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Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure
Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
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2016 (English)In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 172, no 3, p. 2057-2078Article in journal (Refereed) Published
Abstract [en]

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.

Place, publisher, year, edition, pages
2016. Vol. 172, no 3, p. 2057-2078
National Category
Botany
Identifiers
URN: urn:nbn:se:umu:diva-131106DOI: 10.1104/pp.16.01318ISI: 000391172300051PubMedID: 27758847OAI: oai:DiVA.org:umu-131106DiVA, id: diva2:1072562
Available from: 2017-02-08 Created: 2017-02-06 Last updated: 2018-06-09Bibliographically approved
In thesis
1. Black mustard and the butterfly effect: metabolomics of plant-insect interactions under multiple stress conditions
Open this publication in new window or tab >>Black mustard and the butterfly effect: metabolomics of plant-insect interactions under multiple stress conditions
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

One main goal of ecological research is to understand nature´s complexity, in order to predict the potential impact of environmental perturbations. In this thesis, I investigate the ecological interactions between some of the most ancient organisms living on our planet: plants and insects.

Focus of my research is the interaction between the wild brassicaceous plant black mustard (Brassica nigra L.) and its specialist insect herbivore, the large white cabbage butterfly (Pieris brassicae L). Both organisms are well characterized model species used in chemical ecology research.

Using different analytical techniques, such as liquid and gas chromatography coupled to mass-spectrometry (LC- and GC-MS) and headspace collection of volatile organic compounds (VOCs), I apply the approach of metabolomics and systems biology to the field of ecology to explore the metabolic changes occurring inside the plants exposed to biotic and abiotic stresses.

Particularly, I study the plant metabolic responses against P. brassicae chewing caterpillars during sequential treatment exposure to: abiotic stress by the oxidative air pollutant ozone (O3); dual herbivory with specialist Brevicoryne brassicae piercing-sucking aphids; and chemical induction of plant defences with the oxylipin phytohormone methyl-jasmonate (MeJA).

Results show how during herbivore-induced responses, changes in defence- and growth-metabolic processes are tightly connected to stress protection mechanisms, indicating that plants actively reprogram their inner metabolic networks in order to adapt to consecutive changes in the environment.

This thesis illustrates how evaluating the plant metabolome in its entirety rather than single metabolites, can help us understanding plant responses towards abiotic and biotic stresses, and improve our ability to predict how constant shifts in the environment affect plant physiology and ecology.

 

Abstract [sv]

Ett huvudsyfte för ekologisk forskning är att förstå naturens komplexitet för att kunna förutse effekter av störningar i miljön. I min avhandling har jag fokuserat på ekologiska interaktioner mellan växter och insekter, två av de äldsta terrestra organismgrupperna på jorden.

I mina studier har jag undersökt interaktioner mellan den korsblommiga växten svartsenap (Brassica nigra L.) och den specifika herbivoren kålfjäril (Pieris brassicae L.). Båda är väl karaktäriserade modellarter i kemisk-ekologisk forskning.

De metaboliska förändringar som sker när växten utsätts för biotisk och abiotisk stress har analyserats hjälp av metabolomik, det vill säga analyser av metabolomet i sin helhet med hjälp av tekniker som vätske- och gaskromatografi kopplad till masspektrometri (LC- och GC-MS), och så kallad headspace-uppsamling av flyktiga organiska föreningar (VOCs).

Jag har särskilt undersökt de metaboliska förändringar som sker när växten betas av kålfjärilslarver vid samtidig exponering för: abiotisk stress i form av ozon (O3), en oxidativ luftförorening; ytterligare betning i form av stickande och sugande bladlus (Brevicoryne brassicae); tillsats av oxylipinfytohormon metyl-jasmonat (MeJA), ett ämne som inducerar växtens försvar.

Resultaten visar att de metaboliska förändringar som sker i växten vid herbivori med konsekvenser för dess försvar och tillväxt är nära kopplade till de metaboliska förändringar som sker vid stress, vilket visar att växten kan fortlöpande och aktivt omprogrammera sina metaboliska nätverk för att anpassa sig till förändringar i miljön.

Avhandlingen visar att genom att utvärdera växtmetabolomet i sin helhet, snarare än att studera enskilda metaboliter, vi kan få bättre förståelse för hur växter reagerar på olika former av stress och därmed också bidra till att vi kan göra förutsägelser för hur förändringar i miljön kan påverka växters fysiologi och ekologi.

Place, publisher, year, edition, pages
Umeå: Umeå University, 2017. p. 70
Keywords
plant physiology, metabolomics, glucosinolates, multiple stress, ozone, Brassica nigra, Pieris brassicae, Brevicoryne brassicae
National Category
Ecology
Research subject
biology; biology, Environmental Science; Molecular Biology; Entomology
Identifiers
urn:nbn:se:umu:diva-134653 (URN)978-91-7601-728-9 (ISBN)
Public defence
2017-06-02, Lilla hörsalen, KB3A9, Kemiskt Biologiskt Centrum (KBC), Umeå, 10:00 (English)
Opponent
Supervisors
Funder
European Science Foundation (ESF), VR/ESF324–2011–787
Available from: 2017-05-12 Created: 2017-05-10 Last updated: 2018-06-09Bibliographically approved

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Papazian, StefanoAlbrectsen, Benedicte R.

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