Characterization of the maize-Ustilago maydis interaction in a warming climate

Maize is among the most commonly grown crops worldwide. Infections with Ustilago maydis, causing corn smut disease and leading to loss of biomass, yield, and silage quality, occur in all major growing regions. Rising global temperatures are predicted to reshape crop-pathogen interactions and subsequently threaten yield. However, the impact of minimal temperature changes resulting from climate change, and the molecular basis of temperature-modulated susceptibility, remain poorly understood. To investigate these, U. maydis infection trials and RNA-seq profiling across multiple maize cultivars grown under distinct temperature regimes based on the evaluation of climate data for Bavaria (Germany) were conducted. Even a minimal temperature change enhanced disease symptoms, while a brief heatwave greatly increased tumor formation and accelerated disease development. The observed phenotypic changes were accompanied by broad temperature- and cultivar-defined alterations in the host's transcriptional response. Expression-phenotype correlations, followed by in vivo testing, revealed factors contributing to variation in resistance. GIBBERELLIC ACID STIMULATED TRANSCRIPT-LIKE 4 is a broad resistance factor with implications of germplasm-specific variations in expression. The expression of γ-aminobutyric acid (GABA) transaminases, which cleave GABA, which acts as a susceptibility metabolite during U. maydis infection, is regulated in a temperature- and cultivar-dependent manner and correlated with fewer infections.