Autocrine pheromone signalling regulates community behaviour in the fungal pathogen Fusarium oxysporum

Abstract

Autocrine self-signalling via secreted peptides and cognate receptors regulates cell development in eukaryotes and is conserved from protozoans to mammals^1,2. In contrast, secreted peptides from higher fungi have been traditionally associated with paracrine non-self-signalling during sexual reproduction³. For example, cells of the model fungus Saccharomyces cerevisiae fall into two distinct mating types (MAT), which produce either a- or α-pheromone and the cognate receptors Ste2 or Ste3, respectively⁴. Inappropriate autocrine pheromone signalling (APS) during mating is prevented by downregulation of the self-pheromone receptor^4,5 and by a-type cell-specific cleavage of α-pheromone through the protease Bar1 (refs. ^6,7,8). While APS can be artificially induced by manipulation of the pheromone secrete-and-sense circuit^7,9,10,11, its natural occurrence in ascomycete fungi has not been described. Here, we show that Fusarium oxysporum—a devastating plant pathogen that lacks a known sexual cycle¹²—co-expresses both pheromone–receptor pairs, resulting in autocrine regulation of developmental programmes other than mating. We found that unisexual populations of MAT1-1 cells (α-type idiomorphs¹³) secrete and sense both a- and α-pheromone, and that their perception requires the cognate receptors and conserved elements of the cell wall integrity mitogen-activated protein kinase cascade. We further show that F. oxysporum uses APS to regulate spore germination in a cell-density-dependent manner, whereby the α-Ste2 interaction leads to repression of conidial germination while the a-Ste3 interaction relieves repression. Our results reveal the existence of a regulatory function for peptide pheromones in the quorum-sensing-mediated control of fungal development.