Infectious disease is a major causal factor in the demography of human, plant and animal populations. There have been increasing calls for integrating ecological and evolutionary processes into disease management. This proposal is novel in that it combines molecular work characterizing interactions between host resistance [R] and pathogen avirulence [Avr] genes in the cultivated flax/flax rust system with extensive knowledge of a closely related wild host-pathogen system to specifically investigate the coevolution of pathogen virulence and host resistance. Population studies will focus on factors that influence among-population variation in pathogen virulence (e.g. potential for sexual recombination, short-term selection in response to population variation in host resistance). This will be combined with work examining population and regional variation in the genetic basis of host resistance, and it's epidemiological and evolutionary consequences with regard to maintenance of pathogen diversity. Detailed molecular studies (using well-developed techniques) will investigate how sequence divergence in Avr/R genes that leads to altered recognition properties affects phenotypic responses (host susceptibility vs. resistance), and how recognition is mediated. Studies at the molecular and population levels will be further integrated through work specifically aimed at characterizing phenotypic and sequence variation in one family of Avr/R genes in wild flax populations and exploring its coevolutionary implications. Together with complementary modeling work, (using extensions of previously developed spatially explicit simulations), these studies will characterize the evolutionary balance between host resistance and pathogen virulence in a natural system, and how this in turn determines patterns of disease incidence and prevalence. Relevance: There are clear epidemiological and structural similarities between plant resistance and animal innate immune systems, and similar patterns of gene diversification and selection are observed in animal MHC and plant resistance genes. Previous studies have also shown that the virulence mechanisms of pathogenic bacteria are functionally similar between plant and animal hosts, making it possible to utilize plant hosts as models for identifying virulence factors relevant to disease pathogenesis in animals and humans (Rahme et al. 2000). The experimental tractability of the Linum-Melampsora system, and the detailed molecular knowledge available, means that this project has the potential to provide major advances in our understanding of the role of genetic variation in disease, especially with respect to: (i) pathogen and host adaptation and coevolution at local and regional spatial scales;and (ii) the maintenance of genetic polymorphisms at host resistance and pathogen avirulence loci. These questions have broad relevance for understanding patterns of variation in host genes involved in pathogen recognition, as well as in the pathogen genes that are their targets.

National Institute of Health (NIH)
National Institute of General Medical Sciences (NIGMS)
Research Project (R01)
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Genetic Variation and Evolution Study Section (GVE)
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Eckstrand, Irene A
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Commonwealth Scientific & Indust Research Org
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Tack, Ayco J M; Laine, Anna-Liisa; Burdon, Jeremy J et al. (2015) Below-ground abiotic and biotic heterogeneity shapes above-ground infection outcomes and spatial divergence in a host-parasite interaction. New Phytol 207:1159-69
Laine, Anna-Liisa; Burdon, Jeremy J; Nemri, Adnane et al. (2014) Host ecotype generates evolutionary and epidemiological divergence across a pathogen metapopulation. Proc Biol Sci 281:
Burdon, J J; Thrall, P H; Ericson, L (2013) Genes, communities & invasive species: understanding the ecological and evolutionary dynamics of host-pathogen interactions. Curr Opin Plant Biol 16:400-5
Thrall, Peter H; Laine, Anna-Liisa; Ravensdale, Michael et al. (2012) Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation. Ecol Lett 15:425-35
Poisot, Timothée; Thrall, Peter H; Hochberg, Michael E (2012) Trophic network structure emerges through antagonistic coevolution in temporally varying environments. Proc Biol Sci 279:299-308
Tack, A J M; Thrall, P H; Barrett, L G et al. (2012) Variation in infectivity and aggressiveness in space and time in wild host-pathogen systems: causes and consequences. J Evol Biol 25:1918-36
Ravensdale, Michael; Bernoux, Maud; Ve, Thomas et al. (2012) Intramolecular interaction influences binding of the Flax L5 and L6 resistance proteins to their AvrL567 ligands. PLoS Pathog 8:e1003004
Laine, Anna-Liisa; Burdon, Jeremy J; Dodds, Peter N et al. (2011) Spatial variation in disease resistance: from molecules to metapopulations. J Ecol 99:96-112
Antonovics, Janis; Thrall, Peter H; Burdon, Jeremy J et al. (2011) Partial resistance in the Linum-Melampsora host-pathogen system: does partial resistance make the red queen run slower? Evolution 65:512-22
Bernoux, Maud; Ellis, Jeffrey G; Dodds, Peter N (2011) New insights in plant immunity signaling activation. Curr Opin Plant Biol 14:512-8

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