Differential regulation of adenylylcyclases in vegetative and gametic flagella of Chlamydomonas

To learn more about the mechanism of regulation of cAMP during fertilization in Chlamydomonas, we have begun to study the flagellar adenylylcyclase. Recently (Zhang, Y., Ross, E. M., and Snell, W. J. (1991) J. Biol. Chem. 266, 22954-22959) we reported that the adenylylcyclase in gametic flagella is inhibited by ATP and activated by pretreatment at 45°C or by incubation with the protein kinase inhibitor staurosporine. Here we present evidence that this novel regulatory mechanism is unique to gametes and may be required for sexual signaling between mt⁺ and mt^- gametes during fertilization. The vegetative form of the enzyme, which has a specific activity 3-5-fold less than the gametic form, was neither inhibited by ATP nor activated at 45°C. 5′-Adenylylimidodiphosphate, staurosporine, and Mn²⁺, which activated the gametic enzyme, had no effect on the vegetative adenylylcyclase. In addition the gametic enzyme was inhibited by low (0.1-1 μM) Ca²⁺ concentrations, whereas the vegetative form was unaffected by 10 μM Ca²⁺. During gametogenesis acquisition of the ability to undergo sexual signaling was coincident with the appearance of the gametic flagellar adenylylcyclase. Our results suggest that gametogenesis is accompanied by appearance of a new adenylylcyclase that may play a central role in signal transduction during fertilization in Chlamydomonas.