A defect in the map3 gene of the fission yeast Schizosaccharomyces pombe causes h+ mating-type-specific sterility. This gene was cloned by complementation. Nucleotide sequence analysis showed that it has a coding capacity of 365 amino acids. The deduced map3 gene product is a putative seven-transmembrane protein and has 20.0% amino acid identity with the a-factor receptor of Saccharomyces cerevisiae, encoded by STE3. It is also homologous with the Ustilago maydis mating pheromone receptors. The map3 gene is expressed in h+ cells but not in h- cells, and the transcripts are induced in response to nitrogen starvation. h+ cells defective in map3 do not respond to purified M-factor. When map3 is expressed ectopically in h- cells, they apparently acquire the ability to respond to the M-factor produced by themselves. The gpa1 gene, which encodes the alpha-subunit of a G-protein presumed to couple with the mating pheromone receptors, is essential for this function of map3. These observations strongly suggest that map3 encodes the M-factor receptor. Furthermore, this study provides strong support for the notion that pheromone signaling is essential for initiation of meiosis in S. pombe and that either M-factor signaling or P-factor signaling alone is sufficient.