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bioRxiv · 10.1101/2024.11.22.624849

Ustilago maydis disrupts carbohydrate signaling networks to induce hypertrophy in host cells

Lee, Y. J.·Stolze, S. C.·Saraidis, G.·Ebert, M. K.·Nakagami, H.·Doehlemann, G.
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Abstract

Ustilago maydis is a biotrophic fungus infecting maize, secreting effector proteins to manipulate host cellular processes and create nutrient-rich environments for its growth. Three effectors, Hap1-3 (hypertrophy-associated proteins), were identified as virulence factors promoting hypertrophic mesophyll tumor cells (HTT). Immunoprecipitation and mass spectrometry revealed interactions among Hap effectors, suggesting potential effector complex formation. CRISPR-Cas9 triple knockout of hap1-3 demonstrated Hap1s role in HTT formation. Infection assays identified Hap1 as a key virulence factor interacting with maize Snf1-related kinase 1 (SnRK1), a central energy regulator. RNA-seq analysis showed that Hap1 promotes cell cycle and starch biosynthesis genes, while CR-hap1 induced defense-related WRKY transcription factors. Phosphoproteomics revealed increased phosphorylation of SnRK1 and metabolic enzymes during SG200 infection. Our findings support a model where U. maydis induces hypertrophy through Hap1, targeting the SnRK1 subunit to prevent SnRK1 inhibition by high trehalose-6-phosphate (T6P), disrupting the antagonistic relationship between T6P and SnRK1. This reprograms host transcription to enhance starch metabolism and induce endoreduplication, leading to hypertrophy induction, while suppressing sugar-induced immune signaling.

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Lee, Y. J., Stolze, S. C., Saraidis, G., Ebert, M. K., Nakagami, H., Doehlemann, G.. 2024-11-25. Ustilago maydis disrupts carbohydrate signaling networks to induce hypertrophy in host cells. https://doi.org/10.1101/2024.11.22.624849

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