Population genomics demystifies the defoliation phenotype in the plant pathogen Verticillium dahliae.

Verticillium dahliae is a broad host-range pathogen that causes vascular wilts in plants. Interactions between three hosts and specific V. dahliae genotypes result in severe defoliation. The underlying mechanisms of defoliation are unresolved. Genome resequencing, gene deletion and complementation, gene expression analysis, sequence divergence, defoliating phenotype identification, virulence analysis and quantification of V. dahliae secondary metabolites were performed. Population genomics previously revealed that G-LSR2 was horizontally transferred from the fungus Fusarium oxysporum f. sp. vasinfectum to V. dahliae and is exclusively found in the genomes of defoliating (D) strains. Seven gene deletion mutants within G-LSR2, designated as VdDfs, produced a nondefoliating phenotype on cotton, olive, and okra. Genes VdDf5 and VdDf6 associated with defoliation shared homology with polyketide synthases involved in secondary metabolism, while VdDf7 shared homology with proteins involved in the biosynthesis of N-lauroylethanolamine (NAE 12:0), a compound that induces defoliation. NAE over-biosynthesis by D strains also appears to disrupt NAE metabolism in cotton by inducing overexpression of fatty acid amide hydrolase. The VdDfs modulate the synthesis and over-production of secondary metabolites such as NAE 12:0 that causes defoliation either by altering abscisic acid (ABA) sensitivity, hormone disruption, or sensitivity to the pathogen. This article is protected by copyright. All rights reserved.