title: Contrasting Roles of the Apoplastic Aspartyl Protease APOPLASTIC, ENHANCED DISEASE SUSCEPTIBILITY1-DEPENDENT1 and LEGUME LECTIN-LIKE PROTEIN1 in Arabidopsis Systemic Acquired Resistance.
abstract: Systemic acquired resistance (SAR) is an inducible immune response that depends on ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1). Here, we show that Arabidopsis (Arabidopsis thaliana) EDS1 is required for both SAR signal generation in primary infected leaves and SAR signal perception in systemic uninfected tissues. In contrast to SAR signal generation, local resistance remains intact in eds1 mutant plants in response to Pseudomonas syringae delivering the effector protein AvrRpm1. We utilized the SAR-specific phenotype of the eds1 mutant to identify new SAR regulatory proteins in plants conditionally expressing AvrRpm1. Comparative proteomic analysis of apoplast-enriched extracts from AvrRpm1-expressing wild-type and eds1 mutant plants led to the identification of 12 APOPLASTIC, EDS1-DEPENDENT (AED) proteins. The genes encoding AED1, a predicted aspartyl protease, and another AED, LEGUME LECTIN-LIKE PROTEIN1 (LLP1), were induced locally and systemically during SAR signaling and locally by salicylic acid (SA) or its functional analog, benzo 1,2,3-thiadiazole-7-carbothioic acid S-methyl ester. Because conditional overaccumulation of AED1-hemagglutinin inhibited SA-induced resistance and SAR but not local resistance, the data suggest that AED1 is part of a homeostatic feedback mechanism regulating systemic immunity. In llp1 mutant plants, SAR was compromised, whereas the local resistance that is normally associated with EDS1 and SA as well as responses to exogenous SA appeared largely unaffected. Together, these data indicate that LLP1 promotes systemic rather than local immunity, possibly in parallel with SA. Our analysis reveals new positive and negative components of SAR and reinforces the notion that SAR represents a distinct phase of plant immunity beyond local resistance.
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (H.H.B., M.W., F.W., C.K., M.B., E.P., A.C.V.), and Research Unit Protein Science (H.S.), 85764 Neuherberg, Germany;Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions (L.J., J.E.P., A.C.V.) and Mass Spectrometry Unit (T.C.), 50829 Cologne, Germany;John Innes Centre, Norwich NR4 7UH, United Kingdom (A.M.M.-A.); andOhio State University, Department of Horticulture and Crop Science and Department of Molecular Genetics, Columbus, Ohio 43210 (D.M.).
authors.forename: Heiko H
authors.initials: HH
authors.lastname: Breitenbach
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (H.H.B., M.W., F.W., C.K., M.B., E.P., A.C.V.), and Research Unit Protein Science (H.S.), 85764 Neuherberg, Germany;Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions (L.J., J.E.P., A.C.V.) and Mass Spectrometry Unit (T.C.), 50829 Cologne, Germany;John Innes Centre, Norwich NR4 7UH, United Kingdom (A.M.M.-A.); andOhio State University, Department of Horticulture and Crop Science and Department of Molecular Genetics, Columbus, Ohio 43210 (D.M.).
authors.forename: Marion
authors.initials: M
authors.lastname: Wenig
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (H.H.B., M.W., F.W., C.K., M.B., E.P., A.C.V.), and Research Unit Protein Science (H.S.), 85764 Neuherberg, Germany;Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions (L.J., J.E.P., A.C.V.) and Mass Spectrometry Unit (T.C.), 50829 Cologne, Germany;John Innes Centre, Norwich NR4 7UH, United Kingdom (A.M.M.-A.); andOhio State University, Department of Horticulture and Crop Science and Department of Molecular Genetics, Columbus, Ohio 43210 (D.M.).
authors.forename: Finni
authors.initials: F
authors.lastname: Wittek
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (H.H.B., M.W., F.W., C.K., M.B., E.P., A.C.V.), and Research Unit Protein Science (H.S.), 85764 Neuherberg, Germany;Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions (L.J., J.E.P., A.C.V.) and Mass Spectrometry Unit (T.C.), 50829 Cologne, Germany;John Innes Centre, Norwich NR4 7UH, United Kingdom (A.M.M.-A.); andOhio State University, Department of Horticulture and Crop Science and Department of Molecular Genetics, Columbus, Ohio 43210 (D.M.).
authors.forename: Lucia
authors.initials: L
authors.lastname: Jordá
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (H.H.B., M.W., F.W., C.K., M.B., E.P., A.C.V.), and Research Unit Protein Science (H.S.), 85764 Neuherberg, Germany;Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions (L.J., J.E.P., A.C.V.) and Mass Spectrometry Unit (T.C.), 50829 Cologne, Germany;John Innes Centre, Norwich NR4 7UH, United Kingdom (A.M.M.-A.); andOhio State University, Department of Horticulture and Crop Science and Department of Molecular Genetics, Columbus, Ohio 43210 (D.M.).
authors.forename: Ana M
authors.initials: AM
authors.lastname: Maldonado-Alconada
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (H.H.B., M.W., F.W., C.K., M.B., E.P., A.C.V.), and Research Unit Protein Science (H.S.), 85764 Neuherberg, Germany;Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions (L.J., J.E.P., A.C.V.) and Mass Spectrometry Unit (T.C.), 50829 Cologne, Germany;John Innes Centre, Norwich NR4 7UH, United Kingdom (A.M.M.-A.); andOhio State University, Department of Horticulture and Crop Science and Department of Molecular Genetics, Columbus, Ohio 43210 (D.M.).
authors.forename: Hakan
authors.initials: H
authors.lastname: Sarioglu
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (H.H.B., M.W., F.W., C.K., M.B., E.P., A.C.V.), and Research Unit Protein Science (H.S.), 85764 Neuherberg, Germany;Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions (L.J., J.E.P., A.C.V.) and Mass Spectrometry Unit (T.C.), 50829 Cologne, Germany;John Innes Centre, Norwich NR4 7UH, United Kingdom (A.M.M.-A.); andOhio State University, Department of Horticulture and Crop Science and Department of Molecular Genetics, Columbus, Ohio 43210 (D.M.).
authors.forename: Thomas
authors.initials: T
authors.lastname: Colby
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (H.H.B., M.W., F.W., C.K., M.B., E.P., A.C.V.), and Research Unit Protein Science (H.S.), 85764 Neuherberg, Germany;Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions (L.J., J.E.P., A.C.V.) and Mass Spectrometry Unit (T.C.), 50829 Cologne, Germany;John Innes Centre, Norwich NR4 7UH, United Kingdom (A.M.M.-A.); andOhio State University, Department of Horticulture and Crop Science and Department of Molecular Genetics, Columbus, Ohio 43210 (D.M.).
authors.forename: Claudia
authors.initials: C
authors.lastname: Knappe
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (H.H.B., M.W., F.W., C.K., M.B., E.P., A.C.V.), and Research Unit Protein Science (H.S.), 85764 Neuherberg, Germany;Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions (L.J., J.E.P., A.C.V.) and Mass Spectrometry Unit (T.C.), 50829 Cologne, Germany;John Innes Centre, Norwich NR4 7UH, United Kingdom (A.M.M.-A.); andOhio State University, Department of Horticulture and Crop Science and Department of Molecular Genetics, Columbus, Ohio 43210 (D.M.).
authors.forename: Marlies
authors.initials: M
authors.lastname: Bichlmeier
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (H.H.B., M.W., F.W., C.K., M.B., E.P., A.C.V.), and Research Unit Protein Science (H.S.), 85764 Neuherberg, Germany;Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions (L.J., J.E.P., A.C.V.) and Mass Spectrometry Unit (T.C.), 50829 Cologne, Germany;John Innes Centre, Norwich NR4 7UH, United Kingdom (A.M.M.-A.); andOhio State University, Department of Horticulture and Crop Science and Department of Molecular Genetics, Columbus, Ohio 43210 (D.M.).
authors.forename: Elisabeth
authors.initials: E
authors.lastname: Pabst
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (H.H.B., M.W., F.W., C.K., M.B., E.P., A.C.V.), and Research Unit Protein Science (H.S.), 85764 Neuherberg, Germany;Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions (L.J., J.E.P., A.C.V.) and Mass Spectrometry Unit (T.C.), 50829 Cologne, Germany;John Innes Centre, Norwich NR4 7UH, United Kingdom (A.M.M.-A.); andOhio State University, Department of Horticulture and Crop Science and Department of Molecular Genetics, Columbus, Ohio 43210 (D.M.).
authors.forename: David
authors.initials: D
authors.lastname: Mackey
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (H.H.B., M.W., F.W., C.K., M.B., E.P., A.C.V.), and Research Unit Protein Science (H.S.), 85764 Neuherberg, Germany;Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions (L.J., J.E.P., A.C.V.) and Mass Spectrometry Unit (T.C.), 50829 Cologne, Germany;John Innes Centre, Norwich NR4 7UH, United Kingdom (A.M.M.-A.); andOhio State University, Department of Horticulture and Crop Science and Department of Molecular Genetics, Columbus, Ohio 43210 (D.M.).
authors.forename: Jane E
authors.initials: JE
authors.lastname: Parker
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (H.H.B., M.W., F.W., C.K., M.B., E.P., A.C.V.), and Research Unit Protein Science (H.S.), 85764 Neuherberg, Germany;Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions (L.J., J.E.P., A.C.V.) and Mass Spectrometry Unit (T.C.), 50829 Cologne, Germany;John Innes Centre, Norwich NR4 7UH, United Kingdom (A.M.M.-A.); andOhio State University, Department of Horticulture and Crop Science and Department of Molecular Genetics, Columbus, Ohio 43210 (D.M.) corina.vlot@helmholtz-muenchen.de.
authors.forename: A Corina
authors.initials: AC
authors.lastname: Vlot
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