MicroRNA 160 controls the auxin response factor–class III peroxidase module and couples salicylic acid and redox signaling networks in the potato hypersensitive response to potato virus Y

Abstract

Summary Hypersensitive 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. We applied a spatially resolved sRNA‐omics approach to uncover changes at the sRNA level and the dynamics of sRNA–gene regulatory networks in potato ( Solanum tuberosum L.) HR to potato virus Y (PVY). We 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. Mechanistically, we identify a novel miR160– StARF10/StARF17 – StPRX28 module that links miR160 repression to the induction of a Class III apoplastic peroxidase in HR, with SA acting upstream. Together, these findings establish miR160 as an important regulatory node that connects SA–auxin–redox signaling pathways and tunes development, defense, and heat resilience, and highlight miR160 as a promising target for fine‐tuning tolerance to multiple stresses with minimal yield loss.