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 inThe Journal of biological chemistry Vol. 285; no. 18; pp. 13471 - 13479
Main Authors Krol, Elzbieta, Mentzel, Tobias, Chinchilla, Delphine, Boller, Thomas, Felix, Georg, Kemmerling, Birgit, Postel, Sandra, Arents, Michael, Jeworutzki, Elena, Al-Rasheid, Khaled A.S., Becker, Dirk, Hedrich, Rainer
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 30.04.2010
American Society for Biochemistry and Molecular Biology
Subjects
Online AccessGet full text
ISSN0021-9258
1083-351X
1083-351X
DOI10.1074/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.
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.
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  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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Keywords Receptors
Calcium
Ion Channels
Arabidopsis
Pathogen-associated Molecular Pattern (PAMP)
Innate immunity
Pattern Recognition Receptor
Language English
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Snippet Plasma membrane-borne pattern recognition receptors, which recognize microbe-associated molecular patterns and endogenous damage-associated molecular patterns,...
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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
URI https://dx.doi.org/10.1074/jbc.M109.097394
https://www.ncbi.nlm.nih.gov/pubmed/20200150
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https://pubmed.ncbi.nlm.nih.gov/PMC2859507
Volume 285
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