A transcription factor and a phosphatase regulate temperature-dependent morphogenesis in a fungal plant pathogen

Naturally fluctuating temperatures provide a constant environmental stress that requires adaptation. Some fungal pathogens respond to heat stress by producing new morphotypes that maximize their overall fitness. The fungal wheat pathogen Z. tritici responds to heat stress by switching from its yeast-like blastospore form to hyphae or chlamydospores. The regulatory mechanisms underlying this switch are unknown. Here, we demonstrate that a differential heat stress response is ubiquitous in Z. tritici populations around the world. We used QTL mapping to identify a single locus associated with the temperature-dependent morphogenesis and we found two genes, the transcription factor ZtMsr1 and the protein phosphatase ZtYvh1, regulating this mechanism. We find that ZtMsr1 regulates repression of hyphal growth and induces chlamydospore formation whereas ZtYvh1 is required for hyphal growth. We next pinpointed that chlamydospore formation is a response to the intracellular osmotic stress generated by the heat stress. This intracellular stress stimulates the CWI and HOG MAPK pathways resulting in hyphal growth. If cell wall integrity is however compromised, ZtMsr1 represses the hyphal development program and might induce the chlamydospore-inducing genes as a stress-response survival strategy. Taken together, these results suggest a novel mechanism through which morphological transitions are orchestrated in Z. tritici - a mechanism possibly also present in other pleomorphic fungi. IMPORTANCETemperature is an environmental signal constantly monitored by pleomorphic fungi. Our experiments showed that yeast-to-hyphal or yeast-to-chlamydospore transitions are ubiquitous heat stress responses in Z. tritici. QTL mapping allowed us to identify a transcription factor and a protein phosphatase contributing to temperature-dependent morphogenesis. We showed that intracellular osmolarity is the pivotal signal inducing these transitions. We propose a regulatory network controlling Z. tritici morphogenesis, which may have broad implications for temperature sensing of fungal pathogens.