David B Lowry

Michigan State University, Ист-Лансинг, Michigan, United States

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Publications (32)150.27 Total impact

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    ABSTRACT: Genetic and genomic resources have recently been developed for the bioenergy crop switchgrass (Panicum virgatum). Despite these advances, little research has been focused on identifying genetic loci involved in natural variation of important bioenergy traits, including biomass. Quantitative trait locus (QTL) mapping is typically used to discover loci that contribute to trait variation. Once identified, QTLs can be used to improve agronomically important traits through marker-assisted selection. In this study, we conducted QTL mapping in Austin, TX, USA, with a full-sib mapping population derived from a cross between tetraploid clones of two major switchgrass cultivars (Alamo-A4 and Kanlow-K5). We observed significant among-genotype variation for the vast majority of growth, morphological, and phenological traits measured on the mapping population. Overall, we discovered 27 significant QTLs across 23 traits. QTLs for biomass production colocalized on linkage group 9b across years, as well as with a major biomass QTL discovered in another recent switchgrass QTL study. The experiment was conducted under a rainout shelter, which allowed us to examine the effects of differential irrigation on trait values. We found very minimal effects of the reduced watering treatment on traits, with no significant effect on biomass production. Overall, the results of our study set the stage for future crop improvement through marker-assisted selection breeding.
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    ABSTRACT: Soil water availability represents one of the most important selective agents for plants in nature and the single greatest abiotic determinant of agricultural productivity, yet the genetic bases of drought acclimation responses remain poorly understood. Here, we developed a systems-genetic approach to characterize quantitative trait loci (QTLs), physiological traits and genes that affect responses to soil moisture deficit in the TSUxKAS mapping population of Arabidopsis thaliana. To determine the effects of candidate genes underlying QTLs, we analyzed gene expression as a covariate within the QTL model in an effort to mechanistically link markers, RNA expression, and the phenotype. This strategy produced ranked lists of candidate genes for several drought-associated traits, including water use efficiency, growth, abscisic acid concentration (ABA), and proline concentration. As a proof of concept, we recovered known causal loci for several QTLs. For other traits, including ABA, we identified novel loci not previously associated with drought. Furthermore, we documented natural variation at two key steps in proline metabolism and demonstrated that the mitochondrial genome differentially affects genomic QTLs to influence proline accumulation. These findings demonstrate that linking genome, transcriptome, and phenotype data holds great promise to extend the utility of genetic mapping, even when QTL effects are modest or complex. © 2015 American Society of Plant Biologists. All rights reserved.
    The Plant Cell 04/2015; 27(4). DOI:10.1105/tpc.15.00122 · 9.58 Impact Factor
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    ABSTRACT: Evolutionary biology is in an exciting era, in which powerful genomic tools make accessible the answers to long-standing questions about variation, adaptation, and speciation. The availability of a suite of genomic resources, a shared knowledge-base, and a long history of study have made the phenotypically diverse plant genus Mimulus an important system for understanding evolutionary and ecological processes. An international Mimulus Research Meeting was held at Duke University in June 2014 to discuss developments in evolutionary and ecological genetic studies in Mimulus. Here, we report major recent discoveries presented at the meeting that use genomic approaches to advance our understanding of three major themes: the parallel genetic basis of adaptation; the ecological genomics of speciation; and the evolutionary significance of structural genetic variation. We also suggest future research directions for studies of Mimulus and highlight challenges faced when developing new evolutionary and ecological model systems. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Molecular Ecology 04/2015; 24(11). DOI:10.1111/mec.13190 · 6.49 Impact Factor
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    ABSTRACT: The process of plant speciation often involves the evolution of divergent ecotypes in response to differences in soil water availability between habitats. While the same set of traits is frequently associated with xeric/mesic ecotype divergence, it is unknown whether those traits evolve independently or if they evolve in tandem as a result of genetic colocalization either by pleiotropy or genetic linkage. The self-fertilizing C4 grass species Panicum hallii includes two major ecotypes found in xeric (var. hallii) or mesic (var. filipes) habitats. We constructed the first linkage map for P. hallii by genotyping a reduced representation genomic library of an F2 population derived from an intercross of var. hallii and filipes. We then evaluated the genetic architecture of divergence between these ecotypes through quantitative trait locus (QTL) mapping. Overall, we mapped QTLs for nine morphological traits that are involved in the divergence between the ecotypes. QTLs for five key ecotype-differentiating traits all colocalized to the same region of linkage group five. Leaf physiological traits were less divergent between ecotypes, but we still mapped five physiological QTLs. We also discovered a two-locus Dobzhansky–Muller hybrid incompatibility. Our study suggests that ecotype-differentiating traits may evolve in tandem as a result of genetic colocalization.
    New Phytologist 09/2014; 205(1). DOI:10.1111/nph.13027 · 7.67 Impact Factor
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    ABSTRACT: Background In light of the changes in precipitation and soil water availability expected with climate change, understanding the mechanisms underlying plant responses to water deficit is essential. Toward that end we have conducted an integrative analysis of responses to drought stress in the perennial C4 grass and biofuel crop, Panicum virgatum (switchgrass). Responses to soil drying and re-watering were measured at transcriptional, physiological, and metabolomic levels. To assess the interaction of soil moisture with diel light: dark cycles, we profiled gene expression in drought and control treatments under pre-dawn and mid-day conditions. Results Soil drying resulted in reduced leaf water potential, gas exchange, and chlorophyll fluorescence along with differential expression of a large fraction of the transcriptome (37%). Many transcripts responded differently depending on time of day (e.g. up-regulation pre-dawn and down-regulation mid-day). Genes associated with C4 photosynthesis were down-regulated during drought, while C4 metabolic intermediates accumulated. Rapid changes in gene expression were observed during recovery from drought, along with increased water use efficiency and chlorophyll fluorescence. Conclusions Our findings demonstrate that drought responsive gene expression depends strongly on time of day and that gene expression is extensively modified during the first few hours of drought recovery. Analysis of covariation in gene expression, metabolite abundance, and physiology among plants revealed non-linear relationships that suggest critical thresholds in drought stress responses. Future studies may benefit from evaluating these thresholds among diverse accessions of switchgrass and other C4 grasses. Electronic supplementary material The online version of this article (doi:10.1186/1471-2164-15-527) contains supplementary material, which is available to authorized users.
    BMC Genomics 06/2014; 15:527. DOI:10.1186/1471-2164-15-527 · 4.04 Impact Factor
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    ABSTRACT: Gene expression varies widely in natural populations, yet the proximate and ultimate causes of this variation are poorly known. Understanding how variation in gene expression affects abiotic stress tolerance, fitness, and adaptation is central to the field of evolutionary genetics. We tested the hypothesis that genes with natural genetic variation in their expression responses to abiotic stress are likely to be involved in local adaptation to climate in Arabidopsis thaliana. Specifically, we compared genes with consistent expression responses to environmental stress (expression stress responsive, “eSR”) to genes with genetically variable responses to abiotic stress (expression genotype-by-environment interaction, “eGEI”). We found that on average genes that exhibited eGEI in response to drought or cold had greater polymorphism in promoter regions and stronger associations with climate than eSR genes or genomic controls. We also found that transcription factor binding sites known to respond to environmental stressors, especially abscisic acid responsive elements, showed significantly higher polymorphism in drought eGEI genes in comparison to eSR genes. By contrast, eSR genes tended to exhibit relatively greater pairwise haplotype sharing, lower promoter diversity, and fewer non-synonymous polymorphisms, suggesting purifying selection or selective sweeps. Our results indicate that cis-regulatory evolution and genetic variation in stress responsive gene expression may be important mechanisms of local adaptation to climatic selective gradients.
    Molecular Biology and Evolution 05/2014; 31(9). DOI:10.1093/molbev/msu170 · 14.31 Impact Factor
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    ABSTRACT: Abstract Determining the patterns and mechanisms of natural selection in the wild is of fundamental importance to understanding the differentiation of populations and the evolution of new species. However, it is often unknown the extent to which adaptive genetic variation is distributed among ecotypes between distinct habitats versus along large-scale geographic environmental gradients, such as those that track latitude. Classic studies of selection in the wild in switchgrass, Panicum virgatum, tested for adaptation at both of these levels of natural variation. Here we review what these field experiments and modern agronomic field trials have taught us about natural variation and selection at both the ecotype and environmental gradient levels in P. virgatum. With recent genome sequencing efforts in P. virgatum, it is poised to become an excellent system for understanding the adaptation of grassland species across the eastern half of North America. The identification of genetic loci involved in different types of adaptations will help to understand the evolutionary mechanisms of diversification within P. virgatum and provide useful information for the breeding of high-yielding cultivars for different ecoregions.
    The American Naturalist 05/2014; 183(5):682-92. DOI:10.1086/675760 · 4.45 Impact Factor
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    ABSTRACT: Chromosomal rearrangement polymorphisms are common and increasingly found to be associated with adaptive ecological divergence and speciation. Rearrangements, such as inversions, reduce recombination in heterozygous individuals and thus can protect favorable allelic combinations at linked loci, facilitating their spread in the presence of gene flow. Recently, we identified a chromosomal inversion polymorphism that contributes to ecological adaptation and reproductive isolation between annual and perennial ecotypes of the yellow monkeyflower, Mimulus guttatus. Here we evaluate the population genetic structure of this inverted region in comparison with the collinear regions of the genome across the M. guttatus species complex. We tested whether annual and perennial M. guttatus exhibit different patterns of divergence for loci in the inverted and noninverted regions of the genome. We then evaluated whether there are contrasting climate associations with these genomic regions through redundancy analysis. We found that the inversion exhibits broadly different patterns of divergence among annual and perennial M. guttatus and is associated with environmental variation across population accessions. This study is the first widespread population genetic survey of the diversity of the M. guttatus species complex. Our findings contribute to a greater understanding of morphological, ecological, and genetic evolutionary divergence across this highly diverse group of closely related ecotypes and species. Finally, understanding species relationships among M. guttatus sp. has hitherto been stymied by accumulated evidence of substantial gene flow among populations as well as designated species. Nevertheless, our results shed light on these relationships and provide insight into adaptation in life history traits within the complex.This article is protected by copyright. All rights reserved.
    Molecular Ecology 05/2014; 23(11). DOI:10.1111/mec.12778 · 6.49 Impact Factor
  • David Lowry
    2013 Society for Advancement of Hispanics/Chicanos and Native Americans in Science National Conference; 10/2013
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    ABSTRACT: The regulation of gene expression is crucial for an organism's development and response to stress, and an understanding of the evolution of gene expression is of fundamental importance to basic and applied biology. To improve this understanding, we conducted expression quantitative trait locus (eQTL) mapping in the Tsu-1 (Tsushima, Japan) × Kas-1 (Kashmir, India) recombinant inbred line population of Arabidopsis thaliana across soil drying treatments. We then used genome resequencing data to evaluate whether genomic features (promoter polymorphism, recombination rate, gene length, and gene density) are associated with genes responding to the environment (E) or with genes with genetic variation (G) in gene expression in the form of eQTLs. We identified thousands of genes that responded to soil drying and hundreds of main-effect eQTLs. However, we identified very few statistically significant eQTLs that interacted with the soil drying treatment (GxE eQTL). Analysis of genome resequencing data revealed associations of several genomic features with G and E genes. In general, E genes had lower promoter diversity and local recombination rates. By contrast, genes with eQTLs (G) had significantly greater promoter diversity and were located in genomic regions with higher recombination. These results suggest that genomic architecture may play an important a role in the evolution of gene expression.
    The Plant Cell 09/2013; 25. DOI:10.1105/tpc.113.115352 · 9.58 Impact Factor
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    ABSTRACT: Background/Question/Methods Fluxes of carbon in terrestrial ecosystems are key indicators of their productivity and carbon storage potential. Ecosystem fluxes will be impacted by climate change, especially changes in rainfall amount. Fluxes may also be affected by plant traits, including aboveground biomass (AGB), leaf photosynthesis (ACO2), leaf area index (LAI), leaf nitrogen (N) and chlorophyll (Chl) contents. Plant traits differ among genotypes adapted to different climate regimes, hence ecosystem fluxes may differ among genotypes. Here we demonstrate genotypic variation in trait-based control of net ecosystem exchange (NEE) in the native C4 tallgrass species Panicum virgatum L. (switchgrass), a widespread, dominant component of tallgrass prairie, and a potential bioenergy crop. Nine genotypes of P. virgatumoriginating from 27 to 35° N latitude were established under a rainfall exclusion shelter in central Texas, USA. The genotypes received rainfall treatments representing dry, average and wet years in a randomized complete blocks design. NEE [and its components, gross primary production (GPP), ecosystem respiration (Re)], plant traits, and normalized difference vegetation index (NDVI) were measured during rapid tiller growth (June) and near peak growth (August), and AGB was measured at the end of the growing season. Results/Conclusions NEE increased 22-83% with increasing rainfall (0.003<p<0.08) and varied 80-300% among genotypes (0.004<p<0.0001), because of strong responses in both GPP and Re. Genotypes varied up to 5-fold in NEE, GPP, and Re at high rainfall, compared to ~ 2-fold at low rainfall, indicating that genotypic differences in ecosystem carbon fluxes were magnified at high rainfall (0.04 < p < 0.08). NEE, GPP, and Re were strongly correlated with AGB, ACO2, and LAI (0.0001<p<0.04). Significant AGB x genotype, ACO2 x genotype, and NDVI x genotype interactions (0.001<p<0.04) indicated that AGB, ACO2 , and NDVI relationships with fluxes differed among the genotypes. Leaf N and Chl contents and NDVI were mostly unrelated to ecosystem fluxes and did not interact with genotype or treatment. These results indicate that P. virgatum genotypes varied in the control of ecosystem fluxes by plant traits related to biomass and photosynthetic carbon uptake. These results extend previous research by demonstrating genotypic variation in traits controlling ecosystem carbon fluxes in a widespread dominant native grassland species which is responsive to precipitation amount and may become more prevalent in bioenergy cropping systems.
    98th ESA Annual Convention 2013; 08/2013
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    ABSTRACT: Background/Question/Methods Variation in precipitation expected with climate change may impact plant fitness and alter ecosystem dynamics by modifying species phenology, productivity, and physiology. Species responses to varied precipitation will depend in part on plastic responses of genotypes adapted to local climate. Here, we examined the effects of variable precipitation on genotype reproductive phenology, aboveground net primary productivity (ANPP), leaf area index (LAI), and leaf functional traits in Panicum virgatum L. (switchgrass), an ecologically dominant tallgrass prairie species. We hypothesized that plastic responses of genotypes (genotype plasticity index) to varied precipitation would depend upon genotype climate of origin. To test this hypothesis, we collected nine P. virgatum genotypes adapted to different climates and grew them under rainout shelters located at two sites in Central Texas, differing in soil depth (deep, shallow). The genotypes received six experimental precipitation treatments, representing the driest to wettest years (based on mean annual precipitation) for each site, in a randomized complete block design. Days to flowering (DF), LAI, and ANPP were measured in all treatments, and leaf water potentials (Ψ), net photosynthetic rates (ACO2), leaf nitrogen (N), and leaf mass area (LMA) were measured in the low, mean, and high precipitation treatments during June and August. Results/Conclusions Decreased precipitation delayed DF up to 21 days (P<0.001), reduced LAI 9% - 37% (0.5<P<0.04), and reduced ANPP 8% - 144% (P<0.001). Genotypes differed in DF by up to 134 days (P<0.0001), and showed substantial differences in LAI (0.7–5.2 m2 m-2; P<0.0001) and ANPP (39–2870 g m-2; P<0.0001). Predawn Ψ and ACO2 increased with increasing precipitation, with higher values in June and at the deeper soil site. Precipitation × genotype effects were significant for DF (P<0.01) and ANPP at both sites (P<0.001), and LAI at the deep soil site (P=0.04). Genotypes showed substantial variation in leaf traits with few significant precipitation × genotype effects. In terms of plasticity, genotypes from warmer climates showed lower ANPP and LAI plasticity at the deep soil site. Genotypes from climates with warm dry summers also showed lower LMA plasticity at the deep soil site. Our results indicate that adaptation to local climate may influence genotypic plasticity to variable precipitation. Such plasticity may have important implications for species and ecosystem responses to climate change.
    98th ESA Annual Convention 2013; 08/2013
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    ABSTRACT: Examining intraspecific variation in growth and function in relation to climate may provide insight into physiological evolution and adaptation, and is important for predicting species responses to climate change. Under common garden conditions, we grew nine genotypes of the C4 species Panicum virgatum originating from different temperature and precipitation environments. We hypothesized that genotype productivity, morphology and physiological traits would be correlated with climate of origin, and a suite of adaptive traits would show high broad-sense heritability (H(2) ). Genotype productivity and flowering time increased and decreased, respectively, with home-climate temperature, and home-climate temperature was correlated with genotypic differences in a syndrome of morphological and physiological traits. Genotype leaf and tiller size, leaf lamina thickness, leaf mass per area (LMA) and C : N ratios increased with home-climate temperature, whereas leaf nitrogen per unit mass (Nm ) and chlorophyll (Chl) decreased with home-climate temperature. Trait variation was largely explained by genotypic differences (H(2) = 0.33-0.85). Our results provide new insight into the role of climate in driving functional trait coordination, local adaptation and genetic divergence within species. These results emphasize the importance of considering intraspecific variation in future climate change scenarios.
    New Phytologist 05/2013; 199(4). DOI:10.1111/nph.12341 · 7.67 Impact Factor
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    David B Lowry · Colin T Purmal · Thomas E Juenger
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    ABSTRACT: • Premise of study: Understanding the relationship between climate, adaptation, and population structure is of fundamental importance to botanists because these factors are crucial for the evolution of biodiversity and the response of species to future climate change. Panicum hallii is an emerging model system for perennial grass and bioenergy research, yet very little is known about the relationship between climate and population structure in this system. • Methods: We analyzed geographic population differentiation across 39 populations of P. hallii along a longitudinal transect from the savannas of central Texas through the deserts of Arizona and New Mexico. A combination of morphological and genetic (microsatellite) analysis was used to explore patterns of population structure. • Key results: We found strong differentiation between high elevation western desert populations and lower elevation eastern populations of P. hallii, with a pronounced break in structure occurring in western Texas. In addition, we confirmed that there are high levels of morphological and genetic structure between previous recognized varieties (var. hallii and var. filipes) within this species. • Conclusions: The results of this study suggest that patterns of population structure within P. hallii may be driven by climatic variation over space. Overall, this study lays the groundwork for future studies on the genetics of local adaptation and reproductive isolation in this system.
    American Journal of Botany 03/2013; 100(3):592-601. DOI:10.3732/ajb.1200379 · 2.46 Impact Factor
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    ABSTRACT: Most species are superbly and intricately adapted to the environments in which they live. Adaptive evolution by natural selection is the primary force shaping biological diversity. Differences between closely related species in ecologically selected characters such as habitat preference, reproductive timing, courtship behavior, or pollinator attraction may prevent interbreeding in nature, causing reproductive isolation. But does ecological adaptation cause reproductive incompatibilities such as hybrid sterility or lethality? Although several genes causing hybrid incompatibilities have been identified, there is intense debate over whether the genes that contribute to ecological adaptations also cause hybrid incompatibilities. Thirty years ago, a genetic study of local adaptation to copper mine soils in the wildflower identified a locus that appeared to cause copper tolerance and hybrid lethality in crosses to other populations. But do copper tolerance and hybrid lethality have the same molecular genetic basis? Here we show, using high-resolution genome mapping, that copper tolerance and hybrid lethality are not caused by the same gene but are in fact separately controlled by two tightly linked loci. We further show that selection on the copper tolerance locus indirectly caused the hybrid incompatibility allele to go to high frequency in the copper mine population because of hitchhiking. Our results provide a new twist on Darwin's original supposition that hybrid incompatibilities evolve as an incidental by-product of ordinary adaptation to the environment.
    PLoS Biology 02/2013; 11(2):e1001497. DOI:10.1371/journal.pbio.1001497 · 11.77 Impact Factor
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    ABSTRACT: Background/Question/Methods Theoretical models have suggested that gene flow coupled with selection are critical determinants of species’ range limits. To evaluate these models, population size, genetic diversity, and contemporary gene flow were examined along three transects spanning the entire warm-to-cold elevational range of the annual plant, Mimulus laciniatus, in the California Sierra Nevada Mountains. By examining both range edges, climate patterns were separated from those of peripherality per se. Results/Conclusions Plant density increased gradually towards both climate limits. Despite this increased density, populations at both climate limits had reduced genetic diversity, suggesting increased drift, selfing, and/or selection at limits. Populations occupying similar climates were more genetically similar, perhaps owing to elevation-based selection or phenological differences. Warm- and cold-climate limits likely stem from limited genetic variation, a result supported by a prior experimental study at the warm edge in this system. Neither the earlier nor this approach supports contemporary, maladaptive center-edge gene flow as a mechanism generating range limits, as predicted by some models.
    97th ESA Annual Convention 2012; 08/2012
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    David B Lowry
    New Phytologist 06/2012; 194(4):888-90. DOI:10.1111/j.1469-8137.2012.04146.x · 7.67 Impact Factor
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    DAVID B. LOWRY
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    ABSTRACT: Recent interest in the role of ecology in species formation has led to renewed discussion of the stages in the process of speciation. Although attempts to classify the stages in the process of species formation date back at least as far as Alfred Russel Wallace, one of the most intense debates on the subject occurred among botanists during the mid‐20th Century. The present review outlines the progression of the historical debate about stages in the evolution of species, which was instigated by the genecological classification scheme of Göte Turesson in the 1920s, championed in the mid‐century by Jens Clausen, and then brought under harsh scrutiny by many in the 1960s and 1970s. At the heart of the controversy is the question of whether speciation occurs rapidly on a local scale or gradually through the formation of geographically widespread ecotypes that evolve as precursors to species. A corollary to this debate is the question of whether speciation is reversible and, if so, how does it become irreversible? A third wave of interest in stages in the process of speciation is currently underway, thus making a modern historical narrative of the debate important. Both contemporary and past evolutionary biologists have argued that viewing speciation as being composed of stages can free researchers from concerns over species definitions and focus attention on the mechanisms involved in the process. How speciation becomes irreversible and whether ecogeographically isolated ecotypes are integral to this process remain as important unresolved issues. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 241–257.
    Biological Journal of the Linnean Society 06/2012; 106(2). DOI:10.1111/j.1095-8312.2012.01867.x · 2.54 Impact Factor

Publication Stats

755 Citations
150.27 Total Impact Points

Institutions

  • 2015
    • Michigan State University
      Ист-Лансинг, Michigan, United States
  • 2012–2014
    • University of Texas at Austin
      • Department of Integrative Biology
      Austin, Texas, United States
  • 2008–2012
    • Duke University
      • Department of Biology
      Durham, North Carolina, United States
  • 2008–2009
    • Duke University Medical Center
      Durham, North Carolina, United States