miR160 controls class III peroxidase via StARF10/17 and couples salicylic acid and ROS signaling networks in potato hypersensitive response to potato virus Y

Abstract

O_LIHypersensitive response (HR) is an effector-triggered immune response leading to pathogen restriction and local cell death. Small RNAs (sRNAs), mediating RNA silencing, have a well-established role in antiviral immunity, however, their role in HR has not been addressed to date. C_LIO_LIWe applied a spatially resolved sRNAomics approach to uncover changes at the sRNA level and the dynamics of sRNA-gene regulatory networks in potato HR response to potato virus Y (PVY). C_LIO_LIWe show that miR160 is repressed in cells adjacent to HR lesions in the resistant cultivar, but not in PVY-sensitive, salicylic acid (SA)-depleted plants. Beyond its canonical regulation of StARF10 and StARF17, miR160 controls a broader regulatory network spanning auxin signaling, cell-wall remodeling, redox homeostasis, and tuberization. Elevated miR160 levels promote susceptibility-associated traits, reduce thermotolerance, and suppress genes strongly activated in HR. C_LIO_LIMechanistically, we identify a novel miR160-StARF10/StARF17-StPRX28 module that links miR160 repression to the induction of a class III apoplastic peroxidase during HR, with SA acting upstream. Together, these findings establish miR160 as a crucial integrator of SA-auxin-ROS signaling pathways that tunes development, defense, and heat resilience, and highlight miR160 as a promising target for fine-tuning tolerance to multiple stresses with minimal yield loss. C_LI