Causes and Consequences of Condensed Tannin Variation in Populus

Condensed tannins (CTs), synthesized via the phenylpropanoid and malonic acid pathways, occur in Populus tissues at widely varying concentrations. Both concentration and molecular structure are determined by the independent and interactive effects of genetic, ontogenetic, and environmental factors that influence molecular control of CT synthesis, other secondary metabolite production, and plant growth. CTs have a limited role in defending Populus against herbivores, but are associated with pathogen resistance, structuring of herbivore and soil microbial communities, and regulation of soil ecosystem processes (e.g. respiration, decomposition, nutrient cycling) with feedbacks to plant fitness. Shifts in CT expression and distribution resulting from human-mediated environmental changes are likely to alter organismal interactions, community and ecosystem functions, and evolutionary processes. Future research should aim to strengthen understanding of causal connections between CTs and their biological effects across scales of organization, space and time, and to elucidate how environmental change influences CT production, biochemical tradeoffs, and interrelationships with plant fitness that drive evolutionary processes

Data from: Chemical defense over decadal scales: ontogenetic allocation trajectories and consequences for fitness in a foundation tree species

1. Expression of herbivore defense traits can change dramatically during the course of plant development. Little is known, however, about the degree of genetic or sexual variation in these ontogenetic defense trajectories or whether the trajectories themselves are adaptive, especially in long‐lived species. 2. We used a 13‐year dataset of chemical defense traits, growth, and survivorship from a common garden of trembling aspen (Populus tremuloides) genotypes to document long‐term defense trajectories and their relationship to tree fitness during juvenile and early mature stages. 3. Overall, concentrations of the two principal classes of aspen defense compounds (salicinoid phenolic glycosides [SPGs] and condensed tannins [CTs]) decreased to differing degrees in foliage of juvenile trees and then remained relatively constant in maturity. Initial values, juvenile rates of change, and average mature values all exhibited significant genetic variation for both SPGs and CTs. 4. Relationships between defense trajectory parameters and metrics of tree fitness (growth and survivorship) depended on compound type and tree sex. Females with higher‐allocation SPG trajectories (high initial juvenile concentrations, slow juvenile declines, high mature concentrations) grew more slowly relative to females with lower‐allocation trajectories. In males, higher‐allocation SPG trajectories had a lesser effect on growth but were associated with reduced mortality. Juvenile CT trajectories were not correlated with tree fitness, but average CT concentration in maturity was positively related to growth in females. 5. These results suggest that ontogenetic defense trajectories are adaptive and subject to natural selection. Genotypic variation and ontogeny shape tree defensive chemistry, both independently and interactively. These patterns of defense expression have the potential to structure trophic interactions and the genetic composition of forests in both space and time

Chemical Defense Over Decadal Scales: Ontogenetic Allocation Trajectories and Consequences for Fitness in a Foundation Tree Species

Expression of herbivore defense traits can change dramatically during the course of plant development. Little is known, however, about the degree of genetic or sexual variation in these ontogenetic defense trajectories or whether the trajectories themselves are adaptive, especially in long‐lived species. We used a 13‐year dataset of chemical defense traits, growth and survivorship from a common garden of trembling aspen (Populus tremuloides) genotypes to document long‐term defense trajectories and their relationship to tree fitness during juvenile and early mature stages. Overall, concentrations of the two principal classes of aspen defense compounds (salicinoid phenolic glycosides [SPGs] and condensed tannins [CTs]) decreased to differing degrees in foliage of juvenile trees and then remained relatively constant in maturity. Initial values, juvenile rates of change and average mature values all exhibited significant genetic variation for both SPGs and CTs. Relationships between defense trajectory parameters and metrics of tree fitness (growth and survivorship) depended on compound type and tree sex. Females with higher‐allocation SPG trajectories (high initial juvenile concentrations, slow juvenile declines, high mature concentrations) grew more slowly relative to females with lower‐allocation trajectories. In males, higher‐allocation SPG trajectories had a lesser effect on growth but were associated with reduced mortality. Juvenile CT trajectories were not correlated with tree fitness, but average CT concentration in maturity was positively related to growth in females. These results suggest that ontogenetic defense trajectories are adaptive and subject to natural selection. Genotypic variation and ontogeny shape tree defensive chemistry, both independently and interactively. These patterns of defense expression have the potential to structure trophic interactions and the genetic composition of forests in both space and time

Root Secondary Metabolites in Populus tremuloides: Effects of Simulated Climate Warming, Defoliation, and Genotype

Climate warming can influence interactions between plants and associated organisms by altering levels of plant secondary metabolites. In contrast to studies of elevated temperature on aboveground phytochemistry, the consequences of warming on root chemistry have received little attention. Herein, we investigated the effects of elevated temperature, defoliation, and genotype on root biomass and phenolic compounds in trembling aspen (Populus tremuloides). We grew saplings of three aspen genotypes under ambient or elevated temperatures (+4–6 °C), and defoliated (by 75%) half of the trees in each treatment. After 4 months, we harvested roots and determined their condensed tannin and salicinoid (phenolic glycoside) concentrations. Defoliation reduced root biomass, with a slightly larger impact under elevated, relative to ambient, temperature. Elevated temperature decreased condensed tannin concentrations by 21–43% across the various treatment combinations. Warming alone did not alter salicinoid concentrations but eliminated a small negative impact of defoliation on those compounds. Graphical vector analysis suggests that effects of warming and defoliation on condensed tannins and salicinoids were predominantly due to reduced biosynthesis of these metabolites in roots, rather than to changes in root biomass. In general, genotypes did not differ in their responses to temperature or temperature by defoliation interactions. Collectively, our results suggest that future climate warming will alter root phytochemistry, and that effects will vary among different classes of secondary metabolites and be influenced by concurrent ecological interactions such as herbivory. Temperature- and herbivory-mediated changes in root chemistry have the potential to influence belowground trophic interactions and soil nutrient dynamics

Interactions Between Bacteria and Aspen Defense Chemicals at the Phyllosphere – Herbivore Interface

Plant- and insect-associated microorganisms encounter a diversity of allelochemicals, and require mechanisms for contending with these often deleterious and broadly-acting compounds. Trembling aspen, Populus tremuloides, contains two principal groups of defenses, phenolic glycosides (salicinoids) and condensed tannins, which differentially affect the folivorous gypsy moth, Lymantria dispar, and its gut symbionts. The bacteria genus Acinetobacter is frequently associated with both aspen foliage and gypsy moth consuming that tissue, and one isolate, Acinetobacter sp. R7-1, previously has been shown to metabolize phenolic glycosides. In this study, we aimed to characterize further interactions between this Acinetobacter isolate and aspen secondary metabolites. We assessed bacterial carbon utilization and growth in response to different concentrations of phenolic glycosides and condensed tannins. We also tested if enzyme inhibitors reduce bacterial growth and catabolism of phenolic glycosides. Acinetobacter sp.R7-1 utilized condensed tannins but not phenolic glycosides or glucose as carbon sources. Growth in nutrient-rich medium was increased by condensed tannins, but reduced by phenolic glycosides. Addition of the P450 enzyme inhibitor piperonyl butoxide increased the effects of phenolic glycosides on Acinetobacter sp. R7-1. In contrast, the esterase inhibitor S, S,S,-tributyl-phosphorotrithioate did not affect phenolic glycoside inhibition of bacterial growth. Degradation of phenolic glycosides by Acinetobacter sp. R7-1 appears to alleviate the cytotoxicity of these compounds, rather than provide an energy source. Our results further suggest this bacterium utilizes additional, complementary mechanisms to degrade antimicrobial phytochemicals. Collectively, these results provide insight into mechanisms by which microorganisms contend with their environment within the context of plant-herbivore interactions

Photosynthetic acclimation of an evergreen broadleaved shrub (Ammopiptanthus mongolicus) to seasonal climate extremes on the Alxa Plateau, a cold desert ecosystem

Key message: Survival of Ammopiptanthus mongolicus in a cold desert environment is facilitated by high photosynthesis rates in spring and summer, and efficient photoprotective strategies in winter cold. Woody evergreen plants inhabiting cold desert ecosystems must retain their foliage amidst chronically dry conditions and large seasonal temperature variations. To understand the strategies enabling survival of evergreens in these environments, we monitored seasonal changes in foliar gas exchange and photosynthetic traits of Ammopiptanthus mongolicus, an evergreen broadleaved shrub native to the cold desert of northwestern China. We found that photosynthesis was relatively higher in spring and summer and lower in fall and winter. Transitioning from spring to summer, A. mongolicus maintained high photosynthetic capacity (Amax). Transitioning into fall, the Amax and maximum stomatal conductance (gsmax) decreased, while the relative stomatal limitation to photosynthesis (Ls) increased. In winter, A. mongolicus decreased Amax, maximum quantum efficiency of photosystem II (Fv/Fm), maximum RuBisCo carboxylation rates (Vcmax), maximum RuBP regeneration rates (Jmax), and photosynthetic nitrogen-use efficiency (PNUEmax) relative to other seasons. Collectively, these results suggest that A. mongolicus adapts physiologically to maximize carbon assimilation during spring and summer, and to maximize foliar resistance to cold stress at the expense of photosynthesis in winter. Foliage was protected against photo-oxidative damage during temperature extremes in winter by dark-sustained thermal energy dissipation. Overall, our study reveals that multiple photosynthetic adjustments, varying among the seasons, enable the survival of cold desert evergreens