Adaptive mechanisms for communication in fungal biotrophy

• Applicant: Professor Dr. Kai Heimel
• Subject Area: Organismic Interactions, Chemical Ecology and Microbiomes of Plant Systems ; Plant Genetics and Genomics
• Term: since 2021
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 458329234

Biotrophic fungi rely on an optimized intracellular infrastructure for efficient communication with their host plants by virtue of secreted proteinaceous molecules, termed effectors. During their life cycle, hundreds of effectors are deployed into the host plant to suppress the plant defense and establish a well-balanced and fine-tuned fungal/plant interaction. In the biotrophic plant pathogen Ustilago maydis the unfolded proteins response (UPR), a conserved counter response to endoplasmic reticulum stress, is specifically activated during biotrophic growth and provides the intracellular capacities required for the folding, processing and secretion of effectors. UPR activity is crucial for effector secretion but also mediates plant defense suppression via the signal peptide peptidase (SPP) Spp1. Spp1 operates independently of effector secretion, suggesting a novel layer of fungal-plant communication that is dependent on the conserved catalytic activity of Spp1 but not related to known physiological roles of SPPs. In the first project of this proposal a combination of transcriptomic, metabolomic and novel genetic approaches enabling the stage-specific analysis protein functions and interactomes will be used. We will explore the principles, molecular mechanisms and conservation of Spp1-mediated plant defense suppression. Our research will provide a comprehensive picture of Spp1-dependent alterations on the plant and fungal side, identify and characterize potential substrates and address the conservation of the virulence-specific Spp1 function in closely and more distantly related biotrophic fungal pathogens. In the second project we will investigate how UPR-dependent regulation of MAPK signaling via the dual-specificity phosphatase Rok1 is used to prevent hypervirulence and thus to maintain fungal biotrophy. Rok1 activity is regulated by the UPR and inversely correlated with the virulence potential of U. maydis. Using a conditional gene expression approach, we will address in a time-resolved manner, the biotrophy-specific function of the Rok1-targeted MAPK Kpp6 and the relevance of the Rok1-Kpp6 interplay in controlling the virulence potential of U. maydis. Both projects address the adaptation of conserved pathway to the specific requirements of biotrophic plant pathogens and will provide novel insights into the principles of interspecies communication during fungal biotrophy.

• DFG Programme: Research Grants