Distribution, Function, and Evolution of a Gene Essential for Trichothecene Toxin Biosynthesis in Trichoderma

Trichothecenes are terpenoid toxins produced by species in 10 fungal genera, including 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 tric...

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Autores principales: Santiago Gutiérrez, Susan P. McCormick, Rosa E. Cardoza, Hye-Seon Kim, Laura Lindo Yugueros, Martha Marie Vaughan, Guzmán Carro-Huerga, Mark Busman, Luis E. Sáenz de Miera, Walter M. Jaklitsch, Wen-Ying Zhuang, Chao Wang, Pedro A. Casquero, Robert Henry Proctor
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Publicado: Frontiers Media S.A. 2021
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Acceso en línea:https://doaj.org/article/04248366ba344f17b3ba2afec72bf6e9
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spelling oai:doaj.org-article:04248366ba344f17b3ba2afec72bf6e92021-12-02T11:37:17ZDistribution, Function, and Evolution of a Gene Essential for Trichothecene Toxin Biosynthesis in Trichoderma1664-302X10.3389/fmicb.2021.791641https://doaj.org/article/04248366ba344f17b3ba2afec72bf6e92021-12-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fmicb.2021.791641/fullhttps://doaj.org/toc/1664-302XTrichothecenes are terpenoid toxins produced by species in 10 fungal genera, including 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 representing 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. tri5 was not located 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.Santiago GutiérrezSusan P. McCormickRosa E. CardozaHye-Seon KimLaura Lindo YuguerosMartha Marie VaughanGuzmán Carro-HuergaMark BusmanLuis E. Sáenz de MieraWalter M. JaklitschWen-Ying ZhuangChao WangPedro A. CasqueroRobert Henry ProctorFrontiers Media S.A.articleTrichodermatrichothecenestri5 genepositive selectiongene deletion and complementationantifungal activityMicrobiologyQR1-502ENFrontiers in Microbiology, Vol 12 (2021)
institution DOAJ
collection DOAJ
language EN
topic Trichoderma
trichothecenes
tri5 gene
positive selection
gene deletion and complementation
antifungal activity
Microbiology
QR1-502
spellingShingle Trichoderma
trichothecenes
tri5 gene
positive selection
gene deletion and complementation
antifungal activity
Microbiology
QR1-502
Santiago Gutiérrez
Susan P. McCormick
Rosa E. Cardoza
Hye-Seon Kim
Laura Lindo Yugueros
Martha Marie Vaughan
Guzmán Carro-Huerga
Mark Busman
Luis E. Sáenz de Miera
Walter M. Jaklitsch
Wen-Ying Zhuang
Chao Wang
Pedro A. Casquero
Robert Henry Proctor
Distribution, Function, and Evolution of a Gene Essential for Trichothecene Toxin Biosynthesis in Trichoderma
description Trichothecenes are terpenoid toxins produced by species in 10 fungal genera, including 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 representing 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. tri5 was not located 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.
format article
author Santiago Gutiérrez
Susan P. McCormick
Rosa E. Cardoza
Hye-Seon Kim
Laura Lindo Yugueros
Martha Marie Vaughan
Guzmán Carro-Huerga
Mark Busman
Luis E. Sáenz de Miera
Walter M. Jaklitsch
Wen-Ying Zhuang
Chao Wang
Pedro A. Casquero
Robert Henry Proctor
author_facet Santiago Gutiérrez
Susan P. McCormick
Rosa E. Cardoza
Hye-Seon Kim
Laura Lindo Yugueros
Martha Marie Vaughan
Guzmán Carro-Huerga
Mark Busman
Luis E. Sáenz de Miera
Walter M. Jaklitsch
Wen-Ying Zhuang
Chao Wang
Pedro A. Casquero
Robert Henry Proctor
author_sort Santiago Gutiérrez
title Distribution, Function, and Evolution of a Gene Essential for Trichothecene Toxin Biosynthesis in Trichoderma
title_short Distribution, Function, and Evolution of a Gene Essential for Trichothecene Toxin Biosynthesis in Trichoderma
title_full Distribution, Function, and Evolution of a Gene Essential for Trichothecene Toxin Biosynthesis in Trichoderma
title_fullStr Distribution, Function, and Evolution of a Gene Essential for Trichothecene Toxin Biosynthesis in Trichoderma
title_full_unstemmed Distribution, Function, and Evolution of a Gene Essential for Trichothecene Toxin Biosynthesis in Trichoderma
title_sort distribution, function, and evolution of a gene essential for trichothecene toxin biosynthesis in trichoderma
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/04248366ba344f17b3ba2afec72bf6e9
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