First published online February 21, 2003; 10.1105/tpc.009159
The Plant Cell, Vol. 15, 760-770,
March 2003, Copyright © 2003,
American Society of Plant Biologists
NPR1 Modulates Cross-Talk between Salicylate- and Jasmonate-Dependent Defense Pathways through a Novel Function in the Cytosol
Steven H. Spoela,b,
Annemart Koornneefa,
Susanne M. C. Claessensa,
Jerôme P. Korzeliusa,
Johan A. Van Pelta,
Martin J. Muellerc,
Antony J. Buchalad,
Jean-Pierre Métrauxd,
Rebecca Browne,
Kemal Kazane,
L. C. Van Loona,
Xinnian Dongb and
Corné M. J. Pieterse1,a
a Graduate School of Experimental Plant Sciences, Section of Phytopathology, Faculty of Biology, Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, The Netherlands
b Developmental, Cell, and Molecular Biology Group, Department of Biology, Duke University, Durham, North Carolina 27708-1000
c Pharmaceutical Biology, Julius-von-Sachs Institute of Biological Sciences, University of Wuerzburg, D-97082 Wuerzburg, Germany
d Department of Biology, University of Fribourg, CH-1700 Fribourg, Switzerland
e Cooperative Research Centre for Tropical Plant Pathology, University of Queensland, St. Lucia, Queensland 4072, Australia
1 To whom correspondence should be addressed. E-mail c.m.j.pieterse{at}bio.uu.nl; fax 31-30-2518366
Plant defenses against pathogens and insects are regulated differentially by cross-communicating signal transduction pathways in which salicylic acid (SA) and jasmonic acid (JA) play key roles. In this study, we investigated the molecular mechanism of the antagonistic effect of SA on JA signaling. Arabidopsis plants unable to accumulate SA produced 25-fold higher levels of JA and showed enhanced expression of the JA-responsive genes LOX2, PDF1.2, and VSP in response to infection by Pseudomonas syringae pv tomato DC3000, indicating that in wild-type plants, pathogen-induced SA accumulation is associated with the suppression of JA signaling. Analysis of the Arabidopsis mutant npr1, which is impaired in SA signal transduction, revealed that the antagonistic effect of SA on JA signaling requires the regulatory protein NPR1. Nuclear localization of NPR1, which is essential for SA-mediated defense gene expression, is not required for the suppression of JA signaling, indicating that cross-talk between SA and JA is modulated through a novel function of NPR1 in the cytosol.
This article has been cited by other articles:

|
 |

|
 |
 
R. D. Girling, R. Madison, M. Hassall, G. M. Poppy, and J. G. Turner
Investigations into plant biochemical wound-response pathways involved in the production of aphid-induced plant volatiles
J. Exp. Bot.,
August 1, 2008;
59(11):
3077 - 3085.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Koornneef, A. Leon-Reyes, T. Ritsema, A. Verhage, F. C. Den Otter, L.C. Van Loon, and C. M.J. Pieterse
Kinetics of Salicylate-Mediated Suppression of Jasmonate Signaling Reveal a Role for Redox Modulation
Plant Physiology,
July 1, 2008;
147(3):
1358 - 1368.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M.-H. Weech, M. Chapleau, L. Pan, C. Ide, and J. C. Bede
Caterpillar saliva interferes with induced Arabidopsis thaliana defence responses via the systemic acquired resistance pathway
J. Exp. Bot.,
June 1, 2008;
59(9):
2437 - 2448.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Yasuda, A. Ishikawa, Y. Jikumaru, M. Seki, T. Umezawa, T. Asami, A. Maruyama-Nakashita, T. Kudo, K. Shinozaki, S. Yoshida, et al.
Antagonistic Interaction between Systemic Acquired Resistance and the Abscisic Acid-Mediated Abiotic Stress Response in Arabidopsis
PLANT CELL,
June 1, 2008;
20(6):
1678 - 1692.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D.-L. Yang, Q. Li, Y.-W. Deng, Y.-G. Lou, M.-Y. Wang, G.-X. Zhou, Y.-Y. Zhang, and Z.-H. He
Altered Disease Development in the eui Mutants and Eui Overexpressors Indicates that Gibberellins Negatively Regulate Rice Basal Disease Resistance
Mol Plant,
May 13, 2008;
(2008)
ssn021v2.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Zhang, A. Lenk, M. X. Andersson, T. Gjetting, C. Pedersen, M. E. Nielsen, M.-A. Newman, B.-H. Hou, S. C. Somerville, and H. Thordal-Christensen
A Lesion-Mimic Syntaxin Double Mutant in Arabidopsis Reveals Novel Complexity of Pathogen Defense Signaling
Mol Plant,
May 1, 2008;
1(3):
510 - 527.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Li, H. Liu, H. Zhang, X. Wang, and F. Song
OsBIRH1, a DEAD-box RNA helicase with functions in modulating defence responses against pathogen infection and oxidative stress
J. Exp. Bot.,
May 1, 2008;
59(8):
2133 - 2146.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Herde, K. Gartner, T. G. Kollner, B. Fode, W. Boland, J. Gershenzon, C. Gatz, and D. Tholl
Identification and Regulation of TPS04/GES, an Arabidopsis Geranyllinalool Synthase Catalyzing the First Step in the Formation of the Insect-Induced Volatile C16-Homoterpene TMTT
PLANT CELL,
April 1, 2008;
20(4):
1152 - 1168.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Kazan and J. M. Manners
Jasmonate Signaling: Toward an Integrated View
Plant Physiology,
April 1, 2008;
146(4):
1459 - 1468.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Koornneef and C. M.J. Pieterse
Cross Talk in Defense Signaling
Plant Physiology,
March 1, 2008;
146(3):
839 - 844.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. B. Runyon, M. C. Mescher, and C. M. De Moraes
Parasitism by Cuscuta pentagona Attenuates Host Plant Defenses against Insect Herbivores
Plant Physiology,
March 1, 2008;
146(3):
987 - 995.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Fabro, J. A. Di Rienzo, C. A. Voigt, T. Savchenko, K. Dehesh, S. Somerville, and M. E. Alvarez
Genome-Wide Expression Profiling Arabidopsis at the Stage of Golovinomyces cichoracearum Haustorium Formation
Plant Physiology,
March 1, 2008;
146(3):
1421 - 1439.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Anand, S. R. Uppalapati, C.-M. Ryu, S. N. Allen, L. Kang, Y. Tang, and K. S. Mysore
Salicylic Acid and Systemic Acquired Resistance Play a Role in Attenuating Crown Gall Disease Caused by Agrobacterium tumefaciens
Plant Physiology,
February 1, 2008;
146(2):
703 - 715.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. B. Rossel, P. B. Wilson, D. Hussain, N. S. Woo, M. J. Gordon, O. P. Mewett, K. A. Howell, J. Whelan, K. Kazan, and B. J. Pogson
Systemic and Intracellular Responses to Photooxidative Stress in Arabidopsis
PLANT CELL,
December 1, 2007;
19(12):
4091 - 4110.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M.-Y. Cheung, N.-Y. Zeng, S.-W. Tong, F. Wing-Yen Li, K.-J. Zhao, Q. Zhang, S. Sai-Ming Sun, and H.-M. Lam
Expression of a RING-HC protein from rice improves resistance to Pseudomonas syringae pv. tomato DC3000 in transgenic Arabidopsis thaliana
J. Exp. Bot.,
December 1, 2007;
58(15-16):
4147 - 4159.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. H. Spoel, J. S. Johnson, and X. Dong
Regulation of tradeoffs between plant defenses against pathogens with different lifestyles
PNAS,
November 20, 2007;
104(47):
18842 - 18847.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Yan, S. Stolz, A. Chetelat, P. Reymond, M. Pagni, L. Dubugnon, and E. E. Farmer
A Downstream Mediator in the Growth Repression Limb of the Jasmonate Pathway
PLANT CELL,
August 1, 2007;
19(8):
2470 - 2483.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Mao, M. Duan, C. Wei, and Y. Li
WRKY62 Transcription Factor Acts Downstream of Cytosolic NPR1 and Negatively Regulates Jasmonate-Responsive Gene Expression
Plant Cell Physiol.,
June 1, 2007;
48(6):
833 - 842.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. A.T. Adie, J. Perez-Perez, M. M. Perez-Perez, M. Godoy, J.-J. Sanchez-Serrano, E. A. Schmelz, and R. Solano
ABA Is an Essential Signal for Plant Resistance to Pathogens Affecting JA Biosynthesis and the Activation of Defenses in Arabidopsis
PLANT CELL,
May 1, 2007;
19(5):
1665 - 1681.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Heiber, E. Stroher, B. Raatz, I. Busse, U. Kahmann, M. W. Bevan, K.-J. Dietz, and M. Baier
The redox imbalanced Mutants of Arabidopsis Differentiate Signaling Pathways for Redox Regulation of Chloroplast Antioxidant Enzymes
Plant Physiology,
April 1, 2007;
143(4):
1774 - 1788.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Miao and U. Zentgraf
The Antagonist Function of Arabidopsis WRKY53 and ESR/ESP in Leaf Senescence Is Modulated by the Jasmonic and Salicylic Acid Equilibrium
PLANT CELL,
March 1, 2007;
19(3):
819 - 830.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Little, C. Gouhier-Darimont, F. Bruessow, and P. Reymond
Oviposition by Pierid Butterflies Triggers Defense Responses in Arabidopsis
Plant Physiology,
February 1, 2007;
143(2):
784 - 800.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. I. Zarate, L. A. Kempema, and L. L. Walling
Silverleaf Whitefly Induces Salicylic Acid Defenses and Suppresses Effectual Jasmonic Acid Defenses
Plant Physiology,
February 1, 2007;
143(2):
866 - 875.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Truman, M. H. Bennett, I. Kubigsteltig, C. Turnbull, and M. Grant
Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates
PNAS,
January 16, 2007;
104(3):
1075 - 1080.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Bulow, M. Schindler, and R. Hehl
PathoPlant(R): a platform for microarray expression data to analyze co-regulated genes involved in plant defense responses
Nucleic Acids Res.,
January 12, 2007;
35(suppl_1):
D841 - D845.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. De Vos, W. Van Zaanen, A. Koornneef, J. P. Korzelius, M. Dicke, L.C. Van Loon, and C. M.J. Pieterse
Herbivore-Induced Resistance against Microbial Pathogens in Arabidopsis
Plant Physiology,
September 1, 2006;
142(1):
352 - 363.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X. Xu, C. Chen, B. Fan, and Z. Chen
Physical and Functional Interactions between Pathogen-Induced Arabidopsis WRKY18, WRKY40, and WRKY60 Transcription Factors
PLANT CELL,
May 1, 2006;
18(5):
1310 - 1326.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. A. Thompson and F. L. Goggin
Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects
J. Exp. Bot.,
March 1, 2006;
57(4):
755 - 766.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Liechti, A. Gfeller, and E. E. Farmer
Jasmonate Signaling Pathway
Sci. Signal.,
February 14, 2006;
2006(322):
cm2 - cm2.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Veronese, H. Nakagami, B. Bluhm, S. AbuQamar, X. Chen, J. Salmeron, R. A. Dietrich, H. Hirt, and T. Mengiste
The Membrane-Anchored BOTRYTIS-INDUCED KINASE1 Plays Distinct Roles in Arabidopsis Resistance to Necrotrophic and Biotrophic Pathogens
PLANT CELL,
January 1, 2006;
18(1):
257 - 273.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. A.J. Mur, P. Kenton, R. Atzorn, O. Miersch, and C. Wasternack
The Outcomes of Concentration-Specific Interactions between Salicylate and Jasmonate Signaling Include Synergy, Antagonism, and Oxidative Stress Leading to Cell Death
Plant Physiology,
January 1, 2006;
140(1):
249 - 262.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. P. Delmer
Inaugural Article: Agriculture in the developing world: Connecting innovations in plant research to downstream applications
PNAS,
November 1, 2005;
102(44):
15739 - 15746.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. C. McGrath, B. Dombrecht, J. M. Manners, P. M. Schenk, C. I. Edgar, D. J. Maclean, W.-R. Scheible, M. K. Udvardi, and K. Kazan
Repressor- and Activator-Type Ethylene Response Factors Functioning in Jasmonate Signaling and Disease Resistance Identified via a Genome-Wide Screen of Arabidopsis Transcription Factor Gene Expression
Plant Physiology,
October 1, 2005;
139(2):
949 - 959.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Coego, V. Ramirez, M. J. Gil, V. Flors, B. Mauch-Mani, and P. Vera
An Arabidopsis Homeodomain Transcription Factor, OVEREXPRESSOR OF CATIONIC PEROXIDASE 3, Mediates Resistance to Infection by Necrotrophic Pathogens
PLANT CELL,
July 1, 2005;
17(7):
2123 - 2137.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Mewis, H. M. Appel, A. Hom, R. Raina, and J. C. Schultz
Major Signaling Pathways Modulate Arabidopsis Glucosinolate Accumulation and Response to Both Phloem-Feeding and Chewing Insects
Plant Physiology,
June 1, 2005;
138(2):
1149 - 1162.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. A. Salzman, J. A. Brady, S. A. Finlayson, C. D. Buchanan, E. J. Summer, F. Sun, P. E. Klein, R. R. Klein, L. H. Pratt, M.-M. Cordonnier-Pratt, et al.
Transcriptional Profiling of Sorghum Induced by Methyl Jasmonate, Salicylic Acid, and Aminocyclopropane Carboxylic Acid Reveals Cooperative Regulation and Novel Gene Responses
Plant Physiology,
May 1, 2005;
138(1):
352 - 368.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. R. Weigel, U. M. Pfitzner, and C. Gatz
Interaction of NIMIN1 with NPR1 Modulates PR Gene Expression in Arabidopsis
PLANT CELL,
April 1, 2005;
17(4):
1279 - 1291.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Cui, A. K. Bahrami, E. G. Pringle, G. Hernandez-Guzman, C. L. Bender, N. E. Pierce, and F. M. Ausubel
Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores
PNAS,
February 1, 2005;
102(5):
1791 - 1796.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Kariola, G. Brader, J. Li, and E. T. Palva
Chlorophyllase 1, a Damage Control Enzyme, Affects the Balance between Defense Pathways in Plants
PLANT CELL,
January 1, 2005;
17(1):
282 - 294.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. P. Anderson, E. Badruzsaufari, P. M. Schenk, J. M. Manners, O. J. Desmond, C. Ehlert, D. J. Maclean, P. R. Ebert, and K. Kazan
Antagonistic Interaction between Abscisic Acid and Jasmonate-Ethylene Signaling Pathways Modulates Defense Gene Expression and Disease Resistance in Arabidopsis
PLANT CELL,
December 1, 2004;
16(12):
3460 - 3479.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H.-P. Dong, J. Peng, Z. Bao, X. Meng, J. M. Bonasera, G. Chen, S. V. Beer, and H. Dong
Downstream Divergence of the Ethylene Signaling Pathway for Harpin-Stimulated Arabidopsis Growth and Insect Defense
Plant Physiology,
November 1, 2004;
136(3):
3628 - 3638.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Ament, M. R. Kant, M. W. Sabelis, M. A. Haring, and R. C. Schuurink
Jasmonic Acid Is a Key Regulator of Spider Mite-Induced Volatile Terpenoid and Methyl Salicylate Emission in Tomato
Plant Physiology,
August 1, 2004;
135(4):
2025 - 2037.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Eulgem, V. J. Weigman, H.-S. Chang, J. M. McDowell, E. B. Holub, J. Glazebrook, T. Zhu, and J. L. Dangl
Gene Expression Signatures from Three Genetically Separable Resistance Gene Signaling Pathways for Downy Mildew Resistance
Plant Physiology,
June 1, 2004;
135(2):
1129 - 1144.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. S. Thaler, B. Owen, and V. J. Higgins
The Role of the Jasmonate Response in Plant Susceptibility to Diverse Pathogens with a Range of Lifestyles
Plant Physiology,
May 1, 2004;
135(1):
530 - 538.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Li, G. Brader, and E. T. Palva
The WRKY70 Transcription Factor: A Node of Convergence for Jasmonate-Mediated and Salicylate-Mediated Signals in Plant Defense
PLANT CELL,
February 1, 2004;
16(2):
319 - 331.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Kumar and D. F. Klessig
High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity
PNAS,
December 23, 2003;
100(26):
16101 - 16106.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Kachroo, L. Lapchyk, H. Fukushige, D. Hildebrand, D. Klessig, and P. Kachroo
Plastidial Fatty Acid Signaling Modulates Salicylic Acid- and Jasmonic Acid-Mediated Defense Pathways in the Arabidopsis ssi2 Mutant
PLANT CELL,
December 1, 2003;
15(12):
2952 - 2965.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. B. Traw and J. Bergelson
Interactive Effects of Jasmonic Acid, Salicylic Acid, and Gibberellin on Induction of Trichomes in Arabidopsis
Plant Physiology,
November 1, 2003;
133(3):
1367 - 1375.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Despres, C. Chubak, A. Rochon, R. Clark, T. Bethune, D. Desveaux, and P. R. Fobert
The Arabidopsis NPR1 Disease Resistance Protein Is a Novel Cofactor That Confers Redox Regulation of DNA Binding Activity to the Basic Domain/Leucine Zipper Transcription Factor TGA1
PLANT CELL,
September 1, 2003;
15(9):
2181 - 2191.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. T. Nishimura, M. Stein, B.-H. Hou, J. P. Vogel, H. Edwards, and S. C. Somerville
Loss of a Callose Synthase Results in Salicylic Acid-Dependent Disease Resistance
Science,
August 15, 2003;
301(5635):
969 - 972.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|