Even though pathogens enjoy the advantage of rapid generation times and enormous population sizes, hosts don’t typically die of infection in nature. Why not? We have discovered the prevalence of ancient balanced polymorphisms segregating at plant R-genes in Arabidopsis, indicating the preservation of particular resistance alleles. Our efforts to understand how selection maintains such a balanced polymorphism revealed an important role of community context, including microbes sharing a focal host as well as alternative hosts for a focal pathogen. We are thus exploring this complexity to understand how plants and pathogens interact in realistic community contexts. Our current focus is on how the coevolution of generalist microbes influences microbiome development, plant health/fitness, and the evolution of resistance.
Comparative R-gene evolution
When multiple host species share the same generalist pathogen, there is the potential for these species to drive convergent molecular evolution of R-genes. In this project, we aim to develop a comprehensive map of R-gene evolution across the genome of A. thaliana and two other Brassicaceous species with which Arabidopsis co-occurs in France.
The Microbiome and Evolution
The hologenome concept posits that genes harbored in the microbiome should be considered an extension of the host’s genome, as opposed to an environmental condition with which the host must contend. Within this framework, selection is believed to act on the host, on individual microbes, and on the combined host-microbiome entity (holobiont), with its unique, emergent properties. This hypothesis is highly controversial and requires explicit tests.
MacQueen, A., Sun, X., and J. Bergelson (2016) Genetic architecture and pleiotropy shape costs of Rps2-mediated resistance in Arabidopsis thaliana. Nature Plants 2 (July), 16110. https://doi.org/10.1038/nplants.2016.110
Growing evidence that R genes harbor large costs of resistance raised questions about their cumulative genetic load. This paper describes our first exploration of the cost of resistance for a locus harboring an ancient balanced polymorphism between two functional alleles. Isolines carrying the R allele were just as fit as those carrying the S allele. In addition, isolines carrying either allele were more fit than those with a deletion of Rps2, due to its role as a negative regulator of defense. These results reveal a complex interplay between genetic architecture and costs of resistance.
Karasov, T. L., Kniskern, J. M., Gao, L., DeYoung, B. J., Ding, J., Dubiella, U., Lastra, R. O., Nallu, S., Roux, F., Innes, R.W., Barrett, L.G., Hudson, R.R. and J. Bergelson (2014) The long-term maintenance of a resistance polymorphism through diffuse interactions. Nature, 512 (7515), 436–40. https://doi.org/10.1038/nature13439
This project revealed that community context is essential for understanding plant-pathogen coevolution, even which considering only a single pair of plant Resistance and microbial avr genes. This work motivates our project on comparative R-gene evolution.
Stahl, E. A., Dwyer, G., Mauricio, R., Kreitman, M. and J. Bergelson (1999) Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature, 400 (6745), 667–671. https://doi.org/10.1038/23260
Our first demonstration of an ancient balanced polymorphism segregating at a plant R-gene was important in debunking the notion that arms races govern all plant-pathogen coevolutionary dynamics. This paper also embeds an ecological model into a coalescent framework to demonstrate how ecological cycling shapes patterns of molecular evolution.