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Intramolecular isotope analysis reveals plant ecophysiological signals covering multiple timescales
Umeå University, Faculty of Medicine, Department of Medical Biochemistry and Biophysics.
2019 (English)Doctoral thesis, comprehensive summary (Other academic)Alternative title
Intramolekylär isotopanalys avslöjar växtekofysiologiska signaler som täcker multipla tidsskalor (Swedish)
Abstract [en]

Our societies' wellbeing relies on stable and healthy environments. However, our current lifestyles, growth-oriented economic policies and the population explosion are leading to potentially catastrophic degradation of ecosystems and progressive disruption of food chains. Hopefully, more clarity about what the future holds in store will trigger stronger efforts to find, and adopt, problem-focused coping strategies and encourage environmentally friendly lifestyles.

Forecasting environmental change/destruction is complicated (inter alia) by lack of complete understanding of plant-environment interactions, particularly those involved in slow processes such as plant acclimatisation and adaptation. This stems from deficiencies in tools to analyse such slow processes. The present work aims at developing tools that can provide retrospective ecophysiological information covering timescales from days to millennia.

Natural archives, such as tree-rings, preserve plant metabolites over long timescales. Analyses of intramolecular isotope abundances in plant metabolites have the potential to provide retrospective information about metabolic processes and underlying environmental controls. Thus, my colleagues and I (hereafter we) analysed intramolecular isotope patterns in tree rings to develop analytical tools that can convey information about clearly-defined plant metabolic processes over multiple timescales. Such tools might help (inter alia) to constrain plants' capacities to sequester excess amounts of anthropogenic CO2; the so-called CO2 fertilisation effect. This, in turn, might shed light on plants' sink strength for the greenhouse gas CO2, and future plant performance and growth under climate change.

In the first of three studies, reported in appended papers, we analysed intramolecular 13C/12C ratios in tree-ring glucose. In six angiosperm and six gymnosperm species we found pronounced intramolecular 13C/12C differences, exceeding 10‰. These differences are transmitted into major global C pools, such as soil organic matter. Taking intramolecular 13C/12C differences into account might improve isotopic characterisation of soil metabolic processes and soil CO2 effluxes. In addition, we analysed intramolecular 13C/12C ratios in a Pinus nigra tree-ring archive spanning the period 1961 to 1995. These data revealed new ecophysiological 13C/12C signals, which can facilitate climate reconstructions and assessments of plant-environment interactions at higher resolution; thus providing higher quality information. We proposed that 13C/12C signals at glucose C-1 to C-2 derive from carbon injection into the Calvin-Benson cycle via the oxidative pentose phosphate pathway. We concluded that intramolecular 13C/12C measurements provide valuable new information about long-term metabolic dynamics for application in biogeochemistry, plant physiology, plant breeding, and paleoclimatology.

In the second study, we developed a comprehensive theory on the metabolic and ecophysiological origins of 13C/12C signals at tree-ring glucose C-5 and C-6. According to this theory and theoretical implications of the first study on signals at C-1 to C-3, analysis of such intramolecular signals can provide information about several metabolic processes. At C-3, a well-known signal reflecting CO2 uptake is preserved. The glucose-6-phosphate shunt around the Calvin-Benson cycle affects 13C/12C compositions at C-1 and C-2, while the 13C/12C signals at C-5 and C-6 reflect carbon fluxes into downstream metabolism. This theoretical framework enables further experimental studies to be conducted in a hypothesis-driven manner. In conclusion, the intramolecular approach provides information about carbon allocation in plant leaves. Thus, it gives access to long-term information on key ecophysiological processes, which could not be acquired by previous approaches.

The abundance of the hydrogen isotope deuterium, δD, is important for linking the water cycle with plant ecophysiology. The main factors affecting δD in plant organic matter are commonly assumed to be the δD in source water and leaf-level evaporative enrichment. Current δD models incorporate biochemical D fractionations as constants. In the third study we showed that biochemical D fractionations respond strongly to low ambient CO2 levels and low light intensity. Thus, models of δD values in plant organic matter should incorporate biochemical fractionations as variables. In addition, we found pronounced leaf-level δD differences between α-cellulose and wax n-alkanes. We explained this by metabolite-specific contributions of distinct hydrogen sources during biosynthesis.

Overall, this work advances our understanding of isotope distributions and isotope fractionations in plants. It reveals the immense potential of intramolecular isotope analyses for retrospective assessment of plant metabolism and associated environmental controls.

Place, publisher, year, edition, pages
Umeå: Umeå Universitet , 2019. , p. 33
Series
Umeå University medical dissertations, ISSN 0346-6612 ; 2004
Keywords [en]
NMR spectroscopy, tree ring, isotope ratio, isotope effect, intramolecular 13C/12C signal, carbon allocation, acclimation, plant performance, climate reconstruction, plant ecophysiology
National Category
Cell Biology Biochemistry and Molecular Biology Biophysics Other Biological Topics Climate Research Geosciences, Multidisciplinary Environmental Sciences
Identifiers
URN: urn:nbn:se:umu:diva-154968ISBN: 978-91-7855-001-2 (print)OAI: oai:DiVA.org:umu-154968DiVA, id: diva2:1275743
Public defence
2019-01-23, N440, Naturvetarhuset, Umeå, 09:00 (English)
Opponent
Supervisors
Available from: 2019-01-09 Created: 2019-01-07 Last updated: 2019-01-07Bibliographically approved
List of papers
1. Intramolecular 13C analysis of tree rings provides multiple plant ecophysiology signals covering decades
Open this publication in new window or tab >>Intramolecular 13C analysis of tree rings provides multiple plant ecophysiology signals covering decades
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2018 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 8, article id 5048Article in journal (Refereed) Published
Abstract [en]

Measurements of carbon isotope contents of plant organic matter provide important information in diverse fields such as plant breeding, ecophysiology, biogeochemistry and paleoclimatology. They are currently based on 13C/12C ratios of specific, whole metabolites, but we show here that intramolecular ratios provide higher resolution information. In the glucose units of tree-ring cellulose of 12 tree species, we detected large differences in 13C/12C ratios (>10‰) among carbon atoms, which provide isotopically distinct inputs to major global C pools, including wood and soil organic matter. Thus, considering position-specific differences can improve characterisation of soil-to-atmosphere carbon fluxes and soil metabolism. In a Pinus nigra tree-ring archive formed from 1961 to 1995, we found novel 13C signals, and show that intramolecular analysis enables more comprehensive and precise signal extraction from tree rings, and thus higher resolution reconstruction of plants’ responses to climate change. Moreover, we propose an ecophysiological mechanism for the introduction of a 13C signal, which links an environmental shift to the triggered metabolic shift and its intramolecular 13C signature. In conclusion, intramolecular 13C analyses can provide valuable new information about long-term metabolic dynamics for numerous applications.

National Category
Other Earth and Related Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-145978 (URN)10.1038/s41598-018-23422-2 (DOI)000428033900002 ()29567963 (PubMedID)
Funder
Knut and Alice Wallenberg Foundation, 2015.0047
Available from: 2018-03-24 Created: 2018-03-24 Last updated: 2019-01-07Bibliographically approved
2. Intramolecular 13C/12C signals reflect carbon allocation in plant leaves
Open this publication in new window or tab >>Intramolecular 13C/12C signals reflect carbon allocation in plant leaves
(English)Manuscript (preprint) (Other academic)
National Category
Cell Biology Biophysics Biochemistry and Molecular Biology Other Biological Topics Climate Research Geosciences, Multidisciplinary Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-154967 (URN)
Available from: 2019-01-07 Created: 2019-01-07 Last updated: 2019-01-07
3. 2H-fractionations during the biosynthesis of carbohydrates and lipids imprint a metabolic signal on the δ2H values of plant organic compounds
Open this publication in new window or tab >>2H-fractionations during the biosynthesis of carbohydrates and lipids imprint a metabolic signal on the δ2H values of plant organic compounds
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2018 (English)In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 218, no 2, p. 479-491Article in journal (Refereed) Published
Abstract [en]

Hydrogen (H) isotope ratio (δ2H) analyses of plant organic compounds have been applied to assess ecohydrological processes in the environment despite a large part of the δ2H variability observed in plant compounds not being fully elucidated.

We present a conceptual biochemical model based on empirical H isotope data that we generated in two complementary experiments that clarifies a large part of the unexplained variability in the δ2H values of plant organic compounds.

The experiments demonstrate that information recorded in the δ2H values of plant organic compounds goes beyond hydrological signals and can also contain important information on the carbon and energy metabolism of plants. Our model explains where 2H‐fractionations occur in the biosynthesis of plant organic compounds and how these 2H‐fractionations are tightly coupled to a plant's carbon and energy metabolism. Our model also provides a mechanistic basis to introduce H isotopes in plant organic compounds as a new metabolic proxy for the carbon and energy metabolism of plants and ecosystems.

Such a new metabolic proxy has the potential to be applied in a broad range of disciplines, including plant and ecosystem physiology, biogeochemistry and palaeoecology.

Place, publisher, year, edition, pages
Wiley-Blackwell, 2018
Keywords
alkanes, biomarker, cellulose, hydrogen isotopes, plant metabolism
National Category
Other Earth and Related Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-145979 (URN)10.1111/nph.15016 (DOI)000428070100011 ()29460486 (PubMedID)
Available from: 2018-03-24 Created: 2018-03-24 Last updated: 2019-01-07Bibliographically approved

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