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This study demonstrates the new sources of resistance available in potato cv. Etola, which represent multiple strain-specific resistance genes against three strains of Potato virus Y (PVY). Etola is the first documented cultivar of this sort in Europe that exhibits hypersensitive resistance (HR) to PVYNTN isolate PVY-3202, and different levels of partial resistance to PVYN-Wi isolate PVY-3411 and PVYZ-NTN isolate PVY-3303. The isolate PVY-3411 induced severe symptoms and faster systemic viral coat protein and RNA accumulation in the noninoculated upper leaves, whereas PVY-3303 caused mild symptoms and delayed viral spreading. This study provides the first example of strain-specific alteration of a set of host microRNAs (miRNAs) and their targets in the potato–PVY interaction. The tested miRNAs and targets are altered only in plants of cv. Etola infected with PVY-3411 but not those infected with PVY-3303 nor PVY-3202. The up-regulation of stu-miR162, stu-miR168a and miR172e, together with their target transcripts, DCL1, AGO1-2 and TOE3, respectively, in PVY-3411-infected plants correlates with high abundance of HC-Pro RNA encoding an RNA-silencing suppressor and might be linked with the severe symptoms in leaves. Moreover, PVY-3411 causes parallel increases in two members of stu-miR482 and their mRNA targets Gpa2 and CC-NBS-LRR that are involved in the defence response.