Plasmopara viticola effector PvRXLR131 suppresses plant immunity by targeting plant receptor-like kinase inhibitor BKI1

Mol Plant Pathol. 2019 Jun;20(6):765-783. doi: 10.1111/mpp.12790. Epub 2019 Apr 4.

Abstract

The grapevine downy mildew pathogen Plasmopara viticola secretes a set of RXLR effectors (PvRXLRs) to overcome host immunity and facilitate infection, but how these effectors function is unclear. Here, the biological function of PvRXLR131 was investigated via heterologous expression. Constitutive expression of PvRXLR131 in Colletotrichum gloeosporioides significantly enhanced its pathogenicity on grapevine leaves. Constitutive expression of PvRXLR131 in Arabidopsis promoted Pseudomonas syringae DC3000 and P. syringae DC3000 (hrcC- ) growth as well as suppressed defence-related callose deposition. Transient expression of PvRXLR131 in Nicotiana benthamiana leaves could also suppress different elicitor-triggered cell death and inhibit plant resistance to Phytophthora capsici. Further analysis revealed that PvRXLR131 interacted with host Vitis vinifera BRI1 kinase inhibitor 1 (VvBKI1), and its homologues in N. benthamiana (NbBKI1) and Arabidopsis (AtBKI1). Moreover, bimolecular fluorescence complementation analysis revealed that PvRXLR131 interacted with VvBKI1 in the plasma membrane. Deletion assays showed that the C-terminus of PvRXLR131 was responsible for the interaction and mutation assays showed that phosphorylation of a conserved tyrosine residue in BKI1s disrupted the interaction. BKI1 was a receptor inhibitor of growth- and defence-related brassinosteroid (BR) and ERECTA (ER) signalling. When silencing of NbBKI1 in N. benthamiana, the virulence function of PvRXLR131 was eliminated, demonstrating that the effector activity is mediated by BKI1. Moreover, PvRXLR131-transgenic plants displayed BKI1-overexpression dwarf phenotypes and suppressed BR and ER signalling. These physiological and genetic data clearly demonstrate that BKI1 is a virulence target of PvRXLR131. We propose that P. viticola secretes PvRXLR131 to target BKI1 as a strategy for promoting infection.

Keywords: Plasmopara viticola; BKI1; ERECTA; RXLR effector; brassinosteroid; downy mildew.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Brassinosteroids / metabolism
  • Gene Expression Regulation, Plant / genetics
  • Gene Expression Regulation, Plant / physiology
  • Oomycetes / genetics
  • Oomycetes / immunology*
  • Oomycetes / pathogenicity*
  • Plant Diseases / genetics
  • Plant Diseases / microbiology*
  • Plant Immunity / genetics
  • Plant Immunity / immunology*
  • Plant Immunity / physiology*
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*

Substances

  • Brassinosteroids
  • Plant Proteins