Potyviruses replicate and express their genomes in the cytoplasm in closely related membranous structures such as the endoplasmic reticulum or in the vicinity of the ER. The present research demonstrates the participation of plant cell organelles based on ultrastructural examination of compatible and incompatible interactions in tobacco- and potato-potato virus Y (PVY) necrotic strains. In two interaction types, PVYN Wi and PVYNTN particles were documented inside cell nuclei. Virus cytoplasmic inclusions and particles were associated with nuclear envelope pore complexes. Moreover, the PVY capsid protein was immunolocalised in the cell nucleus and nucleolus. Our results for the first time show PVY particles and capsid proteins inside the mitochondrion in compatible interactions, whereas in hypersensitive responses these interactions were identified inside chloroplasts. The PVY particles attached to mitochondria caused association groups of these organelles. The ultrastructural analysis clearly demonstrated both the dynamics of the endoplasmatic reticulum in two types of PVY interactions and connections between PVY cytoplasmic inclusions and particles with its membranous structures. Moreover, we demonstrated strongly localised immunodetection of the PVY capsid protein on the surface and in the vicinity of ER in cases of hypersensitive response as well as in compatible interaction.