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 will be essential if we are to maintain adaptability 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.
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 and Norway (above left) show major differences in their allocation of resources to reproductive vs. vegetative processes when grown in a common environment (above right). 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 have not been studied to date in an integrated manner. In collaboration with Outi Savolainen (University of Oulu, Finland), we combined QTL mapping with structural equation modeling to characterize resource allocation trade-offs in Norway x North Carolina crosses tested in both parental environments (Remington et al. 2013). A key finding was that QTL regions affected resource allocation largely by regulating early lateral shoot development, leading to cascading effects on later development. North Carolina alleles increased reproduction and concurrently reduced vegetative development in North Carolina, while reducing both survival and reproduction in Norway. These effects appeared to involve shifts in developmental timing between the two environments, not direct trade-offs between reproduction and survival. Thus, while genes affecting resource allocation appear to have important roles in local adaptation, this may involve complex interactions between developmental patterns and environment instead of traditional models involving direct costs of reproduction.
A subsequent study involving the research of two undergraduates (Jennifer Figueroa and Mitali Rane) provided evidence that the developmental differences between populations -- essentially variation in the degree of perenniality -- involve the amount of time individual shoots grow vegetatively before undergoing reproductive transitions (Remington et al. 2015). This model, in which the allocated resource is the time shoots spend in vegetative vs. reproductive growth, could have very different consequences for survival under (a) long vs. (b) short growing seasons (diagram above).
To test the time allocation model, we have developed and grown additional F2 crosses in a greenhouse environment (mimicking a North Carolina-like climate) and scored them for a much larger set of developmental traits. Since we lack funding for genome-wide genotyping of the newer crosses, undergraduates in the lab have been genotyping plants for candidate genes in the previously-identified QTL regions and characterizing their developmental functions.
Two doctoral students have been pursuing the identities of the genes underlying the resource allocation/perenniality QTLs. Bishwa Kiran Giri's recently-completed doctoral research evaluated allele-specific expression in F1 plants to identify possible candidate genes, and he investigated the potential role of auxin transport in developmental variation using auxin transport and inhibition assays. Anslei Foster is using transgenic approaches to test effects of candidate genes on perenniality. Together, this set of studies will help achieve our goal of establishing the connections between gene identity, physiological and developmental processes, and adaptive evolution in plant resource allocation patterns.
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-related suites of traits. Multiple traits involved in plant resource allocation processes are predicted to have cause-effect relationships, which can be described in terms of trait networks. Tools to model the effects of genetic variation in such networks date back nearly a century to the pioneering research of geneticist Sewall Wright, but ironically have been little-used by geneticists until recently. 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 have extended 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) made major contributions to developing these models (Gove et al. 2012).
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.
More recently, I have been interested in exploring the evolution of different patterns of genetic architecture; i.e. the extent to which variation in individual genes contributes to complex trait variation and how this variation evolves. With the expansion of the molecular "toolkit" for these studies, it is important to distinguish the effects of individual variants from the overall effects of the alleles in which they occur (Remington 2015). We are using genetic simulations to model the evolution of genetic architecture under different natural-selection scenarios.
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 participated in a collaborative effort to identify ecological, functional and genomic approaches that could be used 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. 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. While these efforts have been on hold in recent years, I think it would be exciting to develop genomic tools and crosses as tools for understanding the gene-to-phenotype processes underlying this spectacular adaptive radiation.
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 (right), and their hybrids (bottom left). 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.
The fully sequenced genome of Arabidopsis thaliana includes some 28 Aux/IAA genes and 23 related AUXIN RESPONSE FACTOR (ARF) genes. The Aux/IAA and ARF proteins regulate auxin responses and affect a number of aspects of plant growth and form, making these loci prospects for "biodiversity genes." In collaboration with Jason Reed and Todd Vision at UNC-Chapel Hill, I reconstructed the phylogenetic histories of the two gene families (click here to access the sequences and alignments). Using Todd Vision's database of chromosomal duplications in Arabidopsis, we were able to relate the evolution of the gene families to the history of genome duplications in flowering plants and their ancestors (Remington et al. 2004). We found that the two gene families have evolved by different modes, with the ARF family expanding mostly by duplication of individual genes, while most of the expansion of the Aux/IAA family has been due to duplications of the entire genome (i.e. polyploidy).
I am seeking motivated undergraduate and graduate students who are interested in working on facets of the research projects described above. 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!