Perception of the Arabidopsis Danger Signal Peptide 1 Involves the Pattern Recognition Receptor AtPEPR1 and Its Close Homologue AtPEPR2
Plasma membrane-borne pattern recognition receptors, which recognize microbe-associated molecular patterns and endogenous damage-associated molecular patterns, provide the first line of defense in innate immunity. In plants, leucine-rich repeat receptor kinases fulfill this role, as exemplified by F...
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Published in | The Journal of biological chemistry Vol. 285; no. 18; pp. 13471 - 13479 |
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Main Authors | , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Elsevier Inc
30.04.2010
American Society for Biochemistry and Molecular Biology |
Subjects | |
Online Access | Get full text |
ISSN | 0021-9258 1083-351X 1083-351X |
DOI | 10.1074/jbc.M109.097394 |
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Abstract | Plasma membrane-borne pattern recognition receptors, which recognize microbe-associated molecular patterns and endogenous damage-associated molecular patterns, provide the first line of defense in innate immunity. In plants, leucine-rich repeat receptor kinases fulfill this role, as exemplified by FLS2 and EFR, the receptors for the microbe-associated molecular patterns flagellin and elongation factor Tu. Here we examined the perception of the damage-associated molecular pattern peptide 1 (AtPep1), an endogenous peptide of Arabidopsis identified earlier and shown to be perceived by the leucine-rich repeat protein kinase PEPR1. Using seedling growth inhibition, elicitation of an oxidative burst and induction of ethylene biosynthesis, we show that wild type plants and the pepr1 and pepr2 mutants, affected in PEPR1 and in its homologue PEPR2, are sensitive to AtPep1, but that the double mutant pepr1/pepr2 is completely insensitive. As a central body of our study, we provide electrophysiological evidence that at the level of the plasma membrane, AtPep1 triggers a receptor-dependent transient depolarization through activation of plasma membrane anion channels, and that this effect is absent in the double mutant pepr1/pepr2. The double mutant also fails to respond to AtPep2 and AtPep3, two distant homologues of AtPep1 on the basis of homology screening, implying that the PEPR1 and PEPR2 are responsible for their perception too. Our findings provide a basic framework to study the biological role of AtPep1-related danger signals and their cognate receptors. |
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AbstractList | Plasma membrane-borne pattern recognition receptors, which recognize microbe-associated molecular patterns and endogenous damage-associated molecular patterns, provide the first line of defense in innate immunity. In plants, leucine-rich repeat receptor kinases fulfill this role, as exemplified by FLS2 and EFR, the receptors for the microbe-associated molecular patterns flagellin and elongation factor Tu. Here we examined the perception of the damage-associated molecular pattern peptide 1 (AtPep1), an endogenous peptide of Arabidopsis identified earlier and shown to be perceived by the leucine-rich repeat protein kinase PEPR1. Using seedling growth inhibition, elicitation of an oxidative burst and induction of ethylene biosynthesis, we show that wild type plants and the pepr1 and pepr2 mutants, affected in PEPR1 and in its homologue PEPR2, are sensitive to AtPep1, but that the double mutant pepr1/pepr2 is completely insensitive. As a central body of our study, we provide electrophysiological evidence that at the level of the plasma membrane, AtPep1 triggers a receptor-dependent transient depolarization through activation of plasma membrane anion channels, and that this effect is absent in the double mutant pepr1/pepr2. The double mutant also fails to respond to AtPep2 and AtPep3, two distant homologues of AtPep1 on the basis of homology screening, implying that the PEPR1 and PEPR2 are responsible for their perception too. Our findings provide a basic framework to study the biological role of AtPep1-related danger signals and their cognate receptors. Plasma membrane-borne pattern recognition receptors, which recognize microbe-associated molecular patterns and endogenous damage-associated molecular patterns, provide the first line of defense in innate immunity. In plants, leucine-rich repeat receptor kinases fulfill this role, as exemplified by FLS2 and EFR, the receptors for the microbe-associated molecular patterns flagellin and elongation factor Tu. Here we examined the perception of the damage-associated molecular pattern peptide 1 ( At Pep1), an endogenous peptide of Arabidopsis identified earlier and shown to be perceived by the leucine-rich repeat protein kinase PEPR1. Using seedling growth inhibition, elicitation of an oxidative burst and induction of ethylene biosynthesis, we show that wild type plants and the pepr1 and pepr2 mutants, affected in PEPR1 and in its homologue PEPR2, are sensitive to At Pep1, but that the double mutant pepr1 / pepr2 is completely insensitive. As a central body of our study, we provide electrophysiological evidence that at the level of the plasma membrane, At Pep1 triggers a receptor-dependent transient depolarization through activation of plasma membrane anion channels, and that this effect is absent in the double mutant pepr1 / pepr2 . The double mutant also fails to respond to At Pep2 and At Pep3, two distant homologues of At Pep1 on the basis of homology screening, implying that the PEPR1 and PEPR2 are responsible for their perception too. Our findings provide a basic framework to study the biological role of At Pep1-related danger signals and their cognate receptors. Plasma membrane-borne pattern recognition receptors, which recognize microbe-associated molecular patterns and endogenous damage-associated molecular patterns, provide the first line of defense in innate immunity. In plants, leucine-rich repeat receptor kinases fulfill this role, as exemplified by FLS2 and EFR, the receptors for the microbe-associated molecular patterns flagellin and elongation factor Tu. Here we examined the perception of the damage-associated molecular pattern peptide 1 (AtPep1), an endogenous peptide of Arabidopsis identified earlier and shown to be perceived by the leucine-rich repeat protein kinase PEPR1. Using seedling growth inhibition, elicitation of an oxidative burst and induction of ethylene biosynthesis, we show that wild type plants and the pepr1 and pepr2 mutants, affected in PEPR1 and in its homologue PEPR2, are sensitive to AtPep1, but that the double mutant pepr1/pepr2 is completely insensitive. As a central body of our study, we provide electrophysiological evidence that at the level of the plasma membrane, AtPep1 triggers a receptor-dependent transient depolarization through activation of plasma membrane anion channels, and that this effect is absent in the double mutant pepr1/pepr2. The double mutant also fails to respond to AtPep2 and AtPep3, two distant homologues of AtPep1 on the basis of homology screening, implying that the PEPR1 and PEPR2 are responsible for their perception too. Our findings provide a basic framework to study the biological role of AtPep1-related danger signals and their cognate receptors.Plasma membrane-borne pattern recognition receptors, which recognize microbe-associated molecular patterns and endogenous damage-associated molecular patterns, provide the first line of defense in innate immunity. In plants, leucine-rich repeat receptor kinases fulfill this role, as exemplified by FLS2 and EFR, the receptors for the microbe-associated molecular patterns flagellin and elongation factor Tu. Here we examined the perception of the damage-associated molecular pattern peptide 1 (AtPep1), an endogenous peptide of Arabidopsis identified earlier and shown to be perceived by the leucine-rich repeat protein kinase PEPR1. Using seedling growth inhibition, elicitation of an oxidative burst and induction of ethylene biosynthesis, we show that wild type plants and the pepr1 and pepr2 mutants, affected in PEPR1 and in its homologue PEPR2, are sensitive to AtPep1, but that the double mutant pepr1/pepr2 is completely insensitive. As a central body of our study, we provide electrophysiological evidence that at the level of the plasma membrane, AtPep1 triggers a receptor-dependent transient depolarization through activation of plasma membrane anion channels, and that this effect is absent in the double mutant pepr1/pepr2. The double mutant also fails to respond to AtPep2 and AtPep3, two distant homologues of AtPep1 on the basis of homology screening, implying that the PEPR1 and PEPR2 are responsible for their perception too. Our findings provide a basic framework to study the biological role of AtPep1-related danger signals and their cognate receptors. |
Author | Arents, Michael Postel, Sandra Becker, Dirk Mentzel, Tobias Jeworutzki, Elena Krol, Elzbieta Kemmerling, Birgit Hedrich, Rainer Chinchilla, Delphine Felix, Georg Boller, Thomas Al-Rasheid, Khaled A.S. |
Author_xml | – sequence: 1 givenname: Elzbieta surname: Krol fullname: Krol, Elzbieta organization: Department of Molecular Plant Physiology and Biophysics, University of Wuerzburg, 97082 Wuerzburg, Germany – sequence: 2 givenname: Tobias surname: Mentzel fullname: Mentzel, Tobias organization: Zuerich-Basel Plant Science Centre, Botanical Institute, University of Basel, 4056 Basel, Switzerland – sequence: 3 givenname: Delphine surname: Chinchilla fullname: Chinchilla, Delphine organization: Zuerich-Basel Plant Science Centre, Botanical Institute, University of Basel, 4056 Basel, Switzerland – sequence: 4 givenname: Thomas surname: Boller fullname: Boller, Thomas organization: Zuerich-Basel Plant Science Centre, Botanical Institute, University of Basel, 4056 Basel, Switzerland – sequence: 5 givenname: Georg surname: Felix fullname: Felix, Georg organization: Zentrum für Molekularbiologie der Pflanzen, Plant Biochemistry, University Tuebingen, Auf der Morgenstelle 5, 72076 Tuebingen, Germany – sequence: 6 givenname: Birgit surname: Kemmerling fullname: Kemmerling, Birgit organization: Zentrum für Molekularbiologie der Pflanzen, Plant Biochemistry, University Tuebingen, Auf der Morgenstelle 5, 72076 Tuebingen, Germany – sequence: 7 givenname: Sandra surname: Postel fullname: Postel, Sandra organization: Zentrum für Molekularbiologie der Pflanzen, Plant Biochemistry, University Tuebingen, Auf der Morgenstelle 5, 72076 Tuebingen, Germany – sequence: 8 givenname: Michael surname: Arents fullname: Arents, Michael organization: Department of Molecular Plant Physiology and Biophysics, University of Wuerzburg, 97082 Wuerzburg, Germany – sequence: 9 givenname: Elena surname: Jeworutzki fullname: Jeworutzki, Elena organization: Department of Molecular Plant Physiology and Biophysics, University of Wuerzburg, 97082 Wuerzburg, Germany – sequence: 10 givenname: Khaled A.S. surname: Al-Rasheid fullname: Al-Rasheid, Khaled A.S. organization: King Saud University, Zoology Department, College of Science, P. O. Box 2455, Riyadh 11451, Saudi Arabia – sequence: 11 givenname: Dirk surname: Becker fullname: Becker, Dirk email: dbecker@botanik.uni-wuerzburg.de organization: Department of Molecular Plant Physiology and Biophysics, University of Wuerzburg, 97082 Wuerzburg, Germany – sequence: 12 givenname: Rainer surname: Hedrich fullname: Hedrich, Rainer organization: Department of Molecular Plant Physiology and Biophysics, University of Wuerzburg, 97082 Wuerzburg, Germany |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/20200150$$D View this record in MEDLINE/PubMed |
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ContentType | Journal Article |
Copyright | 2010 © 2010 ASBMB. Currently published by Elsevier Inc; originally published by American Society for Biochemistry and Molecular Biology. 2010 by The American Society for Biochemistry and Molecular Biology, Inc. |
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Keywords | Receptors Calcium Ion Channels Arabidopsis Pathogen-associated Molecular Pattern (PAMP) Innate immunity Pattern Recognition Receptor |
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SubjectTerms | Arabidopsis Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Calcium Cell Biology Cell Membrane - genetics Cell Membrane - metabolism Innate immunity Ion Channels Membrane Potentials - physiology Mutation Pathogen-associated Molecular Pattern (PAMP) Pattern Recognition Receptor Plant Biology Receptors Receptors, Pattern Recognition - genetics Receptors, Pattern Recognition - metabolism Seedlings - genetics Seedlings - metabolism Sequence Homology, Amino Acid Signal Transduction - physiology Trans-Activators - genetics Trans-Activators - metabolism |
Title | Perception of the Arabidopsis Danger Signal Peptide 1 Involves the Pattern Recognition Receptor AtPEPR1 and Its Close Homologue AtPEPR2 |
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