David Remington
Associate Professor
Department of Biology
University of North Carolina at Greensboro
Greensboro, NC 27402-6170
office and lab: 226 Eberhart Building
phone: (336) 334-4967
e-mail: dlreming@uncg.edu
BS: University of Montana, 1976
PhD: North Carolina State University, 1999
Postdoctoral: North Carolina State University
Genetics of resource allocation in Arabidopsis lyrata
Modeling adaptive trait variation
Evolution of growth form in the Hawaiian silversword alliance
Evolution of the Aux/IAA and ARF gene families in Arabidopsis thaliana
Student Research Opportunities
Publications and Presentations
Human civilization relies heavily on plants for our survival. Plants provide us with food, shelter, fiber, and the atmospheric oxygen we breathe. As human populations and resource consumption increase, we place ever-greater demands on plant communities and are now changing the climates in which they grow. Breeding plants to be efficient and inexpensive carbohydrate delivery systems has had adverse impacts on human health, while simultaneously selecting for undesirable side-effects such as inefficient use of water and nutrients by crop plants. Discovering the evolutionary, ecological and genetic basis for the wide natural variation in how plants acquire and allocate developmental, energetic and nutritional resources is be essential if we are to maintain adaptibility in crop plants and natural populations alike. This topic is the focus of research in my laboratory.
Adaptive life history traits in plants, such as growth rates and patterns, reproductive output, and resource allocation, are complex traits. Variation in complex traits is usually influenced by multiple genes (called quantitative trait loci, or QTLs), environment, and their interactions, and these traits typically show a continuous range of variation. Variation in different complex traits is often genetically correlated, and such correlations are expected when life history trade-offs are involved. Thus, we are interested in knowing the locations and ultimately the identities of genes underlying trait variation, the molecular and developmental pathways by which they affect suites of traits, how large their effects are, and how they interact with other genes and the environment.
Specific areas of research in my laboratory include:
Genetics of resource allocation in Arabidopsis lyrata: The rock cress Arabidopsis lyrata, which is native to parts of North Carolina, is a close relative of Arabidopsis thaliana, an important model plant for genetics research and the first plant to have its complete genome sequenced. Unlike A. thaliana, A. lyrata is an outcrossing perennial that shows strong evidence of local adaptation throughout its North American and Eurasian range. The A. lyrata genome sequence has also been completed recently. This combination of features and genomic resources makes it an ideal plant for investigating the molecular genetic basis of adaptation.
We have found that A. lyrata plants from populations in different environments, such as North Carolina (top) and Norway (center) show major differences in their allocation of resources to reproductive vs. vegetative processes when grown in a common environment (bottom). Thus, A. lyrata provides an outstanding system for dissecting the developmental and genetic basis for variation in resource allocation patterns, which are a key aspect of local adaptation in plants but has not been studied to date in an integrated manner. A basic question is whether allocation primarily involves developmental resources (alternative meristem fates) or physiological resources (differential allocation of stored energy to vegetative or reproductive tissues). Secondly, does local adaptation result directly from the environment-specific fitness consequences of resource allocation trade-offs, or from more complex interactions of genetic mechanisms, developmental processes and environmental variables? To address these questions, we are mapping QTLs for resource allocation traits in Norway x North Carolina crosses tested in both parental environments, evaluating their effects on fitness, and using trait network modeling approaches (see below) to establish the traits on which QTLs act directly. Much of this research involves an international collaboration with Outi Savolainen (University of Oulu, Finland).
Future objectives are to identify the actual genes responsible for resource allocation QTLs and characterize their functions more specifically through more detailed phenotypic analysis. This will help achieve our goal of establishing the connections between gene identity, physiological and developmental processes, and adaptive evolution in plant resource allocation patterns. We are also initiating an association study to investigate the extent and genetic basis for within-population life-history variation in A. lyrata, as part of our collaboration with Outi Savolainen.
Modeling adaptive trait variation: To support our empirical research on plant life history evolution, we are developing modeling approaches for making better inferences about the nature of gene-to-phenotype relationships in complex developmentally-relates suites of traits. Multiple traits involved in plant resource allocation processes (top) have theoretically predicted cause-effect relationships, which can be described as trait networks (center). Tools to model the effects of genetic variation in such networks date back nearly a century to the pioneering research of Sewall Wright. Recent advances in molecular genetic and genomic techniques have facilitated the use of network approaches to evaluate causal relationships between genetic variation, gene expression, and phenotypes in the emerging field of systems biology. We are extending these approaches to evaluate how QTLs regulating trait variation at particular points in development can produce cascading effects on "downstream" traits, potentially leading to complex variation in life histories. Undergraduates participating in UNCG's NSF-funded Math-Bio Program (Robert Gove and Becca Fogel Erwin) and Quantitative Science REU Program (Will Chen, Nick Zweber and Erika Helgeson) have made major contributions to developing these models. We next plan to model the interface of seasonal constraints on development with the trait networks to gain understanding of the complex behaviors of resource allocation QTLs observed in contrasting environments (bottom).
The thesis research of a previous graduate student, Jolly Shrivastava, involved development of a Bayesian model to infer the parental genotypes and effects of multiple quantitative trait loci (QTLs) from trait data in diallel mating designs. Such models may be useful for inferring the presence and population frequency of large-effect QTLs prior to initiating expensive genetic mapping projects in previously unstudied species.
Evolution of growth form in the Hawaiian silversword alliance: The silversword alliance originated from a North American tarweed ancestor (related to sunflowers) within the past 6 million years, and has evolved into some 30 species with a spectacular variety of growth forms and habitats. Several of these are shown here -- (clockwise, from upper left) Argyroxiphium sandwicense (silversword); Dubautia scabra; D. reticulata (photo from Gerald Carr's silversword alliance website); Wilkesia gymnoxiphium (iliau); and D. raillardioides.
I am particpating in a collaborative effort to integrate ecological, functional and genomic approaches to understand the environmental factors that have shaped this adaptive radiation, the traits that provide adaptation to these environments, the genetic mechanisms underlying the trait differences, and how different copies of the responsible genes have become distributed among species (see Hawaiian Silversword Alliance Project website). Identifying the genes responsible for adaptive evolution and the functional mechanisms by which they contribute to environmental adaptation may provide a key to understanding how plants evolve to occupy new environments. We hope to develop genomic tools and crosses for genetic mapping as part of this effort.
In addition, I have used techniques of molecular evolution and population genetics to study the possible role of DELLA genes, which regulate gibberellin response, in phenotypic evolution within the silversword alliance. Mutations in DELLA genes have been important in producing dwarf "green revolution" wheat varieties, but their importance in evolution of natural populations has yet to be determined. Finally, we have conducted detailed population genetic analyses using AFLP markers to investigate speciation processes in Dubautia ciliolata (top left) and D. arborea (top right), and their hybrids (bottom). These two species are among the smallest and largest plants in the silversword alliance, respectively, yet they are so closely related that no consistent genetic differences between them have been found yet. Our results, along with those of related studies by Elizabeth Friar (Rancho Santa Ana Botanic Garden) and Amy Lawton-Rauh (Clemson University) suggest that the two species have remained distinct in spite of extensive hybridization, suggesting that strong natural selection has favored the parental forms in their respective shrubland and woodland environments. Our results provide indirect support for models of "collective evolution," in which evolution across most of the genome may be poorly correlated with that of the genes that actually underlie speciation.
Student Research Opportunities
I am seeking motivated undergraduate and graduate students who are interested in working on facets of the research projects described above. Special opportunities currently exist for highly capable students interested in spending a semester taking courses and conducting genetics research in Finland, and for capable undergraduates interested in participating in an NSF-funded Math-Bio program combining education and research in mathematics and biology. If you are fascinated by genetic variation and evolution in plants, and are interested in research opportunities, please e-mail me or stop by and visit!
Publications and Presentations
Publications:
Gove, R.P., W. Chen, N.B. Zweber, R. Erwin, J. Rychtář, and D.L. Remington. 2011. Effects of cause-effect networks on the structure and stability of resource allocation trait correlations. Journal of Theoretical Biology, accepted for publication.
Leinonen, P.H., D.L. Remington, and O. Savolainen. 2011. Local adaptation, phenotypic differentiation and hybrid fitness in diverged natural populations of Arabidopsis lyrata. Evolution 65:90-107.
Remington, D. L. 2009. Effects of genetic and environmental factors on trait network predictions from quantitative trait locus data. Genetics 181:1087-1099.
Crowe, M., M. Fitzgerald, D.L. Remington, and J. Rychtář. 2009. On deterministic and stochastic models of kleptoparasitism. Journal of Interdisciplinary Mathematics 12: 161-180.
Crowe, M., M. Fitzgerald, D.L. Remington, G.D. Ruxton, and J. Rychtář. 2009. Game theoretic model of brood parasitism in a dung beetle Onthophagus taurus. Evolutionary Ecology 23: 765-776.
von Wettberg, E.J., D.L. Remington, and J. Schmitt. 2008. Partitioning adaptive differentiation across a patchy landscape: shade avoidance traits in Impatiens capensis. Evolution, 62: 654-667.
Remington, D.L., and R.H. Robichaux. 2007. Influences of gene flow on adaptive speciation in the Dubautia arborea – D. ciliolata complex. Mol. Ecol., 16: 4014-4027.
Kirchoff, B.K., S.J. Richter, and D.L. Remington. 2007. Characters as groups: a new approach to morphological characters in phylogenetic analysis. Taxon 56:479-492.
Fan, C., Q.-Y. Xiang, D.L. Remington, M.D. Purugganan, and B.M. Wiegmann. 2006. Evolutionary pattern in the antR-cor gene in the dwarf dogwood complex (Cornus, Cornaceae). Genetica 130:19-37.
Rublee, P.A., D. Remington, E. Schaefer, and M.M. Marshall. 2005. Detection of the Dinozoans Pfiesteria piscicida and P. shumwayae: A review of detection methods and geographic distribution. J. Eukaryot. Microbiol. 52:83-89.
Remington, D. L., T. J. Vision, T. J. Guilfoyle, and J. W. Reed. 2004. Contrasting modes of diversification in the Aux/IAA and ARF gene families. Plant Physiol. 135:1738-1752 .
Kirchoff, B.K., S.J. Richter, D.L. Remington, and E. Wisniewski. 2004. Complex traits produce better characters. Syst. Biol. 53:1-17.
Remington, D.L., and M.D. Purugganan. 2003. Candidate genes, quantitative trait loci, and functional trait evolution in plants. Int. J. Plant Sci. 164:S7-S20 .
Purugganan, M.D., D.L. Remington, and R.H. Robichaux. 2003. Molecular evolution of regulatory genes in the silversword alliance. In Carlquist, S., B.G. Baldwin, and G.D. Carr (eds.) Tarweeds and Silverswords: Evolution of the Madiinae (Asteraceae), 171-182. Missouri Botanical Garden Press, St. Louis.
Remington, D.L., and M.D. Purugganan. 2002. GAI homologues in the Hawaiian silversword alliance (Asteraceae-Madiinae): molecular evolution of growth regulators in a rapidly diversifying plant lineage. Mol. Biol. Evol. 19:1563-1574 .
Remington, D.L., M.C. Ungerer, and M.D. Purugganan. 2001. Map-based cloning of quantitative trait loci: progress and prospects. Genet. Res. 78:213-218.
Remington, D.L., J.M. Thornsberry, Y. Matsuoka, L.M. Wilson, S.R. Whitt, J. Doebley, S. Kresovich, M.M. Goodman, and E.S. Buckler IV. 2001. Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc. Natl. Acad. Sci. USA 98:11479-11484 .
Myburg, A.A., D.L. Remington, D.M. O’Malley, R.R. Sederoff, and R.W. Whetten. 2001. High-throughput AFLP analysis using infrared dye-labeled primers and an automated DNA sequencer. Biotechniques 30:348-357.
Remington, D.L., and D.M. O’Malley. 2000. Evaluation of major genetic loci contributing to inbreeding depression for survival and early growth in a selfed family of Pinus taeda . Evolution 54:1580-1589 .
Remington, D.L., and D.M. O'Malley. 2000. Whole-genome characterization of embryonic stage inbreeding depression in a selfed loblolly pine family. Genetics 155:337-348 .
Cervera, M.T., D. Remington, J.-M. Frigerio, V. Storme, B. Ivens, W. Boerjan, and C. Plomion. 2000. Improved AFLP analysis of tree species. Can. J. For. Res. 30: 1608-1616.
Costa P., D. Pot, C. Dubos, J.-M. Frigerio, C. Pionneau, C. Bodenes, E. Bertocchi, M.-T. Cervera, D.L. Remington, and C. Plomion. 2000. A genetic map of maritime pine based on AFLP, RAPD and protein markers. Theor. Appl. Genet. 100:39-48.
Remington, D.L., R.W. Whetten, B.-H. Liu, and D.M. O’Malley. 1999. Construction of an AFLP genetic map with nearly complete genome coverage in Pinus taeda . Theor. Appl. Genet. 98:1279-1292 .
Wu, R.L., D.M. O’Malley, D.L. Remington, J.J. MacKay, and S. McKeand. 1999. Average effect of a mutation in lignin biosynthesis in loblolly pine. Theor. Appl. Genet. 99:705-710.
Selected Presentations:
Remington, D.L., P.H. Leinonen, and O. Savolainen. 2011. Genetic architecture and mechanisms of resource allocation in Arabidopsis lyrata in contrasting environments. Oral presentation at Evolution 2011 meeting, Norman, OK, June 17-22, 2011.
Remington, D.L. 2009. How does development shape plant life history evolution . . . and why should we care? Invited seminar, University of Oulu, Finland, September 17, 2009.
Remington, D.L., P.H. Leinonen, J. Leppälä, and O. Savolainen. 2009. Bloom or grow? Genes that repattern resource allocation contribute to adaptive differentiation in Arabidopsis lyrata. Oral presentation at Evolution 2009 meeting, Moscow, ID, June 12-16, 2009.
Remington, D.L. 2008. A systems biology framework for life history variation in Arabidopsis lyrata. Oral presentation at AMEGO Conference, Jotunheimen, Norway, Aug. 25-30, 2008.
Remington, D.L., R. Fogel, R. Gove, and J. Rychtář. 2008. Toward a systems biology of plant life history variation. Oral presentation at Botany 2008 Conference, Vancouver, BC., July 26-30, 2008.
Remington, D.L. 2007. Opening the resource allocation “black box”: genetic insights from Arabidopsis lyrata. Invited seminar, Department of Biology, Duke University, September 13, 2007.
Remington, D.L. 2007. Genetics of resource allocation trade-offs in Arabidopsis lyrata . Oral presentation at Botany & Plant Biology 2007, Chicago, IL, July 7-11, 2007 .
Remington, D.L. 2007. Genetic analysis of plant life history trade-offs: from "black box" to functional mechanisms. Invited seminar, University of Oulu, Finland, May 10, 2007 .
Remington, D.L. 2006. Beyond pleiotropy: functional dissection of multiple-trait QTL using structural equation models. Oral presentation at Evolution 2006 Meeting, Stony Brook, NY, June 23-27, 2006.
Remington, D.L., and R.H. Robichaux. 2005. Genome-level analysis of speciation mechanisms in the Dubautia arborea – D. ciliolata complex. Invited presentation in symposium on Patterns and Mechanisms of Evolution of Island Plants, Botany 2005 Meeting, Austin, TX, Aug. 13-17, 2005.
Remington, D.L., and R.H. Robichaux. 2004. AFLP analysis of genetic structure in the Dubautia arborea/D. ciliolata complex. Oral presentation at Evolution 2004 Meeting, Fort Collins, CO, June 26-30, 2004.
Remington, D.L., T.J. Vision, and J.W. Reed. 2002. Genomic insights into Aux/IAA gene family evolution in Arabidopsis. Oral presentation at Evolution 2002 conference; June 28- July 2, 2002 ; Champaign , IL .
Remington, D.L., and M.D. Purugganan. 2001. The hunt for biodiversity genes: GAI homologues in the Hawaiian silversword alliance. Oral presentation at Evolution 2001 conference; June 26-30, 2001 ; Knoxville , TN.
Remington, D.L., J.M. Thornsberry, S. Kresovich, M.M. Goodman, J.F. Doebley, and E.S. Buckler. 2000. Evaluating disequilibrium among polymorphisms within and between candidate genes in maize. Poster presentation at 42nd Annual Maize Genetics Conference; March 16-19, 2000 ; Coeur d’Alene , ID.
Remington, D.L., and D.M. O’Malley. 1999. Whole-genome characterization of inbreeding depression in a selfed loblolly pine family. Oral presentation at 25th Biennial Southern Forest Tree Improvement Conference; July 11-14, 1999 ; New Orleans , LA.
Remington, D.L., and D.M. O'Malley. 1999. Whole-genome evaluation of embryonic stage inbreeding depression in a selfed loblolly pine family. Oral presentation at Evolution '99; June 22-26, 1999 ; Madison , WI .
Remington, D.L., R.W. Whetten, and D.M. O’Malley. 1999. Genetic mapping reveals a number of embryonic lethal loci in a selfed family of loblolly pine. Workshop oral presentation at Plan and Animal Genome VII ; Jan. 17-21, 1999 ; San Diego , CA .
Remington, D.L. 1998. Automated AFLP detection for genetic mapping in loblolly pine using a Li-Cor system and specialized software. Oral presentation at Li-Cor User’s Meeting; May 19-20, 1998 ; Lincoln , NE.
Remington, D.L., D.M. O’Malley, and R.W. Whetten. 1998. Automated AFLP mapping in loblolly pine using the Li-Cor automated sequencer and specialized software. Workshop oral presentation at Plant and Animal Genome VI; Jan. 18-22, 1998 ; San Diego , CA .
Remington, D.L., R.W. Whetten, and D.M. O’Malley. 1998. Genetic map construction with AFLP markers in loblolly pine. Workshop oral presentation at Plant and Animal Genome VI; Jan. 18-22, 1998 ; San Diego , CA .
Remington, D.L., S.E. Surles, B.S. Crane, D.M. O’Malley, and B. Goldfarb. 1997. Identification of quantitative trait loci affecting rooting in loblolly pine. Poster presentation at 24th Biennial Southern Forest Tree Improvement Conference; June 9-12, 1997 ; Orlando , FL.
Remington, D.L., R.W. Whetten, and D.M. O’Malley. 1996. Applicability of the AFLP marker system in loblolly pine. Poster presentation at 1996 SRIEG Meeting: Novel Applications of Molecular Markers in Forest Trees: the Next Five Years; June 23-26, 1996; Houston, TX.
Remington, D. 1993. Biodiversity and State forest lands in Montana. Oral presentation at Montana Academy of Sciences Symposium on Biodiversity in Montana ; April 16, 1993 ; Helena , MT.