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Environment and Genotype Influence Quantitative and Qualitative Variation in Condensed Tannins in Aspen

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Abstract

Condensed tannins (CTs) are abundant, ecologically-relevant secondary metabolites in many plants, which respond to variables associated with anthropogenic environmental change. While many studies have reported how genetic and environmental factors affect CT concentrations, few have explored how they influence CT molecular structure. Here, using trembling aspen (Populus tremuloides) as a model organism, we report how foliar CT concentrations, polymer sizes, representation of procyanidins and prodelphinidins, and stereochemistry vary in response to changes in air temperature (warming and freeze damage), air composition (elevated CO2 and O3), soil quality (nutrients and microbiome), and herbivory (mammal and lepidopteran). Use of multiple aspen genotypes enabled assessment of genetic influences on aspen CTs. CT concentration and composition were analyzed by thiolysis-ultra high performance liquid chromatography/mass spectrometry in archived leaf samples from prior experiments. All environmental variables explored except for soil microbiome influenced both CT quantity and quality, with climate factors appearing to have larger effect magnitudes than herbivory. Climate, soil, and herbivory effects varied among genotypes, while air composition effects were consistent across genotypes. Considering that CT properties (concentrations and molecular structures) mediate functions at the organismal through ecosystem scales, intraspecific variation in responses of CT properties to environmental factors could provide a pathway through which environmental change exerts selective pressure on Populus populations. Future studies are needed to identify the molecular-level mechanisms by which environmental factors influence CT concentrations and structures, and to establish their ecological and evolutionary significance.

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https://doi.org/10.5061/dryad.vx0k6djx6.

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Acknowledgements

Specimens analyzed herein were provided by investigators associated with the studies represented: John Couture oversaw the study of O3 and CO2 and assisted with statistical analysis of the corresponding data; Mary Jamieson oversaw the study of warming and lepidopteran defoliation; Ken Keefover-Ring oversaw the study of soil nutrients and mammal browsing; Elizabeth Gryzmala assisted with execution of the study of freeze damage; Zhengzhen Li provided advice on statistical analyses. We thank the two anonymous reviewers whose feedback improved the manuscript.

Funding

This research was funded by the National Science Foundation (DEB-0841609) and the USDA National Institute of Food and Agriculture (AFRI grant 2016–7013–25088).

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K. Rubert-Nason and R. Lindroth conceived this study and developed the manuscript. P. Yang collaborated with K. Rubert-Nason on the development and execution of the method used for analysis of condensed tannin quality. C. Morrow conducted and interpreted principal component ordination statistical analyses and R. Lindroth secured funding for the research.

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Correspondence to Kennedy F Rubert-Nason.

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The authors have no relevant financial or non-financial interests to disclose.

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Rubert-Nason, K.F., Yang, P., Morrow, C.J. et al. Environment and Genotype Influence Quantitative and Qualitative Variation in Condensed Tannins in Aspen. J Chem Ecol 49, 325–339 (2023). https://doi.org/10.1007/s10886-023-01430-5

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  • DOI: https://doi.org/10.1007/s10886-023-01430-5

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