Online citations, reference lists, and bibliographies.
← Back to Search

Dynamic Changes In The Localization Of MAPK Cascade Components Controlling Pathogenesis-related (PR) Gene Expression During Innate Immunity In Parsley*

J. Lee, J. Rudd, V. Macioszek, D. Scheel
Published 2004 · Biology, Medicine

Cite This
Download PDF
Analyze on Scholarcy
Share
The activation of mitogen-activated protein kinase (MAPK) cascades is an important mechanism for stress adaptation through the control of gene expression in mammals, yeast, and plants. MAPK activation has emerged as a common mechanism by which plants trigger pathogen defense responses following innate immune recognition of potential microbial pathogens. We are studying the non-host plant defense response of parsley to attempted infection by Phytophthora species using an experimental system of cultured parsley cells and the Phytophthora-derived Pep-13 peptide elicitor. Following receptor-mediated recognition of this peptide, parsley cells trigger a multifaceted innate immune response, involving the activation of three MAPKs that have been shown to function in the oxidative burst-independent activation of defense gene expression. Using this same experimental model we now report the identification of a MAPK kinase (MAPKK) that functions upstream in this pathway. This kinase, referred to as PcMKK5 based on sequence similarity to Arabidopsis thaliana AtMKK5, is activated in parsley cells following Pep-13 treatment and functions as an in vivo activator of all three MAPKs previously shown to be involved in this response. Gain- and loss-of-function mutant versions of PcMKK5, when used in protoplast co-transfection assays, demonstrated that kinase activity of PcMKK5 is required for PR gene promoter activation following Pep-13 treatment. Furthermore, using specific antibodies and immunofluorescent labeling, we demonstrate that activation of MAPKs in parsley cells correlates with an increase in their nuclear localization, which is not detectable for activated PcMKK5. These results suggest that activation of gene expression through MAPK cascades during innate immune responses in plants involves dynamic changes in the localization of the proteins involved, which may reflect the distribution of key protein substrates for the activated MAPKs.
This paper references
10.1038/415977a
MAP kinase signalling cascade in Arabidopsis innate immunity
T. Asai (2002)
10.1073/PNAS.93.2.765
A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana.
T. Mizoguchi (1996)
10.1146/ANNUREV.IMMUNOL.20.083001.084359
Innate immune recognition.
C. Janeway (2002)
10.1016/S1369-5266(02)00265-0
Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns.
T. Nürnberger (2002)
10.1074/jbc.M007418200
Differential Activation of Four Specific MAPK Pathways by Distinct Elicitors*
F. Cardinale (2000)
10.1046/J.1432-1033.2003.03707.X
Fidelity and spatio-temporal control in MAP kinase (ERKs) signalling.
J. Pouyssegur (2002)
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)
10.1105/tpc.10.3.435
Activation of the Tobacco SIP Kinase by Both a Cell Wall–Derived Carbohydrate Elicitor and Purified Proteinaceous Elicitins from Phytophthora spp
S. Zhang (1998)
10.1074/JBC.M109495200
Cell Death Mediated by MAPK Is Associated with Hydrogen Peroxide Production in Arabidopsis *
Dongtao Ren (2002)
10.1073/PNAS.92.10.4150
Oligopeptide elicitor-mediated defense gene activation in cultured parsley cells.
K. Hahlbrock (1995)
10.1104/PP.122.4.1301
ATMPK4, an Arabidopsis homolog of mitogen-activated protein kinase, is activated in vitro by AtMEK1 through threonine phosphorylation.
Y. Huang (2000)
10.3905/jpm.1991.50
Trends
Martin S. Fridson (1991)
10.1094/MPMI.2000.13.1.118
Molecular cloning and characterization of a tobacco MAP kinase kinase that interacts with SIPK.
Y. Liu (2000)
10.1023/A:1010633215445
Activation of tomato PR and wound-related genes by a mutagenized tomato MAP kinase kinase through divergent pathways
T. Xing (2004)
10.1083/JCB.142.3.625
Growth Factor–induced p42/p44 MAPK Nuclear Translocation and Retention Requires Both MAPK Activation and Neosynthesis of Nuclear Anchoring Proteins
P. Lenormand (1998)
10.4049/jimmunol.166.7.4416
Nuclear Shuttling of Mitogen-Activated Protein (MAP) Kinase (Extracellular Signal-Regulated Kinase (ERK) 2) Was Dynamically Controlled by MAP/ERK Kinase After Antigen Stimulation in RBL-2H3 Cells
T. Furuno (2001)
10.1002/j.1460-2075.1996.tb00953.x
Interaction of elicitor‐induced DNA‐binding proteins with elicitor response elements in the promoters of parsley PR1 genes.
P. Rushton (1996)
A cell cycle regulated MAP kinase with a possible role in cytokinesis in tobacco cells.
O. Calderini (1998)
Results Probl
T. Mizoguchi (2000)
10.1093/emboj/17.19.5606
Regulated nucleo/cytoplasmic exchange of HOG1 MAPK requires the importin β homologs NMD5 and XPO1
P. Ferrigno (1998)
10.1093/emboj/18.17.4689
Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors
T. Eulgem (1999)
10.1073/PNAS.92.6.2338
Covalent cross-linking of the Phytophthora megasperma oligopeptide elicitor to its receptor in parsley membranes.
T. Nürnberger (1995)
10.1006/PREP.1994.1020
pJC20 and pJC40--two high-copy-number vectors for T7 RNA polymerase-dependent expression of recombinant genes in Escherichia coli.
J. Clos (1994)
10.1126/SCIENCE.1068883
Decoding the Patterns of Self and Nonself by the Innate Immune System
R. Medzhitov (2002)
10.1016/S0092-8674(00)81189-7
Phosphorylation of the MAP Kinase ERK2 Promotes Its Homodimerization and Nuclear Translocation
A. V. Khokhlatchev (1998)
10.1073/PNAS.98.2.741
Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco.
K. Yang (2001)
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)
Protein Expres
Y. Liu (1994)
10.1126/SCIENCE.276.5321.2054
Receptor-mediated activation of a MAP kinase in pathogen defense of plants.
W. Ligterink (1997)
10.1105/tpc.11.1.101
A MAP Kinase Is Activated Late in Plant Mitosis and Becomes Localized to the Plane of Cell Division
L. Bögre (1999)
Osjab (Accession No. AF072849): a rice homolog of the human AB1transcriptional coactivator (PGR98-149).
A. Meijer (1998)
10.1105/TPC.010256
Convergence and divergence of stress-induced mitogen-activated protein kinase signaling pathways at the level of two distinct mitogen-activated protein kinase kinases.
F. Cardinale (2002)
10.1016/S1047-8477(02)00542-7
MAPKs entry into the nucleus at specific interchromatin domains in plant differentiation and proliferation processes.
M. Coronado (2002)
10.1074/JBC.273.25.15507
Rapid Activation and Nuclear Translocation of Mitogen-activated Protein Kinases in Response to Physiological Concentration of Glucose in the MIN6 Pancreatic β Cell Line*
C. Benes (1998)
10.1016/S0167-4781(02)00298-1
Leucine zipper-containing WRKY proteins widen the spectrum of immediate early elicitor-induced WRKY transcription factors in parsley.
R. S. Cormack (2002)
10.1126/science.270.5244.1988
Tobacco MAP Kinase: A Possible Mediator in Wound Signal Transduction Pathways
S. Seo (1995)
10.1074/JBC.M300878200
Stress-induced Protein Phosphatase 2C Is a Negative Regulator of a Mitogen-activated Protein Kinase*
I. Meskiene (2003)
10.1016/S1360-1385(02)02302-6
Mitogen-activated protein kinase cascades in plants: a new nomenclature.
Kazuya Ichimura (2002)
10.1093/emboj/16.8.1901
Interaction of MAP kinase with MAP kinase kinase: its possible role in the control of nucleocytoplasmic transport of MAP kinase
M. Fukuda (1997)
10.1006/JSBI.2000.4249
Defined nuclear changes accompany the reprogramming of the microspore to embryogenesis.
P. Testillano (2000)
10.1007/BF00333403
Gene structure and in situ transcript localization of pathogenesis-related protein 1 in parsley
I. Somssich (2004)
10.1016/0092-8674(94)90423-5
High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses
T. Nürnberger (1994)
10.1515/BC.2001.142
Recent Advances in Plant MAP Kinase Signalling
K. Zwerger (2001)
10.1093/emboj/cdf349
Involvement of the mitogen‐activated protein kinase SIMK in regulation of root hair tip growth
Jozef Šamaj (2002)
10.1073/PNAS.95.13.7433
Resistance gene N-mediated de novo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection.
S. Zhang (1998)
10.1046/J.1365-313X.2000.00741.X
Ozone treatment rapidly activates MAP kinase signalling in plants.
M. Samuel (2000)
10.1093/emboj/18.3.664
Nuclear translocation of p42/p44 mitogen‐activated protein kinase is required for growth factor‐induced gene expression and cell cycle entry
A. Brunet (1999)
10.1093/emboj/cdf667
Pep‐13, a plant defense‐inducing pathogen‐associated pattern from Phytophthora transglutaminases
F. Brunner (2002)
10.1007/978-3-540-49166-8_3
MAP kinase cascades in Arabidopsis: their roles in stress and hormone responses.
T. Mizoguchi (2000)
10.1046/J.1365-313X.1999.00528.X
MAP kinase activation by hypoosmotic stress of tobacco cell suspensions: towards the oxidative burst response?
Cazalé (1999)
10.1016/S1360-1385(01)02103-3
MAPK cascades in plant defense signaling.
S. Zhang (2001)
10.1074/JBC.M208200200
Mitogen-activated Protein Kinases Play an Essential Role in Oxidative Burst-independent Expression of Pathogenesis-related Genes in Parsley*
T. Kroj (2003)
10.1016/S1360-1385(01)02019-2
Signal transmission in the plant immune response.
T. Nürnberger (2001)
10.1074/jbc.M908723199
Significance of Nuclear Relocalization of ERK1/2 in Reactivation of c-fos Transcription and DNA Synthesis in Senescent Fibroblasts*
J. Kim‐Kaneyama (2000)
10.1105/tpc.12.8.1425
Receptor-Mediated Increase in Cytoplasmic Free Calcium Required for Activation of Pathogen Defense in Parsley
B. Blume (2000)
10.1073/PNAS.94.9.4800
Elicitor-stimulated ion fluxes and O2- from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley.
T. Jabs (1997)



This paper is referenced by
10.1093/jnci/djn365
Effect of disrupting seven-in-absentia homolog 2 function on lung cancer cell growth.
A. Ahmed (2008)
10.1371/journal.pgen.1004015
Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana
Kenichi Tsuda (2013)
10.1101/266171
Phosphorylation of the exocyst subunit Exo70B2 contributes to the regulation of its function
Ooi-Kock Teh (2018)
10.1016/J.PBI.2005.07.006
Role of mitogen-activated protein kinases in plant immunity.
K. Pedley (2005)
10.1186/1471-2229-13-121
Interaction between two rice mitogen activated protein kinases and its possible role in plant defense
A. Sheikh (2012)
OsRac1 and Heterotrimeric G-Protein in Rice 1(w)
Damien Lieberherr (2005)
10.1074/mcp.M500007-MCP200
High Throughput Identification of Potential Arabidopsis Mitogen-activated Protein Kinases Substrates*S
Tanja Feilner (2005)
10.1016/J.PBI.2004.07.012
WRKY transcription factors: from DNA binding towards biological function.
Bekir Ulker (2004)
10.1007/978-3-540-28516-8_7
Signal Perception and Transduction in Plant Innate Immunity
T. Nürnberger (2006)
10.1007/s13258-010-0010-0
Comparative genomic analysis of mitogen activated protein kinase gene family in grapevine
T. Hyun (2010)
10.3390/plants3010160
Functions of Calcium-Dependent Protein Kinases in Plant Innate Immunity
Xiquan Gao (2014)
10.1101/825323
Phosphorylation of the CAMTA3 transcription factor triggers its destabilization and nuclear export
Xiyuan Jiang (2019)
10.1007/978-3-319-21033-9_7
Nuclear Dismantling Events: Crucial Steps During the Execution of Plant Programmed Cell Death
F. Domínguez (2015)
10.1104/pp.112.200071
Rice Mitogen-Activated Protein Kinase Interactome Analysis Using the Yeast Two-Hybrid System1[C][W]
Raksha Singh (2012)
Plant pathogens: how can molecular genetic information on plant pathogens assist in breeding disease resistant crops
K. Hammond-Kosack (2004)
10.3389/fpls.2017.01292
Stress-Related Mitogen-Activated Protein Kinases Stimulate the Accumulation of Small Molecules and Proteins in Arabidopsis thaliana Root Exudates
Nadine Strehmel (2017)
10.1093/jxb/ers086
Cotton GhMKK5 affects disease resistance, induces HR-like cell death, and reduces the tolerance to salt and drought stress in transgenic Nicotiana benthamiana
L. Zhang (2012)
10.1073/pnas.0810206106
Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling
Gerit Bethke (2009)
10.2478/s11658-010-0024-2
R proteins as fundamentals of plant innate immunity
Sylwester Głowacki (2010)
10.1007/s11103-017-0641-5
A novel family of proline/serine-rich proteins, which are phospho-targets of stress-related mitogen-activated protein kinases, differentially regulates growth and pathogen defense in Arabidopsis thaliana
M. A. T. Palm-Forster (2017)
10.1111/j.1469-8137.2012.04226.x
StCDPK5 confers resistance to late blight pathogen but increases susceptibility to early blight pathogen in potato via reactive oxygen species burst.
Michie Kobayashi (2012)
10.1104/pp.106.091389
MEKK1 Is Required for flg22-Induced MPK4 Activation in Arabidopsis Plants1[C][W]
M. Suarez-Rodriguez (2006)
10.1104/pp.112.210724
The MPK6-ERF6-ROS-Responsive cis-Acting Element7/GCC Box Complex Modulates Oxidative Gene Transcription and the Oxidative Response in Arabidopsis1[W][OA]
P. Wang (2013)
10.1093/jxb/err313
In Posidonia oceanica cadmium induces changes in DNA methylation and chromatin patterning
M. Greco (2012)
10.1016/j.ab.2012.05.015
A mutagenesis-based screen to rapidly identify phosphorylation sites in mitogen-activated protein kinase substrates.
Mieder A. T. Palm-Forster (2012)
10.1111/J.1365-313X.2006.03022.X
A high-throughput screen of cell-death-inducing factors in Nicotiana benthamiana identifies a novel MAPKK that mediates INF1-induced cell death signaling and non-host resistance to Pseudomonas cichorii.
Yoshihiro Takahashi (2007)
The MPK 6-ERF 6-ROS-Responsive cis-Acting Element 7 / GCC Box Complex Modulates Oxidative Gene Transcription and the Oxidative Response in Arabidopsis 1 [ W ] [ OA ]
P. Wang (2013)
10.4161/psb.4.7.9039
Sometimes new results raise new questions
Gerit Bethke (2009)
Involvement of PPS 3 Phosphorylated by Elicitor-Responsive Mitogen-Activated Protein Kinases in the Regulation of Plant Cell Death 1
S. Katou (2005)
10.1104/pp.108.119511
The Wheat Mitogen-Activated Protein Kinases TaMPK3 and TaMPK6 Are Differentially Regulated at Multiple Levels during Compatible Disease Interactions with Mycosphaerella graminicola1[W]
J. Rudd (2008)
MEKK 1 Is Required for flg 22-Induced MPK 4 Activation in Arabidopsis Plants 1 [ C ] [ W ]
M. Suarez-Rodriguez (2007)
10.5451/unibas-003915394
Characterization of a novel bacterial PAMP - elongation factor Tu - and its role in "Arabidopsis thaliana" defense and immunity
G. Kunze (2005)
See more
Semantic Scholar Logo Some data provided by SemanticScholar