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Black mustard and the butterfly effect: metabolomics of plant-insect interactions under multiple stress conditions
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå Plant Science Centre. (Benedicte Albrectsen)ORCID iD: 0000-0003-2538-8702
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 [en]
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: urn:nbn:se:umu:diva-134653ISBN: 978-91-7601-728-9 (print)OAI: oai:DiVA.org:umu-134653DiVA: diva2:1094683
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
List of papers
1. Ozone affects growth and development of Pieris brassicae on the wild host plant Brassica nigra
Open this publication in new window or tab >>Ozone affects growth and development of Pieris brassicae on the wild host plant Brassica nigra
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2015 (English)In: Environmental Pollution, ISSN 0269-7491, E-ISSN 1873-6424, Vol. 199, 119-129 p.Article in journal (Refereed) Published
Abstract [en]

When plants are exposed to ozone they exhibit changes in both primary and secondary metabolism, which may affect their interactions with herbivorous insects. Here we investigated the performance and preferences of the specialist herbivore Pieris brassicae on the wild plant Brassica nigra under elevated ozone conditions. The direct and indirect effects of ozone on the plant-herbivore system were studied. In both cases ozone exposure had a negative effect on P. brassicae development. However, in dual-choice tests larvae preferentially consumed plant material previously fumigated with the highest concentration tested, showing a lack of correlation between larval preference and performance on ozone exposed plants. Metabolomic analysis of leaf material subjected to combinations of ozone and herbivore-feeding, and focussing on known defence metabolites, indicated that P. brassicae behaviour and performance were associated with ozone-induced alterations to glucosinolate and phenolic pools. 

Keyword
Brassica nigra, Pieris brassicae, Ozone exposure, Growth and performance, Defence compounds, enolics, Glucosinolates
National Category
Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-102346 (URN)10.1016/j.envpol.2015.01.019 (DOI)000351972900016 ()25645061 (PubMedID)
Available from: 2015-06-23 Created: 2015-04-23 Last updated: 2017-05-10Bibliographically approved
2. Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure
Open this publication in new window or tab >>Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure
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2016 (English)In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 172, no 3, 2057-2078 p.Article 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.

National Category
Botany
Identifiers
urn:nbn:se:umu:diva-131106 (URN)10.1104/pp.16.01318 (DOI)000391172300051 ()27758847 (PubMedID)
Available from: 2017-02-08 Created: 2017-02-06 Last updated: 2017-05-10Bibliographically approved
3. Dual herbivore attack and herbivore density affect metabolic profiles of Brassica nigra leaves
Open this publication in new window or tab >>Dual herbivore attack and herbivore density affect metabolic profiles of Brassica nigra leaves
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2017 (English)In: Plant, Cell and Environment, ISSN 0140-7791, E-ISSN 1365-3040, Vol. 40, no 8, 1356-1367 p.Article in journal (Refereed) Published
Abstract [en]

Plant responses to dual herbivore attack are increasingly studied, but effects on the metabolome have largely been restricted to volatile metabolites and defence-related non-volatile metabolites. However, plants subjected to stress, such as herbivory, undergo major changes in both primary and secondary metabolism. Using a naturally occurring system, we investigated metabolome-wide effects of single or dual herbivory on Brassica nigra plants by Brevicoryne brassicae aphids and Pieris brassicae caterpillars, while also considering the effect of aphid density. Metabolomic analysis of leaf material showed that single and dual herbivory had strong effects on the plant metabolome, with caterpillar feeding having the strongest influence. Additionally, aphid-density-dependent effects were found in both the single and dual infestation scenarios. Multivariate analysis revealed treatment-specific metabolomic profiles, and effects were largely driven by alterations in the glucosinolate and sugar pools. Our work shows that analysing the plant metabolome as a single entity rather than as individual metabolites provides new insights into the subcellular processes underlying plant defence against multiple herbivore attackers. These processes appear to be importantly influenced by insect density.

Keyword
Brevicoryne brassicae, dual herbivory, induced defence, metabolomics, Pieris brassicae
National Category
Biochemistry and Molecular Biology
Research subject
biology
Identifiers
urn:nbn:se:umu:diva-134649 (URN)10.1111/pce.12926 (DOI)000405275300010 ()
Available from: 2017-05-10 Created: 2017-05-10 Last updated: 2017-08-04Bibliographically approved
4. Herbivore-Induced Metabolic Responses in Brassica nigra are Shaped by Leaf Ontogeny
Open this publication in new window or tab >>Herbivore-Induced Metabolic Responses in Brassica nigra are Shaped by Leaf Ontogeny
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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:nbn:se:umu:diva-134659 (URN)
Funder
European Science Foundation (ESF)
Available from: 2017-05-10 Created: 2017-05-10 Last updated: 2017-05-11

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