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Hierarchy And Roles Of Pathogen-Associated Molecular Pattern-Induced Responses In Nicotiana Benthamiana1[W]

C. Segonzac, Doreen Feike, Selena Giménez-Ibañez, Dagmar R. Hann, C. Zipfel, J. Rathjen
Published 2011 · Biology, Medicine

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Our current understanding of pathogen-associated molecular pattern (PAMP)-triggered immunity signaling pathways in plants is limited due to the redundancy of several components or the lethality of mutants in Arabidopsis (Arabidopsis thaliana). To overcome this, we used a virus-induced gene silencing-based approach in combination with pharmacological studies to decipher links between early PAMP-triggered immunity events and their roles in immunity following PAMP perception in Nicotiana benthamiana. Two different calcium influx inhibitors suppressed the reactive oxygen species (ROS) burst: activation of the mitogen-activated protein kinases (MAPKs) and PAMP-induced gene expression. The calcium burst was unaffected in plants specifically silenced for components involved in ROS generation or for MAPKs activated by PAMP treatment. Importantly, the ROS burst still occurred in plants silenced for the two major defense-associated MAPK genes NbSIPK (for salicylic acid-induced protein kinase) and NbWIPK (for wound-induced protein kinase) or for both genes simultaneously, demonstrating that these MAPKs are dispensable for ROS production. We further show that NbSIPK silencing is sufficient to prevent PAMP-induced gene expression but that both MAPKs are required for bacterial immunity against two virulent strains of Pseudomonas syringae and their respective nonpathogenic mutants. These results suggest that the PAMP-triggered calcium burst is upstream of separate signaling branches, one leading to MAPK activation and then gene expression and the other to ROS production. In addition, this study highlights the essential roles of NbSIPK and NbWIPK in antibacterial immunity. Unexpectedly, negative regulatory mechanisms controlling the intensity of the PAMP-triggered calcium and ROS bursts were also revealed by this work.
This paper references
10.1111/j.1365-313X.2007.03192.x
Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses
T. Nühse (2007)
10.1146/annurev.arplant.57.032905.105346
A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors.
T. Boller (2009)
10.1093/PCP/41.6.692
Phytophthora parasitica elicitor-induced reactions in cells of Petroselinum crispum.
G. Fellbrich (2000)
10.1074/mcp.M600429-MCP200
Quantitative Phosphoproteomics of Early Elicitor Signaling in Arabidopsis*S
J. Benschop (2007)
10.1016/J.CECA.2005.06.036
Proteinaceous and oligosaccharidic elicitors induce different calcium signatures in the nucleus of tobacco cells.
D. Lecourieux (2005)
10.1038/415977a
MAP kinase signalling cascade in Arabidopsis innate immunity
T. Asai (2002)
10.1104/pp.107.3.1025
Nucleotide Sequence of cDNA for a Putative Cysteine Protease from Rice Seeds
A. Shintani (1995)
10.4161/psb.4.4.8103
Cyclic nucleotide gated channels and related signaling components in plant innate immunity
W. Ma (2009)
10.1073/pnas.1003347107
Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1
F. Boutrot (2010)
10.1046/J.1365-313X.2002.029005569.X
An EDS1 orthologue is required for N-mediated resistance against tobacco mosaic virus.
J. Peart (2002)
10.1104/pp.104.042069
Reactive Oxygen Species Activation of Plant Ca2+ Channels. A Signaling Mechanism in Polar Growth, Hormone Transduction, Stress Signaling, and Hypothetically Mechanotransduction1
I. Mori (2004)
10.1111/j.1365-2958.2006.05350.x
The type III effector repertoire of Pseudomonas syringae pv. syringae B728a and its role in survival and disease on host and non‐host plants
B. Vinatzer (2006)
10.1016/S1360-1385(03)00099-2
CNGCs: prime targets of plant cyclic nucleotide signalling?
I. Talke (2003)
10.1073/pnas.0705306104
The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants
Antje Heese (2007)
10.1074/jbc.M708106200
Synergistic Activation of the Arabidopsis NADPH Oxidase AtrbohD by Ca2+ and Phosphorylation*
Y. Ogasawara (2008)
Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase
M Kobayashi (2007)
10.1093/PCP/PCE123
Oxidative stress activates ATMPK6, an Arabidopsis homologue of MAP kinase.
T. Yuasa (2001)
10.1016/S0005-2736(02)00509-6
Genes for calcium-permeable channels in the plasma membrane of plant root cells.
P. White (2002)
10.1016/j.cub.2009.01.054
AvrPtoB Targets the LysM Receptor Kinase CERK1 to Promote Bacterial Virulence on Plants
Selena Giménez-Ibañez (2009)
10.1074/JBC.275.11.7521
Microbial Elicitors Induce Activation and Dual Phosphorylation of the Arabidopsis thaliana MAPK 6*
T. Nühse (2000)
10.1111/j.1364-3703.2009.00537.x
Microbe-associated molecular pattern (MAMP) signatures, synergy, size and charge: influences on perception or mobility and host defence responses.
Shazia N Aslam (2009)
10.1046/J.1365-313X.1998.00269.X
Activation of MAPK homologues by elicitors in tobacco cells.
A. Lebrun-Garcia (1998)
10.1016/J.BBRC.2004.03.114
Identification of putative voltage-dependent Ca2+-permeable channels involved in cryptogein-induced Ca2+ transients and defense responses in tobacco BY-2 cells.
Yasuhiro Kadota (2004)
10.1073/PNAS.0502954102
Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants.
A. Ludwig (2005)
10.1023/A:1006345302589
A high-affinity calmodulin-binding site in a tobacco plasma-membrane channel protein coincides with a characteristic element of cyclic nucleotide-binding domains
T. Arazi (2004)
10.1105/tpc.107.055855
MAPK Signaling Regulates Nitric Oxide and NADPH Oxidase-Dependent Oxidative Bursts in Nicotiana benthamiana[W][OA]
S. Asai (2008)
10.1007/s11103-007-9198-z
Arabidopsis MEKK1 can take a short cut: it can directly interact with senescence-related WRKY53 transcription factor on the protein level and can bind to its promoter
Ying Miao (2007)
10.1073/pnas.0905532106
Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR
J. Li (2009)
10.1073/pnas.0907711106
Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele
Xunli Lu (2009)
10.1111/J.1365-313X.2006.02981.X
Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana.
Dagmar R. Hann (2007)
10.1105/tpc.12.8.1425
Receptor-Mediated Increase in Cytoplasmic Free Calcium Required for Activation of Pathogen Defense in Parsley
B. Blume (2000)
10.1016/j.cell.2006.03.037
Perception of the Bacterial PAMP EF-Tu by the Receptor EFR Restricts Agrobacterium-Mediated Transformation
C. Zipfel (2006)
10.1105/tpc.11.2.273
Rapid Avr9- and Cf-9–Dependent Activation of MAP Kinases in Tobacco Cell Cultures and Leaves: Convergence of Resistance Gene, Elicitor, Wound, and Salicylate Responses
T. Romeis (1999)
10.1042/bj20081465
Activation of a nuclear-localized SIPK in tobacco cells challenged by cryptogein, an elicitor of plant defence reactions.
J. Dahan (2009)
10.1016/S1097-2765(00)80265-8
FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis.
L. Gómez-Gómez (2000)
10.1105/tpc.106.048298
Stomatal Development and Patterning Are Regulated by Environmentally Responsive Mitogen-Activated Protein Kinases in Arabidopsis[W]
H. Wang (2007)
10.1105/tpc.9.11.2077
Early Events Induced by the Elicitor Cryptogein in Tobacco Cells: Involvement of a Plasma Membrane NADPH Oxidase and Activation of Glycolysis and the Pentose Phosphate Pathway.
A. Pugin (1997)
10.1094/MPMI-23-8-0991
Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana.
Hanh P Nguyen (2010)
10.1074/jbc.M110.116657
The Lysin Motif Receptor-like Kinase (LysM-RLK) CERK1 Is a Major Chitin-binding Protein in Arabidopsis thaliana and Subject to Chitin-induced Phosphorylation*♦
E. Petutschnig (2010)
10.1073/PNAS.95.12.7225
The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK.
S. Zhang (1998)
Accumulation and Resistance to Phytophthora infestans
H. Yoshioka (2003)
Reactive oxygen species activation of plant Ca 2+ channels: a signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction
I C Mori (2004)
10.1038/emboj.2009.262
Control of the pattern‐recognition receptor EFR by an ER protein complex in plant immunity
V. Nekrasov (2009)
10.1105/tpc.6.11.1529
Emerging themes of plant signal transduction.
C. Bowler (1994)
10.1105/tpc.108.058032
Haplo-Insufficiency of MPK3 in MPK6 Mutant Background Uncovers a Novel Function of These Two MAPKs in Arabidopsis Ovule Development[W]
H. Wang (2008)
10.1073/pnas.0905831106
Ca2+, cAMP, and transduction of non-self perception during plant immune responses
W. Ma (2009)
10.1038/nature08794
Differential innate immune signalling via Ca2+ sensor protein kinases
Marie Boudsocq (2010)
10.1046/J.1365-313X.2002.01342.X
The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells.
F. Simon-Plas (2002)
10.1105/tpc.12.8.1393
Identification of a Calmodulin-Regulated Soybean Ca2+-ATPase (SCA1) That Is Located in the Plasma Membrane
W. Chung (2000)
10.1038/nature05999
A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence
D. Chinchilla (2007)
10.1105/tpc.015552
Silencing of the Mitogen-Activated Protein Kinase MPK6 Compromises Disease Resistance in Arabidopsis
F. Menke (2004)
10.1111/J.1365-313X.2005.02382.X
SIPK signaling controls multiple components of harpin-induced cell death in tobacco.
M. Samuel (2005)
10.1128/JB.01757-07
Naturally occurring nonpathogenic isolates of the plant pathogen Pseudomonas syringae lack a type III secretion system and effector gene orthologues.
Toni J Mohr (2008)
10.1104/pp.103.036749
The Transcriptional Innate Immune Response to flg22. Interplay and Overlap with Avr Gene-Dependent Defense Responses and Bacterial Pathogenesis1[w]
Lionel Navarro (2004)
10.1105/tpc.104.026765
The N Terminus of Bacterial Elongation Factor Tu Elicits Innate Immunity in Arabidopsis Plants
G. Kunze (2004)
10.1038/nature05286
The plant immune system
J. Jones (2006)
10.1038/nature02485
Bacterial disease resistance in Arabidopsis through flagellin perception
C. Zipfel (2004)
10.1083/JCB.121.1.83
Imaging calcium dynamics in living plants using semi-synthetic recombinant aequorins
M. Knight (1993)
10.1016/S1360-1385(03)00108-0
Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants?
Séverine Lorrain (2003)
10.1146/ANNUREV.ARPLANT.55.031903.141624
The generation of Ca(2+) signals in plants.
A. Hetherington (2004)
10.1111/j.1469-8137.2006.01888.x
Calcium-calmodulin is required for abscisic acid-induced antioxidant defense and functions both upstream and downstream of H2 O2 production in leaves of maize (Zea mays) plants.
X. Hu (2007)
10.1038/emboj.2009.263
Receptor quality control in the endoplasmic reticulum for plant innate immunity
Y. Saijo (2009)
10.1111/J.1469-8137.2006.01777.X
Calcium in plant defence-signalling pathways.
D. Lecourieux (2006)
10.1104/pp.106.080697
Activation of Ntf4, a Tobacco Mitogen-Activated Protein Kinase, during Plant Defense Response and Its Involvement in Hypersensitive Response-Like Cell Death1
Dongtao Ren (2006)
10.1126/science.270.5244.1988
Tobacco MAP Kinase: A Possible Mediator in Wound Signal Transduction Pathways
S. Seo (1995)
10.1074/jbc.M109.027540
Direct Binding of a Plant LysM Receptor-like Kinase, LysM RLK1/CERK1, to Chitin in Vitro*
Ei'ichi Iizasa (2009)
10.1094/PHYTO-79-974
Active oxygen production during a bacteria-induced hypersensitive reaction in tobacco suspension cells
L. Keppler (1989)
10.1016/J.CHOM.2007.03.006
A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants.
J. Zhang (2007)
10.1105/tpc.008680
Nicotiana benthamiana gp91phox Homologs NbrbohA and NbrbohB Participate in H2O2 Accumulation and Resistance to Phytophthora infestans Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.008680.
H. Yoshioka (2003)
10.1046/J.1365-313X.2002.01297.X
Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus.
Y. Liu (2002)
10.1146/annurev-arplant-070109-104628
The language of calcium signaling.
A. Dodd (2010)
10.1074/jbc.273.2.1099
A Novel Calmodulin-regulated Ca2+-ATPase (ACA2) from Arabidopsis with an N-terminal Autoinhibitory Domain*
J. Harper (1998)
10.1094/MPMI-21-8-1015
Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions.
M. Goodin (2008)
10.1111/J.1365-313X.2005.02529.X
Basal resistance against bacteria in Nicotiana benthamiana leaves is accompanied by reduced vascular staining and suppressed by multiple Pseudomonas syringae type III secretion system effector proteins.
Hye-sook Oh (2005)
10.1016/S0014-5793(96)01448-2
A calmodulin‐stimulated Ca2+‐ATPase from plant vacuolar membranes with a putative regulatory domain at its N‐terminus 1
S. Malmström (1997)
10.1007/s00438-003-0872-9
Virus-induced silencing of WIPK and SIPK genes reduces resistance to a bacterial pathogen, but has no effect on the INF1-induced hypersensitive response (HR) in Nicotiana benthamiana
P. Sharma (2003)
10.1105/tpc.106.045096
Death Don't Have No Mercy and Neither Does Calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and Innate Immunity[W]
R. Ali (2007)
10.1105/tpc.13.5.1079
A Harpin Binding Site in Tobacco Plasma Membranes Mediates Activation of the Pathogenesis-Related Gene HIN1 Independent of Extracellular Calcium but Dependent on Mitogen-Activated Protein Kinase Activity
J. Lee (2001)
10.1111/J.1365-313X.2004.02033.X
Activation of a mitogen-activated protein kinase cascade induces WRKY family of transcription factors and defense genes in tobacco.
C. Kim (2004)
10.1073/pnas.0909705107
A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity
Dongping Lu (2009)
10.1111/j.1399-3054.2009.01326.x
ROS in biotic interactions.
M. Torres (2010)
10.1073/pnas.0705147104
CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis
A. Miya (2007)
10.1016/j.chom.2010.03.007
Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector.
J. Zhang (2010)
10.1016/J.COPBIO.2007.01.012
RNAi for revealing and engineering plant gene functions.
I. Small (2007)
Calcium in plant defencesignalling pathways
D Lecourieux (2006)
10.1046/J.1365-313X.2000.00741.X
Ozone treatment rapidly activates MAP kinase signalling in plants.
M. Samuel (2000)
10.1111/j.1365-313X.2010.04155.x
Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca-associated opening of plasma membrane anion channels.
Elena Jeworutzki (2010)
10.1105/tpc.105.036574
The Arabidopsis Receptor Kinase FLS2 Binds flg22 and Determines the Specificity of Flagellin Perception[W]
D. Chinchilla (2005)
10.1104/pp.109.3.1025
Involvement of Free Calcium in Action of Cryptogein, a Proteinaceous Elicitor of Hypersensitive Reaction in Tobacco Cells
E. Tavernier (1995)
Indicator Technique for Antimetabolic Toxin Production by Phytopathogenic Species of Pseudomonas
D. Taylor
10.1105/tpc.005579
Analysis and Effects of Cytosolic Free Calcium Increases in Response to Elicitors in Nicotiana plumbaginifolia Cells Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.005579.
D. Lecourieux (2002)
10.1094/MPMI-19-0711
Early signaling events induced by elicitors of plant defenses.
Angela Garcia-Brugger (2006)



This paper is referenced by
Understanding the role of L-type lectin receptor kinases in Phytophthora resistance
Y. Wang (2014)
10.1111/mpp.12840
Chloroplast clustering around the nucleus is a general response to pathogen perception in Nicotiana benthamiana
Xue Ding (2019)
Development of a Proteomics Platform for Analysis of the Plant-pathogen Interface
Brenden A. Hurley (2015)
Elicitation and evasion of plant innate immunity by beneficial and pathogenic bacteria
Sebastian Pfeilmeier (2017)
10.1371/journal.pone.0159107
The Xanthomonas campestris pv. vesicatoria Type-3 Effector XopB Inhibits Plant Defence Responses by Interfering with ROS Production
J. P. R. Priller (2016)
10.1371/journal.ppat.1002707
Functional Analysis of NopM, a Novel E3 Ubiquitin Ligase (NEL) Domain Effector of Rhizobium sp. Strain NGR234
D. Xin (2012)
10.1101/2020.05.11.086728
Lumi-Map, a real-time luciferase bioluminescence screen of mutants combined with MutMap, reveals Arabidopsis genes involved in PAMP-triggered immunity
Hiroaki Kato (2020)
10.1038/srep20579
Role of brassinosteroid signaling in modulating Tobacco mosaic virus resistance in Nicotiana benthamiana
Xing-guang Deng (2016)
UvA-DARE ( Digital Academic Repository ) Insights into Nod factor signaling mediated by Medicago truncatula LysM receptor-like kinases , MtNFP and MtLYK 3
Oldroyd GED (2012)
10.1111/plb.12321
Two guard cell mitogen-activated protein kinases, MPK9 and MPK12, function in methyl jasmonate-induced stomatal closure in Arabidopsis thaliana.
M. A. R. Khokon (2015)
10.1104/pp.111.192575
Plasma Membrane Calcium ATPases Are Important Components of Receptor-Mediated Signaling in Plant Immune Responses and Development1[C][W][OA]
Nicolas Frei dit Frey (2012)
Apoplastic ROS and transcriptional response in plant stress signaling
Lauri Vaahtera (2016)
10.1128/mBio.00359-16
Ralstonia solanacearum Type III Effector RipAY Is a Glutathione-Degrading Enzyme That Is Activated by Plant Cytosolic Thioredoxins and Suppresses Plant Immunity
T. Mukaihara (2016)
10.1371/journal.pone.0114921
The Pseudomonas syringae Type III Effector HopF2 Suppresses Arabidopsis Stomatal Immunity
Brenden A. Hurley (2014)
10.1146/annurev-phyto-082712-102314
MAPK cascades in plant disease resistance signaling.
Xiangzong Meng (2013)
10.1111/nph.12651
The bacterial effector HopM1 suppresses PAMP-triggered oxidative burst and stomatal immunity.
Rosa Lozano-Durán (2014)
10.4172/2329-955X.1000131
Role of Antioxidant Enzymes, Hydrogen Peroxide and PRProteins in the Compatible and Incompatible Interactions of Cowpea (Vigna unguiculata)Genotypes with the Fungus Colletotrichum gloeosporioides
Oliveira Jta (2014)
Running title: Regulation of RBOHD during plant immunity Corresponding author:
Yasuhiro Kadota (2015)
10.1111/tpj.14654
Rpa1 mediates an immune response to avrRpm1Psa and confers resistance against Pseudomonas syringae pv. actinidiae.
Minsoo Yoon (2019)
10.3390/plants8110441
Genome-Wide Computational Identification of Biologically Significant Cis-Regulatory Elements and Associated Transcription Factors from Rice
C. Ho (2019)
10.1016/j.redox.2016.12.009
A review of redox signaling and the control of MAP kinase pathway in plants
Y. Liu (2017)
10.1105/tpc.114.125682
RETRACTED: The Arabidopsis Malectin-Like Leucine-Rich Repeat Receptor-Like Kinase IOS1 Associates with the Pattern Recognition Receptors FLS2 and EFR and Is Critical for Priming of Pattern-Triggered Immunity[C][W]
Ching-Wei Chen (2014)
10.1104/pp.114.245944
Distinct Roles for Mitogen-Activated Protein Kinase Signaling and CALMODULIN-BINDING TRANSCRIPTIONAL ACTIVATOR3 in Regulating the Peak Time and Amplitude of the Plant General Stress Response1[W][OPEN]
Marta Bjornson (2014)
10.1016/J.PMPP.2016.03.004
Hierarchical regulation of NADPH oxidase by protein kinases in plant immunity
H. Yoshioka (2016)
10.1016/j.chom.2014.02.009
The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity.
L. Li (2014)
10.1093/pcp/pcx053
Using GCaMP3 to Study Ca2+ Signaling in Nicotiana Species
Thomas A. DeFalco (2017)
10.1101/015479
The NLR helper protein NRC3 but not NRC1 is required for Pto-mediated cell death in Nicotiana benthamiana
C. Wu (2015)
10.1093/bfgp/elv004
Kinase-mediated orchestration of NADPH oxidase in plant immunity.
H. Adachi (2015)
10.3186/JJPHYTOPATH.81.1
Molecular mechanisms of ROS burst conferred by protein phosphorylation.
H. Yoshioka (2015)
Dissecting the role of plant immunity in plant-aphid interactions
David Prince (2012)
University of Dundee A potato STRUBBELIG-RECEPTOR FAMILY member , StLRPK 1 , associates with StSERK 3 A / BAK 1 and activates immunity
H. Wang (2018)
10.1007/978-94-007-7426-1_2
PAMP Signaling in Plant Innate Immunity
P. Vidhyasekaran (2014)
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