoreceptors tracked through metamorphosis using rh5 > H2B::YFP (red), anti-Rh6 (green) and anti-Rh5 (blue): g, during third-instar larva; h, mid-pupation (neither Rh5 nor Rh6 detectable); i, eyelet photoreceptors now expressing Rh6. j, By mid-pupation, Rh6 photoreceptors have degenerated whereas Rh5 photoreceptors are now empty, they later switch to express Rh6. k, No rh5 > lacZ expression can be detected in the eyelet. l, Genetic memory experiment (rh5-Gal4/UAS-Flp;Act-FRT > STOP > FRT-nlacZ): lacZ detected in eyelet (anti β-Gal, red; anti-RH6, green). m, n, Projections of Rh6 photoreceptors undergo fragmentation during prepupation (n, arrow, labelled with anti-Rh6), whereas Rh5 photoreceptor projections remain (m, Rh5 photoreceptor projections are shown by rh5-GFP; anti-Elav, red).
Figure 2
Figure 2. Larval Rh5 photoreceptors give rise to the eyelet and express Rh5 photoreceptor markers
a, Inhibition of larval Rh6 photoreceptor development (so > H2B::YFP,EGFRDN): only the Rh5 subtype is present in larvae (blue), whereas (d) the eyelet remains unaffected (anti-Rh6, green; anti-Rh5, blue; anti-YFP, red). b, In the larva, Svp (svp > H2B::YFP, red) is expressed in Rh6 (green) but not Rh5 photoreceptors (blue), whereas (e) the eyelet does not express Svp (anti-Rh6, green). c, In the larva, Sal (sal > H2B::YFP, red) is expressed in Rh5 photoreceptors (blue) but not in Rh6 photoreceptors (green) (f). Sal (red) is expressed in the eyelet (anti-Rh6, green). g, h, rh5-Gal4,UAS-hid,rpr ablates Rh5 photoreceptors (g, arrow) and eyelet (h, arrow) (anti-Rh5, blue; anti Rh6, green; anti Elav, red). i, rh6-Gal4/UAS-p35 prevents apoptosis of Rh6 photoreceptors (anti-Rh6, green; anti-YFP, red). j, k, Sens (red) is detected in the larval Rh5 subtype (rh5 > H2B::YFP, blue; anti-Chp, green) and the eyelet (rh6 > H2B::YFP; anti-YFP, blue; anti-Rh6, green). l, Misexpression of UAS-sens in Rh6 photoreceptors (rh6 > H2B::YFP > sens) prevents their apoptosis (anti-Rh6, green; anti-YFP, red; anti-Rh5, blue). The same phenotype is obtained with GMR-Gal4;UAS-sens (data not shown).
Figure 3
Figure 3. EcR expression and activity in larval photoreceptors before metamorphosis
a, b, d, e, In third-instar larvae, EcR protein (red) is detected in Rh6 photoreceptors (rh6 > H2B::YFP; green) (a) and in Rh5 photoreceptors (rh5 > H2B::YFP; green) (d); anti-Elav (blue). b, e, The same as a, d showing only EcR expression (broken circles highlight Rh6 photoreceptors in a and b, Rh5 photoreceptors in d and e). c, f, EcR activity monitored using 7×EcRE-lacZ (β-Gal, green). Anti-Chp (red) and anti-Elav (blue) marked photoreceptors. No EcR activity is detected during mid-third instar (c) but is present from late third-instar larval (f) to prepupal stages.
Figure 4
Figure 4. EcR is required autonomously for the fate switch of Rh5 photoreceptors and apoptosis of Rh6 photoreceptors
Eyelet expressing so-Gal4/UAS-H2B::YFP (AaAc), rh5-Gal4,UAS-H2B::YFP, and UAS-EcRDN (BaBc), rh5-Gal4,UAS-H2B::YFP,UAS-EcRRNAi (CaCc), rh6-Gal4,UAS-H2B::YFP,UAS-EcRDN (DaDc) or rh6-Gal4,UAS-H2B::YFP,UAS-EcRRNAi (EaEc), anti-Rh6 (green), anti-Rh5 (blue) and anti-YFP (red). Interfering with EcR in Rh5 photoreceptors prevents cells from switching to Rh6 (b, c). In Rh6 photoreceptors, it prevents apoptosis (D, E). The eyelet (F) after manipulation of Rh5 (G) or Rh6 photoreceptors (H). I, Transformation of the larval eye into the eyelet. EcR function leads to apoptosis of the Rh6 photoreceptors and the switch to Rh6 of Rh5 photoreceptors.

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