1. The effect of Mg2+ on the light-sensitive conductance in Drosophila photoreceptors was examined with the use of whole cell voltage-clamp recordings from dissociated ommatidia. In wild type (WT) photoreceptors, at resting potential (-70 mV), Mg-0(2+) reduces response amplitude by up to similar to 4-fold in the presence of normal (1.5 mM) Ca-0(2+) and by up to 20-fold in the absence of Ca-0(2+). The Mg2+ concentration required for 50% maximum block (K-1/2) was similar to 1 mM with 1.5 mM Ca-0(2+) and similar to 280 mu M in Ca2+-free Ringer. 2. The Mg2+ block was largely relieved in photoreceptors of the transient receptor potential mutant (tip): the maximum block being only approximately twofold with a K-1/2 of similar to 4 mM in both Ca2+-free and 1.5 mM Ca-0(2+). 3. The Mg2+ block in WT, but not in trp, was strongly voltage dependent, being relieved by both hyperpolarization and depolarization. The Mg2+ block in WT also resulted in slower response kinetics because of the associated decrease in Ca2+ influx. 4. Noise analysis indicates that, with normal Ca-0(2+), the Mg2+ block in WT is associated with a similar to 10-fold reduction in effective single-channel conductance at resting potential. 5. The results support the hypothesis that the trp gene encodes a subunit of a light-sensitive channel, which is required for sensitivity to block by Mg2+. The concentration and voltage dependence of the Mg2+ block suggest it plays an important physiological role in determining the gain, kinetics, and signal-to-noise of transduction.