skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: A Genetic Screen Identifies a Requirement for Cysteine-Rich–Receptor-Like Kinases in Rice NH1 (OsNPR1)-Mediated Immunity

Abstract

Systemic acquired resistance, mediated by the Arabidopsis NPR1 gene and the rice NH1 gene, confers broad-spectrum immunity to diverse pathogens. NPR1 and NH1 interact with TGA transcription factors to activate downstream defense genes. Despite the importance of this defense response, the signaling components downstream of NPR1/NH1 and TGA proteins are poorly defined. Here we report the identification of a rice mutant, snim1, which suppresses NH1-mediated immunity and demonstrate that two genes encoding previously uncharacterized cysteine-rich-receptor-like kinases (CRK6 and CRK10), complement the snim1 mutant phenotype. Silencing of CRK6 and CRK10 genes individually in the parental genetic background recreates the snim1 phenotype. We identified a rice mutant in the Kitaake genetic background with a frameshift mutation in crk10; this mutant also displays a compromised immune response highlighting the important role of crk10. We also show that elevated levels of NH1 expression lead to enhanced CRK10 expression and that the rice TGA2.1 protein binds to the CRK10 promoter. Furthermore, these experiments demonstrate a requirement for CRKs in NH1-mediated immunity and establish a molecular link between NH1 and induction of CRK10 expression.

Authors:
; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Univ. of California, Davis, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1338422
Alternate Identifier(s):
OSTI ID: 1288267
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
PLoS Genetics
Additional Journal Information:
Journal Name: PLoS Genetics Journal Volume: 12 Journal Issue: 5; Journal ID: ISSN 1553-7404
Publisher:
Public Library of Science (PLoS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; systemic acquired-resistance; enhanced disease resistance; lesion mimic mutants; salicylic-acid; transcription factors; arabidopsis npr1; pseudomonas-syringae; negative regulator; xanthomonas-oryzae; btb/poz domain

Citation Formats

Chern, Mawsheng, Xu, Qiufang, Bart, Rebecca S., Bai, Wei, Ruan, Deling, Sze-To, Wing Hoi, Canlas, Patrick E., Jain, Rashmi, Chen, Xuewei, Ronald, Pamela C., and Wang, ed., Guo-Liang. A Genetic Screen Identifies a Requirement for Cysteine-Rich–Receptor-Like Kinases in Rice NH1 (OsNPR1)-Mediated Immunity. United States: N. p., 2016. Web. doi:10.1371/journal.pgen.1006049.
Chern, Mawsheng, Xu, Qiufang, Bart, Rebecca S., Bai, Wei, Ruan, Deling, Sze-To, Wing Hoi, Canlas, Patrick E., Jain, Rashmi, Chen, Xuewei, Ronald, Pamela C., & Wang, ed., Guo-Liang. A Genetic Screen Identifies a Requirement for Cysteine-Rich–Receptor-Like Kinases in Rice NH1 (OsNPR1)-Mediated Immunity. United States. doi:10.1371/journal.pgen.1006049.
Chern, Mawsheng, Xu, Qiufang, Bart, Rebecca S., Bai, Wei, Ruan, Deling, Sze-To, Wing Hoi, Canlas, Patrick E., Jain, Rashmi, Chen, Xuewei, Ronald, Pamela C., and Wang, ed., Guo-Liang. Fri . "A Genetic Screen Identifies a Requirement for Cysteine-Rich–Receptor-Like Kinases in Rice NH1 (OsNPR1)-Mediated Immunity". United States. doi:10.1371/journal.pgen.1006049.
@article{osti_1338422,
title = {A Genetic Screen Identifies a Requirement for Cysteine-Rich–Receptor-Like Kinases in Rice NH1 (OsNPR1)-Mediated Immunity},
author = {Chern, Mawsheng and Xu, Qiufang and Bart, Rebecca S. and Bai, Wei and Ruan, Deling and Sze-To, Wing Hoi and Canlas, Patrick E. and Jain, Rashmi and Chen, Xuewei and Ronald, Pamela C. and Wang, ed., Guo-Liang},
abstractNote = {Systemic acquired resistance, mediated by the Arabidopsis NPR1 gene and the rice NH1 gene, confers broad-spectrum immunity to diverse pathogens. NPR1 and NH1 interact with TGA transcription factors to activate downstream defense genes. Despite the importance of this defense response, the signaling components downstream of NPR1/NH1 and TGA proteins are poorly defined. Here we report the identification of a rice mutant, snim1, which suppresses NH1-mediated immunity and demonstrate that two genes encoding previously uncharacterized cysteine-rich-receptor-like kinases (CRK6 and CRK10), complement the snim1 mutant phenotype. Silencing of CRK6 and CRK10 genes individually in the parental genetic background recreates the snim1 phenotype. We identified a rice mutant in the Kitaake genetic background with a frameshift mutation in crk10; this mutant also displays a compromised immune response highlighting the important role of crk10. We also show that elevated levels of NH1 expression lead to enhanced CRK10 expression and that the rice TGA2.1 protein binds to the CRK10 promoter. Furthermore, these experiments demonstrate a requirement for CRKs in NH1-mediated immunity and establish a molecular link between NH1 and induction of CRK10 expression.},
doi = {10.1371/journal.pgen.1006049},
journal = {PLoS Genetics},
number = 5,
volume = 12,
place = {United States},
year = {2016},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1371/journal.pgen.1006049

Citation Metrics:
Cited by: 3 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants?
journal, June 2003


Alteration of TGA factor activity in rice results in enhanced tolerance to Xanthomonas oryzae pv. oryzae: Role of rice TGA factors in bacterial tolerance
journal, July 2005


Plant and Animal Sensors of Conserved Microbial Signatures
journal, November 2010


Systemic Acquired Resistance
journal, September 2004


Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance.
journal, July 1995

  • Delaney, T. P.; Friedrich, L.; Ryals, J. A.
  • Proceedings of the National Academy of Sciences, Vol. 92, Issue 14
  • DOI: 10.1073/pnas.92.14.6602

Reduced expression of glycolate oxidase leads to enhanced disease resistance in rice
journal, January 2013


NLR functions in plant and animal immune systems: so far and yet so close
journal, August 2011

  • Maekawa, Takaki; Kufer, Thomas A.; Schulze-Lefert, Paul
  • Nature Immunology, Vol. 12, Issue 9
  • DOI: 10.1038/ni.2083

Mode of action of acibenzolar- S -methyl against sheath blight of rice, caused by Rhizoctonia solani Kühn : Mode of action of acibenzolar-
journal, December 2001

  • Rohilla, Rashmi; Singh, U. S.; Singh, R. L.
  • Pest Management Science, Vol. 58, Issue 1
  • DOI: 10.1002/ps.423

Arabidopsis cysteine-rich receptor-like kinase 45 positively regulates disease resistance to Pseudomonas syringae
journal, December 2013


Rice WRKY45 Plays a Crucial Role in Benzothiadiazole-Inducible Blast Resistance
journal, June 2007

  • Shimono, Masaki; Sugano, Shoji; Nakayama, Akira
  • The Plant Cell, Vol. 19, Issue 6
  • DOI: 10.1105/tpc.106.046250

Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance.
journal, October 1991


Probenazole induces systemic acquired resistance in Arabidopsis with a novel type of action
journal, January 2001


The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium
journal, July 2015

  • Pruitt, Rory N.; Schwessinger, Benjamin; Joe, Anna
  • Science Advances, Vol. 1, Issue 6
  • DOI: 10.1126/sciadv.1500245

Cysteine-rich receptor-like kinase CRK5 as a regulator of growth, development, and ultraviolet radiation responses in Arabidopsis thaliana
journal, May 2015

  • Burdiak, Paweł; Rusaczonek, Anna; Witoń, Damian
  • Journal of Experimental Botany, Vol. 66, Issue 11
  • DOI: 10.1093/jxb/erv143

The BTB/POZ Domain of the Arabidopsis Disease Resistance Protein NPR1 Interacts with the Repression Domain of TGA2 to Negate Its Function
journal, November 2009


The Arabidopsis NPR1 Protein Is a Receptor for the Plant Defense Hormone Salicylic Acid
journal, June 2012


A Superfamily of Proteins with Novel Cysteine-Rich Repeats
journal, June 2001


Overexpression of a Rice NPR1 Homolog Leads to Constitutive Activation of Defense Response and Hypersensitivity to Light
journal, June 2005

  • Chern, Mawsheng; Fitzgerald, Heather A.; Canlas, Patrick E.
  • Molecular Plant-Microbe Interactions, Vol. 18, Issue 6
  • DOI: 10.1094/MPMI-18-0511

The Arabidopsis thaliana cysteine-rich receptor-like kinase CRK20 modulates host responses to Pseudomonas syringae pv. tomato DC3000 infection
journal, October 2011


An XA21-Associated Kinase (OsSERK2) Regulates Immunity Mediated by the XA21 and XA3 Immune Receptors
journal, May 2014

  • Chen, Xuewei; Zuo, Shimin; Schwessinger, Benjamin
  • Molecular Plant, Vol. 7, Issue 5
  • DOI: 10.1093/mp/ssu003

NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants
journal, May 2012

  • Fu, Zheng Qing; Yan, Shunping; Saleh, Abdelaty
  • Nature, Vol. 486, Issue 7402
  • DOI: 10.1038/nature11162

Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance.
journal, November 1994


Knockout Analysis of Arabidopsis Transcription Factors TGA2 , TGA5 , and TGA6 Reveals Their Redundant and Essential Roles in Systemic Acquired Resistance
journal, October 2003

  • Zhang, Yuelin; Tessaro, Mark J.; Lassner, Michael
  • The Plant Cell, Vol. 15, Issue 11
  • DOI: 10.1105/tpc.014894

Interaction of NIMIN1 with NPR1 Modulates PR Gene Expression in Arabidopsis
journal, March 2005

  • Weigel, Ralf R.; Pfitzner, Ursula M.; Gatz, Christiane
  • The Plant Cell, Vol. 17, Issue 4
  • DOI: 10.1105/tpc.104.027441

NIM1 Overexpression in Arabidopsis Potentiates Plant Disease Resistance and Results in Enhanced Effectiveness of Fungicides
journal, September 2001

  • Friedrich, Leslie; Lawton, Kay; Dietrich, Robert
  • Molecular Plant-Microbe Interactions, Vol. 14, Issue 9
  • DOI: 10.1094/MPMI.2001.14.9.1114

The Coactivator Function of Arabidopsis NPR1 Requires the Core of Its BTB/POZ Domain and the Oxidation of C-Terminal Cysteines
journal, December 2006


Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat.
journal, April 1996

  • Görlach, J.; Volrath, S.; Knauf-Beiter, G.
  • The Plant Cell, Vol. 8, Issue 4
  • DOI: 10.1105/tpc.8.4.629

Identification and distribution of the NBS-LRR gene family in the Cassava genome
journal, May 2015


The Arabidopsis NPR1 Gene That Controls Systemic Acquired Resistance Encodes a Novel Protein Containing Ankyrin Repeats
journal, January 1997


Transcriptional regulation of the CRK/DUF26 group of Receptor-like protein kinases by ozone and plant hormones in Arabidopsis
journal, January 2010

  • Wrzaczek, Michael; Brosché, Mikael; Salojärvi, Jarkko
  • BMC Plant Biology, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2229-10-95

The Arabidopsis NPR1/NIM1 Protein Enhances the DNA Binding Activity of a Subgroup of the TGA Family of bZIP Transcription Factors
journal, February 2000

  • Després, Charles; DeLong, Catherine; Glaze, Sarah
  • The Plant Cell, Vol. 12, Issue 2
  • DOI: 10.1105/tpc.12.2.279

Enhanced disease resistance and hypersensitivity to BTH by introduction of an NH1/OsNPR1 paralog: Enhanced disease resistance by NH3
journal, January 2011


A glucocorticoid-mediated transcriptional induction system in transgenic plants
journal, March 1997


Salicylic Acid, a Multifaceted Hormone to Combat Disease
journal, September 2009


Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene
journal, May 1999

  • Zhang, Y.; Fan, W.; Kinkema, M.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 11
  • DOI: 10.1073/pnas.96.11.6523

Characterizing Rice Lesion Mimic Mutants and Identifying a Mutant with Broad-Spectrum Resistance to Rice Blast and Bacterial Blight
journal, August 2000


Rice NRR, a negative regulator of disease resistance, interacts with Arabidopsis NPR1 and rice NH1: NRR, a negative regulator of resistance
journal, August 2005


Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance
journal, May 1998

  • Cao, H.; Li, X.; Dong, X.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 11
  • DOI: 10.1073/pnas.95.11.6531

The Arabidopsis NIMIN proteins affect NPR1 differentially
journal, January 2013


A benzothiadiazole derivative induces systemic acquired resistance in tobacco
journal, July 1996


Sensitization of defense responses and activation of programmed cell death by a pathogen-induced receptor-like protein kinase in Arabidopsis
journal, September 2003


Rice Snl6, a Cinnamoyl-CoA Reductase-Like Gene Family Member, Is Required for NH1-Mediated Immunity to Xanthomonas oryzae pv. oryzae
journal, September 2010

  • Bart, Rebecca S.; Chern, Mawsheng; Vega-Sánchez, Miguel E.
  • PLoS Genetics, Vol. 6, Issue 9, Article No. e1001123
  • DOI: 10.1371/journal.pgen.1001123

    Works referencing / citing this record:

    Cas9/sgRNA-based genome editing and other reverse genetic approaches for functional genomic studies in rice
    journal, March 2018

    • Moin, Mazahar; Bakshi, Achala; Madhav, M. S.
    • Briefings in Functional Genomics, Vol. 17, Issue 5
    • DOI: 10.1093/bfgp/ely010