Fusarium head blight (FHB), caused by a fungus, reduces wheat crop yield and introduces toxins into the harvest. From the assembly of the genome of Thinopyrum elongatum, a wild relative of wheat used in breeding programs to improve cultivated wheat, Wang et al. cloned a gene that can address both problems (see the Perspective by Wulff and Jones). The encoded glutathione S-transferase detoxifies the trichothecene toxin and, when expressed in wheat, confers resistance to FHB.

Structured Abstract

INTRODUCTION Fusarium head blight (FHB) is a fungal disease that devastates global wheat production, with losses of billions of dollars annually. Unlike foliar diseases, FHB occurs directly on wheat spikes (inflorescences). The infection lowers grain yield and also causes the grain to be contaminated by mycotoxins produced by the Fusarium pathogen, thus imposing health threats to humans and livestock. Although plant breeders have improved wheat resistance to FHB, the lack of wheat strains with stable FHB resistance has limited progress.

RATIONALE Many genetic loci in wheat affect FHB resistance but most only have minor effects; only a few exhibit a stable major effect on resistance. Wheat relatives in the Triticeae tribe carry resistant genes to different diseases including FHB and thus can be alternative sources of FHB resistance for wheat breeding. Thinopyrum wheatgrass has been used as a source of beneficial genes transferable to wheat by distant hybridization breeding since the 1930s. Fhb7, a gene transferred from Thinopyrum to wheat, showed a stable large effect on FHB resistance. However, the lack of a Thinopyrum reference genome hampered gene cloning and marker development, delaying the use of Fhb7 in wheat breeding. Here, we cloned Fhb7 using a reference assembly that we generated for Th. elongatum and characterized its resistance mechanisms and evolutionary history.

RESULTS Using sequence data from Th. elongatum, we assembled the Triticeae E reference genome with 44,474 high-confidence genes annotated. Using this reference, we genetically mapped Fhb7 and located it to a 245-kb genomic region. We determined a gene encoding a glutathione S-transferase (GST) as Fhb7 by virus-induced gene silencing and evaluated mutants and transgenic plants. We discovered that Fhb7 detoxifies pathogen-produced trichothecene toxins by conjugating a glutathione (GSH) unit onto the epoxide moieties of type A and B trichothecenes. Fhb7 GST homologs are absent in the plant kingdom, but one sequence showing ~97% identity with Fhb7 was found in endophytic fungi of an Epichloë species that establishes symbiosis with temperate grasses. This result suggests that Fhb7 might have been transferred from Epichloë to Th. elongatum through horizontal gene transfer. Finally, we demonstrated that Fhb7, when introgressed into diverse wheat backgrounds by distant hybridization, confers broad resistance to both FHB and crown rot without penalizing wheat yield. Our results suggest a source of Fusarium resistance for wheat improvement.