Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana

Tsuda, Kenichi; Mine, Akira; Bethke, Gerit; Igarashi, Daisuke; Botanga, Christopher J.; Tsuda, Yayoi; Glazebrook, Jane; Sato, Masanao; Katagiri, Fumiaki

doi:10.1371/journal.pgen.1004015

Title: Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana

Journal Article · Thu Dec 12 00:00:00 EST 2013 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1004015· OSTI ID:1904660

Tsuda, Kenichi ^[1]; Mine, Akira ^[2]; Bethke, Gerit ^[3]; Igarashi, Daisuke ^[4]; Botanga, Christopher J. ^[5]; Tsuda, Yayoi ^[3]; Glazebrook, Jane ^[3]; Sato, Masanao ^[6]; Katagiri, Fumiaki ^[3]

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)

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of Minnesota, Minneapolis, MN (United States)

Sponsoring Organization:: 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)

Grant/Contract Number:: FG02-05ER15670; MCB-0918908; IOS-1121425

OSTI ID:: 1904660

Journal Information:: PLoS Genetics, Vol. 9, Issue 12; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (57)

MAP Kinase Cascades in Arabidopsis Innate Immunity Rasmussen, Magnus W.; Roux, Milena; Petersen, Morten Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00169	journal	January 2012
How to build a pathogen detector: structural basis of NB-LRR function Takken, Frank LW; Goverse, Aska Current Opinion in Plant Biology, Vol. 15, Issue 4 https://doi.org/10.1016/j.pbi.2012.05.001	journal	August 2012
Robustness: mechanisms and consequences Masel, Joanna; Siegal, Mark L. Trends in Genetics, Vol. 25, Issue 9 https://doi.org/10.1016/j.tig.2009.07.005	journal	September 2009
Design principles for robust biochemical reaction networks: What works, what cannot work, and what might almost work Shinar, Guy; Feinberg, Martin Mathematical Biosciences, Vol. 231, Issue 1 https://doi.org/10.1016/j.mbs.2011.02.012	journal	May 2011
Protein kinase signaling networks in plant innate immunity Tena, Guillaume; Boudsocq, Marie; Sheen, Jen Current Opinion in Plant Biology, Vol. 14, Issue 5 https://doi.org/10.1016/j.pbi.2011.05.006	journal	October 2011
Arabidopsis EDS1 Connects Pathogen Effector Recognition to Cell Compartment-Specific Immune Responses Heidrich, K.; Wirthmueller, L.; Tasset, C. Science, Vol. 334, Issue 6061 https://doi.org/10.1126/science.1211641	journal	December 2011
Cell Death Mediated by MAPK Is Associated with Hydrogen Peroxide Production in Arabidopsis Ren, Dongtao; Yang, Heping; Zhang, Shuqun Journal of Biological Chemistry, Vol. 277, Issue 1 https://doi.org/10.1074/jbc.M109495200	journal	January 2002
Direct Ubiquitination of Pattern Recognition Receptor FLS2 Attenuates Plant Innate Immunity Lu, D.; Lin, W.; Gao, X. Science, Vol. 332, Issue 6036 https://doi.org/10.1126/science.1204903	journal	June 2011
Phosphorylation of 1-Aminocyclopropane-1-Carboxylic Acid Synthase by MPK6, a Stress-Responsive Mitogen-Activated Protein Kinase, Induces Ethylene Biosynthesis in Arabidopsis Liu, Yidong; Zhang, Shuqun The Plant Cell, Vol. 16, Issue 12 https://doi.org/10.1105/tpc.104.026609	journal	November 2004
An efficient Agrobacterium-mediated transient transformation of Arabidopsis: An efficient transient transformation Tsuda, Kenichi; Qi, Yiping; Nguyen, Le V. The Plant Journal, Vol. 69, Issue 4 https://doi.org/10.1111/j.1365-313X.2011.04819.x	journal	November 2011
The type III effector HopF2 _Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence Wilton, Mike; Subramaniam, Rajagopal; Elmore, James Proceedings of the National Academy of Sciences, Vol. 107, Issue 5 https://doi.org/10.1073/pnas.0904739107	journal	January 2010
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 Traverse, S.; Gomez, N.; Paterson, H. Biochemical Journal, Vol. 288, Issue 2 https://doi.org/10.1042/bj2880351	journal	December 1992
Plant Innate Immunity: Perception of Conserved Microbial Signatures Schwessinger, Benjamin; Ronald, Pamela C. Annual Review of Plant Biology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev-arplant-042811-105518	journal	June 2012
Bacterial virulence effectors and their activities Hann, Dagmar R.; Gimenez-Ibanez, Selena; Rathjen, John P. Current Opinion in Plant Biology, Vol. 13, Issue 4 https://doi.org/10.1016/j.pbi.2010.04.003	journal	August 2010
The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity Igarashi, Daisuke; Tsuda, Kenichi; Katagiri, Fumiaki The Plant Journal, Vol. 71, Issue 2 https://doi.org/10.1111/j.1365-313X.2012.04950.x	journal	May 2012
Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity Tsuda, Kenichi; Katagiri, Fumiaki Current Opinion in Plant Biology, Vol. 13, Issue 4 https://doi.org/10.1016/j.pbi.2010.04.006	journal	August 2010
Dual-Level Regulation of ACC Synthase Activity by MPK3/MPK6 Cascade and Its Downstream WRKY Transcription Factor during Ethylene Induction in Arabidopsis Li, Guojing; Meng, Xiangzong; Wang, Ruigang PLoS Genetics, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pgen.1002767	journal	June 2012
The HSF-like Transcription Factor TBF1 Is a Major Molecular Switch for Plant Growth-to-Defense Transition Pajerowska-Mukhtar, Karolina M.; Wang, Wei; Tada, Yasuomi Current Biology, Vol. 22, Issue 2 https://doi.org/10.1016/j.cub.2011.12.015	journal	January 2012
A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis Ren, Dongtao; Liu, Yidong; Yang, Kwang-Yeol Proceedings of the National Academy of Sciences, Vol. 105, Issue 14 https://doi.org/10.1073/pnas.0711301105	journal	April 2008
Bacterial disease resistance in Arabidopsis through flagellin perception Zipfel, Cyril; Robatzek, Silke; Navarro, Lionel Nature, Vol. 428, Issue 6984 https://doi.org/10.1038/nature02485	journal	April 2004
Disruption of PAMP-Induced MAP Kinase Cascade by a Pseudomonas syringae Effector Activates Plant Immunity Mediated by the NB-LRR Protein SUMM2 Zhang, Zhibin; Wu, Yaling; Gao, Minghui Cell Host & Microbe, Vol. 11, Issue 3 https://doi.org/10.1016/j.chom.2012.01.015	journal	March 2012
A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence Chinchilla, Delphine; Zipfel, Cyril; Robatzek, Silke Nature, Vol. 448, Issue 7152 https://doi.org/10.1038/nature05999	journal	July 2007
A Pseudomonas syringae Effector Inactivates MAPKs to Suppress PAMP-Induced Immunity in Plants Zhang, Jie; Shao, Feng; Li, Yan Cell Host & Microbe, Vol. 1, Issue 3 https://doi.org/10.1016/j.chom.2007.03.006	journal	May 2007
Isochorismate synthase is required to synthesize salicylic acid for plant defence Wildermuth, Mary C.; Dewdney, Julia; Wu, Gang Nature, Vol. 414, Issue 6863 https://doi.org/10.1038/35107108	journal	November 2001
The Pseudomonas syringae type III effector tyrosine phosphatase HopAO1 suppresses innate immunity in Arabidopsis thaliana: Virulence action of Pst DC3000 effector HopAO1 Underwood, William; Zhang, Shuqun; He, Sheng Y. The Plant Journal, Vol. 52, Issue 4 https://doi.org/10.1111/j.1365-313X.2007.03262.x	journal	September 2007
The plant immune system Jones, Jonathan D. G.; Dangl, Jeffery L. Nature, Vol. 444, Issue 7117 https://doi.org/10.1038/nature05286	journal	November 2006
The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats Mindrinos, Michael; Katagiri, Fumiaki; Yu, Guo-Liang Cell, Vol. 78, Issue 6 https://doi.org/10.1016/0092-8674(94)90282-8	journal	September 1994
Network Properties of Robust Immunity in Plants Tsuda, Kenichi; Sato, Masanao; Stoddard, Thomas PLoS Genetics, Vol. 5, Issue 12 https://doi.org/10.1371/journal.pgen.1000772	journal	December 2009
Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure Ahlfors, Reetta; Macioszek, Violetta; Rudd, Jason The Plant Journal, Vol. 40, Issue 4 https://doi.org/10.1111/j.1365-313X.2004.02229.x	journal	September 2004
A Pseudomonas syringae ADP-Ribosyltransferase Inhibits Arabidopsis Mitogen-Activated Protein Kinase Kinases Wang, Yujing; Li, Jifeng; Hou, Shuguo The Plant Cell, Vol. 22, Issue 6 https://doi.org/10.1105/tpc.110.075697	journal	June 2010
Coronatine Promotes Pseudomonas syringae Virulence in Plants by Activating a Signaling Cascade that Inhibits Salicylic Acid Accumulation Zheng, Xiao-yu; Spivey, Natalie Weaver; Zeng, Weiqing Cell Host & Microbe, Vol. 11, Issue 6 https://doi.org/10.1016/j.chom.2012.04.014	journal	June 2012
VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression Pitzschke, Andrea; Djamei, Armin; Teige, Markus Proceedings of the National Academy of Sciences, Vol. 106, Issue 43 https://doi.org/10.1073/pnas.0905599106	journal	October 2009
Dynamic Changes in the Localization of MAPK Cascade Components Controlling Pathogenesis-related (PR) Gene Expression during Innate Immunity in Parsley Lee, Justin; Rudd, Jason J.; Macioszek, Violetta K. Journal of Biological Chemistry, Vol. 279, Issue 21 https://doi.org/10.1074/jbc.M401099200	journal	May 2004
The Arabidopsis NPR1 Gene That Controls Systemic Acquired Resistance Encodes a Novel Protein Containing Ankyrin Repeats Cao, Hui; Glazebrook, Jane; Clarke, Joseph D. Cell, Vol. 88, Issue 1 https://doi.org/10.1016/S0092-8674(00)81858-9	journal	January 1997
Fls2 Gómez-Gómez, Lourdes; Boller, Thomas Molecular Cell, Vol. 5, Issue 6 https://doi.org/10.1016/S1097-2765(00)80265-8	journal	June 2000
Sustained versus Transient ERK1/2 Signaling Underlies the Anti- and Proapoptotic Effects of Oxidative Stress in Human RPE Cells Glotin, Anne-Lise; Calipel, Armelle; Brossas, Jean-Yves Investigative Opthalmology & Visual Science, Vol. 47, Issue 10 https://doi.org/10.1167/iovs.06-0297	journal	October 2006
Arabidopsis snc2-1D Activates Receptor-Like Protein-Mediated Immunity Transduced through WRKY70 Zhang, Yaxi; Yang, Yuanai; Fang, Bin The Plant Cell, Vol. 22, Issue 9 https://doi.org/10.1105/tpc.110.074120	journal	September 2010
Cluster analysis and display of genome-wide expression patterns Eisen, M. B.; Spellman, P. T.; Brown, P. O. Proceedings of the National Academy of Sciences, Vol. 95, Issue 25 https://doi.org/10.1073/pnas.95.25.14863	journal	December 1998
How do plants achieve immunity? Defence without specialized immune cells Spoel, Steven H.; Dong, Xinnian Nature Reviews Immunology, Vol. 12, Issue 2 https://doi.org/10.1038/nri3141	journal	January 2012
Emerging functions for plant MAP kinase phosphatases Bartels, Sebastian; Besteiro, Marina A. González; Lang, Daniel Trends in Plant Science, Vol. 15, Issue 6 https://doi.org/10.1016/j.tplants.2010.04.003	journal	June 2010
Exploration, normalization, and summaries of high density oligonucleotide array probe level data Irizarry, Rafael A.; Hobbs, Bridget; Collin, Francois Biostatistics, Vol. 4, Issue 2, p. 249-264 https://doi.org/10.1093/biostatistics/4.2.249	journal	April 2003
Salicylic Acid, a Multifaceted Hormone to Combat Disease Vlot, A. Corina; Dempsey, D'Maris Amick; Klessig, Daniel F. Annual Review of Phytopathology, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.phyto.050908.135202	journal	September 2009
Stomatal Development and Patterning Are Regulated by Environmentally Responsive Mitogen-Activated Protein Kinases in Arabidopsis Wang, Huachun; Ngwenyama, Njabulo; Liu, Yidong The Plant Cell, Vol. 19, Issue 1 https://doi.org/10.1105/tpc.106.048298	journal	January 2007
The Coronatine Toxin of Pseudomonas syringae Is a Multifunctional Suppressor of Arabidopsis Defense Geng, Xueqing; Cheng, Jiye; Gangadharan, Anju The Plant Cell, Vol. 24, Issue 11 https://doi.org/10.1105/tpc.112.105312	journal	November 2012
How filamentous pathogens co-opt plants: the ins and outs of fungal effectors de Jonge, Ronnie; Bolton, Melvin D.; Thomma, Bart PHJ Current Opinion in Plant Biology, Vol. 14, Issue 4 https://doi.org/10.1016/j.pbi.2011.03.005	journal	August 2011
Mitogen-Activated Protein Kinases 3 and 6 Are Required for Full Priming of Stress Responses in Arabidopsis thaliana Beckers, Gerold J. M.; Jaskiewicz, Michal; Liu, Yidong The Plant Cell, Vol. 21, Issue 3 https://doi.org/10.1105/tpc.108.062158	journal	March 2009
A Genomic Approach to Identify Regulatory Nodes in the Transcriptional Network of Systemic Acquired Resistance in Plants Wang, Dong; Amornsiripanitch, Nita; Dong, Xinnian PLoS Pathogens, Vol. 2, Issue 11 https://doi.org/10.1371/journal.ppat.0020123	journal	January 2006
Specificity of MAP Kinase Signaling in Yeast Differentiation Involves Transient versus Sustained MAPK Activation Sabbagh, Walid; Flatauer, Laura J.; Bardwell, A. Jane Molecular Cell, Vol. 8, Issue 3 https://doi.org/10.1016/S1097-2765(01)00322-7	journal	September 2001
Interplay between MAMP-triggered and SA-mediated defense responses Tsuda, Kenichi; Sato, Masanao; Glazebrook, Jane The Plant Journal, Vol. 53, Issue 5 https://doi.org/10.1111/j.1365-313X.2007.03369.x	journal	March 2008
Regulatory interactions between the Hrp type III protein secretion system and coronatine biosynthesis in Pseudomonas syringae pv. tomato DC3000 Peñaloza-Vázquez, Alejandro; Preston, Gail M.; Collmer, Alan Microbiology, Vol. 146, Issue 10 https://doi.org/10.1099/00221287-146-10-2447	journal	October 2000
Trojan Horse Strategy in Agrobacterium Transformation: Abusing MAPK Defense Signaling Djamei, A.; Pitzschke, A.; Nakagami, H. Science, Vol. 318, Issue 5849 https://doi.org/10.1126/science.1148110	journal	October 2007
Structure and function of the feed-forward loop network motif Mangan, S.; Alon, U. Proceedings of the National Academy of Sciences, Vol. 100, Issue 21 https://doi.org/10.1073/pnas.2133841100	journal	October 2003
Understanding the Plant Immune System Katagiri, Fumiaki; Tsuda, Kenichi Molecular Plant-Microbe Interactions®, Vol. 23, Issue 12 https://doi.org/10.1094/MPMI-04-10-0099	journal	December 2010
Bacterial Effector HopF2 Suppresses Arabidopsis Innate Immunity at the Plasma Membrane Wu, Shujing; Lu, Dongping; Kabbage, Mehdi Molecular Plant-Microbe Interactions®, Vol. 24, Issue 5 https://doi.org/10.1094/MPMI-07-10-0150	journal	May 2011
Exploring the evolutionary path of plant MAPK networks Dóczi, Róbert; Ökrész, László; Romero, Alfonso E. Trends in Plant Science, Vol. 17, Issue 9 https://doi.org/10.1016/j.tplants.2012.05.009	journal	September 2012
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 Lindeberg, Magdalen; Cartinhour, Samuel; Myers, Christopher R. Molecular Plant-Microbe Interactions®, Vol. 19, Issue 11 https://doi.org/10.1094/MPMI-19-1151	journal	November 2006
Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis Robatzek, S. Genes & Development, Vol. 20, Issue 5 https://doi.org/10.1101/gad.366506	journal	March 2006

Similar Records

Pattern-Triggered Immunity Suppresses Programmed Cell Death Triggered by Fumonisin B1

Journal Article · Mon Apr 01 00:00:00 EDT 2013 · PLoS ONE · OSTI ID:1904660

Igarashi, Daisuke; Bethke, Gerit; Xu, Yuan; +3 more

Arabidopsis SDG8 Potentiates the Sustainable Transcriptional Induction of the Pathogenesis-Related Genes PR1 and PR2 During Plant Defense Response

Journal Article · Wed Mar 11 00:00:00 EDT 2020 · Frontiers in Plant Science · OSTI ID:1904660

Zhang, Xue; Ménard, Rozenn; Li, Ying; +4 more

CAMTA-Mediated Regulation of Salicylic Acid Immunity Pathway Genes in Arabidopsis Exposed to Low Temperature and Pathogen Infection

Journal Article · Sun Oct 01 00:00:00 EDT 2017 · The Plant Cell · OSTI ID:1904660

Kim, Yong Sig; An, Chuanfu; Park, Sunchung; +6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
MAPK signaling cascades
gene regulation
leaves
Arabidopsis thaliana
signaling networks
gene expression
plant disease resistance
seedings

Title: Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana

Citation Formats

References (57)

Similar Records

Related Subjects