Joy Bergelson is the Dorothy Schiff Professor of Genomics in the Department of Biology at New York University. Joy has worked for the past two decades with key collaborators to reveal that A. thaliana has clear patterns of isolation by distance across the globe, as well as patterns of linkage disequilibrium, that make it eminently suitable for genome wide association mapping and testing the roles of ecologically important genes.
This work has culminated in the first GWA mapping study in any plant species, and reveals that there is high power to detect many common alleles of major effect. This began with a series of studies to characterize the population structure of the species (e.g., Horton et al. 2012) and its patterns of polymorphism (e.g., Platt et al. 2010), and culminated in the Atwell paper (Atwell et al. 2010). It also facilitated studies of climate adaptation using a novel method to map SNPs associated with particular climate regimes (Hancock et al. 2011).
Key accomplishments
> Evolution of resistance genes
> Cost of resistance
> Importance of life-history strategy on coevolutionary dynamics
> Transgenic technologies and genetic control in molecular ecology
> Interactions between A. thaliana and its microbiome
Evolution of resistance genes
Plant-pathogen coevolution is often characterized as a molecular arms race between resistance and virulence. My work with A. thaliana, however, revealed an evolutionarily stable stalemate manifest as ancient balanced polymorphisms for resistance and susceptibility alleles (Karasov et al. 2014; Bakker et al. 2006; Mauricio et al. 2003; Stahl et al. 1999). We have studied in detail the ancient balanced polymorphisms for three R genes (Karasov et al. 2014; Bakker et al. 2006; Stahl et al. 1999), and provided evidence that ~30% of R genes in the genome reveal high levels of ancient polymorphism and clear evidence of balancing selection (Mauricio et al. 2003).
Cost of resistance
After describing the evolutionary patterns of R gene loci, we examined the ecological mechanisms driving these ancient balanced polymorphisms. This includes the first demonstration that R genes can exhibit large costs of resistance in the absence of a pathogen, consistent with the action of balancing selection, but raising questions about the mechanistic basis of these fitness costs. Specifically, we have dissected the forces driving balancing selection for a couple of these cases, all of which are facilitated by the presence of costs of resistance (Karasov et al. 2014; Tian et al. 2003). Rpm1 is notable in suggesting a role of frequency dependent selection and provides the first evidence of ecological dynamics in patterns of molecular evolution (Karasov, Horton, and Bergelson 2014). Rps5 is notable in showing that even ecologically complex interactions, involving many species and multiple effectors, can lead to a signature of balancing selection (Karasov et al. 2014; Tian et al. 2002). This latter observation wasn’t obvious because host-pathogen models permitting long-term coexistence have historically assumed an obligate association between a single host and a single pathogen (Stahl et al. 1999).
Importance of life-history strategy on coevolutionary dynamics
My research has revealed that A. thaliana behaves very differently from agricultural systems where pathogens quickly overcome resistance. This is because A. thaliana is almost never the primary host to a pathogen species, and therefore does not impose strong selection upon it. There are many repercussions of this realization. First, A. thaliana adapts to local pathogens (rather than vice-versa) as we have shown using cross-inoculation experiments (Karasov TL, Barrett LG, Herschberg R, Bergelson J. in press). Second, the relative success of bacterial species within A. thaliana may prove to have as much to do with microbe-microbe interactions as plant microbe interactions (Horton et al. 2014; Kniskern, Barrett, and Bergelson 2011). Third, while A. thaliana genomes clearly encode host factors that shape the microbial community (Barrett et al. 2011), there may be no need to engage in warfare with particular pathogens. These ideas highlight the importance of community ecology in understanding evolutionary dynamics, and suggest a paradigm shift in how to think about the persistence of some natural systems.
Transgenic technologies and genetic control in molecular ecology
While developing my research program, I shaped the field of molecular ecology by introducing transgenic technologies and notions of genetic controls. I have led by example in advocating for careful control of host genetics and environment in ecological experiments. My early review (Joy Bergelson and Roux 2010) was influential in introducing the importance of genetic control, and my early work on chlorsulfuron resistance was the first time that plant transgenics were created for ecological studies (Wichmann and Bergelson 2004). That approach has continued with growing sophistication throughout my R gene work, and has been adopted into several other projects, for example revealing costs, benefits and epistatic interactions among virulence genes in Xanthomonas (J Bergelson et al. 1996). Application of these ideas to GWAs is discussed in (Joy Bergelson and Purrington 1996).
Interactions between A. thaliana and its microbiome
Although the field of plant-microbe interactions originated with studies of A. thaliana and P. syringae, these species were not known to co-occur in nature before our contributions (Brachi et al. 2015). We also identified P. viridiflava as a common pathogen of A. thaliana, and studied both its population biology e.g., (Traw, Kniskern, and Bergelson 2007) and mode of action – revealing differences in the population biology of necrotrophs and biotrophs and long-lived virulence polymorphism. Our surveys of the microbiome of A. thaliana, first using culture based methods (Goss, Kreitman, and Bergelson 2005) and later non-culture based methods (our most recent papers), set the stage for community-wide efforts to understand the factors shaping host associated microbes. One of these factors, host defenses, has been an on-going focus of ours for decades e.g., (Goss, Kreitman, and Bergelson 2005; Jakob et al. 2002).
Our current projects expand on our work examining the molecular ecology and evolution of Arabidopsis thaliana and it’s microbiome. Our newest approaches involve 1) expanding the plant microbiome work to include fungi, 2) determining which bacterial genes are required for bacterial strains to colonize a plant, and 3) the role of epigenetics in plant defense.
Background
Joy completed her undergraduate degree at Brown University (ScB summa cum laude in Biology, 1984) then travelled to the University of York with a Marshall Fellowship (MPhil in Biology, 1986). She did her doctorate at the University of Washington (PhD in Zoology, 1990) and post-doctoral studies at Oxford.
Following two years at Washington University, St. Louis, she joined the faculty at the University of Chicago in 1994. She is a member of the three University Committees: Evolutionary Biology, Genetics, and Microbiology, and has directed the research of 27 post-doctoral scholars, 19 graduate students, 22 visiting scientists, 29 undergraduate students, 22 high school students, and has served on the graduate student committee for 36 other students. Joy has served on dozens of Departmental and University committees, dozens of NSF and USDA panels, and has served as reviewer or editor for scores of journals.
Joy has authored > 100 papers that have accumulated > 19,000 citations. Joy has received numerous awards including; Phi Beta Kappa 1983, Brown University Scholarship Award 1983, Sigma Xi 1984, Marshall Scholarship 1984, NSF Graduate Student Fellowship 1986, Sloane Fellowship in Molecular Evolution 1990 (declined), American Fellowship, Association of University Women 1989, NATO Fellowship in Biological Science 1990, Richard Lounsbery Foundation Fellow of the Life Sciences Research Foundation 1990, Packard Fellowship 1993, NSF Presidential Faculty Fellow Award 1993, American Society of Naturalists Young Investigator Award 1993, and Fellow of the American Association for the Advancement of Science 2004.
Joy is currently serving as Chair of the AAAS Biology section and is a member of the Multinational Arabidopsis Steering Committee, subcommittee on Natural Variation. In 2018, Joy was elected to the National Academy.