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Herbivore-Induced Metabolic Responses in Brassica nigra are Shaped by Leaf Ontogeny
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå Plant Science Centre. (Benedicte Albrectsen)ORCID iD: 0000-0003-2538-8702
Umeå University, Faculty of Science and Technology, Department of Chemistry.
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

In order to defend, plants rely on quick metabolic reconfigurations. Here weinvestigated plant herbivore-induced responses asking: 1) how exposure to methyljasmonate(MeJA) and herbivory alter plant defence and growth metabolism, and 2)are herbivore-induced responses concentrated in tissues with higher fitness value, aspredicted by the optimal defence (OD) theory? We analysed the leaf metabolome of black mustard (B. nigra) in response to MeJAand/or feeding by specialist caterpillars of the large white cabbage butterfly (Pierisbrassicae). Shifts in defence-related (secondary) and growth-related (primary)metabolites were initially evaluated on fully expanded mature leaves and thenfollowed across leaf ontogeny. MeJA enhanced herbivore induced-responses and increased the plant resistanceagainst sequential herbivory. Responses were focused in young leaves andcharacterized by changes in defence- (glucosinolates, phenolics) and growth- (aminoacids, sugars, organic acids) metabolism, including asymmetric accumulation ofcentral tricarboxylic acid cycle (TCA) intermediates. MeJA application enhanced the plant resistance towards herbivory and, consistentlywith the OD theory, herbivore-induced responses were prioritized in young leaves.However, shifts in the plant were not limited to higher defences but affected growthmetabolism including regulation of energy pathways and increased leaf senescence.These effects deserve attention by future ecological and applied research on plantinsectinteractions.

National Category
Ecology
Research subject
Ecological Botany
Identifiers
URN: urn:nbn:se:umu:diva-134659OAI: oai:DiVA.org:umu-134659DiVA: diva2:1094677
Funder
European Science Foundation (ESF)
Available from: 2017-05-10 Created: 2017-05-10 Last updated: 2017-05-11
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. 70 p.
Keyword
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: 2017-05-12Bibliographically approved

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