Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana
Abstract
Network robustness is a crucial property of the plant immune signaling network because pathogens are under a strong selection pressure to perturb plant network components to dampen plant immune responses. Nevertheless, modulation of network robustness is an area of network biology that has rarely been explored. While two modes of plant immunity, Effector-Triggered Immunity (ETI) and Pattern-Triggered Immunity (PTI), extensively share signaling machinery, the network output is much more robust against perturbations during ETI than PTI, suggesting modulation of network robustness. Here, we report a molecular mechanism underlying the modulation of the network robustness in Arabidopsis thaliana. The salicylic acid (SA) signaling sector regulates a major portion of the plant immune response and is important in immunity against biotrophic and hemibiotrophic pathogens. In Arabidopsis, SA signaling was required for the proper regulation of the vast majority of SA-responsive genes during PTI. However, during ETI, regulation of most SA-responsive genes, including the canonical SA marker gene PR1, could be controlled by SA-independent mechanisms as well as by SA. The activation of the two immune-related MAPKs, MPK3 and MPK6, persisted for several hours during ETI but less than one hour during PTI. Sustained MAPK activation was sufficient to confer SA-independent regulation ofmore »
- Authors:
-
- Max Planck Institute for Plant Breeding Research, Cologne (Germany); University of Minnesota, Minneapolis, MN (United States)
- Max Planck Institute for Plant Breeding Research, Cologne (Germany)
- University of Minnesota, Minneapolis, MN (United States)
- University of Minnesota, Minneapolis, MN (United States); Institute for Innovation, Ajinomoto Co., Inc., Kawasaki (Japan)
- Chicago State University, IL (United States)
- National Institutes of Natural Sciences, Okazaki (Japan)
- Publication Date:
- Research Org.:
- Univ. of Minnesota, Minneapolis, MN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB); Max Planck Society; National Science Foundation (NSF); Japan Society for the Promotion of Science (JSPS)
- OSTI Identifier:
- 1904660
- Grant/Contract Number:
- FG02-05ER15670; MCB-0918908; IOS-1121425
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Genetics
- Additional Journal Information:
- Journal Volume: 9; Journal Issue: 12; Journal ID: ISSN 1553-7404
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; MAPK signaling cascades; gene regulation; leaves; Arabidopsis thaliana; signaling networks; gene expression; plant disease resistance; seedings
Citation Formats
Tsuda, Kenichi, Mine, Akira, Bethke, Gerit, Igarashi, Daisuke, Botanga, Christopher J., Tsuda, Yayoi, Glazebrook, Jane, Sato, Masanao, and Katagiri, Fumiaki. Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana. United States: N. p., 2013.
Web. doi:10.1371/journal.pgen.1004015.
Tsuda, Kenichi, Mine, Akira, Bethke, Gerit, Igarashi, Daisuke, Botanga, Christopher J., Tsuda, Yayoi, Glazebrook, Jane, Sato, Masanao, & Katagiri, Fumiaki. Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana. United States. https://doi.org/10.1371/journal.pgen.1004015
Tsuda, Kenichi, Mine, Akira, Bethke, Gerit, Igarashi, Daisuke, Botanga, Christopher J., Tsuda, Yayoi, Glazebrook, Jane, Sato, Masanao, and Katagiri, Fumiaki. Thu .
"Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana". United States. https://doi.org/10.1371/journal.pgen.1004015. https://www.osti.gov/servlets/purl/1904660.
@article{osti_1904660,
title = {Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana},
author = {Tsuda, Kenichi and Mine, Akira and Bethke, Gerit and Igarashi, Daisuke and Botanga, Christopher J. and Tsuda, Yayoi and Glazebrook, Jane and Sato, Masanao and Katagiri, Fumiaki},
abstractNote = {Network robustness is a crucial property of the plant immune signaling network because pathogens are under a strong selection pressure to perturb plant network components to dampen plant immune responses. Nevertheless, modulation of network robustness is an area of network biology that has rarely been explored. While two modes of plant immunity, Effector-Triggered Immunity (ETI) and Pattern-Triggered Immunity (PTI), extensively share signaling machinery, the network output is much more robust against perturbations during ETI than PTI, suggesting modulation of network robustness. Here, we report a molecular mechanism underlying the modulation of the network robustness in Arabidopsis thaliana. The salicylic acid (SA) signaling sector regulates a major portion of the plant immune response and is important in immunity against biotrophic and hemibiotrophic pathogens. In Arabidopsis, SA signaling was required for the proper regulation of the vast majority of SA-responsive genes during PTI. However, during ETI, regulation of most SA-responsive genes, including the canonical SA marker gene PR1, could be controlled by SA-independent mechanisms as well as by SA. The activation of the two immune-related MAPKs, MPK3 and MPK6, persisted for several hours during ETI but less than one hour during PTI. Sustained MAPK activation was sufficient to confer SA-independent regulation of most SA-responsive genes. Furthermore, the MPK3 and SA signaling sectors were compensatory to each other for inhibition of bacterial growth as well as for PR1 expression during ETI. These results indicate that the duration of the MAPK activation is a critical determinant for modulation of robustness of the immune signaling network. Our findings with the plant immune signaling network imply that the robustness level of a biological network can be modulated by the activities of network components.},
doi = {10.1371/journal.pgen.1004015},
journal = {PLoS Genetics},
number = 12,
volume = 9,
place = {United States},
year = {Thu Dec 12 00:00:00 EST 2013},
month = {Thu Dec 12 00:00:00 EST 2013}
}
Works referenced in this record:
MAP Kinase Cascades in Arabidopsis Innate Immunity
journal, January 2012
- Rasmussen, Magnus W.; Roux, Milena; Petersen, Morten
- Frontiers in Plant Science, Vol. 3
How to build a pathogen detector: structural basis of NB-LRR function
journal, August 2012
- Takken, Frank LW; Goverse, Aska
- Current Opinion in Plant Biology, Vol. 15, Issue 4
Robustness: mechanisms and consequences
journal, September 2009
- Masel, Joanna; Siegal, Mark L.
- Trends in Genetics, Vol. 25, Issue 9
Design principles for robust biochemical reaction networks: What works, what cannot work, and what might almost work
journal, May 2011
- Shinar, Guy; Feinberg, Martin
- Mathematical Biosciences, Vol. 231, Issue 1
Protein kinase signaling networks in plant innate immunity
journal, October 2011
- Tena, Guillaume; Boudsocq, Marie; Sheen, Jen
- Current Opinion in Plant Biology, Vol. 14, Issue 5
Arabidopsis EDS1 Connects Pathogen Effector Recognition to Cell Compartment-Specific Immune Responses
journal, December 2011
- Heidrich, K.; Wirthmueller, L.; Tasset, C.
- Science, Vol. 334, Issue 6061
Cell Death Mediated by MAPK Is Associated with Hydrogen Peroxide Production in Arabidopsis
journal, January 2002
- Ren, Dongtao; Yang, Heping; Zhang, Shuqun
- Journal of Biological Chemistry, Vol. 277, Issue 1
Direct Ubiquitination of Pattern Recognition Receptor FLS2 Attenuates Plant Innate Immunity
journal, June 2011
- Lu, D.; Lin, W.; Gao, X.
- Science, Vol. 332, Issue 6036
Phosphorylation of 1-Aminocyclopropane-1-Carboxylic Acid Synthase by MPK6, a Stress-Responsive Mitogen-Activated Protein Kinase, Induces Ethylene Biosynthesis in Arabidopsis
journal, November 2004
- Liu, Yidong; Zhang, Shuqun
- The Plant Cell, Vol. 16, Issue 12
An efficient Agrobacterium-mediated transient transformation of Arabidopsis: An efficient transient transformation
journal, November 2011
- Tsuda, Kenichi; Qi, Yiping; Nguyen, Le V.
- The Plant Journal, Vol. 69, Issue 4
The type III effector HopF2
Pto
targets
Arabidopsis
RIN4 protein to promote
Pseudomonas syringae
virulence
journal, January 2010
- Wilton, Mike; Subramaniam, Rajagopal; Elmore, James
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 5
Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Comparison of the effects of nerve growth factor and epidermal growth factor
journal, December 1992
- Traverse, S.; Gomez, N.; Paterson, H.
- Biochemical Journal, Vol. 288, Issue 2
Plant Innate Immunity: Perception of Conserved Microbial Signatures
journal, June 2012
- Schwessinger, Benjamin; Ronald, Pamela C.
- Annual Review of Plant Biology, Vol. 63, Issue 1
Bacterial virulence effectors and their activities
journal, August 2010
- Hann, Dagmar R.; Gimenez-Ibanez, Selena; Rathjen, John P.
- Current Opinion in Plant Biology, Vol. 13, Issue 4
The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity
journal, May 2012
- Igarashi, Daisuke; Tsuda, Kenichi; Katagiri, Fumiaki
- The Plant Journal, Vol. 71, Issue 2
Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity
journal, August 2010
- Tsuda, Kenichi; Katagiri, Fumiaki
- Current Opinion in Plant Biology, Vol. 13, Issue 4
Dual-Level Regulation of ACC Synthase Activity by MPK3/MPK6 Cascade and Its Downstream WRKY Transcription Factor during Ethylene Induction in Arabidopsis
journal, June 2012
- Li, Guojing; Meng, Xiangzong; Wang, Ruigang
- PLoS Genetics, Vol. 8, Issue 6
The HSF-like Transcription Factor TBF1 Is a Major Molecular Switch for Plant Growth-to-Defense Transition
journal, January 2012
- Pajerowska-Mukhtar, Karolina M.; Wang, Wei; Tada, Yasuomi
- Current Biology, Vol. 22, Issue 2
A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in
Arabidopsis
journal, April 2008
- Ren, Dongtao; Liu, Yidong; Yang, Kwang-Yeol
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 14
Bacterial disease resistance in Arabidopsis through flagellin perception
journal, April 2004
- Zipfel, Cyril; Robatzek, Silke; Navarro, Lionel
- Nature, Vol. 428, Issue 6984
Disruption of PAMP-Induced MAP Kinase Cascade by a Pseudomonas syringae Effector Activates Plant Immunity Mediated by the NB-LRR Protein SUMM2
journal, March 2012
- Zhang, Zhibin; Wu, Yaling; Gao, Minghui
- Cell Host & Microbe, Vol. 11, Issue 3
A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence
journal, July 2007
- Chinchilla, Delphine; Zipfel, Cyril; Robatzek, Silke
- Nature, Vol. 448, Issue 7152
A Pseudomonas syringae Effector Inactivates MAPKs to Suppress PAMP-Induced Immunity in Plants
journal, May 2007
- Zhang, Jie; Shao, Feng; Li, Yan
- Cell Host & Microbe, Vol. 1, Issue 3
Isochorismate synthase is required to synthesize salicylic acid for plant defence
journal, November 2001
- Wildermuth, Mary C.; Dewdney, Julia; Wu, Gang
- Nature, Vol. 414, Issue 6863
The Pseudomonas syringae type III effector tyrosine phosphatase HopAO1 suppresses innate immunity in Arabidopsis thaliana: Virulence action of Pst DC3000 effector HopAO1
journal, September 2007
- Underwood, William; Zhang, Shuqun; He, Sheng Y.
- The Plant Journal, Vol. 52, Issue 4
The plant immune system
journal, November 2006
- Jones, Jonathan D. G.; Dangl, Jeffery L.
- Nature, Vol. 444, Issue 7117
The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats
journal, September 1994
- Mindrinos, Michael; Katagiri, Fumiaki; Yu, Guo-Liang
- Cell, Vol. 78, Issue 6
Network Properties of Robust Immunity in Plants
journal, December 2009
- Tsuda, Kenichi; Sato, Masanao; Stoddard, Thomas
- PLoS Genetics, Vol. 5, Issue 12
Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure
journal, September 2004
- Ahlfors, Reetta; Macioszek, Violetta; Rudd, Jason
- The Plant Journal, Vol. 40, Issue 4
A Pseudomonas syringae ADP-Ribosyltransferase Inhibits Arabidopsis Mitogen-Activated Protein Kinase Kinases
journal, June 2010
- Wang, Yujing; Li, Jifeng; Hou, Shuguo
- The Plant Cell, Vol. 22, Issue 6
Coronatine Promotes Pseudomonas syringae Virulence in Plants by Activating a Signaling Cascade that Inhibits Salicylic Acid Accumulation
journal, June 2012
- Zheng, Xiao-yu; Spivey, Natalie Weaver; Zeng, Weiqing
- Cell Host & Microbe, Vol. 11, Issue 6
VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression
journal, October 2009
- Pitzschke, Andrea; Djamei, Armin; Teige, Markus
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 43
Dynamic Changes in the Localization of MAPK Cascade Components Controlling Pathogenesis-related (PR) Gene Expression during Innate Immunity in Parsley
journal, May 2004
- Lee, Justin; Rudd, Jason J.; Macioszek, Violetta K.
- Journal of Biological Chemistry, Vol. 279, Issue 21
The Arabidopsis NPR1 Gene That Controls Systemic Acquired Resistance Encodes a Novel Protein Containing Ankyrin Repeats
journal, January 1997
- Cao, Hui; Glazebrook, Jane; Clarke, Joseph D.
- Cell, Vol. 88, Issue 1
Sustained versus Transient ERK1/2 Signaling Underlies the Anti- and Proapoptotic Effects of Oxidative Stress in Human RPE Cells
journal, October 2006
- Glotin, Anne-Lise; Calipel, Armelle; Brossas, Jean-Yves
- Investigative Opthalmology & Visual Science, Vol. 47, Issue 10
Arabidopsis snc2-1D Activates Receptor-Like Protein-Mediated Immunity Transduced through WRKY70
journal, September 2010
- Zhang, Yaxi; Yang, Yuanai; Fang, Bin
- The Plant Cell, Vol. 22, Issue 9
Cluster analysis and display of genome-wide expression patterns
journal, December 1998
- Eisen, M. B.; Spellman, P. T.; Brown, P. O.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 25
How do plants achieve immunity? Defence without specialized immune cells
journal, January 2012
- Spoel, Steven H.; Dong, Xinnian
- Nature Reviews Immunology, Vol. 12, Issue 2
Emerging functions for plant MAP kinase phosphatases
journal, June 2010
- Bartels, Sebastian; Besteiro, Marina A. González; Lang, Daniel
- Trends in Plant Science, Vol. 15, Issue 6
Exploration, normalization, and summaries of high density oligonucleotide array probe level data
journal, April 2003
- Irizarry, Rafael A.; Hobbs, Bridget; Collin, Francois
- Biostatistics, Vol. 4, Issue 2, p. 249-264
Salicylic Acid, a Multifaceted Hormone to Combat Disease
journal, September 2009
- Vlot, A. Corina; Dempsey, D'Maris Amick; Klessig, Daniel F.
- Annual Review of Phytopathology, Vol. 47, Issue 1
Stomatal Development and Patterning Are Regulated by Environmentally Responsive Mitogen-Activated Protein Kinases in Arabidopsis
journal, January 2007
- Wang, Huachun; Ngwenyama, Njabulo; Liu, Yidong
- The Plant Cell, Vol. 19, Issue 1
The Coronatine Toxin of Pseudomonas syringae Is a Multifunctional Suppressor of Arabidopsis Defense
journal, November 2012
- Geng, Xueqing; Cheng, Jiye; Gangadharan, Anju
- The Plant Cell, Vol. 24, Issue 11
How filamentous pathogens co-opt plants: the ins and outs of fungal effectors
journal, August 2011
- de Jonge, Ronnie; Bolton, Melvin D.; Thomma, Bart PHJ
- Current Opinion in Plant Biology, Vol. 14, Issue 4
Mitogen-Activated Protein Kinases 3 and 6 Are Required for Full Priming of Stress Responses in Arabidopsis thaliana
journal, March 2009
- Beckers, Gerold J. M.; Jaskiewicz, Michal; Liu, Yidong
- The Plant Cell, Vol. 21, Issue 3
A Genomic Approach to Identify Regulatory Nodes in the Transcriptional Network of Systemic Acquired Resistance in Plants
journal, January 2006
- Wang, Dong; Amornsiripanitch, Nita; Dong, Xinnian
- PLoS Pathogens, Vol. 2, Issue 11
Specificity of MAP Kinase Signaling in Yeast Differentiation Involves Transient versus Sustained MAPK Activation
journal, September 2001
- Sabbagh, Walid; Flatauer, Laura J.; Bardwell, A. Jane
- Molecular Cell, Vol. 8, Issue 3
Interplay between MAMP-triggered and SA-mediated defense responses
journal, March 2008
- Tsuda, Kenichi; Sato, Masanao; Glazebrook, Jane
- The Plant Journal, Vol. 53, Issue 5
Regulatory interactions between the Hrp type III protein secretion system and coronatine biosynthesis in Pseudomonas syringae pv. tomato DC3000
journal, October 2000
- Peñaloza-Vázquez, Alejandro; Preston, Gail M.; Collmer, Alan
- Microbiology, Vol. 146, Issue 10
Trojan Horse Strategy in Agrobacterium Transformation: Abusing MAPK Defense Signaling
journal, October 2007
- Djamei, A.; Pitzschke, A.; Nakagami, H.
- Science, Vol. 318, Issue 5849
Structure and function of the feed-forward loop network motif
journal, October 2003
- Mangan, S.; Alon, U.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 21
Understanding the Plant Immune System
journal, December 2010
- Katagiri, Fumiaki; Tsuda, Kenichi
- Molecular Plant-Microbe Interactions®, Vol. 23, Issue 12
Bacterial Effector HopF2 Suppresses Arabidopsis Innate Immunity at the Plasma Membrane
journal, May 2011
- Wu, Shujing; Lu, Dongping; Kabbage, Mehdi
- Molecular Plant-Microbe Interactions®, Vol. 24, Issue 5
Exploring the evolutionary path of plant MAPK networks
journal, September 2012
- Dóczi, Róbert; Ökrész, László; Romero, Alfonso E.
- Trends in Plant Science, Vol. 17, Issue 9
Closing the Circle on the Discovery of Genes Encoding Hrp Regulon Members and Type III Secretion System Effectors in the Genomes of Three Model Pseudomonas syringae Strains
journal, November 2006
- Lindeberg, Magdalen; Cartinhour, Samuel; Myers, Christopher R.
- Molecular Plant-Microbe Interactions®, Vol. 19, Issue 11
Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis
journal, March 2006
- Robatzek, S.
- Genes & Development, Vol. 20, Issue 5