TPO1-based polyamines transport contributes to pathogenicity of sugarcane smut fungus

The basidiomycete Sporisorium scitamineum causes sugarcane smut disease, leading to a significant impairment in the quality and yield of sugarcane. Polyamines affect the intracellular redox balance, which is important for the pathogenic development of S. scitamineum, including sexual mating, dikaryotic hyphae growth, and host invasion. In the present study, we identified a polyamine transporter, SsTPO1, in S. scitamineum. Deletion or overexpression of SsTPO1 led to the disruption of intracellular levels of putrescine, spermidine, and spermine in opposite directions. SsTPO1-based polyamine homeostasis contributes to dikaryotic hyphal growth and host invasion after sexual mating, likely by affecting the cAMP-PKA signaling pathway and collaboratively regulating redox homeostasis. Environmental pH affected SsTPO1-mediated polyamine transport, so S. scitamineum hyphae growth favoured neutral to alkaline environments rather than acidic conditions. The SsTPO1-based polyamine transport also participates in stress resistance and autophagy induction. In summary, our work revealed that SsTPO1 facilitates polyamine transport to regulate cell growth, differentiation, and fungal pathogenicity in S. scitamineum.