title: Bacteria-triggered systemic immunity in barley is associated with WRKY and ETHYLENE RESPONSIVE FACTORs but not with salicylic acid.
abstract: Leaf-to-leaf systemic immune signaling known as systemic acquired resistance is poorly understood in monocotyledonous plants. Here, we characterize systemic immunity in barley (Hordeum vulgare) triggered after primary leaf infection with either Pseudomonas syringae pathovar japonica (Psj) or Xanthomonas translucens pathovar cerealis (Xtc). Both pathogens induced resistance in systemic, uninfected leaves against a subsequent challenge infection with Xtc. In contrast to systemic acquired resistance in Arabidopsis (Arabidopsis thaliana), systemic immunity in barley was not associated with NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 or the local or systemic accumulation of salicylic acid. Instead, we documented a moderate local but not systemic induction of abscisic acid after infection of leaves with Psj. In contrast to salicylic acid or its functional analog benzothiadiazole, local applications of the jasmonic acid methyl ester or abscisic acid triggered systemic immunity to Xtc. RNA sequencing analysis of local and systemic transcript accumulation revealed unique gene expression changes in response to both Psj and Xtc and a clear separation of local from systemic responses. The systemic response appeared relatively modest, and quantitative reverse transcription-polymerase chain reaction associated systemic immunity with the local and systemic induction of two WRKY and two ETHYLENE RESPONSIVE FACTOR (ERF)-like transcription factors. Systemic immunity against Xtc was further associated with transcriptional changes after a secondary/systemic Xtc challenge infection; these changes were dependent on the primary treatment. Taken together, bacteria-induced systemic immunity in barley may be mediated in part by WRKY and ERF-like transcription factors, possibly facilitating transcriptional reprogramming to potentiate immunity.
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Sanjukta
authors.initials: S
authors.lastname: Dey
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Marion
authors.initials: M
authors.lastname: Wenig
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Gregor
authors.initials: G
authors.lastname: Langen
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Sapna
authors.initials: S
authors.lastname: Sharma
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Karl G
authors.initials: KG
authors.lastname: Kugler
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Claudia
authors.initials: C
authors.lastname: Knappe
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Bettina
authors.initials: B
authors.lastname: Hause
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Marlies
authors.initials: M
authors.lastname: Bichlmeier
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Valiollah
authors.initials: V
authors.lastname: Babaeizad
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Jafargholi
authors.initials: J
authors.lastname: Imani
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Ingar
authors.initials: I
authors.lastname: Janzik
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Thomas
authors.initials: T
authors.lastname: Stempfl
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Ralph
authors.initials: R
authors.lastname: Hückelhoven
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Karl-Heinz
authors.initials: KH
authors.lastname: Kogel
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.).
authors.forename: Klaus F X
authors.initials: KF
authors.lastname: Mayer
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology (S.D., M.W., C.K., M.B., A.C.V.) and Research Unit Plant Genome and Systems Biology (S.S., K.G.K., K.F.X.M.), 85764 Neuherberg, Germany;Justus Liebig University, Research Centre for BioSystems, Land Use, and Nutrition, 35392 Giessen, Germany (G.L., V.B., J.I., K.-H.K.);Leibniz Institute of Plant Biochemistry, Department of Cell and Metabolic Biology, 06120 Halle/Saale, Germany (B.H.);Plant Sciences, Institute for Biosciences and Geosciences, Forschungszentrum Jülich, 52425 Juelich, Germany (I.J.);University of Regensburg, Center of Excellence for Fluorescent Bioanalytics, 93053 Regensburg, Germany (T.S.); andTechnische Universität München, Department of Phytopathology, 85350 Freising, Germany (R.H.) corina.vlot@helmholtz-muenchen.de.
authors.forename: A Corina
authors.identifier: http://orcid.org/0000-0002-8146-6018
authors.initials: AC
authors.lastname: Vlot
mesh_terms: D000040:Abscisic Acid / Q000494:pharmacology; D000085:Acetates / Q000494:pharmacology; D003517:Cyclopentanes / Q000494:pharmacology; D005030:Ethylenes / Q000494:pharmacology; D001467:Hordeum / Q000187:drug effects / Q000235:genetics / Q000276:immunology*; D054883:Oxylipins / Q000494:pharmacology; D010935:Plant Diseases / Q000276:immunology* / Q000382:microbiology; D010937:Plant Growth Regulators / Q000494:pharmacology*; D057865:Plant Immunity; D018515:Plant Leaves / Q000187:drug effects / Q000235:genetics / Q000276:immunology; D044224:Pseudomonas syringae / Q000502:physiology*; D020156:Salicylic Acid / Q000494:pharmacology; D013830:Thiadiazoles / Q000494:pharmacology; D014974:Xanthomonas / Q000502:physiology*
chemical_list: D000085:Acetates; D003517:Cyclopentanes; D005030:Ethylenes; D054883:Oxylipins; D010937:Plant Growth Regulators; D013830:Thiadiazoles; C015700:benzo-1,2,3-thiadiazole; D000040:Abscisic Acid; C072239:methyl jasmonate; C036216:ethylene; D020156:Salicylic Acid