Role of Trichoderma arundinaceum tri10 in regulation of terpene biosynthetic genes and in control of metabolic flux

Authors: LINDO, LAURA - University Of Leon; McCormick, Susan; CARDOZA, ROSA - University Of Leon; Brown, Daren; ALEXANDER, NANCY - Retired ARS Employee; Proctor, Robert; GUTIERREZ, SANTIAGO - University Of Leon; Kim, Hye-Seon

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/7/2018
Publication Date: 11/12/2018
Citation: Lindo, L., McCormick, S.P., Cardoza, R.E., Kim, H.-S., Brown, D.W., Alexander, N.J., Proctor, R.H., Gutierrez, S. 2018. Role of Trichoderma arundinaceum tri10 in regulation of terpene biosynthetic genes and in control of metabolic flux. Applied and Environmental Microbiology. 122:31-46. https://doi.org/10.1016/j.fgb.2018.11.001.
DOI: https://doi.org/10.1016/j.fgb.2018.11.001

Interpretive Summary: Trichothecenes are toxins produced by multiple species of fungi. Some trichothecenes have a negative impact on humans because they can accumulate in fungus-infected crops where they pose health risks to humans and domestic animals. In contrast, other trichothecenes have a potential positive impact on humans by contributing to the ability of species of the fungus Trichoderma to control plant diseases. For example, production of the trichothecene harzianum A by the fungus Trichoderma arundinaceum contributes to its ability to inhibit other fungi that cause plant diseases. Previous research indicates that the gene tri10 controls expression of genes required for trichothecene production in the plant pathogenic fungus Fusarium. In the current study, we discovered that tri10 also controls expression of trichothecene production genes in T. arundinaceum. Inactivation of tri10 in T. arundinaceum caused a marked reduction in trichothecene production and, in contrast, an increase in production of ergosterol, which is an essential component of fungal membranes. Knowledge of the genetics of how fungi control production of trichothecenes and other metabolites should aid in the design of safe and effective biocontrol organisms to combat crop diseases caused by fungi.

Technical Abstract: Production of trichothecene toxins occurs in phylogenetically diverse fungi with different lifestyles. In these fungi, most homologs of the trichothecene biosynthetic gene cluster include the transcription factor genes tri6 and tri10. Analyses of phytopathogenic species of Fusarium indicate that the TRI6 and TRI10 proteins positively regulate genes required for synthesis of trichothecenes as well as farnesyl diphosphate (FPP), a precursor of the trichothecene and other terpenoids (e.g., ergosterol). However, the apparent absence of tri6 and tri10 in some trichothecene-producing fungi, and the presence of multiple paralogs of the genes in others suggest considerable variability in genetic regulation of trichothecene biosynthesis. To begin to investigate this variability, we functionally characterized tri10 in the saprotrophic fungus Trichoderma arundinaceum. We found that TRI10 is required for wild-type expression of tri genes and trichothecene production during the first 12 h of growth of T. arundinaceum. Comparison of the effect of tri10 deletion in T. arundinaceum and Fusarium species has provided evidence for similarities in the genetic regulation of trichothecene biosynthesis in these two fungi with different lifestyles. In contrast to trichothecenes, tri10 deletion increased production of ergosterol and the polyketidederived metabolites aspinolides, which is more likely caused by an increase in the intracellular pool of FPP resulting from loss of trichothecene production. Furthermore, although it is unclear how TRI10 affects polyketide production, one possibility is that it does so by rechanneling terpene precursors.