From pathogen to endophyte: an endophytic population of Verticillium dahliae evolved from a sympatric pathogenic population.

The fungus Verticillium dahliae causes wilts of several hundred plant species, including potato and mint. Verticillium spp. also colonize sympatric hosts such as mustards and grasses as endophytes. The evolutionary history of and interactions between pathogenic and endophytic of this fungus are unknown. Verticillium dahliae isolates recovered from sympatric potato, mint, mustard and grasses were characterized genotypically with microsatellite markers and phenotypically for pathogenicity. The evolutionary history of pathogenic and endophytic populations was reconstructed and gene flow between populations quantified. Verticillium dahliae was recovered from all hosts. Endophytic populations were genetically and genotypically similar to but marginally differentiated from the potato population, from which they evolved. Bidirectional migration was detected between these populations and endophytic isolates were pathogenic to potato and behaved as endophytes in mustard and barley. Verticillium dahliae colonizes plants as both endophytes and pathogens. A historical host-range expansion together with endophytic and pathogenic capabilities are likely to have enabled infection of and gene flow between asymptomatic and symptomatic host populations despite minor differentiation. The ability of hosts to harbor asymptomatic infections and the stability of asymptomatic infections over time warrants investigation to elucidate the mechanisms involved in the maintenance of endophytism and pathogenesis.