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Perception of MAMPs and DAMPs by PRRs in plants

English title Perception of MAMPs and DAMPs by PRRs in plants
Applicant Boller Thomas
Number 127563
Funding scheme Project funding
Research institution Botanisches Institut Universität Basel
Institution of higher education University of Basel - BS
Main discipline Botany
Start/End 01.10.2009 - 30.09.2012
Approved amount 836'451.00
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All Disciplines (3)

Discipline
Botany
Molecular Biology
Biochemistry

Keywords (8)

Plant-Microbe Interactions; Innate Immunity; Disease Resistance; Symbiosis; plant defense; pattern recognition receptors; microbe-associated molecular patterns; damage-associated molecular patterns

Lay Summary (English)

Lead
Lay summary
Plants are exposed to myriads of potential microbial pathogens, but the world is still green. Why? One reason is that the plants have a highly efficient innate immunity system to ward off potential pathogens. The term "innate immunity", widely used in medicine as well as plant biology, stands for an active defense response against microbial attack. It is based on the perception of characteristic microbial molecules, collectively called "MAMPs" ("microbe-associated molecular patterns"). These "MAMPs" are recognized by so-called "pattern-recognition receptors", receptors at the cell surface that recognize the MAMP and send a danger signal to the cell's interior.Bacterial flagellin acts as such a MAMP, both in plants and animals. In our previous work supported by the SNF, we have identified the PRR responsible for flagellin perception in the model plant Arabidopsis, namely the leucine-rich repeat receptor kinase FLS2. We have analyzed flagellin perception by FLS2 extensively already, as summarized in a recent scientific review (Boller and Felix, Annual Review of Plant Biology, 60, 379-406, 2009).In the current project, we want to find out, in molecular detail, how flagellin interacts with the pattern-recognition receptor FLS2, and how signal transduction is initiated. We want to use the current knowledge to define the structural requirements of flagellin to act as functional stimulus when bound to its receptor, FLS2.We also want to address a question that has thus far received little attention in plant innate immunity but seems to become an emerging field in biomedical research, namely innate-immunity stimulation through "damage-associated molecular patterns" (DAMPs). DAMPs are molecules that are released from within the cells into the extracellular space, due to damage caused by an invading pathogen, and then are perceived by PRRs on the surface of neighboring cells. In this respect, we want to take up fascinating work by the group of Clarence A. Ryan, who has described such a DAMP, AtPep1, and its PRR, PEPR1, in the model plant Arabidopsis, shortly before his untimely death in 2007. We want to compare the signal pathways induced by MAMPs (such as flagellin) and DAMPs (such as AtPep1). Do these signaling pathways converge at some point? Do they act synergistically or independently?Overall, our research helps to make use of the plants' natural resistance mechanisms as an environmentally friendly alternative to chemical plant protection. Because of the striking similarities of the innate immunity pathways in animals and plants, our work is not only relevant to plant biology per se, but also to animal science and human medicine.
Direct link to Lay Summary Last update: 21.02.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
Contamination Risks in Work with Synthetic Peptides: flg22 as an Example of a Pirate in Commercial Peptide Preparations
Mueller Katharina, Chinchilla Delphine, Albert Markus, Jehle Anna K., Kalbacher Hubert, Boller Thomas, Felix Georg (2012), Contamination Risks in Work with Synthetic Peptides: flg22 as an Example of a Pirate in Commercial Peptide Preparations, in The Plant Cell Online, 24, 3193-3197.
Chimeric FLS2 receptors reveal the basis for differential flagellin perception in Arabidopsis and tomato
Mueller K., Bittel P., Chinchilla D., Jehle A. K., Albert M., Boller T., Felix G. (2012), Chimeric FLS2 receptors reveal the basis for differential flagellin perception in Arabidopsis and tomato, in Plant Cell, 24, 2213-2224.
Functional analysis of NopM, a novel E3 ubiquitin ligase (NEL) domain effector of
Xin D.-W., Liao S., Xie Z.-P., Hann D. R., Steinle L., Boller T., Staehelin C. (2012), Functional analysis of NopM, a novel E3 ubiquitin ligase (NEL) domain effector of, in PLoS Pathogens, 8, 1002707-1002707.
The lectin receptor kinase-VI.2 is required for priming and positively regulates Arabidopsis pattern-triggered immunity
Singh P., Kuo Y.-C., Mishra S., Tsai C.-H., Chien C.-C., Chen C.-W., Desclos-Theveniau M., Chu P.-W., Schulze B., Chinchilla D., Boller T., Zimmerli L. (2012), The lectin receptor kinase-VI.2 is required for priming and positively regulates Arabidopsis pattern-triggered immunity, in Plant Cell, 24, 1256-1270.
Probing the Arabidopsis flagellin receptor: FLS2-FLS2 association and the contributions of specific domains to signaling function
Sun W., Cao Y., Jansen Labby K., Bittel P., Boller T., Bent A. F. (2012), Probing the Arabidopsis flagellin receptor: FLS2-FLS2 association and the contributions of specific domains to signaling function, in Plant Cell, 24, 1096-1113.
Interplay of flg22-induced defence responses and nodulation in
Lopez-Gomez M., Sandal N., Stougaard J., Boller T. (2011), Interplay of flg22-induced defence responses and nodulation in, in Journal of Experimental Botany, 63, 393-401.
Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions
Blom D., Fabbri C., Connor E. C., Schiestl F. P., Klauser D. R., Boller T., Eberl L., Weisskopf L. (2011), Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions, in Environmental Microbiology, 13, 3047-3058.
Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca2+-associated opening of plasma membrane anion channels
Jeworutzki E., Roelfsema M. R. G., Anschutz U., Krol E., Elzenga J. T. M., Felix G., Boller T., Hedrich R., Becker D. (2010), Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca2+-associated opening of plasma membrane anion channels, in Plant Journal, 62, 367-378.
Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2
Krol E., Mentzel T., Chinchilla D., Boller T., Felix G., Kemmerling B., Postel S., Arents M., Jeworutzki E., Al-Rasheid K. A. S., Becker D., Hedrich R. (2010), Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2, in Journal of Biological Chemistry, 285, 13471-13479.
Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1
Schulze B., Mentzel T., Jehle A. K., Mueller K., Beeler S., Boller T., Felix G., Chinchilla D. (2010), Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1, in Journal of Biological Chemistry, 285, 9444-9451.
A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors
Boller T., Felix G. (2009), A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors, in Annual Review of Plant Biology, 60, 379-406.
Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens
Boller T., He S. Y. (2009), Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens, in Science, 324, 742-744.
Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele
Lu X., Tintor N., Mentzel T., Kombrink E., Boller T., Robatzek S., Schulze-Lefert P., Saijo Y. (2009), Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele, in Proceedings of the National Academy of Sciences of the United States of America, 106, 22522-22527.

Collaboration

Group / person Country
Types of collaboration
Department of Biology and Biochemistry, University of Bath: Richard Cooper Great Britain and Northern Ireland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Sainsbury Laboratories, John Innes Centre, Norwich: Silke Robatzek, Cyril Zipfel Great Britain and Northern Ireland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel
Max-Planck-Institut für Züchtungsforschung, Köln: Paul Schulze-Lefert Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Department of Plant Pathology, University of Wisconsin, Madison: Andrew Bent United States of America (North America)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Institute of Plant Biology, National Taiwan University, Taipeh: Laurent Zimmerli Taiwan (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
ZMBP, Universität Tübingen: Georg Felix. Birgit Kemmerling, Thorsten Nürnberger Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Lehrstuhl für Botanik, Universität Würzburg: Rainer Hedrich Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
Institut für Pflanzenbiologie, Universität Zürich: Leo Eberl, Laure Weisskopf, Florian Schiestl Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel
Sun Yat-sen University, Guangzhou: Christian Staehelin China (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication

Associated projects

Number Title Start Funding scheme
144084 Perception of MAMPs and DAMPs by PRRs in Plants 01.10.2012 Project funding
105852 Perception and transduction of microbial signals in plants 01.10.2004 Project funding

Abstract

Plants are exposed to myriads of potential microbial pathogens, but the world is still green, because plants possess an efficient innate immune system to detect and ward off potentially dangerous microbes. How does the plant's innate immune system work? In the course of my current project of the Swiss National Science Foundation (2004-2009), our studies firmly established the importance of the perception of microbe-associated molecular patterns (MAMPs) by pattern recognition receptors (PRRs) for innate immunity in plants, and caused a renaissance of the "elicitor concept", as we summarized in a recent review (Boller and Felix, ANNUAL REVIEW OF PLANT BIOLOGY, 2009). In fact, the two MAMP/PRR pairs of Arabidopsis that we discovered and analyzed, initially bacterial flagellin and the plant's leucine-rich-repeat receptor kinase (LRR-RK) FLS2, and subsequently bacterial elongation factor EF-Tu and the plant's LRR-RK EFR, have now become widely-used models to study the plants' innate immune system.In the proposal for the next three years (2009-2012), we want to continue and expand promising aspects of our current work. Our first focus will be on structure-function relationships in the interaction between the MAMP signals and the MAMP binding sites on the LRR-domains of the PRRs. Here, we have advanced particularly well during recent months, and we want to use the current knowledge to define the structural requirements of MAMP ligands to act as functional stimuli when bound to their receptors.We also want to address a question that has thus far received little attention in plant innate immunity but seems to become an emerging field in biomedical research, namely innate-immunity stimulation through "damage-associated molecular patterns" (DAMPs). DAMPs are molecules (or characteristic "epitopes") that are released from within the cells, or from the intact cell wall, into the extracellular space, due to damage caused by an invading pathogen, and then are perceived by PRRs on neighboring cells. In this respect, we want to take up fascinating work by the group of Clarence A. Ryan, who has described AtPep1 and PEPR1 as a DAMP/PRR pair in Arabidopsis, shortly before his untimely death in 2007. AtPep1 is a 23 amino acid peptide derived from a small cytoplasmic protein, PROPEP1. AtPep1 provokes a type of innate immunity response when exogenously applied to Arabidopsis cells, in subnanomolar concentrations. The receptor of AtPep1 appears to be a LRR-RK similar to FLS2 and EFR, named PEPR1. We want to compare the AtPep1/PEPR1 response, as a model of a DAMP/PRR interaction, with the flagellin/FLS2 and the EF-Tu/EFR response, as models of the MAMP/PRR interaction. Do these signaling pathways converge at some point, or do they act independently? Are the ligand-binding processes similar, and can the extracellular domains of the receptors be "swapped" to obtain functional chimeric receptors?DAMP signaling might be systemic, spreading throughout the plant from the initially locally confined area of signal perception. In this respect, we want to test, for both MAMPs and DAMPs, whether they can provoke a systemic response upon local application, through unknown second messengers, or whether they can be transported themselves through the plant's vascular system and function as signals at a distant systemic site.Finally, we want to make use of our MAMP/PRR and DAMP/PRR models to further investigate the ways successful pathogens circumvent this first line of defense. We want to focus on bacterial effectors that interfere with signaling at the earliest stages, ideally at the level of the receptor complexes themselves, as recently described for two classic bacterial effectors, AvrPto and AvrPtoB.We hope that the research outlined in the present project, in conjunction with studies on BAK1 currently performed by Delphine Chinchilla in our institute, with her separate independent SNF project, and also in conjunction with the planned studies by Misha Pooggin on the role of innate immunity in the plants' defense, who has just submitted an SNF proposal, will further enrich and expand our knowledge of plant innate immunity.
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