How Yeast Cells Find Their Mates

Abstract

Extracellular chemical gradients provide signals that guide a broad spectrum of different cellular processes. By accurately sensing and responding to chemical gradients, immune cells can chase down invading pathogens, sperm cells can locate a distant egg, and growing axons can form connections in the developing nervous system. Haploid cells of the budding yeast Saccharomyces cerevisiae grow up gradients of pheromone in order to locate and fuse with nearby mating partners. Gradient sensing should be challenging for yeast, because they must detect a minute difference in concentration across their small cell bodies. Nevertheless, yeast cells can orient with remarkable accuracy in shallow pheromone gradients. Several mechanisms have been proposed to explain how yeast cells locate their partners, but it remains unclear whether, and to what degree each of the proposed mechanisms contributes. We imaged fluorescent polarity probes in real time during mating events and found that cells located their partners in a multi-step process. First, cells placed a weak cluster of polarity proteins in approximately the correct location, despite a previously unappreciated challenge posed by asymmetrically distributed pheromone receptors. Cells were able to overcome receptor asymmetry by sensing the ratio, rather than the number, of active pheromone receptors. Second, the polarity cluster proceeded to move erratically around the cortex during an “indecisive phase.” We found evidence that cells switched to a local sensing mechanism during the indecisive phase, wherein cells used the mobile polarity cluster like a nose to search for areas where the local pheromone concentration was high. Third, the polarity cluster stabilized adjacent to a partner cell’s cluster and remained stationary until the partners met in the middle and fused.