Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen

Abstract

Genomic plasticity enables adaptation to changing environments, which is especially relevant for pathogens that engage in "arms races" with their hosts. In many pathogens, genes mediating virulence cluster in highly variable, transposon-rich, physically distinct genomic compartments. However, understanding of the evolution of these compartments, and the role of transposons therein, remains limited. Here, we show that transposons are the major driving force for adaptive genome evolution in the fungal plant pathogen Verticillium dahliae. We show that highly variable lineage-specific (LS) regions evolved by genomic rearrangements that are mediated by erroneous double-strand repair, often utilizing transposons. We furthermore show that recent genetic duplications are enhanced in LS regions, against an older episode of duplication events. Finally, LS regions are enriched in active transposons, which contribute to local genome plasticity. Thus, we provide evidence for genome shaping by transposons, both in an active and passive manner, which impacts the evolution of pathogen virulence.

The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat

“…In many fungal genomes, genes involved in virulence show a pattern of presence/absence polymorphism among populations (22, 55–57). In the case of disease outbreaks caused by singular clones, focusing genomic analyses on the causal pathogen lineage is appropriate.…”

“…A key question to address is how orphan regions arise in genomes and are maintained over evolutionary time. The role played by transposable elements will provide important clues to explain the emergence of genome compartmentalization (22). …”

“…A key step in the evolution of genome compartmentalization was shown to be the emergence of structural variation driven by transposable elements (20, 22). However, the emergence of compartmentalization through chromosomal rearrangements was until now only found among asexual lineages.…”

A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch

“…In addition, transposable elements contribute to variability by favouring nonhomologous recombination or through repeat‐induced point mutations (RIPs) (Möller & Stukenbrock, 2017; Seidl & Thomma, 2017). Pathogens carrying these highly plastic genome regions are thought to benefit from an increased versatility to adapt to different conditions or to an evolving host (Dong et al ., 2015; Faino et al ., 2016). …”

Durum wheat and septoria tritici blotch: genes and prospects for breeding

“…The highly polymorphic region comprising AvrStb6 fits the "two-speed genome" hypothesis (Faino et al 2016) involved in rapid evolution to overcome the Stb6 gene (Zhong et al 2017). Expression profiling of the identified effector suggests that it is operating during the latent phase of the infection, which suggests an important role during the switch from the biotrophic phase to the necrotrophic phase of pathogenesis.…”