Allopolyploidization, genome duplication through interspecific hybridization, is an important evolutionary mechanism that can enable organisms to adapt to environmental changes or stresses. This increased adaptive potential of allopolyploids can be particularly relevant for plant pathogens in their quest for host immune response evasion. Allodiploidization likely caused the shift in host range of the fungal pathogen plant Verticillium longisporum, as V. longisporum mainly infects Brassicaceae plants in contrast to haploid Verticillium spp. In this study, we investigated the allodiploid genome structure of V. longisporum and its evolution in the hybridization aftermath. The nuclear genome of V. longisporum displays a mosaic structure, as numerous contigs consists of sections of both parental origins. V. longisporum encountered extensive genome rearrangements, whereas the contribution of gene conversion is negligible. Thus, the mosaic genome structure mainly resulted from genomic rearrangements between parental chromosome sets. Furthermore, a mosaic structure was also found in the mitochondrial genome, demonstrating its bi-parental inheritance. In conclusion, the nuclear and mitochondrial genomes of V. longisporum parents interacted dynamically in the hybridization aftermath. Conceivably, novel combinations of DNA sequence of different parental origin facilitated genome stability after hybridization and consecutive niche adaptation of V. longisporum.

Population genetic structures illustrate evolutionary trajectories of organisms adapting to differential environmental conditions. Pathogen populations are typically shaped by coevolution with their hosts through genetic co-structuring. Verticillium stem striping was mainly observed in continental Europe, but has recently emerged in other countries including the United Kingdom. The disease is caused by the hybrid fungal species Verticillium longisporum that originates from at least three separate hybridization events, yet strains from the hybridization event between Verticillium progenitor species A1 and D1 are mainly responsible for Verticillium stem striping. By using multi-locus genotype analysis, we reveal a hitherto un-described dichotomy within V. longisporum lineage A1/D1 that correlates with the geographic distribution of the isolates with an "A1/D1 West" and an "A1/D1 East" cluster according to their relative location in Europe. Genome comparison between representatives of the A1/D1 West and East clusters confirmed mutual common origin, excluding distinctiveness through separate hybridization events. The A1/D1 West population is responsible for the sudden emergence of Verticillium stem striping in the UK. Remarkably, this emergence is caused by a British V. longisporum population that is genetically more diverse than the entire A1/D1 East cluster. Conceivably, V. longisporum has previously established in the UK, but remained latent or undiagnosed as an oilseed rape pathogen until recently. This finding illustrates that a recent introduction is not a prerequisite for a pathogen to emerge, as environmental factors and cultural practices can also play a pivotal role in outbreaks of novel diseases.

The Verticillium genus comprises economically important plant pathogens that collectively affect a broad range of annual and perennial crops. Verticillium longisporum mainly infects brassicaceous hosts, including oilseed rape. The most conspicuous symptom of V. longisporum infection on oilseed rape is black stem striping that appears towards the end of the cropping season. Thus far, the impact of V. longisporum infection on oilseed yield remains unclear. Verticillium stem striping recently emerged as a new disease in UK and currently displays a widespread occurrence in England. In this study, we assessed the impact of Verticillium stem striping on British oilseed rape production. To this end, four cultivars (Incentive, Vision, Harper and Quartz) were grown in field plots with different levels of V.longisporum disease pressure at different locations over two consecutive years. WhereasIncentive and Vision developed relatively few stem striping symptoms, Harper and especially Quartz showed severe symptoms during these field experiments. Furthermore, higher inoculum levels induced more severe symptoms in these cultivars. Intriguingly, significant yield reductions upon V. longisporum infection only occurred in a single field trial on all tested oilseed rape cultivars. Thus we conclude that Verticillium stem striping does not consistently impact oilseed rape yield, despite the occurrence of abundant disease symptoms.