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

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 Zymoseptoria 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 showed that chlamydospore formation is a response to the intracellular osmotic stress generated by the heat stress. This intracellular stress stimulates the cell wall integrity (CWI) and high-osmolarity glycerol (HOG) MAPK pathways resulting in hyphal growth. If cell wall integrity is compromised, however, ZtMsr1 represses the hyphal development program and may 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 that may also be present in other pleomorphic fungi.