The Potato Cyst Nematode Effector RHA1B Is a Ubiquitin Ligase and Uses Two Distinct Mechanisms to Suppress Plant Immune Signaling

PLoS Pathog. 2019 Apr 12;15(4):e1007720. doi: 10.1371/journal.ppat.1007720. eCollection 2019 Apr.


Plant pathogens, such as bacteria, fungi, oomycetes and nematodes, rely on wide range of virulent effectors delivered into host cells to suppress plant immunity. Although phytobacterial effectors have been intensively investigated, little is known about the function of effectors of plant-parasitic nematodes, such as Globodera pallida, a cyst nematode responsible for vast losses in the potato and tomato industries. Here, we demonstrate using in vivo and in vitro ubiquitination assays the potato cyst nematode (Globodera pallida) effector RHA1B is an E3 ubiquitin ligase that employs multiple host plant E2 ubiquitin conjugation enzymes to catalyze ubiquitination. RHA1B was able to suppress effector-triggered immunity (ETI), as manifested by suppression of hypersensitive response (HR) mediated by a broad range of nucleotide-binding leucine-rich repeat (NB-LRR) immune receptors, presumably via E3-dependent degradation of the NB-LRR receptors. RHA1B also blocked the flg22-triggered expression of Acre31 and WRKY22, marker genes of pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI), but this did not require the E3 activity of RHA1B. Moreover, transgenic potato overexpressing the RHA1B transgene exhibited enhanced susceptibility to G. pallida. Thus, our data suggest RHA1B facilitates nematode parasitism not only by triggering degradation of NB-LRR immune receptors to block ETI signaling but also by suppressing PTI signaling via an as yet unknown E3-independent mechanism.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Host-Pathogen Interactions / immunology*
  • Plant Diseases / immunology*
  • Plant Diseases / parasitology
  • Plant Immunity / immunology*
  • Plant Proteins / immunology
  • Plant Proteins / metabolism*
  • Secernentea Infections / immunology*
  • Secernentea Infections / metabolism
  • Secernentea Infections / parasitology
  • Signal Transduction
  • Solanum tuberosum / immunology*
  • Solanum tuberosum / parasitology
  • Tylenchoidea / pathogenicity*
  • Ubiquitin
  • Ubiquitin-Protein Ligases
  • Ubiquitination


  • Plant Proteins
  • Ubiquitin
  • Ubiquitin-Protein Ligases

Grant support

Funding was provided by the Agriculture and Food Research Initiative competitive grant (2017-67014-26197 for FX; 2017-67014-26591 for FX and L-MD) of the USDA National Institute of Food and Agriculture (, USDA-NIFA Farm Bill ( and Northwest Potato Consortium (L-MD, JCK, AC, and FX) (, ISDA Specialty Crop (L-MD and FX) (, the Dutch Technology Foundation TTW and Earth and Life Sciences ALW, which are part of the Netherlands Organization for Scientific Research (NWO) (to AG) (, and National Natural Science Foundation of China (31671259 and 31828003, to YL) ( The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.