Effector GpRpb-1 from Globodera pallida targets E3 ubiquitin ligase complexes to promote nematode infection

Endoparasitic plant-pathogenic nematodes manipulate plant cell morphology and physiology to establish sophisticated feeding structures. Modifications to plant cells are achieved through the activity of nematode secreted effectors. SPRYSECs are a remarkably expanded family of effectors identified initially in potato cyst nematodes. While SPRYSECs have been implicated in suppression of plant immunity, their intrinsic role in nematode virulence remains unexplored. GpRpb-1 is a ‘type’ SPRYSEC from Globodera pallida with virulent and avirulent variants present in field populations of the nematode. Y2H screening of a nematode-infected susceptible potato library yielded interacting candidates for a virulent GpRpb-1 that are involved in post-translational modification in the plant. We have independently confirmed that E3 ubiquitin ligase UPL3 can interact with GpRbp-1 in planta. Transcriptomic profiling of upl3 mutant plants shows that Skp-like and F-box-like E3 ubiquitin ligases are regulated upon nematode infection. Furthermore, upon silencing of the corresponding ligase genes in A. thaliana, we observed significant differences in the amount of developing females present in the roots of nematode-infected plants. The interaction of GpRbp-1 with UPL3 and the transcriptional regulation of other E3 ubiquitin ligases suggest that the intrinsic role of the effector is carried out through manipulation of the plant post-translational modification machinery. Our findings suggest that nematodes are able to use the SPRYSEC family of effectors to control different aspects of the plant cell to establish a feeding site. Therefore, our results may provide further insight into the basis of virulence of nematodes in plants.