Population genomics of Fusarium graminearum reveals signatures of divergent evolution within a major cereal pathogen

Abstract

The cereal pathogen Fusarium graminearum is the primary cause of Fusarium head blight (FHB) and a significant threat to food safety and crop production. To elucidate population structure and identify genomic targets of selection within major FHB pathogen populations in North America we sequenced the genomes of 60 diverse F. graminearum isolates. We also assembled the first pan-genome for F. graminearum to clarify population-level differences in gene content potentially contributing to pathogen diversity. Bayesian and phylogenomic analyses revealed genetic structure associated with isolates that produce the novel NX-2 mycotoxin, suggesting a North American population that has remained genetically distinct from other endemic and introduced cereal-infecting populations. Genome scans uncovered distinct signatures of selection within populations, focused in high diversity, frequently recombining regions. These patterns suggested selection for genomic divergence at the trichothecene toxin gene cluster and thirteen additional regions containing genes potentially involved in pathogen specialization. Gene content differences further distinguished populations, in that 121 genes showed population-specific patterns of conservation. Genes that differentiated populations had predicted functions related to pathogenesis, secondary metabolism and antagonistic interactions, though a subset had unique roles in temperature and light sensitivity. Our results indicated that F. graminearum populations are distinguished by dozens of genes with signatures of selection and an array of dispensable accessory genes, suggesting that FHB pathogen populations may be equipped with different traits to exploit the agroecosystem. These findings provide insights into the evolutionary processes and genomic features contributing to population divergence in plant pathogens, and highlight candidate genes for future functional studies of pathogen specialization across evolutionarily and ecologically diverse fungi.

Do black dots on wheat grains have an impact on deoxynivalenol accumulation?

“…Desjardins (2006) has showed that there exists trichothecene-nonproducing mutant of F. graminearum; however, we found that in the FDG samples DON concentrations averaged 7620 µg kg -1 . This suggests that FDG is much more dangerous due to possible higher concentrations of DON compared to BDG (Lowe et al, 2012;Kelly, Ward, 2018). In the welldried wheat grain samples with BDG, the concentrations of DON were below the limit of detection.…”

“…Cereals are a primary source of a human diet, with wheat being the third most produced grain worldwide. The cereal-infecting species Fusarium graminearum (teleomorph Gibberella zeae), F. culmorum and F. pseudograminearum produce a range of type B trichothecenes, including deoxynivalenol (DON) and its acetylated derivatives, which inhibit protein translation in eukaryotes that are known virulence factors on wheat (Kelly, Ward, 2018). Fusarium graminearum (sexual stage Gibberella zeae) is the causal agent of head blight of common wheat (Triticum aestivum L.).…”

Wheat diseases on the prairies: A Canadian story

“…Recently, a novel type A trichothecene mycotoxin (NX‐2), which is very similar in structure to 3DON, was detected in F. graminearum isolates in midwestern USA (Liang et al , ; Varga et al , ) and in southern areas of both eastern and western Canada (Kelly et al , ). These NX‐2‐producing isolates are now recognized as the NA3 population (Kelly and Ward, ). In planta, NX‐2 is converted into a deacetylated derivative, NX‐3, which has the same capacity as DON to inhibit eukaryotic protein synthesis (Varga et al , ).…”

“…The NA3 isolates are genetically distinct from NA1 and NA2, and have high genetic diversity. Their restricted existence in northern USA and southern Canada is probably due to an endemic origin of these isolates exclusively in this part of the world (Kelly and Ward, ).…”

“…These NX-2-producing isolates are now recognized as the NA3 population (Kelly and Ward, 2018). In planta, NX-2 is converted into a deacetylated derivative, NX-3, which has the same capacity as DON to inhibit eukaryotic protein synthesis (Varga et al, 2015).…”