Plant pathogen effector utilizes host susceptibility factor NRL1 to degrade the immune regulator SWAP70

Qin He, Shaista Naqvi, Hazel McLellan, Petra Boevink, Nicolas Champouret, Ingo Hein, Paul Birch (Lead / Corresponding author)

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Abstract

Plant pathogens deliver effectors into plant cells to suppress immunity. Whereas many effectors inactivate positive immune regulators, other effectors associate with negative regulators of immunity: so-called susceptibility (S) factors. Little is known about how pathogens exploit S factors to suppress immunity. Phytophthora infestans RXLR effector Pi02860 interacts with host protein NRL1, which is an S factor whose activity suppresses INF1-triggered cell death (ICD) and is required for late blight disease. We show that NRL1 interacts in yeast and in planta with a guanine nucleotide exchange factor called SWAP70. SWAP70 associates with endosomes and is a positive regulator of immunity. Virus-induced gene silencing of SWAP70 in Nicotiana benthamiana enhances P. infestans colonization and compromises ICD. In contrast, transient overexpression of SWAP70 reduces P. infestans infection and accelerates ICD. Expression of Pi02860 and NRL1, singly or in combination, results in proteasome-mediated degradation of SWAP70. Degradation of SWAP70 is prevented by silencing NRL1, or by mutation of Pi02860 to abolish its interaction with NRL1. NRL1 is a BTB-domain protein predicted to form the substrate adaptor component of a CULLIN3 ubiquitin E3 ligase. A dimerization-deficient mutant, NRL1 NQ, fails to interact with SWAP70 but maintains its interaction with Pi02860. NRL1 NQ acts as a dominant-negative mutant, preventing SWAP70 degradation in the presence of effector Pi02860, and reducing P. infestans infection. Critically, Pi02860 enhances the association between NRL1 and SWAP70 to promote proteasome-mediated degradation of the latter and, thus, suppress immunity. Preventing degradation of SWAP70 represents a strategy to combat late blight disease.

Original languageEnglish
Pages (from-to)E7834-E7843
Number of pages10
JournalProceedings of the National Academy of Sciences
Volume115
Issue number33
Early online date26 Jul 2018
DOIs
Publication statusPublished - 14 Aug 2018

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Phytophthora infestans
Immunity
Cell Death
Proteasome Endopeptidase Complex
Guanine Nucleotide Exchange Factors
Ubiquitin-Protein Ligases
Endosomes
Plant Cells
Dimerization
Gene Silencing
Infection
Tobacco
Proteins
Yeasts
Viruses
Mutation

Keywords

  • potato blight
  • effector-triggered susceptibility
  • disease resistance
  • pathogenicity
  • virulence
  • Pathogenicity
  • Disease resistance
  • Virulence
  • Potato blight
  • Effector-triggered susceptibility
  • Cullin Proteins/genetics
  • Plant Immunity
  • Gene Expression Regulation, Plant/genetics
  • DNA-Binding Proteins/genetics
  • Plant Proteins/genetics
  • Proteolysis
  • Tobacco/genetics
  • Phytophthora infestans/immunology
  • Plant Diseases/genetics

Cite this

@article{42eddd53c4df4816a7a6fbe0489ae417,
title = "Plant pathogen effector utilizes host susceptibility factor NRL1 to degrade the immune regulator SWAP70",
abstract = "Plant pathogens deliver effectors into plant cells to suppress immunity. Whereas many effectors inactivate positive immune regulators, other effectors associate with negative regulators of immunity: so-called susceptibility (S) factors. Little is known about how pathogens exploit S factors to suppress immunity. Phytophthora infestans RXLR effector Pi02860 interacts with host protein NRL1, which is an S factor whose activity suppresses INF1-triggered cell death (ICD) and is required for late blight disease. We show that NRL1 interacts in yeast and in planta with a guanine nucleotide exchange factor called SWAP70. SWAP70 associates with endosomes and is a positive regulator of immunity. Virus-induced gene silencing of SWAP70 in Nicotiana benthamiana enhances P. infestans colonization and compromises ICD. In contrast, transient overexpression of SWAP70 reduces P. infestans infection and accelerates ICD. Expression of Pi02860 and NRL1, singly or in combination, results in proteasome-mediated degradation of SWAP70. Degradation of SWAP70 is prevented by silencing NRL1, or by mutation of Pi02860 to abolish its interaction with NRL1. NRL1 is a BTB-domain protein predicted to form the substrate adaptor component of a CULLIN3 ubiquitin E3 ligase. A dimerization-deficient mutant, NRL1 NQ, fails to interact with SWAP70 but maintains its interaction with Pi02860. NRL1 NQ acts as a dominant-negative mutant, preventing SWAP70 degradation in the presence of effector Pi02860, and reducing P. infestans infection. Critically, Pi02860 enhances the association between NRL1 and SWAP70 to promote proteasome-mediated degradation of the latter and, thus, suppress immunity. Preventing degradation of SWAP70 represents a strategy to combat late blight disease.",
keywords = "potato blight, effector-triggered susceptibility, disease resistance, pathogenicity, virulence, Pathogenicity, Disease resistance, Virulence, Potato blight, Effector-triggered susceptibility, Cullin Proteins/genetics, Plant Immunity, Gene Expression Regulation, Plant/genetics, DNA-Binding Proteins/genetics, Plant Proteins/genetics, Proteolysis, Tobacco/genetics, Phytophthora infestans/immunology, Plant Diseases/genetics",
author = "Qin He and Shaista Naqvi and Hazel McLellan and Petra Boevink and Nicolas Champouret and Ingo Hein and Paul Birch",
note = "We are grateful for financial support from the Biotechnology and Biological Sciences Research Council (BBSRC) (grants BB/G015244/1, BB/K018183/1, BB/L026880/1), and Scottish Government Rural and Environment Science and Analytical Services Division (RESAS).",
year = "2018",
month = "8",
day = "14",
doi = "10.1073/pnas.1808585115",
language = "English",
volume = "115",
pages = "E7834--E7843",
journal = "Proceedings of the National Academy of Sciences",
issn = "0027-8424",
publisher = "National Academy of Sciences",
number = "33",

}

TY - JOUR

T1 - Plant pathogen effector utilizes host susceptibility factor NRL1 to degrade the immune regulator SWAP70

AU - He, Qin

AU - Naqvi, Shaista

AU - McLellan, Hazel

AU - Boevink, Petra

AU - Champouret, Nicolas

AU - Hein, Ingo

AU - Birch, Paul

N1 - We are grateful for financial support from the Biotechnology and Biological Sciences Research Council (BBSRC) (grants BB/G015244/1, BB/K018183/1, BB/L026880/1), and Scottish Government Rural and Environment Science and Analytical Services Division (RESAS).

PY - 2018/8/14

Y1 - 2018/8/14

N2 - Plant pathogens deliver effectors into plant cells to suppress immunity. Whereas many effectors inactivate positive immune regulators, other effectors associate with negative regulators of immunity: so-called susceptibility (S) factors. Little is known about how pathogens exploit S factors to suppress immunity. Phytophthora infestans RXLR effector Pi02860 interacts with host protein NRL1, which is an S factor whose activity suppresses INF1-triggered cell death (ICD) and is required for late blight disease. We show that NRL1 interacts in yeast and in planta with a guanine nucleotide exchange factor called SWAP70. SWAP70 associates with endosomes and is a positive regulator of immunity. Virus-induced gene silencing of SWAP70 in Nicotiana benthamiana enhances P. infestans colonization and compromises ICD. In contrast, transient overexpression of SWAP70 reduces P. infestans infection and accelerates ICD. Expression of Pi02860 and NRL1, singly or in combination, results in proteasome-mediated degradation of SWAP70. Degradation of SWAP70 is prevented by silencing NRL1, or by mutation of Pi02860 to abolish its interaction with NRL1. NRL1 is a BTB-domain protein predicted to form the substrate adaptor component of a CULLIN3 ubiquitin E3 ligase. A dimerization-deficient mutant, NRL1 NQ, fails to interact with SWAP70 but maintains its interaction with Pi02860. NRL1 NQ acts as a dominant-negative mutant, preventing SWAP70 degradation in the presence of effector Pi02860, and reducing P. infestans infection. Critically, Pi02860 enhances the association between NRL1 and SWAP70 to promote proteasome-mediated degradation of the latter and, thus, suppress immunity. Preventing degradation of SWAP70 represents a strategy to combat late blight disease.

AB - Plant pathogens deliver effectors into plant cells to suppress immunity. Whereas many effectors inactivate positive immune regulators, other effectors associate with negative regulators of immunity: so-called susceptibility (S) factors. Little is known about how pathogens exploit S factors to suppress immunity. Phytophthora infestans RXLR effector Pi02860 interacts with host protein NRL1, which is an S factor whose activity suppresses INF1-triggered cell death (ICD) and is required for late blight disease. We show that NRL1 interacts in yeast and in planta with a guanine nucleotide exchange factor called SWAP70. SWAP70 associates with endosomes and is a positive regulator of immunity. Virus-induced gene silencing of SWAP70 in Nicotiana benthamiana enhances P. infestans colonization and compromises ICD. In contrast, transient overexpression of SWAP70 reduces P. infestans infection and accelerates ICD. Expression of Pi02860 and NRL1, singly or in combination, results in proteasome-mediated degradation of SWAP70. Degradation of SWAP70 is prevented by silencing NRL1, or by mutation of Pi02860 to abolish its interaction with NRL1. NRL1 is a BTB-domain protein predicted to form the substrate adaptor component of a CULLIN3 ubiquitin E3 ligase. A dimerization-deficient mutant, NRL1 NQ, fails to interact with SWAP70 but maintains its interaction with Pi02860. NRL1 NQ acts as a dominant-negative mutant, preventing SWAP70 degradation in the presence of effector Pi02860, and reducing P. infestans infection. Critically, Pi02860 enhances the association between NRL1 and SWAP70 to promote proteasome-mediated degradation of the latter and, thus, suppress immunity. Preventing degradation of SWAP70 represents a strategy to combat late blight disease.

KW - potato blight

KW - effector-triggered susceptibility

KW - disease resistance

KW - pathogenicity

KW - virulence

KW - Pathogenicity

KW - Disease resistance

KW - Virulence

KW - Potato blight

KW - Effector-triggered susceptibility

KW - Cullin Proteins/genetics

KW - Plant Immunity

KW - Gene Expression Regulation, Plant/genetics

KW - DNA-Binding Proteins/genetics

KW - Plant Proteins/genetics

KW - Proteolysis

KW - Tobacco/genetics

KW - Phytophthora infestans/immunology

KW - Plant Diseases/genetics

UR - http://www.scopus.com/inward/record.url?scp=85052724351&partnerID=8YFLogxK

U2 - 10.1073/pnas.1808585115

DO - 10.1073/pnas.1808585115

M3 - Article

VL - 115

SP - E7834-E7843

JO - Proceedings of the National Academy of Sciences

JF - Proceedings of the National Academy of Sciences

SN - 0027-8424

IS - 33

ER -