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Research article2016Peer reviewedOpen access

Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure

Papazian, Stefano; Khaling, Eliezer; Bonnet, Christelle; Lassueur, Steve; Reymond, Philippe; Moritz, Thomas; Blande, James D.; Albrectsen, Benedicte R.

Abstract

Plants have evolved adaptive mechanisms that allow them to tolerate a continuous range of abiotic and biotic stressors. Tropospheric ozone (O-3), 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 O-3 and the specialist herbivore Pieris brassicae. Transcriptomics and metabolomics data were evaluated using multivariate, correlation, and network analyses for the O-3 and herbivory responses. O-3 stress symptoms resembled those of senescence and phosphate starvation, while a sequential shift from O-3 to 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 O-3 stress inhibited photosynthesis and carbon assimilation, sequential herbivory counteracted the initial responses induced by O-3, 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.

Published in

Plant Physiology
2016, Volume: 172, number: 3, pages: 2057-2078 Publisher: AMER SOC PLANT BIOLOGISTS

      SLU Authors

      Associated SLU-program

      SLU Plant Protection Network

      Sustainable Development Goals

      SDG13 Climate action

      UKÄ Subject classification

      Botany

      Publication identifier

      DOI: https://doi.org/10.1104/pp.16.01318

      Permanent link to this page (URI)

      https://res.slu.se/id/publ/84279