Population Genetics of Three Important Head Blight Pathogens Fusarium graminearum, F. pseudograminearum and F. culmorum

Abstract

AbstractHomothallic Fusarium graminearum (teleomorph Gibberella zeae) and anamorphic F. culmorum are destructive pathogens causing Fusarium head blight (FHB) of small‐grain cereals worldwide, while heterothallic F. pseudograminearum (G. coronicola) seems to be restricted to Australia as a FHB pathogen. In a comprehensive treatise of pathogen population genetics, this review summarizes global knowledge of genetic diversity among isolates sampled at various spatial and temporal scales, examines the mechanisms that generate this diversity and explores the implications of pathogen diversity and plasticity to resistance breeding. Despite their different modes of reproduction, there is large variation among isolates of all three species originating from different countries and continents. With a few exceptions, haplotype diversity ranges from 60 to 100% even within populations from individual fields. In F. graminearum, over 90% of the variation is found within populations, even when samples are collected from areas as small as 0.25 m2. Variation among populations is low (4–8%) with negligible population subdivision. This indicates a high level of gene flow (Nm = 8–71) with linkage equilibrium for the majority of selectively neutral molecular marker loci analysed. These findings for F. graminearum point to large random mating populations driven by occasional outcrossing, high gene flow across large geographical distances and a relatively low host‐mediated directional selection. Similar conclusions can be drawn for the Canadian population of F. pseudograminearum, but not for populations from Australia, where different pathogen ecology may have reduced the frequency of sexual recombination. Phylogenetic analyses indicate delineation of lineages in F. graminearum, often along geographically separated lines, while the related F. pseudograminearum is a single recombining species with limited or no lineage development. The anamorphic F. culmorum shows no obvious clonal structure in its population as might have been expected. High levels of diversity within fields may have been caused by balancing selection from frequent alternation between saprophytic and parasitical life cycle and/or a hidden or recently extinct teleomorph. Other mechanisms including parasexual cycles or active transposable elements may also be involved but these have not been investigated as yet. Crosses between and among F. graminearum lineages have shown a rather simple, additive inheritance of pathogenicity and aggressiveness with frequent transgressive segregation in crosses among isolates with moderate aggressiveness. This raises the spectre of highly aggressive and/or toxigenic isolates evolving if a limited range of quantitative trait locus for FHB resistance is deployed on a large scale. Combining more than one genetically distinct sources of resistance, possibly with different modes of action against the pathogen, will be necessary to avoid severe FHB outbreaks in the future.