A distinct and genetically diverse lineage of the hybrid fungal pathogen Verticillium longisporum population causes stem striping in British oilseed rape.

Jasper R L Depotter,Bart P H J Thomma,Thomas A Wood,Michael F Seidl,Grardy C M Van Den Berg

doi:10.1111/1462-2920.13801

Jasper R L Depotter, Bart P H J Thomma + Show 3 more

Open Access

https://doi.org/10.1111/1462-2920.13801

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Abstract

Population genetic structures illustrate evolutionary trajectories of organisms adapting to differential environmental conditions. Verticillium stem striping disease on oilseed rape was mainly observed in continental Europe, but has recently emerged in the United Kingdom. The disease is caused by the hybrid fungal species Verticillium longisporum that originates from at least three separate hybridization events, yet hybrids between Verticillium progenitor species A1 and D1 are mainly responsible for Verticillium stem striping. 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. Genome comparison between representatives of the A1/D1 West and East clusters excluded population distinctiveness through separate hybridization events. Remarkably, the A1/D1 West population that is genetically more diverse than the entire A1/D1 East cluster caused the sudden emergence of Verticillium stem striping in the UK, whereas in continental Europe Verticillium stem striping is predominantly caused by the more genetically uniform A1/D1 East population. The observed genetic diversity of the A1/D1 West population argues against a recent introduction of the pathogen into the UK, but rather suggests that the pathogen previously established in the UK and remained latent or unnoticed as oilseed rape pathogen until recently.

Highlights

Interspecific hybridization, the natural or induced combination of two genetically divergent parents, is pervasive among many different eukarotic taxa such as plants, insects, birds, mammals and fungi (Brasier 2000; Mallet 2005)
Genome hybridisation can be a major driver for organismal adaptation and has allowed V. dahliae that infect brassicaceous species relatively infrequently, to become pathogenic on these hosts as V. longisporum (Depotter et al 2016a)
V. longisporum has been subdivided into three lineages: A1/D1, A1/D2 and A1/D3, each representing a separate hybridization event between two Verticillium species (Inderbitzin et al 2011b)

Summary

Introduction

Interspecific hybridization, the natural or induced combination of two genetically divergent parents, is pervasive among many different eukarotic taxa such as plants, insects, birds, mammals and fungi (Brasier 2000; Mallet 2005). Hybrids that receive a genome copy of both parents initially double their chromosome number, and experience a so-called “genome shock” that incites major genomic reorganizations that can manifest by genome rearrangements, extensive gene loss, transposon activation, or alterations in gene expression (Doyle et al 2008) Due to this increased genome plasticity, hybridization can promote the emergence of altered phenotypes that allow adaptation to novel niches or to changing environments. At least two recent hybridization events between the well-known brewing yeast Saccharomyces cerevisiae and its close relative Saccharomyces eubayanus gave rise to Saccharomyces pastorianus, a lineage with high cold tolerance and good maltose/maltotriose utilization capabilities (Gibson & Liti 2015) Both characteristics are exploited in the production of the popular lager beer that is generated from malted barley at very low temperatures. Interspecific hybridization is a potent driver for the evolution of fungal plant pathogens as increased genome plasticity promoted by an hybridization event allows hybrids to differentiate and acquire new pathogenic traits (Depotter et al 2016b)

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