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Ca 2+ has profound effects on response kinetics ( Hardie and Raghu, 2001 Katz and Minke, 2009), but the target proteins and mechanisms are not entirely clear. These processes are attributed to the regulatory effects of Ca 2+ on many phototransduction proteins including PLC ( Toyoshima et al., 1990 Running Deer et al., 1995 Hardie, 2005). However, the mechanism underlying TRP and TRPL channel gating, downstream of PLC activation, remains unresolved (but see Chyb et al., 1999 Leung et al., 2008 Delgado and Bacigalupo, 2009 Katz and Minke, 2009 Parnas et al., 2009 Huang et al., 2010).Ĭa 2+ plays a major role in excitation, positive and negative feedback regulation ( Hardie, 1991), and adaptation ( Gu et al., 2005) of the Drosophila response to light. This apparent inability to hydrolyze GTP bound to G qα without PLC ensures that every activated G-protein eventually encounters a PLC molecule required for TRP channel activation ( Cook et al., 2000).
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Thus, although PLCβ is a functional phospholipase, the latter phenotype has led to the discovery that PLC functions as a GTPase-activating protein (GAP) as well. Mutations in the norpA gene causing reduced levels of the protein show reduced receptor potential amplitude and slow response termination ( Bloomquist et al., 1988). In Drosophila photoreceptors the norpA ( no receptor potential A) gene encodes a β-class PLC, predominately expressed in the signaling compartment (the rhabdomere). PLC is a key enzyme in fly phototransduction with transient receptor potential (TRP) channels as its targets ( Devary et al., 1987 Bloomquist et al., 1988 Selinger and Minke, 1988). The dark bumps are thought to originate from spontaneous G qα activation, as evidenced by absence of dark bumps in the G qα 1 mutant ( Hardie et al., 2002) and by the reduced spontaneous G-protein activation when G qβ is found in excess over G qα ( Elia et al., 2005). Reliable single-photon detection requires accurate differentiation between quantum bumps and dark noise, which in Drosophila, mainly arises from unitary events that are similar in shape to quantum bumps but smaller in amplitude (dark bumps Hardie et al., 2002 Elia et al., 2005). We thus demonstrate how a G-protein-mediated transduction system, with PLC as its target, selectively suppresses its intrinsic noise while preserving reliable signaling.įly photoreceptors use G-protein-mediated phospholipase C (PLC) signaling to achieve ultimate sensitivity to single photons, as manifested in single-photon responses (quantum bumps Yeandle and Spiegler, 1973 Wu and Pak, 1975). This minimal PLC activity level is reliably obtained by photon-induced synchronized activation of several neighboring G qα molecules activating several PLC molecules, but not by random activation of single G qα molecules. The required minimal level of PLC activity selectively suppressed random production of single G qα-activated dark bumps despite a high rate of spontaneous G qα activation. Manipulations of PLC activity using PLC mutant flies and Ca 2+ modulations revealed that a critical level of PLC activity is required to induce bump production. In this study we show that reduced PLC catalytic activity selectively suppressed production of dark bumps but not light-induced bumps. Therefore, it is unclear how phototransduction suppresses dark bump production arising from spontaneous G qα activation, while still maintaining high-fidelity representation of single photons. Nevertheless, this high rate is not manifested in a substantially high rate of dark bumps. We found that in wild-type flies the in vivo rate of spontaneous G qα activation is very high. A high rate of spontaneous G qα activation and dark bump production potentially hampers single-photon detection. In photoreceptor cells, dark activation of G qα molecules occurs spontaneously and produces unitary dark events (dark bumps). This is manifested in the single-photon responses (quantum bumps). Drosophila photoreceptor cells use the ubiquitous G-protein-mediated phospholipase C (PLC) cascade to achieve ultimate single-photon sensitivity.