COP1, a negative regulator of photomorphogenesis, positively regulates plant disease resistance via double-stranded RNA binding proteins

Gah Hyun Lim; Timothy Hoey; Shifeng Zhu; Marion Clavel; Keshun Yu; Duroy Navarre; Aardra Kachroo; Jean Marc Deragon; Pradeep Kachroo

doi:10.1371/journal.ppat.1006894

COP1, a negative regulator of photomorphogenesis, positively regulates plant disease resistance via double-stranded RNA binding proteins

Gah Hyun Lim, Timothy Hoey, Shifeng Zhu, Marion Clavel, Keshun Yu, Duroy Navarre, Aardra Kachroo, Jean Marc Deragon, Pradeep Kachroo

Research output: Contribution to journal › Article › peer-review

27 Scopus citations

Abstract

The E3 ubiquitin ligase COP1 (Constitutive Photomorphogenesis 1) is a well known component of the light-mediated plant development that acts as a repressor of photomorphogenesis. Here we show that COP1 positively regulates defense against turnip crinkle virus (TCV) and avrRPM1 bacteria by contributing to stability of resistance (R) protein HRT and RPM1, respectively. HRT and RPM1 levels and thereby pathogen resistance is significantly reduced in the cop1 mutant background. Notably, the levels of at least two double-stranded RNA binding (DRB) proteins DRB1 and DRB4 are reduced in the cop1 mutant background suggesting that COP1 affects HRT stability via its effect on the DRB proteins. Indeed, a mutation in either drb1 or drb4 resulted in degradation of HRT. In contrast to COP1, a multi-subunit E3 ligase encoded by anaphase-promoting complex (APC) 10 negatively regulates DRB4 and TCV resistance but had no effect on DRB1 levels. We propose that COP1-mediated positive regulation of HRT is dependent on a balance between COP1 and negative regulators that target DRB1 and DRB4.

Original language	English
Article number	e1006894
Journal	PLoS Pathogens
Volume	14
Issue number	3
DOIs	https://doi.org/10.1371/journal.ppat.1006894
State	Published - Mar 2018

Bibliographical note

Publisher Copyright:
© 2018 Public Library of Science. All Rights Reserved.

Funding

This work was supported by grants 0641576 and 0749731 from the National Science Foundation to PK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank Mattias Vermeersch and Dirk Inze for APC10 overexpressing seeds, and Arabidopsis database for seeds from DRB knockout plants. We thank John Christie for helpful suggestions. We thank Wendy Havens and Ludmila Lapchyk for technical help and Amy Crume for managing the plant growth facility.

Funders	Funder number
U.S. Department of Energy Chinese Academy of Sciences Guangzhou Municipal Science and Technology Project Oak Ridge National Laboratory Extreme Science and Engineering Discovery Environment National Science Foundation National Energy Research Scientific Computing Center National Natural Science Foundation of China	0749731
Directorate for Biological Sciences	IOS#051909

ASJC Scopus subject areas

Parasitology
Microbiology
Immunology
Molecular Biology
Genetics
Virology

Access to Document

10.1371/journal.ppat.1006894

Cite this

@article{7b1797823e254874ab5441cc69631051,

title = "COP1, a negative regulator of photomorphogenesis, positively regulates plant disease resistance via double-stranded RNA binding proteins",

abstract = "The E3 ubiquitin ligase COP1 (Constitutive Photomorphogenesis 1) is a well known component of the light-mediated plant development that acts as a repressor of photomorphogenesis. Here we show that COP1 positively regulates defense against turnip crinkle virus (TCV) and avrRPM1 bacteria by contributing to stability of resistance (R) protein HRT and RPM1, respectively. HRT and RPM1 levels and thereby pathogen resistance is significantly reduced in the cop1 mutant background. Notably, the levels of at least two double-stranded RNA binding (DRB) proteins DRB1 and DRB4 are reduced in the cop1 mutant background suggesting that COP1 affects HRT stability via its effect on the DRB proteins. Indeed, a mutation in either drb1 or drb4 resulted in degradation of HRT. In contrast to COP1, a multi-subunit E3 ligase encoded by anaphase-promoting complex (APC) 10 negatively regulates DRB4 and TCV resistance but had no effect on DRB1 levels. We propose that COP1-mediated positive regulation of HRT is dependent on a balance between COP1 and negative regulators that target DRB1 and DRB4.",

author = "Lim, \{Gah Hyun\} and Timothy Hoey and Shifeng Zhu and Marion Clavel and Keshun Yu and Duroy Navarre and Aardra Kachroo and Deragon, \{Jean Marc\} and Pradeep Kachroo",

year = "2018",

month = mar,

doi = "10.1371/journal.ppat.1006894",

language = "English",

volume = "14",

number = "3",

}

TY - JOUR

T1 - COP1, a negative regulator of photomorphogenesis, positively regulates plant disease resistance via double-stranded RNA binding proteins

AU - Lim, Gah Hyun

AU - Hoey, Timothy

AU - Zhu, Shifeng

AU - Clavel, Marion

AU - Yu, Keshun

AU - Navarre, Duroy

AU - Kachroo, Aardra

AU - Deragon, Jean Marc

AU - Kachroo, Pradeep

PY - 2018/3

Y1 - 2018/3

N2 - The E3 ubiquitin ligase COP1 (Constitutive Photomorphogenesis 1) is a well known component of the light-mediated plant development that acts as a repressor of photomorphogenesis. Here we show that COP1 positively regulates defense against turnip crinkle virus (TCV) and avrRPM1 bacteria by contributing to stability of resistance (R) protein HRT and RPM1, respectively. HRT and RPM1 levels and thereby pathogen resistance is significantly reduced in the cop1 mutant background. Notably, the levels of at least two double-stranded RNA binding (DRB) proteins DRB1 and DRB4 are reduced in the cop1 mutant background suggesting that COP1 affects HRT stability via its effect on the DRB proteins. Indeed, a mutation in either drb1 or drb4 resulted in degradation of HRT. In contrast to COP1, a multi-subunit E3 ligase encoded by anaphase-promoting complex (APC) 10 negatively regulates DRB4 and TCV resistance but had no effect on DRB1 levels. We propose that COP1-mediated positive regulation of HRT is dependent on a balance between COP1 and negative regulators that target DRB1 and DRB4.

AB - The E3 ubiquitin ligase COP1 (Constitutive Photomorphogenesis 1) is a well known component of the light-mediated plant development that acts as a repressor of photomorphogenesis. Here we show that COP1 positively regulates defense against turnip crinkle virus (TCV) and avrRPM1 bacteria by contributing to stability of resistance (R) protein HRT and RPM1, respectively. HRT and RPM1 levels and thereby pathogen resistance is significantly reduced in the cop1 mutant background. Notably, the levels of at least two double-stranded RNA binding (DRB) proteins DRB1 and DRB4 are reduced in the cop1 mutant background suggesting that COP1 affects HRT stability via its effect on the DRB proteins. Indeed, a mutation in either drb1 or drb4 resulted in degradation of HRT. In contrast to COP1, a multi-subunit E3 ligase encoded by anaphase-promoting complex (APC) 10 negatively regulates DRB4 and TCV resistance but had no effect on DRB1 levels. We propose that COP1-mediated positive regulation of HRT is dependent on a balance between COP1 and negative regulators that target DRB1 and DRB4.

UR - http://www.scopus.com/inward/record.url?scp=85044838530&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85044838530&partnerID=8YFLogxK

U2 - 10.1371/journal.ppat.1006894

DO - 10.1371/journal.ppat.1006894

M3 - Article

C2 - 29513740

AN - SCOPUS:85044838530

SN - 1553-7366

VL - 14

JO - PLoS Pathogens

JF - PLoS Pathogens

IS - 3

M1 - e1006894

ER -

COP1, a negative regulator of photomorphogenesis, positively regulates plant disease resistance via double-stranded RNA binding proteins

Abstract

Bibliographical note

Funding

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this