Fusarium graminearum effector FgNls1 targets plant nuclei to induce wheat head blight

Authors: Hao, Guixia; Naumann, Todd; CHEN, HUI - Kansas State University; BAI, GUIHUA - University Of Leon; McCormick, Susan; Kim, Hye-Seon; TIAN, BIN - Kansas State University; TRICK, HAROLD - Kansas State University; NALDRETT, MICHAEL - University Of Nebraska; Proctor, Robert

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/24/2023
Publication Date: 9/11/2023
Citation: Hao, G., Naumann, T.A., Chen, H., Bai, G., McCormick, S., Kim, H.-S., Tian, B., Trick, H.N., Naldrett, M.J., Proctor, R. 2023. Fusarium graminearum effector FgNls1 targets plant nuclei to induce wheat head blight. Molecular Plant-Microbe Interactions. https://doi.org/10.1094/MPMI-12-22-0254-R.
DOI: https://doi.org/10.1094/MPMI-12-22-0254-R

Interpretive Summary: The fungus Fusarium graminearum causes Fusarium head blight (FHB). FHB is one of the most devastating diseases of wheat and other cereals and leads to great economic loss. In addition to causing loss in yield, the fungus contaminates grain with vomitoxin, a mycotoxin that is a serious threat to food safety and animal health. To reduce the incidence of FHB and mycotoxin contamination of grain, we need to understand how Fusarium interacts with plants and overcomes plant defenses. In this study, the ARS scientists in Peoria, IL, and Manhattan, KS, in collaboration with scientists at Kansas State University and the University of Nebraska, discovered a Fusarium protein (FgN1s1) that plays an important role in FHB development in wheat. FgNls1 binds to a wheat histone protein in the plant nucleus to suppress plant immunity. They found that transgenic wheat plants that silence the FgNls1 gene have reduced FHB. This study improves our understanding of how the fungus and plant interact during infection and provides a new target to control FHB by RNA interference biotechnology.

Technical Abstract: Fusarium head blight (FHB) caused by Fusarium graminearum is one of the most devastating diseases of wheat and barley worldwide. Effectors suppress host immunity and promote disease development. The genome of F. graminearum contains hundreds of effectors with unknown function. Therefore, investigations of the functions of these effectors will facilitate developing novel strategies to enhance wheat resistance to FHB. We characterized a F. graminearum effector, FgNls1, containing a signal peptide and multiple eukaryotic nuclear localization signals (NLS). A fusion protein of GFP and FgNls1 was accumulated in the plant nucleus when transiently expressed in Nicotiana benthamiana. FgNls1 suppressed Bax-induced cell death when co-expressed in N. benthamiana. Expression of FgNLS1 was induced in wheat spikes infected with F. graminearum. The Fgnls1 mutants significantly reduced initial infection and FHB spread within a spike. The function of FgNLS1 was restored in the Fgnls1-complemented strains. Wheat histone 2B was identified as an interacting protein by FgNls1-affinity chromatography. Transgenic wheat plants that silence FgNLS1 expression had significantly lower FHB severity than control plants. This study demonstrates a critical role of FgNls1 in F. graminearum pathogenesis and indicates that host-induced gene silencing targeting F. graminearum effectors is a promising approach to enhance FHB resistance.