BTB-BACK Domain Protein POB1 Suppresses Immune Cell Death by Targeting Ubiquitin E3 ligase PUB17 for Degradation

Beatriz Orosa, Qin He, Joelle Mesmar, Eleanor M. Gilroy, Hazel McLellan, Chengwei Yang, Adam Craig, Mark Bailey, Cunjin Zhang, Jonathan David Moore, Petra C. Boevink, Zhendong Tian, Paul R. J. Birch (Lead / Corresponding author), Ari Sadanandom (Lead / Corresponding author)

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Abstract

Hypersensitive response programmed cell death (HR-PCD) is a critical feature in plant immunity required for pathogen restriction and prevention of disease development. The precise control of this process is paramount to cell survival and an effective immune response. The discovery of new components that function to suppress HR-PCD will be instrumental in understanding the regulation of this fundamental mechanism. Here we report the identification and characterisation of a BTB domain E3 ligase protein, POB1, that functions to suppress HR-PCD triggered by evolutionarily diverse pathogens. Nicotiana benthamiana and tobacco plants with reduced POB1 activity show accelerated HR-PCD whilst those with increased POB1 levels show attenuated HR-PCD. We demonstrate that POB1 dimerization and nuclear localization are vital for its function in HR-PCD suppression. Using protein-protein interaction assays, we identify the Plant U-Box E3 ligase PUB17, a well established positive regulator of plant innate immunity, as a target for POB1-mediated proteasomal degradation. Using confocal imaging and in planta immunoprecipitation assays we show that POB1 interacts with PUB17 in the nucleus and stimulates its degradation. Mutated versions of POB1 that show reduced interaction with PUB17 fail to suppress HR-PCD, indicating that POB1-mediated degradation of PUB17 U-box E3 ligase is an important step for negative regulation of specific immune pathways in plants. Our data reveals a new mechanism for BTB domain proteins in suppressing HR-PCD in plant innate immune responses.

Original languageEnglish
Article numbere1006540
Pages (from-to)1-26
Number of pages26
JournalPLoS Genetics
Volume13
Issue number1
DOIs
Publication statusPublished - 5 Jan 2017

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ubiquitin-protein ligase
Ubiquitin-Protein Ligases
hypersensitive response
targeting
cell death
Cell Death
apoptosis
degradation
protein
Plant Immunity
Proteins
proteins
ligases
immunity
immune response
pathogen
Innate Immunity
assay
Tobacco
tobacco

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Orosa, Beatriz ; He, Qin ; Mesmar, Joelle ; Gilroy, Eleanor M. ; McLellan, Hazel ; Yang, Chengwei ; Craig, Adam ; Bailey, Mark ; Zhang, Cunjin ; Moore, Jonathan David ; Boevink, Petra C. ; Tian, Zhendong ; Birch, Paul R. J. ; Sadanandom, Ari. / BTB-BACK Domain Protein POB1 Suppresses Immune Cell Death by Targeting Ubiquitin E3 ligase PUB17 for Degradation. In: PLoS Genetics. 2017 ; Vol. 13, No. 1. pp. 1-26.
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title = "BTB-BACK Domain Protein POB1 Suppresses Immune Cell Death by Targeting Ubiquitin E3 ligase PUB17 for Degradation",
abstract = "Hypersensitive response programmed cell death (HR-PCD) is a critical feature in plant immunity required for pathogen restriction and prevention of disease development. The precise control of this process is paramount to cell survival and an effective immune response. The discovery of new components that function to suppress HR-PCD will be instrumental in understanding the regulation of this fundamental mechanism. Here we report the identification and characterisation of a BTB domain E3 ligase protein, POB1, that functions to suppress HR-PCD triggered by evolutionarily diverse pathogens. Nicotiana benthamiana and tobacco plants with reduced POB1 activity show accelerated HR-PCD whilst those with increased POB1 levels show attenuated HR-PCD. We demonstrate that POB1 dimerization and nuclear localization are vital for its function in HR-PCD suppression. Using protein-protein interaction assays, we identify the Plant U-Box E3 ligase PUB17, a well established positive regulator of plant innate immunity, as a target for POB1-mediated proteasomal degradation. Using confocal imaging and in planta immunoprecipitation assays we show that POB1 interacts with PUB17 in the nucleus and stimulates its degradation. Mutated versions of POB1 that show reduced interaction with PUB17 fail to suppress HR-PCD, indicating that POB1-mediated degradation of PUB17 U-box E3 ligase is an important step for negative regulation of specific immune pathways in plants. Our data reveals a new mechanism for BTB domain proteins in suppressing HR-PCD in plant innate immune responses.",
author = "Beatriz Orosa and Qin He and Joelle Mesmar and Gilroy, {Eleanor M.} and Hazel McLellan and Chengwei Yang and Adam Craig and Mark Bailey and Cunjin Zhang and Moore, {Jonathan David} and Boevink, {Petra C.} and Zhendong Tian and Birch, {Paul R. J.} and Ari Sadanandom",
note = "The following funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Biotechnology and Biological Sciences Research Council (BBSRC) (grants BB/G015244/1, BB/K018183/1, BB/L026880/1, BB/M002136/1) URL; http://www.bbsrc.ac.uk/funding/.",
year = "2017",
month = "1",
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doi = "10.1371/journal.pgen.1006540",
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Orosa, B, He, Q, Mesmar, J, Gilroy, EM, McLellan, H, Yang, C, Craig, A, Bailey, M, Zhang, C, Moore, JD, Boevink, PC, Tian, Z, Birch, PRJ & Sadanandom, A 2017, 'BTB-BACK Domain Protein POB1 Suppresses Immune Cell Death by Targeting Ubiquitin E3 ligase PUB17 for Degradation', PLoS Genetics, vol. 13, no. 1, e1006540, pp. 1-26. https://doi.org/10.1371/journal.pgen.1006540

BTB-BACK Domain Protein POB1 Suppresses Immune Cell Death by Targeting Ubiquitin E3 ligase PUB17 for Degradation. / Orosa, Beatriz; He, Qin; Mesmar, Joelle; Gilroy, Eleanor M.; McLellan, Hazel; Yang, Chengwei; Craig, Adam; Bailey, Mark; Zhang, Cunjin; Moore, Jonathan David; Boevink, Petra C.; Tian, Zhendong; Birch, Paul R. J. (Lead / Corresponding author); Sadanandom, Ari (Lead / Corresponding author).

In: PLoS Genetics, Vol. 13, No. 1, e1006540, 05.01.2017, p. 1-26.

Research output: Contribution to journalArticle

TY - JOUR

T1 - BTB-BACK Domain Protein POB1 Suppresses Immune Cell Death by Targeting Ubiquitin E3 ligase PUB17 for Degradation

AU - Orosa, Beatriz

AU - He, Qin

AU - Mesmar, Joelle

AU - Gilroy, Eleanor M.

AU - McLellan, Hazel

AU - Yang, Chengwei

AU - Craig, Adam

AU - Bailey, Mark

AU - Zhang, Cunjin

AU - Moore, Jonathan David

AU - Boevink, Petra C.

AU - Tian, Zhendong

AU - Birch, Paul R. J.

AU - Sadanandom, Ari

N1 - The following funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Biotechnology and Biological Sciences Research Council (BBSRC) (grants BB/G015244/1, BB/K018183/1, BB/L026880/1, BB/M002136/1) URL; http://www.bbsrc.ac.uk/funding/.

PY - 2017/1/5

Y1 - 2017/1/5

N2 - Hypersensitive response programmed cell death (HR-PCD) is a critical feature in plant immunity required for pathogen restriction and prevention of disease development. The precise control of this process is paramount to cell survival and an effective immune response. The discovery of new components that function to suppress HR-PCD will be instrumental in understanding the regulation of this fundamental mechanism. Here we report the identification and characterisation of a BTB domain E3 ligase protein, POB1, that functions to suppress HR-PCD triggered by evolutionarily diverse pathogens. Nicotiana benthamiana and tobacco plants with reduced POB1 activity show accelerated HR-PCD whilst those with increased POB1 levels show attenuated HR-PCD. We demonstrate that POB1 dimerization and nuclear localization are vital for its function in HR-PCD suppression. Using protein-protein interaction assays, we identify the Plant U-Box E3 ligase PUB17, a well established positive regulator of plant innate immunity, as a target for POB1-mediated proteasomal degradation. Using confocal imaging and in planta immunoprecipitation assays we show that POB1 interacts with PUB17 in the nucleus and stimulates its degradation. Mutated versions of POB1 that show reduced interaction with PUB17 fail to suppress HR-PCD, indicating that POB1-mediated degradation of PUB17 U-box E3 ligase is an important step for negative regulation of specific immune pathways in plants. Our data reveals a new mechanism for BTB domain proteins in suppressing HR-PCD in plant innate immune responses.

AB - Hypersensitive response programmed cell death (HR-PCD) is a critical feature in plant immunity required for pathogen restriction and prevention of disease development. The precise control of this process is paramount to cell survival and an effective immune response. The discovery of new components that function to suppress HR-PCD will be instrumental in understanding the regulation of this fundamental mechanism. Here we report the identification and characterisation of a BTB domain E3 ligase protein, POB1, that functions to suppress HR-PCD triggered by evolutionarily diverse pathogens. Nicotiana benthamiana and tobacco plants with reduced POB1 activity show accelerated HR-PCD whilst those with increased POB1 levels show attenuated HR-PCD. We demonstrate that POB1 dimerization and nuclear localization are vital for its function in HR-PCD suppression. Using protein-protein interaction assays, we identify the Plant U-Box E3 ligase PUB17, a well established positive regulator of plant innate immunity, as a target for POB1-mediated proteasomal degradation. Using confocal imaging and in planta immunoprecipitation assays we show that POB1 interacts with PUB17 in the nucleus and stimulates its degradation. Mutated versions of POB1 that show reduced interaction with PUB17 fail to suppress HR-PCD, indicating that POB1-mediated degradation of PUB17 U-box E3 ligase is an important step for negative regulation of specific immune pathways in plants. Our data reveals a new mechanism for BTB domain proteins in suppressing HR-PCD in plant innate immune responses.

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DO - 10.1371/journal.pgen.1006540

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JF - PLoS Genetics

SN - 1553-7390

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M1 - e1006540

ER -