Distribution, function, and evolution of a gene essential for trichothecene toxin biosynthesis in Trichoderma

Authors: GUTTIERREZ, SANTIAGO - University Of Leon; McCormick, Susan; CARDOZA, ROSA - University Of Leon; Kim, Hye-Seon; YUGUEROS, LAURA - University Of Leon; Vaughan, Martha; CARRO-HUERGA, GUZMAN - University Of Leon; Busman, Mark; SAENZ DE MIERA, LUIS - University Of Leon; JAKLITSCH, WALTER - University Of Vienna; ZHUANG, WEN-YIN - Chinese Academy Of Sciences; WANG, CHAO - Chinese Academy Of Sciences; CASQUERO, PEDRO - University Of Leon; Proctor, Robert

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/4/2021
Publication Date: 12/2/2021
Citation: Guttierrez, S., McCormick, S.P., Cardoza, R.E., Kim, H.-S., Yugueros, L.L., Vaughan, M.M., Carro-Huerga, G., Busman, M., Saenz de Miera, L.E., Jaklitsch, W.M., Zhuang, W.-Y., Wang, C., Casquero, P.A., Proctor, R.H. 2022. Distribution, function, and evolution of a gene essential for trichothecene toxin biosynthesis in Trichoderma. Frontiers in Microbiology. 12. Article 791641. https://doi.org/10.3389/fmicb.2021.791641.
DOI: https://doi.org/10.3389/fmicb.2021.791641

Interpretive Summary: Trichothecenes are fungal toxins that pose health hazards to humans, pets and livestock. In the fungi Fusarium and Trichoderma, trichothecenes have contrasting effects on agriculture. In Fusarium trichothecene production helps some species cause diseases of crops, such as wheat and potatoes, whereas in Trichoderma, production helps some species control crop diseases caused by other fungi. In trichothecene-producing fungi, genes that control trichothecene production are typically located adjacent to one another on a chromosome. As part of a study on trichothecene production in multiple fungi, ARS researchers in Peoria, Illinois, in collaboration with researchers at the University of Leon, Leon, Spain, found that the gene tri5, which controls the critical first step in trichothecene production, was present in 22 of 35 Trichoderma species, but only 13 of these had other trichothecene production genes. Further, in Trichoderma species with all the production genes, tri5 was physically separated from the other genes. The researchers also found evidence that in Trichoderma species that lack the other production genes, tri5 can inhibit trichothecene production by other fungi. These results indicate that Trichoderma species with only tri5 have the potential to control crop diseases caused by trichothecene-producing species of Fusarium. Such control should also reduce contamination of crops with the toxins.

Technical Abstract: Trichothecenes are terpenoid toxins produced by species in 10 fungal genera, including two species of Trichoderma. The trichothecene biosynthetic gene (tri) cluster typically includes the tri5 gene, which encodes a terpene synthase that catalyzes formation of trichodiene, the parent compound of all trichothecenes. The two Trichoderma species, Trichoderma arundinaceum and T. brevicompactum, that have been examined are unique in that tri5 is located outside the tri cluster in a genomic region that does not include other known tri genes. In the current study, analysis of 35 species representative of a wide range of the phylogenetic diversity of Trichoderma revealed that 22 species had tri5, but only 13 species had both tri5 and the tri cluster, and tri5 was not in the cluster in any species. Using complementation analysis of a T. arundinaceum tri5 deletion mutant, we demonstrated that some tri5 homologs from species that lack a tri cluster are functional, but others are not. Phylogenetic analyses suggest that Trichoderma tri5 was under positive selection following its divergence from homologs in other fungi but before Trichoderma species began diverging from one another. We propose two models to explain these diverse observations. One model proposes that the location of tri5 outside the tri cluster resulted from loss of tri5 from the cluster in an ancestral species followed by reacquisition via horizontal transfer. The other model proposes that in species that have a functional tri5 but lack the tri cluster, trichodiene production provides a competitive advantage.