Genomic variability as a driver of plant-pathogen coevolution?

Abstract

Pathogens apply one of the strongest selective pressures in plant populations. Understanding plant-pathogen coevolution has therefore been a major research focus for at least sixty years [1]. Recent comparative genomic studies have revealed that the genes involved in plant defense and pathogen virulence are among the most polymorphic in the respective genomes. Which fraction of this diversity influences the host-pathogen interaction? Do coevolutionary dynamics maintain variation? Here we review recent literature on the evolutionary and molecular processes that shape this variation, focusing primarily on gene-for-gene interactions. In summarizing theoretical and empirical studies of the processes that shape this variation in natural plant and pathogen populations, we find a disconnect between the complexity of ecological interactions involving hosts and their myriad microbes, and the models that describe them.

Figure 1

Evaluating the allele frequency spectrum to assess evidence of selection on a locus. Balanced polymorphisms can be distinguished by the (excess) intermediate frequency SNPs that arise on the deepest branches (a) of a genealogy. In this example, because of the long branches, the genealogy on the right is expected to have a higher number of intermediate frequency SNPs than the tree on the left. These common SNPs will tilt Tajima’s D (b), a commonly used test of selection, towards positive values, which are consistent with balancing selection (or complex population structure) and can be distinguished from neutrality using permutations or an outlier approach.

Figure 2

Processes that maintain variation in plant genotypes. This figure presents the hypothetical expected allele frequency, and genomic signatures (outlier statistics) resulting from three distinct selective scenarios capable of maintaining diversity at a resistance locus. Only scenarios (a) and (c) are classically considered scenarios of balancing of selection. Most studies to date have been unable to distinguish between scenarios (a) and (b) in molecular evolution analyses.