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Phenolics, Nitrogen, and Biotic Interactions: A Study of Phenylpropanoid Metabolites and Gene Expression in the Leaves of Populus tremula.
Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. (Benedicte Albrectsen)ORCID iD: 0000-0001-8007-2685
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

European aspen (Populus tremula) is a fast growing tree species, rich in phenolic compounds. Defense theories suggest that soil nitrogen greatly influence plant allocation togrowth and defense; however, the allocation priorities are not well understood. Further,although foliar phenolic compounds are considered defensive, specialist organisms may positively associate with and alter them. There are two classes of phenolics in aspen,condensed tannins (CTs) and salicinoids. They are likely to shape the interactions of themany organisms, for example, herbivorous insects and endophytic fungi and three-way interactions among host genotype, specialist herbivores and endophytic fungi could be greatly altered by aspen geno- and chemotypes’ responses to soil nitrogen.

Firstly, I focused on the allocation of carbon to growth and defense in aspen genotypes with varied tannin content in response to nutrient addition. Nitrogen promoted plant growth and suppressed foliar CT levels. At the molecular level expression of genes of the phenylpropanoid pathway (PPP) decreased under low additions of N (equivalent to 15kg/ha), whereas genes at the beginning and at the end of the pathway increased in response to high levels of N (~150 kg/ha). Aspens high in CTs displayed consistently stronger PPP gene expressions compared to CT-low aspens, and correlations between PPP genes and phenolic products varied with tannin content, as an effect of leaf age, in response to N enrichment, and individually with genotype. More negative correlations (indicative of allocation trade-offs) between PPP gene expressions and phenolic products were found in aspen genets with low tannin levels compared to aspens with inherently high tannin levels.

Secondly, I studied the connection between foliar phenolic compounds and endophytic fungi in the presence and absence of a specialist herbivorous beetle (Chrysomela tremula) and as an effect of soil nitrogen addition. Richness and abundance of fungal endophytes associated with aspen genotypes and phenolic profile, however this specificity disappeared in the presence of the leaf beetles. Herbivory both enhanced endophyte richness andabundance in the leaves and it also increased in response to nitrogen addition.

Place, publisher, year, edition, pages
Umeå: Umeå University , 2016. , 31 p.
Keyword [en]
Populus tremula, condensed tannins, salicinoids, phenolics, genetic variation, soil nitrogen fertilization, herbivory
National Category
Botany
Research subject
biology
Identifiers
URN: urn:nbn:se:umu:diva-126699ISBN: 978-91-7601-590-2 (print)OAI: oai:DiVA.org:umu-126699DiVA: diva2:1034806
Public defence
2016-11-04, KB3B1, KBC-huset, Umeå University, Umeå, 10:00 (English)
Opponent
Supervisors
Funder
Swedish Foundation for Strategic Research , RBb08-0003
Available from: 2016-10-14 Created: 2016-10-13 Last updated: 2016-10-13Bibliographically approved
List of papers
1. Genotypic tannin levels in Populus tremula impact the way nitrogen enrichment affects growth and allocation responses for some traits and not for others
Open this publication in new window or tab >>Genotypic tannin levels in Populus tremula impact the way nitrogen enrichment affects growth and allocation responses for some traits and not for others
2015 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 10, no 10, e0140971Article in journal (Refereed) Published
Abstract [en]

Plant intraspecific variability has been proposed as a key mechanism by which plants adapt to environmental change. In boreal forests where nitrogen availability is strongly limited, nitrogen addition happens indirectly through atmospheric N deposition and directly through industrial forest fertilization. These anthropogenic inputs of N have numerous environmental consequences, including shifts in plant species composition and reductions in plant species diversity. However, we know less about how genetic differences within plant populations determine how species respond to eutrophication in boreal forests. According to plant defense theories, nitrogen addition will cause plants to shift carbon allocation more towards growth and less to chemical defense, potentially enhancing vulnerability to antagonists. Aspens are keystone species in boreal forests that produce condensed tannins to serve as chemical defense. We conducted an experiment using ten Populus tremula genotypes from the Swedish Aspen Collection that express extreme levels of baseline investment into foliar condensed tannins. We investigated whether investment into growth and phenolic defense compounds in young plants varied in response to two nitrogen addition levels, corresponding to atmospheric N deposition and industrial forest fertilization. Nitrogen addition generally caused growth to increase, and tannin levels to decrease; however, individualistic responses among genotypes were found for height growth, biomass of specific tissues, root: shoot ratios, and tissue lignin and N concentrations. A genotype's baseline ability to produce and store condensed tannins also influenced plant responses to N, although this effect was relatively minor. High-tannin genotypes tended to grow less biomass under low nitrogen levels and more at the highest fertilization level. Thus, the ability in aspen to produce foliar tannins is likely associated with a steeper reaction norm of growth responses, which suggests a higher plasticity to nitrogen addition, and potentially an advantage when adapting to higher concentrations of soil nitrogen.

National Category
Botany
Identifiers
urn:nbn:se:umu:diva-111477 (URN)10.1371/journal.pone.0140971 (DOI)000363248400088 ()26488414 (PubMedID)
Available from: 2015-12-09 Created: 2015-11-13 Last updated: 2017-12-01Bibliographically approved
2. Aspen phenylpropanoid genes’ expression levels correlate with genets’ tannin richness and vary both in responses to soil nitrogen and associations with phenolic profiles
Open this publication in new window or tab >>Aspen phenylpropanoid genes’ expression levels correlate with genets’ tannin richness and vary both in responses to soil nitrogen and associations with phenolic profiles
Show others...
2017 (English)In: Tree Physiology, ISSN 0829-318X, E-ISSN 1758-4469, Vol. 37, no 2, 270-279 p.Article in journal (Refereed) Published
Abstract [en]

Condensed tannin (CT) contents of European aspen (Populus tremula L.) vary among genotypes, and increases in nitrogen (N) availability generally reduce plants’ tannin production in favor of growth, through poorly understood mechanisms. We hypothesized that intrinsic tannin production rates may co-vary with gene expression responses to soil N and resource allocation within the phenylpropanoid pathway (PPP). Thus, we examined correlations between soil N levels and both expression patterns of eight PPP genes (measured by quantitative-reverse transcription PCR) and foliar phenolic compounds (measured by liquid chromatography–mass spectrometry) in young aspen genets with intrinsically extreme CT levels. Monitored phenolics included salicinoids, lignins, flavones, flavonols, CT precursors and CTs. The PPP genes were consistently expressed more strongly in high-CT trees. Low N supplements reduced expression of genes throughout the PPP in all genets, while high N doses restored expression of genes at the beginning and end of the pathway. These PPP changes were not reflected in pools of tannin precursors, but varying correlations between gene expression and foliar phenolic pools were detected in young and mature leaves, suggesting that processes linking gene expression and the resulting phenolics vary spatially and temporally. Precursor fluxes suggested that CT-related metabolic rate or sink controls are linked to intrinsic carbon allocation strategies associated with N responses. Overall, we found more negative correlations (indicative of allocation trade-offs) between PPP gene expression and phenolic products following N additions in low-CT plants than in high-CT plants. The tannin-related expression dynamics suggest that, in addition to defense, relative tannin levels may also be indicative of intraspecific variations in the way aspen genets respond to soil fertility. 

Keyword
condensed tannins, European aspen, genotypic variation, nitrogen addition, phenylpropanoid pathway, Populus tremula, salicinoids
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-126704 (URN)10.1093/treephys/tpw118 (DOI)000397052300012 ()
Available from: 2016-10-13 Created: 2016-10-13 Last updated: 2017-11-29Bibliographically approved
3. Specialist Leaf Beetles Enrich Diversity of Endophytic Fungi in Aspen Leaves, and Mask Intra-specific Host Specificity
Open this publication in new window or tab >>Specialist Leaf Beetles Enrich Diversity of Endophytic Fungi in Aspen Leaves, and Mask Intra-specific Host Specificity
(English)Manuscript (preprint) (Other academic)
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-126705 (URN)
Available from: 2016-10-13 Created: 2016-10-13 Last updated: 2016-10-13
4. Foliar fungal endophytes respond to nitrogen fertilization and herbivory in aspen genotypes
Open this publication in new window or tab >>Foliar fungal endophytes respond to nitrogen fertilization and herbivory in aspen genotypes
Show others...
(English)Manuscript (preprint) (Other academic)
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-126706 (URN)
Available from: 2016-10-13 Created: 2016-10-13 Last updated: 2016-10-13

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