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1.
J Chem Ecol ; 49(5-6): 325-339, 2023 Jun.
Artigo em Inglês | MEDLINE | ID: mdl-37183205

RESUMO

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.


Assuntos
Populus , Taninos , Taninos/análise , Populus/química , Populus/genética , Análise de Componente Principal , Folhas de Planta/química , Herbivoria , Mamíferos , Animais , Insetos , Temperatura , Solo/química , Clima
2.
J Chem Ecol ; 49(5-6): 235-250, 2023 Jun.
Artigo em Inglês | MEDLINE | ID: mdl-36765024

RESUMO

Trembling aspen (Populus tremuloides) is arguably the most important deciduous tree species in the Intermountain West of North America. There, as elsewhere in its range, aspen exhibits remarkable genetic variation in observable traits such as morphology and phenology. In contrast to Great Lakes populations, however, relatively little is known about phytochemical variation in western aspen. This survey of phytochemistry in western aspen was undertaken to assess how chemical expression varies among genotypes, cytotypes (diploid vs. triploid), and populations, and in response to development and mammalian browsing. We measured levels of foliar nitrogen, salicinoid phenolic glycosides (SPGs) and condensed tannins (CTs), as those constituents influence organismal interactions and ecosystem processes. Results revealed striking genotypic variation and considerable population variation, but minimal cytotype variation, in phytochemistry of western aspen. Levels of SPGs and nitrogen declined, whereas levels of CTs increased, with tree age. Browsed ramets had much higher levels of SPGs, and lower levels of CTs, than unbrowsed ramets of the same genotype. We then evaluated how composite chemical profiles of western aspen differ from those of Great Lakes aspen (assessed in earlier research). Interestingly, mature western aspen trees maintain much higher levels of SPGs, and lower levels of CTs, than Great Lakes aspen. Phenotypic variation in chemical composition of aspen - a foundation species - in the Intermountain West likely has important consequences for organismal interactions and forest ecosystem dynamics. Moreover, those consequences likely play out over spatial and temporal scales somewhat differently than have been documented for Great Lakes aspen.


Assuntos
Ecossistema , Populus , Animais , Folhas de Planta/metabolismo , Compostos Fitoquímicos/metabolismo , Glicosídeos/metabolismo , Populus/metabolismo , América do Norte , Árvores/metabolismo , Nitrogênio/metabolismo , Fenóis/metabolismo , Variação Biológica da População , Geografia , Mamíferos
3.
Ann Bot ; 127(4): 505-517, 2021 03 24.
Artigo em Inglês | MEDLINE | ID: mdl-32296821

RESUMO

BACKGROUND AND AIMS: Intraspecific variation in foundation species of forest ecosystems can shape community and ecosystem properties, particularly when that variation has a genetic basis. Traits mediating interactions with other species are predicted by simple allocation models to follow ontogenetic patterns that are rarely studied in trees. The aim of this research was to identify the roles of genotype, ontogeny and genotypic trade-offs shaping growth, defence and reproduction in aspen. METHODS: We established a common garden replicating >500 aspen genets in Wisconsin, USA. Trees were measured through the juvenile period into the onset of reproduction, for growth, defence chemistry (phenolic glycosides and condensed tannins), nitrogen, extrafloral nectaries, leaf morphology (specific leaf area), flower production and foliar herbivory and disease. We also assayed the TOZ19 sex marker and heterozygosity at ten microsatellite loci. KEY RESULTS: We found high levels of genotypic variation for all traits, and high heritabilities for both the traits and their ontogenetic trajectories. Ontogeny strongly shaped intraspecific variation, and trade-offs among growth, defence and reproduction supported some predictions while contradicting others. Both direct resistance (chemical defence) and indirect defence (extrafloral nectaries) declined during the juvenile stage, prior to the onset of reproduction. Reproduction was higher in trees that were larger, male and had higher individual heterozygosity. Growth was diminished by genotypic allocation to both direct and indirect defence as well as to reproduction, but we found no evidence of trade-offs between defence and reproduction. CONCLUSIONS: Key traits affecting the ecological communities of aspen have high levels of genotypic variation and heritability, strong patterns of ontogeny and clear trade-offs among growth, defence and reproduction. The architecture of aspen's community genetics - its ontogeny, trade-offs and especially its great variability - is shaped by both its broad range and the diverse community of associates, and in turn further fosters that diversity.


Assuntos
Populus , Ecossistema , Genótipo , Masculino , Folhas de Planta , Populus/genética , Reprodução , Árvores
4.
J Chem Ecol ; 47(3): 313-321, 2021 Mar.
Artigo em Inglês | MEDLINE | ID: mdl-33683546

RESUMO

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.


Assuntos
Desfolhantes Químicos/química , Extratos Vegetais/análise , Folhas de Planta/química , Raízes de Plantas/química , Raízes de Plantas/metabolismo , Populus/química , Populus/metabolismo , Animais , Biomassa , Mudança Climática , Desfolhantes Químicos/metabolismo , Genótipo , Glicosídeos/química , Glicosídeos/metabolismo , Herbivoria , Larva/efeitos dos fármacos , Mariposas , Fenóis/química , Fenóis/metabolismo , Folhas de Planta/metabolismo , Proantocianidinas/química , Proantocianidinas/metabolismo , Metabolismo Secundário , Solo , Temperatura
5.
Mol Ecol ; 28(19): 4404-4421, 2019 10.
Artigo em Inglês | MEDLINE | ID: mdl-31233634

RESUMO

Community genetics aims to understand the effects of intraspecific genetic variation on community composition and diversity, thereby connecting community ecology with evolutionary biology. Thus far, research has shown that plant genetics can underlie variation in the composition of associated communities (e.g., insects, lichen and endophytes), and those communities can therefore be considered as extended phenotypes. This work, however, has been conducted primarily at the plant genotype level and has not identified the key underlying genes. To address this gap, we used genome-wide association mapping with a population of 445 aspen (Populus tremuloides) genets to identify the genes governing variation in plant traits (defence chemistry, bud phenology, leaf morphology, growth) and insect community composition. We found 49 significant SNP associations in 13 Populus genes that are correlated with chemical defence compounds and insect community traits. Most notably, we identified an early nodulin-like protein that was associated with insect community diversity and the abundance of interacting foundation species (ants and aphids). These findings support the concept that particular plant traits are the mechanistic link between plant genes and the composition of associated insect communities. In putting the "genes" into "genes to ecosystems ecology", this work enhances understanding of the molecular genetic mechanisms that underlie plant-insect associations and the consequences thereof for the structure of ecological communities.


Assuntos
Biota , Estudo de Associação Genômica Ampla , Interações Hospedeiro-Parasita , Insetos/fisiologia , Biologia Molecular , Polimorfismo de Nucleotídeo Único/genética , Populus/genética , Animais , Evolução Biológica , Ecologia , Genes de Plantas/genética , Genótipo , Fenótipo
6.
Phytochem Anal ; 30(3): 257-267, 2019 May.
Artigo em Inglês | MEDLINE | ID: mdl-30548354

RESUMO

INTRODUCTION: Condensed tannins (CTs) are proanthocyanidin heteropolymers that are widely distributed among plants. Their biochemical properties are determined by molecular structure (e.g. polymer size, hydroxylation, stereochemistry). In Populus, genetically and environmentally-determined CT concentrations have been related to ecological effects, while the potential role of CT molecular structure has received little attention. OBJECTIVE: Evaluate CT polymerisation, major constituent monomers, stereochemistry and overall content in Populus tremuloides foliage using ultra-high-performance liquid chromatography with photodiode array and mass spectrometry (UPLC-PDA-(-)esi-MS) detection following thiolytic depolymerisation of the CTs. METHODOLOGY: CTs were extracted from dried foliage of six P. tremuloides genotypes into methanol and thiolytically depolymerised into constituent monomers. Calibration standards were prepared by thiolysis of CT mixtures isolated from P. tremuloides foliage on Sephadex LH-20, followed by preparative high-performance liquid chromatography (HPLC). RESULTS: Populus tremuloides CTs contained predominantly repeating subunits of three putative stereoisomers each of catechin and gallocatechin. Linear calibrations for standards of these subunits and their thioethers (purities 44-87%, UPLC-(-)esi-MS) were generally stable over the course of 10 months. CT polymer size, hydroxylation, stereochemistry and concentrations differed among genotypes. CONCLUSION: This thiolysis-UPLC-PDA-(-)esiMS method was optimised for analysis of CT polymer size, hydroxylation, stereochemistry, and total concentration in Populus foliage. It revealed significant variation in each of these properties among P. tremuloides genotypes, and will facilitate evaluation of how environmental factors affect CT molecular structures.


Assuntos
Cromatografia Líquida de Alta Pressão/métodos , Populus/química , Espectrometria de Massas por Ionização por Electrospray/métodos , Compostos de Sulfidrila/química , Taninos/análise , Calibragem , Genes de Plantas , Genótipo , Hidroxilação , Limite de Detecção , Folhas de Planta/química , Polimerização , Populus/genética , Padrões de Referência , Espectrofotometria Ultravioleta/métodos , Estereoisomerismo , Taninos/normas
7.
Plant Cell Environ ; 40(11): 2743-2753, 2017 Nov.
Artigo em Inglês | MEDLINE | ID: mdl-28755489

RESUMO

Anticipated consequences of climate change in temperate regions include early spring warmup punctuated by intermittent hard freezes. Warm weather accelerates leaf flush in perennial woody species, potentially exposing vulnerable young tissues to damaging frosts. We employed a 2 × 6 randomized factorial design to examine how the interplay of vernal (springtime) freeze damage and genetic variation in a hardwood species (Populus tremuloides) influences tree growth, phytochemistry, and interactions with an insect herbivore (Chaitophorus stevensis). Acute effects of freezing included defoliation and mortality. Surviving trees exhibited reduced growth and altered biomass distribution. Reflushed leaves on these trees had lower mass per area, lower lignin concentrations, and higher nitrogen concentrations, altered chemical defence profiles, and supported faster aphid population growth. Many effects varied among plant genotypes and were related with herbivore performance. This study suggests that a single damaging vernal freeze event can alter tree-insect interactions through effects on plant growth and chemistry. Differential responses of various genotypes to freeze damage suggest that more frequent vernal freeze events could also influence natural selection, favouring trees with greater freeze hardiness, and more resistance or tolerance to herbivores following damage.


Assuntos
Afídeos/fisiologia , Congelamento , Variação Genética , Populus/crescimento & desenvolvimento , Populus/genética , Árvores/crescimento & desenvolvimento , Árvores/genética , Análise de Variância , Animais , Biomassa , Genótipo , Análise dos Mínimos Quadrados , Populus/parasitologia , Árvores/parasitologia
8.
J Chem Ecol ; 43(1): 26-38, 2017 Jan.
Artigo em Inglês | MEDLINE | ID: mdl-27943083

RESUMO

Anthropogenic activities are altering levels of atmospheric carbon dioxide (CO2) and tropospheric ozone (O3). These changes can alter phytochemistry, and in turn, influence ecosystem processes. We assessed the individual and combined effects of elevated CO2 and O3 on the phytochemical composition of two tree species common to early successional, northern temperate forests. Trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera) were grown at the Aspen FACE (Free-Air Carbon dioxide and ozone Enrichment) facility under four combinations of ambient and elevated CO2 and O3. We measured, over three years (2006-08), the effects of CO2 and O3 on a suite of foliar traits known to influence forest functioning. Elevated CO2 had minimal effect on foliar nitrogen and carbohydrate levels in either tree species, and increased synthesis of condensed tannins and fiber in aspen, but not birch. Elevated O3 decreased nitrogen levels in both tree species and increased production of sugar, condensed tannins, fiber, and lignin in aspen, but not birch. The magnitude of responses to elevated CO2 and O3 varied seasonally for both tree species. When co-occurring, CO2 offset most of the changes in foliar chemistry expressed under elevated O3 alone. Our results suggest that levels of CO2 and O3 predicted for the mid-twenty-first century will alter the foliar chemistry of northern temperate forests with likely consequences for forest community and ecosystem dynamics.


Assuntos
Betula/efeitos dos fármacos , Dióxido de Carbono/farmacologia , Ozônio/farmacologia , Compostos Fitoquímicos/metabolismo , Populus/efeitos dos fármacos , Betula/metabolismo , Metabolismo dos Carboidratos/efeitos dos fármacos , Lignina/metabolismo , Nitrogênio/metabolismo , Fenóis/metabolismo , Folhas de Planta/efeitos dos fármacos , Folhas de Planta/metabolismo , Populus/metabolismo , Taninos/metabolismo
9.
J Chem Ecol ; 42(3): 193-201, 2016 Mar.
Artigo em Inglês | MEDLINE | ID: mdl-26961755

RESUMO

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.


Assuntos
Acinetobacter/fisiologia , Herbivoria , Mariposas/microbiologia , Compostos Fitoquímicos/metabolismo , Árvores/fisiologia , Animais , Árvores/microbiologia
10.
J Chem Ecol ; 41(1): 75-84, 2015 Jan.
Artigo em Inglês | MEDLINE | ID: mdl-25475786

RESUMO

Microbial symbionts are becoming increasingly recognized as mediators of many aspects of plant - herbivore interactions. However, the influence of plant chemical defenses on gut associates of insect herbivores is less well understood. We used gypsy moth (Lymantria dispar L.), and differing trembling aspen (Populus tremuloides Michx.) genotypes that vary in chemical defenses, to assess the influence of foliar chemistry on bacterial communities of larval midguts. We evaluated the bacterial community composition of foliage, and of midguts of larvae feeding on those leaves, using next-generation high-throughput sequencing. Plant defense chemicals did not influence the composition of foliar communities. In contrast, both phenolic glycosides and condensed tannins affected the bacterial consortia of gypsy moth midguts. The two most abundant operational taxonomic units were classified as Ralstonia and Acinetobacter. The relative abundance of Ralstonia was higher in midguts than in foliage when phenolic glycoside concentrations were low, but lower in midguts when phenolic glycosides were high. In contrast, the relative abundance of Ralstonia was lower in midguts than in foliage when condensed tannin concentrations were low, but higher in midguts when condensed tannins were high. Acinetobacter showed a different relationship with host chemistry, being relatively more abundant in midguts than with foliage when condensed tannin concentrations were low, but lower in midguts when condensed tannins were high. Acinetobacter tended to have a greater relative abundance in midguts of insects feeding on genotypes with high phenolic glycoside concentrations. These results show that plant defense chemicals influence herbivore midgut communities, which may in turn influence host utilization.


Assuntos
Sistema Digestório/microbiologia , Mariposas/microbiologia , Populus/química , Populus/fisiologia , Acinetobacter/genética , Animais , Genótipo , Glucosídeos/análise , Herbivoria/fisiologia , Larva/microbiologia , Fenóis/análise , Folhas de Planta/química , Folhas de Planta/microbiologia , Populus/genética , RNA Ribossômico 16S , Ralstonia/genética , Taninos/análise
11.
J Chem Ecol ; 41(7): 651-61, 2015 Jul.
Artigo em Inglês | MEDLINE | ID: mdl-26099738

RESUMO

Numerous studies have explored the impacts of intraspecific genetic variation and environment on the induction of plant chemical defenses by herbivory. Relatively few, however, have considered how those factors affect within-plant distribution of induced defenses. This work examined the impacts of plant genotype and soil nutrients on the local and systemic phytochemical responses of trembling aspen (Populus tremuloides) to defoliation by gypsy moth (Lymantria dispar). We deployed larvae onto foliage on individual tree branches for 15 days and then measured chemistry in leaves from: 1) branches receiving damage, 2) undamaged branches of insect-damaged trees, and 3) branches of undamaged control trees. The relationship between post-herbivory phytochemical variation and insect performance also was examined. Plant genotype, soil nutrients, and damage all influenced phytochemistry, with genotype and soil nutrients being stronger determinants than damage. Generally, insect damage decreased foliar nitrogen, increased levels of salicinoids and condensed tannins, but had little effect on levels of a Kunitz trypsin inhibitor, TI3. The largest damage-mediated tannin increases occurred in leaves on branches receiving damage, whereas the largest salicinoid increases occurred in leaves of adjacent, undamaged branches. Foliar nitrogen and the salicinoid tremulacin had the strongest positive and negative relationships, respectively, with insect growth. Overall, plant genetics and environment concomitantly influenced both local and systemic phytochemical responses to herbivory. These findings suggest that herbivory can contribute to phytochemical heterogeneity in aspen foliage, which may in turn influence future patterns of herbivory and nutrient cycling over larger spatial scales.


Assuntos
Herbivoria , Mariposas/fisiologia , Populus/fisiologia , Animais , Genoma de Planta , Mariposas/crescimento & desenvolvimento , Nitrogênio/análise , Nitrogênio/metabolismo , Compostos Fitoquímicos/análise , Compostos Fitoquímicos/genética , Compostos Fitoquímicos/metabolismo , Folhas de Planta/química , Folhas de Planta/genética , Folhas de Planta/fisiologia , Populus/química , Populus/genética , Solo/química , Taninos/análise , Taninos/genética , Taninos/metabolismo
12.
Anal Bioanal Chem ; 405(4): 1333-44, 2013 Feb.
Artigo em Inglês | MEDLINE | ID: mdl-23180073

RESUMO

Poplar (Populus) and birch (Betula) species are widely distributed throughout the northern hemisphere, where they are foundation species in forest ecosystems and serve as important sources of pulpwood. The ecology of these species is strongly linked to their foliar chemistry, creating demand for a rapid, inexpensive method to analyze phytochemistry. Our study demonstrates the feasibility of using near-infrared reflectance spectroscopy (NIRS) as an inexpensive, high-throughput tool for determining primary (e.g., nitrogen, sugars, starch) and secondary (e.g., tannins, phenolic glycosides) foliar chemistry of Populus and Betula species, and identifies conditions necessary for obtaining reliable quantitative data. We developed calibrations with high predictive power (residual predictive deviations ≤ 7.4) by relating phytochemical concentrations determined with classical analytical methods (e.g., spectrophotometric assays, liquid chromatography) to NIR spectra, using modified partial least squares regression. We determine that NIRS, although less sensitive and precise than classical methods for some compounds, provides useful predictions in a much faster, less expensive manner than do classical methods.


Assuntos
Betula/química , Extratos Vegetais/análise , Folhas de Planta/química , Populus/química , Espectroscopia de Luz Próxima ao Infravermelho/métodos , Nitrogênio/análise , Amido/análise , Taninos/análise
13.
Sci Total Environ ; 767: 144358, 2021 May 01.
Artigo em Inglês | MEDLINE | ID: mdl-33429270

RESUMO

Plant phenolic compounds (phenylpropanoids) act as defense chemicals against herbivores and can mediate ecosystem processes. Tropospheric ozone (O3) pollution alters concentrations of plant phenolics; however, little is known about how these phytochemicals respond to different levels of O3 exposure. Here, we investigated the effects of five different O3 exposure levels on foliar concentrations of phenylpropanoids (53 compounds in total) and antioxidative capacity in hybrid Populus (Populus euramericana cv. '74/76') saplings grown in the presence of high or low soil nitrogen (N) load. Increasing O3 exposure initially increased and then decreased total concentrations of phenolic compounds, revealing a biphasic exposure-response profile (hormetic zone: 1.1-36.3 ppm h AOT40). This biphasic response pattern was driven by changes in a subset of phenylpropanoids with high antioxidative capacity (e.g. condensed tannins) but not in phenolics with low antioxidative capacity (e.g. salicinoids). The O3 exposure-response relationships of some phenylpropanoids (e.g. flavonoids and chlorogenic acids) varied in response to soil N, with hormesis occurring in high N soil but not in low N soil. Collectively, our findings indicated that plant phenolic compounds exhibit nonlinear responses to increasing O3 exposure, and that the responses vary in relation to phenolic compound class, antioxidative capacity, and soil nitrogen conditions. Our findings further suggest that the impact of O3 on ecological processes mediated by phenolics will be concentration-dependent, highlighting the complexity of the ecological effects of ground-level O3 pollution.


Assuntos
Ozônio , Populus , Ecossistema , Nitrogênio , Folhas de Planta
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