Detoxification and excretion of trichothecenes in transgenic Arabidopsis thaliana expressing Fusarium graminearum trichothecene 3-O-acetyltransferase

Authors: Hao, Guixia; McCormick, Susan; Tiley, Helene; Usgaard, Thomas

Submitted to: Toxins
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/27/2021
Publication Date: 4/29/2021
Citation: Hao, G., McCormick, S., Tiley, H., Usgaard, T. 2021. Detoxification and excretion of trichothecenes in transgenic Arabidopsis thaliana expressing Fusarium graminearum trichothecene 3-O-acetyltransferase. Toxins. 13(5). https://doi.org/10.3390/toxins13050320.
DOI: https://doi.org/10.3390/toxins13050320

Interpretive Summary: The fungal pathogen Fusarium graminearum causes Fusarium head blight (FHB), a disease of wheat and other cereal crops, and produces vomitoxin (deoxynivalenol or DON) and related mycotoxins. These toxins contaminate grain and can cause serious health problems in humans and animals. Control of FHB and mycotoxin contamination remains a challenge due to a lack of completely resistant plant varieties and emerging fungicide resistant strains. To pursue an alternate strategy to reduce FHB and mycotoxin contamination, we expressed a gene (FgTri101) that protects the fungus from its own toxin in Arabidopsis plants, and found that transgenic plants expressing this gene effectively detoxified vomitoxin and the newly identified toxin, NX-2. More importantly, we discovered the toxins were pumped out of plant cells to protect plants. Further research on plant toxin pumps will provide novel targets for reducing FHB and toxin contamination.

Technical Abstract: Fusarium graminearum, the causal agent of Fusarium head blight (FHB), produces trichothecenes including deoxynivalenol (DON), nivalenol (NIV), and 3,7,15-dihydroxy-12,13-epoxytrichothec-9-ene (NX-3). These toxins contaminate grains and cause profound health problems in humans and animals. To explore exploiting a fungal self-protection mechanism in plants, we examined the ability of F. graminearum trichothecene 3-O-acetyltransferase (FgTRI101) to detoxify several key trichothecenes produced by F. graminearum: DON, 15-ADON, NIV, and NX-3. FgTRI101 was cloned from F. graminearum and expressed in Arabidopsis plants. We compared the phytotoxic effects of purified DON, NIV, and NX-3 on the root growth of transgenic Arabidopsis expressing FgTRI101. Compared to GUS controls, FgTri101 transgenic Arabidopsis plants displayed significantly longer root length on media containing DON and NX-3. Furthermore, we confirmed that the FgTri101 transgenic plants acetylated DON to 3-ADON, 15-ADON to 3,15-diADON, and NX-3 to NX2, respectively, but did not acetylate NIV. Over 90% of the converted toxins were excreted to the media. Our study indicates that transgenic Arabidopsis expressing FgTRI101 can provide plant protection by detoxifying trichothecenes and excreting the acetylated toxins out of plant cells. Characterization of plant transporters involved in trichothecene efflux will provide novel targets to reduce FHB and mycotoxin contamination in economically important plant crops.