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Potato virus Y (PVY) is one of the most important constraints to potato production worldwide. There is an increasing occurrence of recombinant PVY strains PVY^NTN and PVY^N-Wi and a decline in the incidence of the nonrecombinant PVY^O. We hypothesized that this may be due to the ability of these recombinant strains to antagonize and/or outcompete PVY^O in mixed infections. To determine this, we investigated interactions between PVY^O and three recombinant PVY strains common in North America: PVY^NTN, PVY^N-Wi, and PVY^N:O. Overall, our study showed that these interactions are tissue-dependent. Specifically, PVY^NTN, the main causal agent of potato tuber necrotic ringspot disease (PTNRD), was found to be more adaptable than PVY^O, especially in potato leaves due, at least in part, to the Ny gene that confers hypersensitive resistance (HR) to PVY^O. Furthermore, PVY^N-Wi was found to repress PVY^O in potato tubers but act synergistically in potato leaves. The PVY^O-induced foliage necrosis in cultivar ‘Ranger Russet’ was observed to be more severe in plants co-infected by PVY^N-Wi and PVY^N:O, respectively, resulting in plant death. Strikingly, this PVY^O -induced necrosis was suppressed by PVY^NTN in doubly infected plants. These interactions may, at least partially, explain the decreasing incidence of PVY^O in United States potato production regions, especially given that many cultivars contain the Ny gene, which likely limits PVY^O enabling PVY^NTN and PVY^N-Wi to outcompete. We also found that replication and cell-to-cell movement of these PVY strains in tubers at 4 °C was similar to levels at ambient temperature.