Enhanced resistance to Fusarium graminearum in transgenic Arabidopsis plants expressing a modified plant thionin

Authors: Hao, Guixia; Bakker, Matthew; Kim, Hye-Seon

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/4/2020
Publication Date: 3/17/2020
Citation: Hao, G., Bakker, M.G., Kim, H.-S. 2020. Enhanced resistance to Fusarium graminearum in transgenic Arabidopsis plants expressing a modified plant thionin. Phytopathology. 110(5):1056-1066. https://doi.org/10.1094/PHYTO-12-19-0447-R.
DOI: https://doi.org/10.1094/PHYTO-12-19-0447-R

Interpretive Summary: Fusarium head blight (FHB) is a devastating disease of wheat and other cereal crops. FHB results in grain yield loss and contaminates grain with mycotoxins (toxic chemicals produced by fungi) that are a top safety concern for humans and animals. The development of FHB resistant cultivars is the most effective and economical method to control FHB and reduce exposure to mycotoxins. However, natural genetic resistance to FHB is lacking among wheat varieties. Thus, it may be useful to introduce new sources of resistance into wheat by transgenic technology. A first step toward this goal is to identify novel genetic traits that could be used to enhance FHB resistance. This work is more easily done in a model plant species, such as Arabidopsis. Arabidopsis interacts with Fusarium in a manner that is similar to wheat-Fusarium interactions, while growing more quickly and allowing for easier transformation. In this study, we inserted a transgene enabling production of a modified defensive thionin protein (Mthionin) into Arabidopsis. This Mthionin protein has been previously shown to effectively inhibit several bacterial diseases in other crops. We showed that addition of the Mthionin gene reduced the growth of Fusarium on Arabidopsis and slowed the development of disease. To test for broader effects of Mthionin, we also examined bacterial and fungal populations on transgenic plants expressing the Mthionin. Addition of the Mthionin gene did not affect the overall distribution and diversity of the microbiome associated with plants. These data suggest that the defensive protein Mthionin is a promising candidate for introduction to wheat, to reduce Fusarium head blight and mycotoxin contamination.

Technical Abstract: The fungal pathogen Fusarium graminearum causes Fusarium head blight (FHB) on wheat, barley, and other grains. FHB results in yield reductions and contaminates grain with trichothecene mycotoxins, which threaten food safety and food security. Innovative mechanisms for controlling FHB are urgently needed. We have previously shown that transgenic tobacco and citrus plants expressing a modified thionin (Mthionin) exhibited enhanced resistance toward several bacterial pathogens. The aim of this study was to investigate whether overexpression of Mthionin could be similarly efficacious against F. graminearum, and whether transgenic expression of Mthionin impacts the plant microbiome. Transgenic Arabidopsis plants expressing Mthionin were generated and confirmed. When challenged with F. graminearum, Mthionin-expressing plants showed less disease and fungal biomass in both leaves and inflorescences compared with control plants. When infiltrated into leaves, macroconidia of F. graminearum germinated at lower rates and produced less hyphal growth in Arabidopsis leaves expressing Mthionin. Moreover, marker genes related to defense signaling pathways were expressed at significantly higher levels after F. graminearum infection in Mthionin transgenic Arabidopsis plants. However, Mthionin expression did not appreciably alter the overall microbiome associated with transgenic plants grown under controlled conditions; across leaves and roots of Mthionin-expressing and control transgenic plants, only a few bacterial and fungal taxa differed, and differences between Mthionin transformants were of similar magnitude compared with control plants. In sum, our data indicate that Mthionin is a promising candidate to produce transgenic crops for reducing FHB severity and ultimately mycotoxin contamination.