Gain and loss of a transcription factor that regulates late trichothecene biosynthetic pathway genes in Fusarium

Authors: Brown, Daren; VILLANI, ALESSANDRA - National Research Council - Italy; SUSCA, ANTONIA - National Research Council - Italy; MORETTI, ANTONIO - National Research Council - Italy; Kim, Hye-Seon; Proctor, Robert; McCormick, Susan; Hao, Guixia

Submitted to: Fungal Genetics and Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/4/2019
Publication Date: 12/11/2019
Citation: Brown, D.W., Villani, A., Susca, A., Moretti,A., Hao, G., Kim, H.-S., Proctor, R.H., McCormick, S.P., 2019. Gain and loss of a transcription factor that regulates late trichothecene biosynthetic pathway genes in Fusarium. Fungal Genetics and Biology. 136:103317. https://doi.org/10.1016/j.fgb.2019.103317.
DOI: https://doi.org/10.1016/j.fgb.2019.103317

Interpretive Summary: Many species of the fungus Fusarium are of concern to agriculture because they cause economically important diseases of cereal crops such as barley, corn and wheat. The diseases not only reduce the yield and quality of the crops, but they can also leave crops contaminated with toxins (mycotoxins) that pose health risks to humans, pets, and livestock animals. Trichothecenes are a type of mycotoxin produced by two genetically distinct groups of species of Fusarium; one group is known as the F. sambucinum species complex (FSAMSC) and other is known as the F. incarnatum-equiseti species complex (FIESC). Previous studies have demonstrated that a Fusarium gene known as TRI6 regulates (i.e., turns on) trichothecene production in FSAMSC, such that the absence of TRI6 stops trichothecene production. In the current study, we demonstrate that TRI6 regulates trichothecene production in FIESC in the same way. We also demonstrate that another Fusarium gene, TRI21, regulates production of some but not all trichothecenes in FIESC. TRI21 is not present in species of FSAMSC and, therefore, its absence does not stop trichothecene production. These research results indicate that even though genetic regulation of trichothecene production differs in FSAMSC and FIESC, control strategies that target TRI6 should be effective at reducing production in both groups of Fusarium. This research will be of use to plant pathologists, plant breeders, and other scientists involved in the development of control strategies aimed at reducing crop diseases and mycotoxin contamination problems caused by Fusarium. The research will also benefit academic, government, and private-sector organizations that assess the risks that Fusarium species pose to human and animal health.

Technical Abstract: Trichothecenes are among the mycotoxins of most concern to food and feed safety and are produced by species in two lineages of Fusarium: the F. incarnatum-equiseti (FIESC) and F. sambucinum (FSAMSC) species complexes. Previous functional analyses of the trichothecene biosynthetic gene (TRI) cluster in members of FSAMSC indicate that the transcription factor gene TRI6 activates expression of other TRI cluster genes. In addition, previous sequence analyses indicate that the FIESC TRI cluster includes TRI6 and another uncharacterized transcription factor gene (hereafter TRI21) that was not reported in FSAMSC. Here, gene deletion analysis indicated that in FIESC TRI6 functions in a manner similar to FSAMSC, whereas TRI21 activated expression of some genes that function late in the trichothecene biosynthetic pathway but not early-pathway genes. Consistent with this finding, TRI21 was required for formation of diacetoxyscripenol, a late-trichothecene-pathway product, but not for isotrichodermin, an early-pathway product. Although intact homologs of TRI21 were not detected in FSAMSC or other trichothecene-producing fungal genera, TRI21 fragments were detected in some FSAMSC species. This suggests that the gene was acquired by Fusarium after divergence from other trichothecene-producing fungi, was subsequently lost in FSAMSC, but was retained in FIESC. Together, our results indicate fundamental differences in regulation of trichothecene biosynthesis in FIESC and FSAMSC.