How transposons drive evolution of virulence in 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 aggressiveness 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. We now show that transposons are the major driving force for adaptive genome evolution in the fungal plant pathogen Verticillium dahliae. Highly variable genomic regions evolved by frequent segmental duplications mediated by erroneous homologous recombination, often utilizing transposons, leading to genetic material that is free to diverge. Intriguingly, the duplicated regions are enriched in active transposons that further 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 aggressiveness.

Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security

“…However, the few genes present in the lineage-specific regions are enriched in plant-induced genes, including genes encoding effectors and determinants of host specificity [56,57]. Faino and co-workers investigated the origin of the lineage-specific fragments using whole-genome assemblies obtained by single molecule real-time sequencing [58]. They showed that lineagespecific fragments are generated mainly by segmental genomic duplications followed by extensive sequence divergence.…”

Verticillium wilt caused by Verticillium dahliae in woody plants with emphasis on olive and shade trees

“…Subsequently, nested-PCR primers were designed and optimized for specific detection of D and ND pathotypes in planta and in soil samples (Mercado-Blanco et al 2002;Pérez-Artés et al 2005). However, although these primers have worked for several isolates tested worldwide, it was found that they do not produce the desired amplicon on all V. dahliae isolates (Collins et al 2005), which may be explained by the high genetic variability that exists among V. dahliae isolates (De Jonge et al 2012Faino et al 2015Faino et al , 2016. Arguably, genetic differences between V. dahliae isolates are underlying their behaviour as D or as ND, and the most reliable molecular marker would be a marker on the gene(s) that is (are) responsible for the differential disease phenotype.…”

Centromere evolution in the fungal genusVerticillium

“…changes in the number of chromosomes within a nucleus, and to chromosomal rearrangements (3)(4)(5). While these processes have been often associated with disease development (6), they can also provide genetic diversity that is beneficial for adaptation to novel or changing environments (7,8). For example, aneuploidy in the budding yeast Saccharomyces cerevisiae can lead to increased fitness under selective conditions, such as the presence of antifungal drugs (9,10).…”

“…However, recent advances in long-read sequencing technologies enables to study the constitution and evolution of centromeres (11,16,(29)(30)(31). By using long-read sequencing technologies in combination with optical mapping, we previously generated gapless genome assemblies of two strains of the fungal plant pathogen Verticillium dahliae (32), whose genomes are characterized by genome rearrangements and the occurrence of lineage-specific (LS) regions (7,8,(33)(34)(35)) that are hypervariable between V. dahliae strains and contain genes with roles in adaptive evolution to plant hosts (7,8,33,35).…”

“…Nine of these species are haploid, while the species Verticillium longisporum is an allodiploid hybrid between a strain that is closely related to V. dahliae and an unknown Verticillium species (37-39). During the evolution of the different Verticillium species frequent chromosomal rearrangements occurred (8,35,40).…”