Phylogenomic analysis of polyketide synthase-encoding genes in Trichoderma

Abstract

Members of the economically important ascomycete genus Trichoderma are ubiquitously distributed around the world. The mycoparasitic lifestyle and plant defence-inducing interactions of Trichoderma spp. make them ideal biocontrol agents. Of the Trichoderma enzymes that produce secondary metabolites, some of which likely play important roles in biocontrol processes, polyketide synthase (PKSs) have garnered less attention than non-ribosomal peptide synthetases such as those that produce peptaibols. We have taken a phylogenomic approach to study the PKS repertoire encoded in the genomes of Trichoderma reesei, Trichoderma atroviride and Trichoderma virens. Our analysis lays a foundation for future research related to PKSs within the genus Trichoderma and in other filamentous fungi. INTRODUCTIONGiven its important roles in bioenergy-related enzyme production and plant and fungal health, the genus Trichoderma has a significant economic footprint (Schuster & Schmoll, 2010). This genus is well known for its opportunistic lifestyle that includes saprotrophy, mycoparasitism, endophytism, and interactions with plants and animals. Because of their ability to antagonize other fungi and stimulate plant defences against phytopathogens, Trichoderma strains have become prominent biocontrol agents (Schuster & Schmoll, 2010). Further highlighting their mycoparasitic lifestyle, sequencing and analysis of the genomes from two mycoparasitic Trichoderma species (Trichoderma virens, Trichoderma atroviride) have shown that these genomes encode a rich catalogue of fungal cell wall-degrading chitinases and a relative paucity of plant cell wall-degrading enzymes (Kubicek et al., 2011;Martinez et al., 2008).As biocontrol agents and pathogens of fungal food crops, secondary metabolite production in Trichoderma spp. is of particular importance. Trichoderma and other filamentous fungi are well known for the production of a diverse array of secondary metabolites. Non-ribosomal peptides and polyketides comprise a major portion of these products, which are synthesized by large proteins composed of various domains for the individual enzymic steps (Cox, 2007). Both broad and genus-specific phylogenomic and functional analysis of polyketide synthase (PKS)-and non-ribosomal peptide synthetase (NRPS)-encoding genes have been performed, which has accelerated the pace at which genes and pathways are being linked to specific secondary metabolites (Bushley & Turgeon, 2010;Bushley et al., 2008;Chiang et al., 2010;Cramer et al., 2006;Gaffoor et al., 2005;Kroken et al., 2003;Kubicek et al., 2011;Lee et al., 2005).Trichoderma spp. are probably best known for their production of peptaibols, which are non-ribosomal peptides with antimicrobial and plant defence-stimulating activity (Viterbo et al., 2007). Relatively less studied in Trichoderma are PKSs. The recent analysis of the three available Trichoderma genome sequences has indicated that the genomes of these organisms encode only a small catalogue of PKSs: T. atroviride and T. virens each encode 18, and Tric...

The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species

“…Finally, the genome of T. atroviride is predicted to contain genes for 14 NRPSs, 18 PKSs, a single NRPS-PKS hybrid, and 14 terpenoid synthase domains (4, 23) (see Table S1 in the supplemental material). Phylogenetic analysis has been conducted on the inventory of both PKSs and NRPSs predicted in these genomes, and the results recapitulate much of what has been seen previously from similar multigenome studies looking at a wider breadth of ascomycetes (4,(531)(532)(533). In particular, the variability of secondary metabolite backbone genes both in total and for each class is not only found across the ascomycetes with sequenced genomes but also within the genomes from the genus Trichoderma.…”

Evolution of Chemical Diversity in Echinocandin Lipopeptide Antifungal Metabolites

“…Under either of these hypotheses, we might have expected to encounter evidence of cluster degradation or to find at least a few cluster fragments or pseudogenes interspersed across the genomes of major secondary-metabolite-producing sister lineages of the Sordariomycetes, Dothideomycetes, and Lecanoromycetes or in other orders of the Leotiomycetes and Eurotiomycetes beyond the Helotiales and Eurotiales. However, in contrast to what has been observed in some fungal secondary-metabolite pathways (2,(56)(57)(58), ec.asm.org 705 Eukaryotic Cell this was not the case. BLAST searches using each of the shared pathway genes always retrieved the corresponding genes of other echinocandin-producing species as the most likely hits.…”

Trichoderma Research in the Genome Era

“…The Trichoderma genomes have now been shown to contain a large repertoire of small cysteine-rich secreted protein-like genes (67), potentially encoding hundreds of possible elicitors. The challenge is to identify which are relevant and then test the proteins for activity (11 Figure 1) (3,91,92,96). Trichoderma secondary metabolites may be grouped into peptaibols, small NRPs (e.g., gliotoxin, siderophores), polyketides, terpenes, or pyrones.…”