title: Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure.
abstract: Plants have evolved adaptive mechanisms that allow them to tolerate a continuous range of abiotic and biotic stressors. Tropospheric ozone (O3), a global anthropogenic pollutant, directly affects living organisms and ecosystems, including plant-herbivore interactions. In this study, we investigate the stress responses of Brassica nigra (wild black mustard) exposed consecutively to O3and the specialist herbivore Pieris brassicae Transcriptomics and metabolomics data were evaluated using multivariate, correlation, and network analyses for the O3and herbivory responses. O3stress symptoms resembled those of senescence and phosphate starvation, while a sequential shift from O3to herbivory induced characteristic plant defense responses, including a decrease in central metabolism, induction of the jasmonic acid/ethylene pathways, and emission of volatiles. Omics network and pathway analyses predicted a link between glycerol and central energy metabolism that influences the osmotic stress response and stomatal closure. Further physiological measurements confirmed that while O3stress inhibited photosynthesis and carbon assimilation, sequential herbivory counteracted the initial responses induced by O3, resulting in a phenotype similar to that observed after herbivory alone. This study clarifies the consequences of multiple stress interactions on a plant metabolic system and also illustrates how omics data can be integrated to generate new hypotheses in ecology and plant physiology.
authors.affiliation: Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187 Umeå (S.P., B.R.A.); Department of Forest Genetic and Plant Physiology, Swedish University of Agricultural Sciences, 90183 Umeå, Sweden (T.M.).|Department of Environmental and Biological Sciences, University of Eastern Finland, FIN-70211 Kuopio, Finland (E.K., J.D.B.); and.|Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne, Switzerland (C.B., S.L., P.R.).
authors.forename: Stefano
authors.identifier: 0000-0003-2538-8702
authors.initials: S
authors.lastname: Papazian
authors.affiliation: Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187 Umeå (S.P., B.R.A.); Department of Forest Genetic and Plant Physiology, Swedish University of Agricultural Sciences, 90183 Umeå, Sweden (T.M.).|Department of Environmental and Biological Sciences, University of Eastern Finland, FIN-70211 Kuopio, Finland (E.K., J.D.B.); and.|Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne, Switzerland (C.B., S.L., P.R.).
authors.forename: Eliezer
authors.initials: E
authors.lastname: Khaling
authors.affiliation: Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187 Umeå (S.P., B.R.A.); Department of Forest Genetic and Plant Physiology, Swedish University of Agricultural Sciences, 90183 Umeå, Sweden (T.M.).|Department of Environmental and Biological Sciences, University of Eastern Finland, FIN-70211 Kuopio, Finland (E.K., J.D.B.); and.|Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne, Switzerland (C.B., S.L., P.R.).
authors.forename: Christelle
authors.identifier: 0000-0001-5472-7297
authors.initials: C
authors.lastname: Bonnet
authors.affiliation: Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187 Umeå (S.P., B.R.A.); Department of Forest Genetic and Plant Physiology, Swedish University of Agricultural Sciences, 90183 Umeå, Sweden (T.M.).|Department of Environmental and Biological Sciences, University of Eastern Finland, FIN-70211 Kuopio, Finland (E.K., J.D.B.); and.|Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne, Switzerland (C.B., S.L., P.R.).
authors.forename: Steve
authors.initials: S
authors.lastname: Lassueur
authors.affiliation: Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187 Umeå (S.P., B.R.A.); Department of Forest Genetic and Plant Physiology, Swedish University of Agricultural Sciences, 90183 Umeå, Sweden (T.M.).|Department of Environmental and Biological Sciences, University of Eastern Finland, FIN-70211 Kuopio, Finland (E.K., J.D.B.); and.|Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne, Switzerland (C.B., S.L., P.R.).
authors.forename: Philippe
authors.identifier: 0000-0002-3341-6200
authors.initials: P
authors.lastname: Reymond
authors.affiliation: Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187 Umeå (S.P., B.R.A.); Department of Forest Genetic and Plant Physiology, Swedish University of Agricultural Sciences, 90183 Umeå, Sweden (T.M.).|Department of Environmental and Biological Sciences, University of Eastern Finland, FIN-70211 Kuopio, Finland (E.K., J.D.B.); and.|Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne, Switzerland (C.B., S.L., P.R.).
authors.forename: Thomas
authors.identifier: 0000-0002-4258-3190
authors.initials: T
authors.lastname: Moritz
authors.affiliation: Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187 Umeå (S.P., B.R.A.); Department of Forest Genetic and Plant Physiology, Swedish University of Agricultural Sciences, 90183 Umeå, Sweden (T.M.); james.blande@uef.fi benedicte.albrectsen@umu.se.|Department of Environmental and Biological Sciences, University of Eastern Finland, FIN-70211 Kuopio, Finland (E.K., J.D.B.); and james.blande@uef.fi benedicte.albrectsen@umu.se.|Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne, Switzerland (C.B., S.L., P.R.) james.blande@uef.fi benedicte.albrectsen@umu.se.
authors.forename: James D
authors.identifier: 0000-0001-6822-0649
authors.initials: JD
authors.lastname: Blande
authors.affiliation: Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 90187 Umeå (S.P., B.R.A.); Department of Forest Genetic and Plant Physiology, Swedish University of Agricultural Sciences, 90183 Umeå, Sweden (T.M.); james.blande@uef.fi benedicte.albrectsen@umu.se.|Department of Environmental and Biological Sciences, University of Eastern Finland, FIN-70211 Kuopio, Finland (E.K., J.D.B.); and james.blande@uef.fi benedicte.albrectsen@umu.se.|Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne, Switzerland (C.B., S.L., P.R.) james.blande@uef.fi benedicte.albrectsen@umu.se.
authors.forename: Benedicte R
authors.identifier: 0000-0002-9337-4540
authors.initials: BR
authors.lastname: Albrectsen
mesh_terms: D000818:Animals; D004734:Energy Metabolism / Q000187:drug effects / Q000235:genetics; D017343:Genes, Plant; D005990:Glycerol / Q000378:metabolism; D060434:Herbivory / Q000187:drug effects*; D007313:Insecta / Q000502:physiology; D055442:Metabolome / Q000187:drug effects / Q000235:genetics; D008954:Models, Biological; D009149:Mustard Plant / Q000235:genetics / Q000378:metabolism* / Q000469:parasitology*; D010126:Ozone / Q000494:pharmacology*; D010788:Photosynthesis / Q000187:drug effects*; D054046:Plant Stomata / Q000187:drug effects / Q000502:physiology*; D059467:Transcriptome / Q000187:drug effects / Q000235:genetics
chemical_list: D010126:Ozone; D005990:Glycerol