Research Article

Horizontal gene transfer of Fhb7 from fungus underlies Fusarium head blight resistance in wheat

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Science  22 May 2020:
Vol. 368, Issue 6493, eaba5435
DOI: 10.1126/science.aba5435

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Fungal disease meets its match

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.

Science, this issue p. eaba5435; see also p. 822

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.

CONCLUSION

Th. elongatum carries biotic and abiotic resistance genes and is a useful resource for wheat breeding. The assembled Th. elongatum reference genome can aid identification and cloning of such genes for wheat improvement. Cloning of Fhb7 revealed that it encodes a GST that can detoxify trichothecene toxins. Thus, Fhb7 resistance differs from Fhb1 resistance, which depends on a reduction of pathogen growth in spikes, although both confer durable resistance. The ability of Fhb7 to detoxify multiple mycotoxins produced by various Fusarium species demonstrates its potential as a source of resistance to the various diseases for which Fusarium trichothecenes are virulence factors. The deployment of Fhb7 in commercial wheat cultivars could alleviate both the food safety issue for consumers and the yield loss problem for growers. Sequence homologies between fungal and plant Fhb7 suggested that horizontal gene transfer may help to shape plant genomes.

Fhb7 confers FHB resistance by detoxifying trichothecenes.

(A) Fhb7 in Th. elongatum genome likely came from an Epichloë fungus through horizontal gene transfer. Fhb7 drives FHB resistance when introgressed from Thinopyrum into wheat. (B) Fhb7 encodes a GST that detoxifies Fusarium-produced trichothecenes by conjugating GSH (blue) to the epoxy group (red). R1 to R5 refer to the variable groups in trichothecenes.

Abstract

Fusarium head blight (FHB), a fungal disease caused by Fusarium species that produce food toxins, currently devastates wheat production worldwide, yet few resistance resources have been discovered in wheat germplasm. Here, we cloned the FHB resistance gene Fhb7 by assembling the genome of Thinopyrum elongatum, a species used in wheat distant hybridization breeding. Fhb7 encodes a glutathione S-transferase (GST) and confers broad resistance to Fusarium species by detoxifying trichothecenes through de-epoxidation. Fhb7 GST homologs are absent in plants, and our evidence supports that Th. elongatum has gained Fhb7 through horizontal gene transfer (HGT) from an endophytic Epichloë species. Fhb7 introgressions in wheat confers resistance to both FHB and crown rot in diverse wheat backgrounds without yield penalty, providing a solution for Fusarium resistance breeding.

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