A Sugarcane Smut Fungus Effector Hijacks Plant Vacuolar Sorting Receptor-Mediated Trafficking to Evade Host Immune Detection

Abstract

The smut fungus Sporisorium scitamineum is a major pathogen in sugarcane, causing significant agricultural losses worldwide. However, the molecular mechanisms by which its effectors facilitate infection and evade host immunity remain largely unclear. In this study, we identified the sugarcane vacuolar sorting receptor 1 gene (ScVSR1), whose expression negatively correlate with several putative S. scitamineum effector genes in a co-expression network. Overexpression of ScVSR1 in Arabidopsis thaliana reduced resistance to a fungal powdery mildew pathogen, indicating the negative role of ScVSR1 in plant defence. Among the co-expressed S. scitamineum effectors, SsPE15, a secreted cerato-platanin-like protein (CPP), physically interacts with ScVSR1 and is sorted into the prevacuolar compartment (PVC) by interacting with ScVSR1 in plant cells. Deletion of SsPE15 in S. scitamineum enhanced fungal virulence, suggesting that SsPE15 acts as an immune elicitor. Furthermore, the C-terminal domain of the SsPE15, containing the VSR sorting signal, was found to facilitate vesicular location. Notably, fusing this C-terminal domain to the bacterial effector AvrRpt2 significantly reduced AvrRpt2-triggered programmed cell death in Arabidopsis, a process partially dependent on AtVSR1 and AtVSR2. These findings reveal an immune evasion strategy by which S. scitamineum effector SsPE15 hijacks the host's vesicular trafficking system to avoid immune detection.