UDP-glucosyltransferase HvUGT13248 confers type II resistance to Fusarium graminearum in barley

Authors: BETHKE, GERIT - University Of Minnesota; HUANG, YADONG - University Of Minnesota; HENSEL, GOETZ - Leibniz Institute Of Plant Genetics And Crop Plant Research; HEINEN, SHANE - University Of Minnesota; LIU, CHAOCHIH - University Of Minnesota; WYANT, SKYLAR - University Of Minnesota; LI, XIN - University Of Minnesota; QUIN, MAUREEN - University Of Minnesota; McCormick, Susan; MORRELL, PETER - University Of Minnesota; DONG, YANHONG - University Of Minnesota; KUMLEHN, JOCHEN - Leibniz Institute Of Plant Genetics And Crop Plant Research; SALVI, SILVIO - University Of Bologna; BERTHILLER, FRANZ - University Of Natural Resources And Life Sciences, Vienna; MUEHLBAUER, GARY - University Of Minnesota

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/1/2023
Publication Date: 8/23/2023
Citation: Bethke, G., Huang, Y., Hensel, G., Heinen, S., Liu, C., Wyant, S.R., Li, X., Quin, M.B., McCormick, S.P., Morrell, P.L., Dong, Y., Kumlehn, J., Salvi, S., Berthiller, F., Muehlbauer, G.J. 2023. UDP-glucosyltransferase HvUGT13248 confers type II resistance to Fusarium graminearum in barley. Plant Physiology. https://doi.org/10.1093/plphys/kiad467.
DOI: https://doi.org/10.1093/plphys/kiad467

Interpretive Summary: Fusarium head blight is a disease of cereal crops that can cause serious losses in yield and grain quality due to contamination with toxins such as vomitoxin. Vomitoxin is harmful to animals as well as plants. In wheat, vomitoxin helps the fungus spread throughout the wheat head, but barley is protected against this type of disease spread. Previous work identified a barley enzyme that converts vomitoxin to a less toxic compound. In collaboration with an ARS researcher in Peoria, Illinois, researchers at the University of Minnesota looked at the gene for the barley detoxification enzyme in 500 varieties of barley and found two varieties with mutations that changed the enzyme and limited the conversion of vomitoxin to the less toxic compound. In field studies the two barley varieties with mutant enzymes had increased disease spread. This confirmed that this enzyme is responsible for barley resistance to disease spread. Ensuring that the gene that produces this enzyme is intact in barley varieties will help breeders screen for resistance. Additionally, introducing or increasing the effectiveness of this enzyme in other plants will also increase their resistance to Fusarium head blight.

Technical Abstract: Fusarium head blight (FHB) of barley (Hordeum vulgare) predominantly caused by the fungal pathogen F. graminearum leads to yield losses and reduction in grain quality due to the accumulation of trichothecene mycotoxins (e.g., deoxynivalenol, DON). Glucosylation of DON to the nontoxic DON-3-O-glucoside (D3G) is catalyzed by UDP-glucosyltransferases (UGTs). Barley UGT13248, was previously shown to convert DON to D3G in yeast, Arabidopsis and wheat. Here we explored natural diversity of UGT13248 in over 500 barley accessions. No genotypes with mutations that substantially increase seedling sensitivity to DON were identified, suggesting that all barley accessions tested carried functional alleles of UGT13248. In a TILLING population, we identified two lines with mutations (T368I and H369Y) that, based on protein modeling, likely affect UDP-glucose binding of UGT13248. Roots of these plants showed increased sensitivity to DON and DON to D3G conversion was strongly reduced in spikes compared to controls. Plants overexpressing UGT13248 showed increased resistance to DON and increased conversion of DON to D3G. This shows that UGT13248 converts DON to D3G in barley. Field experiments showed increased FHB disease severity and reduced D3G production in plants carrying the T368I and H369Y mutations. Barley is generally considered to have type II resistance that limits the spread of F. graminearum from one infected spikelet to adjacent spikelets. Point inoculation experiments with F. graminearum showed increased spread of infection in T368I and H369Y across the spike compared to wild-type, while overexpression plants showed decreased spread of FHB symptoms. Confocal microscopy revealed that F. graminearum spread to distant rachis nodes in T368I and H369Y but not wild-type Morex plants. Taken together, UGT13248 confers type II resistance to FHB in barley.