Combinations of Abiotic Factors Differentially Alter Production of Plant Secondary Metabolites in Five Woody Plant Species in the Boreal-Temperate Transition Zone.

John L Berini,Ranjan Muthukrishnan,James D Forester,Rebecca A Montgomery,Peter B Reich,Stephen A Brockman,Adrian D Hegeman

doi:10.3389/fpls.2018.01257

Abstract

Plant secondary metabolites (PSMs) are a key mechanism by which plants defend themselves against potential threats, and changes in the abiotic environment can alter the diversity and abundance of PSMs. While the number of studies investigating the effects of abiotic factors on PSM production is growing, we currently have a limited understanding of how combinations of factors may influence PSM production. The objective of this study was to determine how warming influences PSM production and how the addition of other factors may modulate this effect. We used untargeted metabolomics to evaluate how PSM production in five different woody plant species in northern Minnesota, USA are influenced by varying combinations of temperature, moisture, and light in both experimental and natural conditions. We also analysed changes to the abundances of two compounds from two different species – two resin acids in Abies balsamea and catechin and a terpene acid in Betula papyrifera. We used perMANOVA to compare PSM profiles and phytochemical turnover across treatments and NMDS to visualize treatment-specific changes in PSM profiles. We used linear mixed-effects models to examine changes in phytochemical richness and changes in the abundances of our example compounds. Under closed-canopy, experimental warming led to distinct PSM profiles and induced phytochemical turnover in B. papyrifera. In open-canopy sites, warming had no influence on PSM production. In samples collected across northeastern Minnesota, regional temperature differences had no influence on PSM profiles or phytochemical richness but did induce phytochemical turnover in B. papyrifera and Populus tremuloides. Throughout northeast Minnesota, warmer temperatures combined with open canopy resulted in distinct PSM profiles for all species and induced phytochemical turnover in all but Corylus cornuta. Although neither example compound in A. balsamea was influenced by any of the abiotic conditions, both compounds in B. papyrifera exhibited significant changes in response to warming and canopy. Our results demonstrate that the metabolic response of woody plants to combinations of abiotic factors cannot be extrapolated from that of a single factor. This heterogeneous phytochemical response directly affects interactions between plants and other organisms and may yield unexpected results as plant communities adapt to novel environmental conditions.

Highlights

Plant secondary metabolites (PSMs) are one of the primary ways in which plants respond to environmental variability, and regulation of PSM production is strongly influenced by the local environment (Wink, 1988; Bennett and Wallsgrove, 1994; Bray et al, 2000; Hirt and Shinozaki, 2003)
Our study is among the first to explicitly show that combinations of abiotic drivers in forest plants can lead to broad phytochemical responses that are distinct from those that result from single abiotic factors and that different species of woody plants respond to complex sets of conditions in variable ways
In our experimental samples, warming under closed canopy led to distinct PSM profiles in paper birch but not balsam fir, with paper birch exhibiting increased phytochemical turnover

Summary

Introduction

Plant secondary metabolites (PSMs) are one of the primary ways in which plants respond to environmental variability, and regulation of PSM production is strongly influenced by the local environment (Wink, 1988; Bennett and Wallsgrove, 1994; Bray et al, 2000; Hirt and Shinozaki, 2003). Warming has been shown to have no effect on levels of phenolics in red maple (Acer rubrum, Williams et al, 2003), Norway spruce (Picea abies, Sallas et al, 2003), and Scots pine (Pinus sylvestris, Sallas et al, 2003) but resulted in decreased levels of phenolics in dark-leaved willow (Salix myrsinifolia, Veteli et al, 2006) and silver birch (Betula pendula, Kuokkanen et al, 2001). While evidence of warming-induced changes to phytochemistry is important to our understanding of how plants will respond to future climates, in natural settings, elevated temperature often combines with other abiotic conditions to influence PSM production and potentially modulate any changes to phytochemistry that might otherwise be induced by warming alone

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