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

ABSTRACT: Ustilago maydis infection in maize causes hypertrophic leaf tumors; however, the underlying mechanisms driving this excessive cell growth are unknown. In this study, we identify Hap1 (hypertrophy-associated protein 1) as an effector and virulence factor that regulates mesophyll cell hypertrophy. Using CRISPR-Cas9 mutagenesis, we demonstrate that Hap1 contributes to endoreduplication and starch accumulation in infected tissues. Transcriptomics revealed Hap1-dependent upregulation of starch biosynthesis and cell cycle genes, as well as suppression of plant defense. This links Hap1 to metabolic and cell cycle reprogramming, and immune suppression. To identify the target of Hap1 that drives metabolic reprogramming, we investigated its interaction with ZmSnRK1α in maize. We found that Hap1 interferes with the phosphorylation of SnRK1 substrates and that two Hap1-interacting effectors, Hip1 and Hip2, enhance its protein stability. We conclude that Hap1 contributes to the reprogramming of maize metabolism and cell cycle, as well as mesophyll cell hypertrophy, by modulating the SnRK1 signaling pathway to regulate starch biosynthesis and host defense responses.

ORGANISM(S): Zea mays

PROVIDER: GSE282754 | GEO | 2026/01/29

REPOSITORIES: GEO

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Ustilago maydis disrupts carbohydrate signaling networks to induce hypertrophy in maize mesophyll cells (interactome data)

Project description:Ustilago maydis is a biotrophic fungus that infects arial parts of maize, secreting effector proteins to facilitate host colonization and manipulate cellular processes, creating nutrient-rich environments for its growth and reproduction. Here, we identified three effectors (Hap1-3; hypertrophy-associated proteins 1-3) as U. maydis virulence factors involved in the development of hypertrophic mesophyll tumor cells (HTT). Immunoprecipitation followed by mass-spectrometry revealed interactions among Hap effectors within host cells, suggesting potential effector complex formation. To study Hap effectors, triple frameshift U. maydis knockout for hap1, hap2, and hap3 was generated using CRISPR-Cas9. Infection assays and mass-spectrometry identified Hap1 as a key HTT-related virulence factor that interacts with maize Snf1-related protein kinase 1 (SnRK1), a central energy homeostasis 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 SnRK1α 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 HTT formation while suppressing sugar-induced immune signaling.

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Overexpression of ZmSUS1 gene alters the content and composition of endosperm starch in maize (Zea mays L.)

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