The effector GpRbp-1 of Globodera pallida targets a nuclear HECT E3 ubiquitin ligase to modulate gene expression in the host

Amalia Diaz-Granados, Mark G. Sterken, Hein Overmars, Roel Ariaans, Martijn Holterman, Somnath S. Pokhare, Yulin Yuan, Rikus Pomp, Anna Finkers-Tomczak, Jan Roosien, Erik Slootweg, Abdenaser Elashry, Florian M.W. Grundler, Fangming Xiao, Aska Goverse, Geert Smant*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Plant-parasitic nematodes secrete effectors that manipulate plant cell morphology and physiology to achieve host invasion and establish permanent feeding sites. Effectors from the highly expanded SPRYSEC (SPRY domain with a signal peptide for secretion) family in potato cyst nematodes have been implicated in activation and suppression of plant immunity, but the mechanisms underlying these activities remain largely unexplored. To study the host mechanisms used by SPRYSEC effectors, we identified plant targets of GpRbp-1 from the potato cyst nematode Globodera pallida. Here, we show that GpRbp-1 interacts in yeast and in planta with a functional potato homologue of the Homology to E6-AP C-Terminus (HECT)-type ubiquitin E3 ligase UPL3, which is located in the nucleus. Potato lines lacking StUPL3 are not available, but the Arabidopsis mutant upl3-5 displaying a reduced UPL3 expression showed a consistently small but not significant decrease in susceptibility to cyst nematodes. We observed a major impact on the root transcriptome by the lower levels of AtUPL3 in the upl3-5 mutant, but surprisingly only in association with infections by cyst nematodes. To our knowledge, this is the first example that a HECT-type ubiquitin E3 ligase is targeted by a pathogen effector and that a member of this class of proteins specifically regulates gene expression under biotic stress conditions. Together, our data suggest that GpRbp-1 targets a specific component of the plant ubiquitination machinery to manipulate the stress response in host cells.

Original languageEnglish
Pages (from-to)66-82
JournalMolecular Plant Pathology
Volume21
Issue number1
Early online date22 Nov 2019
DOIs
Publication statusPublished - Jan 2020

Keywords

  • Cyst nematodes
  • GpRbp-1
  • HECT E3 ligase
  • nematode effectors
  • ubiquitination
  • UPL3
  • virulence/parasitism

Fingerprint Dive into the research topics of 'The effector GpRbp-1 of Globodera pallida targets a nuclear HECT E3 ubiquitin ligase to modulate gene expression in the host'. Together they form a unique fingerprint.

  • Cite this

    Diaz-Granados, A., Sterken, M. G., Overmars, H., Ariaans, R., Holterman, M., Pokhare, S. S., Yuan, Y., Pomp, R., Finkers-Tomczak, A., Roosien, J., Slootweg, E., Elashry, A., Grundler, F. M. W., Xiao, F., Goverse, A., & Smant, G. (2020). The effector GpRbp-1 of Globodera pallida targets a nuclear HECT E3 ubiquitin ligase to modulate gene expression in the host. Molecular Plant Pathology, 21(1), 66-82. https://doi.org/10.1111/mpp.12880