AUTHOR=Gutiérrez Santiago , McCormick Susan P. , Cardoza Rosa E. , Kim Hye-Seon , Yugueros Laura Lindo , Vaughan Martha Marie , Carro-Huerga Guzmán , Busman Mark , Sáenz de Miera Luis E. , Jaklitsch Walter M. , Zhuang Wen-Ying , Wang Chao , Casquero Pedro A. , Proctor Robert Henry 

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

JOURNAL=Frontiers in Microbiology

VOLUME=12

YEAR=2021

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2021.791641

DOI=10.3389/fmicb.2021.791641

ISSN=1664-302X

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