Molecular mechanisms of chemotropism and cell fusion in unicellular fungi

Abstract

In all eukaryotic phyla, cell fusion is important for many aspects of life, from sexual reproduction to tissue formation. Fungal cells fuse during mating to form the zygote, and during vegetative growth to connect mycelia. Prior to fusion, cells first detect gradients of pheromonal chemoattractants that are released by their partner and polarize growth in their direction. Upon pairing, cells digest their cell wall at the site of contact and merge their plasma membrane. In this Review, I discuss recent work on the chemotropic response of the yeast models Saccharomyces cerevisiae and Schizosaccharomyces pombe, which has led to a novel model of gradient sensing: the cell builds a motile cortical polarized patch, which acts as site of communication where pheromones are released and sensed. Initial patch dynamics serve to correct its position and align it with the gradient from the partner cell. Furthermore, I highlight the transition from cell wall expansion during growth to cell wall digestion, which is imposed by physical and signaling changes owing to hyperpolarization that is induced by cell proximity. To conclude, I discuss mechanisms of membrane fusion, whose characterization remains a major challenge for the future.

Exploratory polarization facilitates mating partner selection inSaccharomyces cerevisiae

“…The exploratory polarization strategy supported by our findings, like the related speed dating strategy proposed for S. pombe (Bendezu and Martin, 2013;Martin, 2019;Merlini et al, 2016), provides an elegant solution to the problem of choosing a partner from among two or more similarly-distant candidates. Classical spatial sensing paradigms that integrate spatial information to extract a single "upgradient" direction are poorly suited to this task, as the presence of two or more nearby chemoattractant sources may create a weak or even non-existent net gradient.…”

“…Pheromone secretion and sensing factors were enriched at these transient sites, and computational models confirmed that local secretion and sensing/signaling would promote effective partner location in realistic geometries and timescales (Merlini et al, 2016). Thus, an exploratory polarization strategy might be conserved between evolutionarily distant fungi (Martin, 2019).…”

“…Spatial information about the pheromone landscape could be extracted by "global" or "local" sensing strategies (Hegemann and Peter, 2017;Kelley et al, 2015;Martin, 2019). In global sensing, cells compare the concentration of ligand-bound receptors around the cell surface to infer the direction of the pheromone source.…”

Type V Myosin focuses the polarisome and shapes the tip of yeast cells

“…The advantage of studying mating is that the behavior of wild type cells and cells with mutated polarisomes can be compared within the same mating experiment. Here, neighboring a-and α-cells grow mating projections towards each other until both cells get into a physical contact and fuse to form a diploid cell ( Figure 6A) (Martin, 2019). The polarisomes form at the prospective mating projections of both cells and stay at their tips during growth and cell fusion ( Figure 6A) (Valtz and Herskowitz, 1996;Sheu et al, 2000;Gehrung and Snyder, 1990).…”

Quorum sensing with pheromones

“…F rom studies on unicellular fungi (yeasts), we understand the mechanism of pheromone signalling in great detail 1,2 . For instance, in Saccharomyces cerevisiae, α-type cells secrete α-pheromone, which is detected by the specific G-protein coupled receptor (GPCR) Ste2 in a-type cells.…”