The Meloidogyne graminicola effector Mg16820 is secreted in the apoplast and cytoplasm to suppress plant host defense responses

Mol Plant Pathol. 2018 Nov;19(11):2416-2430. doi: 10.1111/mpp.12719. Epub 2018 Sep 28.

Abstract

On invasion of roots, plant-parasitic nematodes secrete effectors to manipulate the cellular regulation of the host to promote parasitism. The root-knot nematode Meloidogyne graminicola is one of the most damaging nematodes of rice. Here, we identified a novel effector of this nematode, named Mg16820, expressed in the nematode subventral glands. We localized the Mg16820 effector in the apoplast during the migration phase of the second-stage juvenile in rice roots. In addition, during early development of the feeding site, Mg16820 was localized in giant cells, where it accumulated in the cytoplasm and the nucleus. Using transient expression in Nicotiana benthamiana leaves, we demonstrated that Mg16820 directed to the apoplast was able to suppress flg22-induced reactive oxygen species production. In addition, expression of Mg16820 in the cytoplasm resulted in the suppression of the R2/Avr2- and Mi-1.2-induced hypersensitive response. A potential target protein of Mg16820 identified with the yeast two-hybrid system was the dehydration stress-inducible protein 1 (DIP1). Bimolecular fluorescence complementation resulted in a strong signal in the nucleus. DIP1 has been described as an abscisic acid (ABA)-responsive gene and ABA is involved in the biotic and abiotic stress response. Our results demonstrate that Mg16820 is able to act in two cellular compartments as an immune suppressor and targets a protein involved in the stress response, therefore indicating an important role for this effector in parasitism.

Keywords: Nicotiana benthamiana; Oryza sativa; PAMP-triggered immunity; effector-triggered immunity; parasitism; reactive oxygen species; root-knot nematodes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Amino Acids / metabolism
  • Animals
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism
  • Cytoplasm / drug effects
  • Cytoplasm / metabolism*
  • Flagellin / pharmacology
  • Fluorescence
  • Helminth Proteins / chemistry
  • Helminth Proteins / metabolism*
  • Host-Parasite Interactions* / drug effects
  • Life Cycle Stages / drug effects
  • Nicotiana / drug effects
  • Nicotiana / parasitology
  • Parasites / drug effects
  • Parasites / metabolism
  • Plant Diseases / parasitology
  • Plant Immunity / drug effects
  • Plant Leaves / parasitology
  • Plant Proteins / metabolism
  • Plant Roots / drug effects
  • Plant Roots / parasitology
  • Reactive Oxygen Species / metabolism
  • Stress, Physiological / drug effects
  • Tylenchoidea / drug effects
  • Tylenchoidea / growth & development
  • Tylenchoidea / metabolism*

Substances

  • Amino Acids
  • Helminth Proteins
  • Plant Proteins
  • Reactive Oxygen Species
  • Flagellin