Transgenic Expression of the Dicotyledonous Pattern Recognition Receptor EFR in Rice Leads to Ligand-Dependent Activation of Defense Responses
Plant plasma membrane localized pattern recognition receptors (PRRs) detect extracellular pathogen-associated molecules. PRRs such as Arabidopsis EFR and rice XA21 are taxonomically restricted and are absent from most plant genomes. Here we show that rice plants expressing EFR or the chimeric recept...
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| Published in | PLoS pathogens Vol. 11; no. 3; p. e1004809 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.03.2015
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1553-7374 1553-7366 1553-7374 |
| DOI | 10.1371/journal.ppat.1004809 |
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| Abstract | Plant plasma membrane localized pattern recognition receptors (PRRs) detect extracellular pathogen-associated molecules. PRRs such as Arabidopsis EFR and rice XA21 are taxonomically restricted and are absent from most plant genomes. Here we show that rice plants expressing EFR or the chimeric receptor EFR::XA21, containing the EFR ectodomain and the XA21 intracellular domain, sense both Escherichia coli- and Xanthomonas oryzae pv. oryzae (Xoo)-derived elf18 peptides at sub-nanomolar concentrations. Treatment of EFR and EFR::XA21 rice leaf tissue with elf18 leads to MAP kinase activation, reactive oxygen production and defense gene expression. Although expression of EFR does not lead to robust enhanced resistance to fully virulent Xoo isolates, it does lead to quantitatively enhanced resistance to weakly virulent Xoo isolates. EFR interacts with OsSERK2 and the XA21 binding protein 24 (XB24), two key components of the rice XA21-mediated immune response. Rice-EFR plants silenced for OsSERK2, or overexpressing rice XB24 are compromised in elf18-induced reactive oxygen production and defense gene expression indicating that these proteins are also important for EFR-mediated signaling in transgenic rice. Taken together, our results demonstrate the potential feasibility of enhancing disease resistance in rice and possibly other monocotyledonous crop species by expression of dicotyledonous PRRs. Our results also suggest that Arabidopsis EFR utilizes at least a subset of the known endogenous rice XA21 signaling components. |
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| AbstractList | Plant plasma membrane localized pattern recognition receptors (PRRs) detect extracellular pathogen-associated molecules. PRRs such as Arabidopsis EFR and rice XA21 are taxonomically restricted and are absent from most plant genomes. Here we show that rice plants expressing EFR or the chimeric receptor EFR::XA21, containing the EFR ectodomain and the XA21 intracellular domain, sense both Escherichia coli- and Xanthomonas oryzae pv. oryzae (Xoo)-derived elf18 peptides at sub-nanomolar concentrations. Treatment of EFR and EFR::XA21 rice leaf tissue with elf18 leads to MAP kinase activation, reactive oxygen production and defense gene expression. Although expression of EFR does not lead to robust enhanced resistance to fully virulent Xoo isolates, it does lead to quantitatively enhanced resistance to weakly virulent Xoo isolates. EFR interacts with OsSERK2 and the XA21 binding protein 24 (XB24), two key components of the rice XA21-mediated immune response. Rice-EFR plants silenced for OsSERK2, or overexpressing rice XB24 are compromised in elf18-induced reactive oxygen production and defense gene expression indicating that these proteins are also important for EFR-mediated signaling in transgenic rice. Taken together, our results demonstrate the potential feasibility of enhancing disease resistance in rice and possibly other monocotyledonous crop species by expression of dicotyledonous PRRs. Our results also suggest that Arabidopsis EFR utilizes at least a subset of the known endogenous rice XA21 signaling components.Plant plasma membrane localized pattern recognition receptors (PRRs) detect extracellular pathogen-associated molecules. PRRs such as Arabidopsis EFR and rice XA21 are taxonomically restricted and are absent from most plant genomes. Here we show that rice plants expressing EFR or the chimeric receptor EFR::XA21, containing the EFR ectodomain and the XA21 intracellular domain, sense both Escherichia coli- and Xanthomonas oryzae pv. oryzae (Xoo)-derived elf18 peptides at sub-nanomolar concentrations. Treatment of EFR and EFR::XA21 rice leaf tissue with elf18 leads to MAP kinase activation, reactive oxygen production and defense gene expression. Although expression of EFR does not lead to robust enhanced resistance to fully virulent Xoo isolates, it does lead to quantitatively enhanced resistance to weakly virulent Xoo isolates. EFR interacts with OsSERK2 and the XA21 binding protein 24 (XB24), two key components of the rice XA21-mediated immune response. Rice-EFR plants silenced for OsSERK2, or overexpressing rice XB24 are compromised in elf18-induced reactive oxygen production and defense gene expression indicating that these proteins are also important for EFR-mediated signaling in transgenic rice. Taken together, our results demonstrate the potential feasibility of enhancing disease resistance in rice and possibly other monocotyledonous crop species by expression of dicotyledonous PRRs. Our results also suggest that Arabidopsis EFR utilizes at least a subset of the known endogenous rice XA21 signaling components. Plant plasma membrane localized pattern recognition receptors (PRRs) detect extracellular pathogen-associated molecules. PRRs such as Arabidopsis EFR and rice XA21 are taxonomically restricted and are absent from most plant genomes. Here we show that rice plants expressing EFR or the chimeric receptor EFR::XA21, containing the EFR ectodomain and the XA21 intracellular domain, sense both Escherichia coli- and Xanthomonas oryzae pv. oryzae (Xoo)-derived elf18 peptides at sub-nanomolar concentrations. Treatment of EFR and EFR::XA21 rice leaf tissue with elf18 leads to MAP kinase activation, reactive oxygen production and defense gene expression. Although expression of EFR does not lead to robust enhanced resistance to fully virulent Xoo isolates, it does lead to quantitatively enhanced resistance to weakly virulent Xoo isolates. EFR interacts with OsSERK2 and the XA21 binding protein 24 (XB24), two key components of the rice XA21-mediated immune response. Rice-EFR plants silenced for OsSERK2, or overexpressing rice XB24 are compromised in elf18-induced reactive oxygen production and defense gene expression indicating that these proteins are also important for EFR-mediated signaling in transgenic rice. Taken together, our results demonstrate the potential feasibility of enhancing disease resistance in rice and possibly other monocotyledonous crop species by expression of dicotyledonous PRRs. Our results also suggest that Arabidopsis EFR utilizes at least a subset of the known endogenous rice XA21 signaling components. Plant plasma membrane localized pattern recognition receptors (PRRs) detect extracellular pathogen-associated molecules. PRRs such as Arabidopsis EFR and rice XA21 are taxonomically restricted and are absent from most plant genomes. Here we show that rice plants expressing EFR or the chimeric receptor EFR::XA21, containing the EFR ectodomain and the XA21 intracellular domain, sense both Escherichia coli- and Xanthomonas oryzae pv. oryzae (Xoo)-derived elf18 peptides at sub-nanomolar concentrations. Treatment of EFR and EFR::XA21 rice leaf tissue with elf18 leads to MAP kinase activation, reactive oxygen production and defense gene expression. Although expression of EFR does not lead to robust enhanced resistance to fully virulent Xoo isolates, it does lead to quantitatively enhanced resistance to weakly virulent Xoo isolates. EFR interacts with OsSERK2 and the XA21 binding protein 24 (XB24), two key components of the rice XA21-mediated immune response. Rice-EFR plants silenced for OsSERK2, or overexpressing rice XB24 are compromised in elf18-induced reactive oxygen production and defense gene expression indicating that these proteins are also important for EFR-mediated signaling in transgenic rice. Taken together, our results demonstrate the potential feasibility of enhancing disease resistance in rice and possibly other monocotyledonous crop species by expression of dicotyledonous PRRs. Our results also suggest that Arabidopsis EFR utilizes at least a subset of the known endogenous rice XA21 signaling components. Plants possess multi-layered immune recognition systems. Early in the infection process, plants use receptor proteins to recognize pathogen molecules. Some of these receptors are present in only in a subset of plant species. Transfer of these taxonomically restricted immune receptors between plant species by genetic engineering is a promising approach for boosting the plant immune system. Here we show the successful transfer of an immune receptor from a species in the mustard family, called EFR, to rice. Rice plants expressing EFR are able to sense the bacterial ligand of EFR and elicit an immune response. We show that the EFR receptor is able to use components of the rice immune signaling pathway for its function. Under laboratory conditions, this leads to an enhanced resistance response to two weakly virulent isolates of an economically important bacterial disease of rice. Plant plasma membrane localized pattern recognition receptors (PRRs) detect extracellular pathogen-associated molecules. PRRs such as Arabidopsis EFR and rice XA21 are taxonomically restricted and are absent from most plant genomes. Here we show that rice plants expressing EFR or the chimeric receptor EFR::XA21, containing the EFR ectodomain and the XA21 intracellular domain, sense both Escherichia coli- and Xanthomonas oryzae pv. oryzae (Xoo)-derived elf18 peptides at sub-nanomolar concentrations. Treatment of EFR and EFR::XA21 rice leaf tissue with elf18 leads to MAP kinase activation, reactive oxygen production and defense gene expression. Although expression of EFR does not lead to robust enhanced resistance to fully virulent Xoo isolates, it does lead to quantitatively enhanced resistance to weakly virulent Xoo isolates. EFR interacts with OsSERK2 and the XA21 binding protein 24 (XB24), two key components of the rice XA21-mediated immune response. Rice-EFR plants silenced for OsSERK2, or overexpressing rice XB24 are compromised in elf18-induced reactive oxygen production and defense gene expression indicating that these proteins are also important for EFR-mediated signaling in transgenic rice. Taken together, our results demonstrate the potential feasibility of enhancing disease resistance in rice and possibly other monocotyledonous crop species by expression of dicotyledonous PRRs. Our results also suggest that Arabidopsis EFR utilizes at least a subset of the known endogenous rice XA21 signaling components. |
| Audience | Academic |
| Author | Bahar, Ofir Singan, Vasanth R. Ronald, Pamela C. Chovatia, Mansi Canlas, Patrick E. Daum, Christopher Thomas, Nicolas Zipfel, Cyril Petzold, Christopher J. Daudi, Arsalan Holton, Nicolas Ruan, Deling Kuo, Rita Nekrasov, Vladimir Heazlewood, Joshua L. Schwessinger, Benjamin |
| AuthorAffiliation | University of California Riverside, UNITED STATES 2 Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, United States of America 1 Department of Plant Pathology and the Genome Center, University of California, Davis, Davis, California, United States of America 3 The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom 4 Department of Energy Joint Genome Institute, Walnut Creek, California, United States of America |
| AuthorAffiliation_xml | – name: 2 Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, United States of America – name: 4 Department of Energy Joint Genome Institute, Walnut Creek, California, United States of America – name: 1 Department of Plant Pathology and the Genome Center, University of California, Davis, Davis, California, United States of America – name: 3 The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom – name: University of California Riverside, UNITED STATES |
| Author_xml | – sequence: 1 givenname: Benjamin surname: Schwessinger fullname: Schwessinger, Benjamin – sequence: 2 givenname: Ofir surname: Bahar fullname: Bahar, Ofir – sequence: 3 givenname: Nicolas surname: Thomas fullname: Thomas, Nicolas – sequence: 4 givenname: Nicolas surname: Holton fullname: Holton, Nicolas – sequence: 5 givenname: Vladimir surname: Nekrasov fullname: Nekrasov, Vladimir – sequence: 6 givenname: Deling surname: Ruan fullname: Ruan, Deling – sequence: 7 givenname: Patrick E. surname: Canlas fullname: Canlas, Patrick E. – sequence: 8 givenname: Arsalan surname: Daudi fullname: Daudi, Arsalan – sequence: 9 givenname: Christopher J. surname: Petzold fullname: Petzold, Christopher J. – sequence: 10 givenname: Vasanth R. surname: Singan fullname: Singan, Vasanth R. – sequence: 11 givenname: Rita surname: Kuo fullname: Kuo, Rita – sequence: 12 givenname: Mansi surname: Chovatia fullname: Chovatia, Mansi – sequence: 13 givenname: Christopher surname: Daum fullname: Daum, Christopher – sequence: 14 givenname: Joshua L. surname: Heazlewood fullname: Heazlewood, Joshua L. – sequence: 15 givenname: Cyril surname: Zipfel fullname: Zipfel, Cyril – sequence: 16 givenname: Pamela C. surname: Ronald fullname: Ronald, Pamela C. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25821973$$D View this record in MEDLINE/PubMed https://www.osti.gov/servlets/purl/1191186$$D View this record in Osti.gov |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2015 Public Library of Science 2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Schwessinger B, Bahar O, Thomas N, Holton N, Nekrasov V, Ruan D, et al. (2015) Transgenic Expression of the Dicotyledonous Pattern Recognition Receptor EFR in Rice Leads to Ligand-Dependent Activation of Defense Responses. PLoS Pathog 11(3): e1004809. doi:10.1371/journal.ppat.1004809 |
| Copyright_xml | – notice: COPYRIGHT 2015 Public Library of Science – notice: 2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Schwessinger B, Bahar O, Thomas N, Holton N, Nekrasov V, Ruan D, et al. (2015) Transgenic Expression of the Dicotyledonous Pattern Recognition Receptor EFR in Rice Leads to Ligand-Dependent Activation of Defense Responses. PLoS Pathog 11(3): e1004809. doi:10.1371/journal.ppat.1004809 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AC02-05CH11231 USDOE Office of Science (SC), Biological and Environmental Research (BER) Current address: Department of Plant Pathology and Weed Research, Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel Performed the experiments: BS OB NT NH VN DR PEC AD CJP VRS RK MC CD JLH. Wrote the paper: BS OB NT PCR. Designed Experiments and Analyzed Data: BS OB NT NH CJP VRS JLH PCR. Provided Material: VN CZ. The authors have declared that no competing interests exist. Current address: bio-protocol, Palo Alto, California, United States of America |
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| Snippet | Plant plasma membrane localized pattern recognition receptors (PRRs) detect extracellular pathogen-associated molecules. PRRs such as Arabidopsis EFR and rice... Plant plasma membrane localized pattern recognition receptors (PRRs) detect extracellular pathogen-associated molecules. PRRs such as Arabidopsis EFR and... |
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| SubjectTerms | Arabidopsis Proteins - biosynthesis Arabidopsis Proteins - genetics BASIC BIOLOGICAL SCIENCES Cell membranes Defense Experiments Flowers & plants Gene expression Genetic aspects Genetic engineering Health aspects Identification and classification Kinases Leaves Ligands Ligands (Biochemistry) Oryza - genetics Oryza - metabolism Pattern recognition Plant defenses Plant Proteins - biosynthesis Plant Proteins - genetics Plants, Genetically Modified - genetics Plants, Genetically Modified - metabolism Protein Serine-Threonine Kinases - biosynthesis Protein Serine-Threonine Kinases - genetics Proteins Receptors, Pattern Recognition - biosynthesis Receptors, Pattern Recognition - genetics Recombinant Fusion Proteins - biosynthesis Recombinant Fusion Proteins - genetics Rice Rodents Signal Transduction Statistical analysis Yeast |
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| Title | Transgenic Expression of the Dicotyledonous Pattern Recognition Receptor EFR in Rice Leads to Ligand-Dependent Activation of Defense Responses |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/25821973 https://www.proquest.com/docview/1668236666 https://www.osti.gov/servlets/purl/1191186 https://pubmed.ncbi.nlm.nih.gov/PMC4379099 https://escholarship.org/uc/item/6xp46342 https://doaj.org/article/600aa588f49a4fb3ac57756d5b7e34c6 http://dx.doi.org/10.1371/journal.ppat.1004809 |
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