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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, NRL1NQ, fails to interact with SWAP70 but maintains its interaction with Pi02860. NRL1NQ 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.

SUBMITTER: He Q

PROVIDER: S-EPMC6099861 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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

He Qin Q Naqvi Shaista S McLellan Hazel H Boevink Petra C PC Champouret Nicolas N Hein Ingo I Birch Paul R J PRJ

Proceedings of the National Academy of Sciences of the United States of America 20180726 33

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. <i>Phytophthora infestans</i> 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 la ...[more]

PMID: 30049706

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Project description:Polyphagous aphids often consist of host-specialized lineages, which have greater fitness on their native hosts than on others. The underlying causes are important for understanding of the evolution of diet breadth and host shift of aphids. The cotton-melon aphid Aphis gossypii Glover is extremely polyphagous with many strict host-specialized lineages. Whether and how the lineage specialized on the primary host hibiscus shifts to the secondary host cucumber remains elusive. We found that the hibiscus-specialized lineage suffered high mortality and gave birth to very few nymphs developing into yellow dwarfs on fresh cucumber leaves, and did not inflict any damage symptoms on cucumber plants. The poor performance did not improve with prolonged exposure to cucumber; however, it did significantly improve when the cucumber leaves were pre-infected with a biotrophic phytopathogen Pseudoperonospora cubensis. More importantly, the hibiscus-specialized lineage with two-generation feeding experience on pre-infected cucumber leaves performed as well as the cucumber-specialized lineage did on fresh cucumber leaves, and inflicted typical damage symptoms on intact cucumber plants. Electrical penetration graph (EPG) indicated that the hibiscus-specialized lineage did not ingest phloem sap from fresh cucumber leaves but succeeded in ingesting phloem sap from pre-infected cucumber leaves, which explained the performance improvement of the hibiscus-specialized lineage on pre-infected cucumber leaves. This study revealed a new pathway for the hibiscus-specialized lineage to quickly acclimate to cucumber under the assistance of the phytopathogen. We considered that the short feeding experience on pre-infected cucumber may activate expression of effector genes that are related to specific host utilization. We suggest to identify host-specific effectors by comparing proteomes or/and transcriptomes of the hibiscus-specialized lineage before and after acclimating to cucumber.

Dataset Information

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

Publications

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

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