Auxin dysregulation: a key early event in sugarcane susceptibility to Sporisorium scitamineum.

Sugarcane smut, caused by Sporisorium scitamineum, severely limits global sugarcane yield. Although auxin manipulation is a recognized virulence mechanism in plant-pathogen interactions, biological basis and mechanisms in orchestrating host colonization within the sugarcane-smut pathosystem remain elusive. This knowledge gap constrains a mechanistic understanding of auxin-mediated pathogenesis, thereby limiting opportunities to design auxin-based control strategies. Through integrated approaches combining exogenous hormone treatment, physiological profiling, and spatiotemporal gene expression analysis in susceptible and resistant genotypes, we aim to reveal how IAA coordinates an early host-pathogen dialogue. Our findings showed that IAA promoted infection in a dose-dependent manner: it reprogrammed host physiology at low concentrations in planta while inhibiting fungal growth at higher levels in vitro. IAA-mediated susceptibility involved disrupted redox homeostasis through suppressed activities of SOD and CAT, altered flavonoid metabolism, and upregulation of fungal effector genes such as Tin2 and Nkd1. Expression analysis further revealed temporally and genotype-dependent regulation of IAA-biosynthetic genes, with strong late-stage induction of SsIad13 and SsIad16 exclusively in susceptible plants. The resistant genotype demonstrated a superior ability to maintain redox balance and sustain flavonoid accumulation, underscoring the importance of constitutive host defense in limiting disease progression. Together, this study establishes auxin signaling as a key virulence module in S. scitamineum, synchronizing fungal IAA production, host immunity suppression, and effector deployment. These insights advance our understanding of smut disease mechanisms and propose fungal IAA pathway elements as candidate targets for future resistance breeding.