Genome evolution in fungal plant pathogens: looking beyond the two-speed genome model

Abstract

The interaction of pathogens with their hosts creates strong reciprocal selection pressures. Pathogens often deploy an arsenal of small proteins called effectors that manipulate the plant immune system and promote disease. In the post-genomics era, a major interest has been to understand what shapes the localization of effector genes in pathogen genomes. The two-speed genome model originated with the discovery of repeat-rich and gene-sparse genome compartments with an over-representation of effector-like genes in a subset of plant pathogens. These highly polymorphic genome compartments are thought to create unique niches for effector genes and facilitate rapid adaptation. Research over the past decade has revealed a number of twists to the two-speed genome model and raised questions about the universality among plant pathogens. Here, we critically review the foundations of the two-speed model by presenting recent work on epigenetics, transposable element dynamics, and population genetics. Numerous examples have demonstrated that the location of effector genes in rapidly evolving compartments has created key adaptations. However, recent evidence suggests that the two-speed genome is unlikely to have evolved to specifically benefit the plant pathogen lifestyle. We propose that fundamental drivers of eukaryotic genome evolution have shaped both pathogen and non-pathogen genomes alike. An evolutionary genomics perspective on the two-speed genome model will open up fruitful new research avenues.