Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi

Khaldi, Nora; Collemare, Jérôme; Lebrun, Marc; Wolfe, Kenneth H.

doi:10.1186/gb-2008-9-1-r18

Cited by 208 publications

(196 citation statements)

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“…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.…”

Section: Phylogenetic Affinities Of the Echinocandin-producing Fungicontrasting

confidence: 57%

Evolution of Chemical Diversity in Echinocandin Lipopeptide Antifungal Metabolites

Yue

Chen

et al. 2015

Eukaryot Cell

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The echinocandins are a class of antifungal drugs that includes caspofungin, micafungin, and anidulafungin. Gene clusters encoding most of the structural complexity of the echinocandins provided a framework for hypotheses about the evolutionary history and chemical logic of echinocandin biosynthesis. Gene orthologs among echinocandin-producing fungi were identified. Pathway genes, including the nonribosomal peptide synthetases (NRPSs), were analyzed phylogenetically to address the hypothesis that these pathways represent descent from a common ancestor. The clusters share cooperative gene contents and linkages among the different strains. Individual pathway genes analyzed in the context of similar genes formed unique echinocandinexclusive phylogenetic lineages. The echinocandin NRPSs, along with the NRPS from the inp gene cluster in Aspergillus nidulans and its orthologs, comprise a novel lineage among fungal NRPSs. NRPS adenylation domains from different species exhibited a one-to-one correspondence between modules and amino acid specificity that is consistent with models of tandem duplication and subfunctionalization. Pathway gene trees and Ascomycota phylogenies are congruent and consistent with the hypothesis that the echinocandin gene clusters have a common origin. The disjunct Eurotiomycete-Leotiomycete distribution appears to be consistent with a scenario of vertical descent accompanied by incomplete lineage sorting and loss of the clusters from most lineages of the Ascomycota. We present evidence for a single evolutionary origin of the echinocandin family of gene clusters and a progression of structural diversification in two fungal classes that diverged approximately 290 to 390 million years ago. Lineagespecific gene cluster evolution driven by selection of new chemotypes contributed to diversification of the molecular functionalities.

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Section: Phylogenetic Affinities Of the Echinocandin-producing Fungicontrasting

confidence: 57%

Evolution of Chemical Diversity in Echinocandin Lipopeptide Antifungal Metabolites

Yue

Chen

et al. 2015

Eukaryot Cell

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“…It has yet to be shown that clustered genes have fitness advantages over and above (and in some cases to the detriment of) the fitness benefit conferred by them to the host organism that would justify the term "selfish." However, several fungal gene clusters associated with substratespecific and secondary metabolic pathways, including the GAL cluster, have spread via HGT (14,51,52).…”

Section: Resultsmentioning

confidence: 99%

Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi

Slot

Rokas

2010

Proc. Natl. Acad. Sci. U.S.A.

150

158

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A notable characteristic of fungal genomes is that genes involved in successive steps of a metabolic pathway are often physically linked or clustered. To investigate how such clusters of functionally related genes are assembled and maintained, we examined the evolution of gene sequences and order in the galactose utilization (GAL) pathway in whole-genome data from 80 diverse fungi. We found that GAL gene clusters originated independently and by different mechanisms in three unrelated yeast lineages. Specifically, the GAL cluster found in Saccharomyces and Candida yeasts originated through the relocation of native unclustered genes, whereas the GAL cluster of Schizosaccharomyces yeasts was acquired through horizontal gene transfer from a Candida yeast. In contrast, the GAL cluster of Cryptococcus yeasts was assembled independently from the Saccharomyces/Candida and Schizosaccharomyces GAL clusters and coexists in the Cryptococcus genome with unclustered GAL paralogs. These independently evolved GAL clusters represent a striking example of analogy at the genomic level. We also found that species with GAL clusters exhibited significantly higher rates of GAL pathway loss than species with unclustered GAL genes. These results suggest that clustering of metabolic genes might facilitate fungal adaptation to changing environments both through the acquisition and loss of metabolic capacities. F ungal genes involved in successive steps of a pathway are frequently physically clustered (1-12). Evolutionary analysis of several different fungal gene clusters has shown that they have originated through different mechanisms (13-16). For example, the DAL cluster for allantoin utilization in Saccharomyces cerevisiae and close relatives originated through adaptive gene relocation (13), whereas a nitrate assimilation cluster in Trichoderma originated through horizontal gene transfer (14). However, it is unclear how these mechanisms shape the assembly of gene clusters, or how the evolutionary trajectories differ between species containing clusters and species in which the genes in a pathway are scattered across the genome.To better understand the origins and maintenance of gene clusters over a large evolutionary timescale and a range of ecological conditions, we investigated the evolution of the Leloir galactose utilization (GAL) pathway in fungi. The detailed knowledge on GAL pathway function in S. cerevisiae (15, 16), and the abundance of genomic data from a wide diversity of fungal species (17), make it an excellent model pathway to address these questions. Furthermore, the relative galactose content varies substantially among different plant substrata (from hundreds of mg/g legume seeds and algal mats to less than 1 mg/g in some fruits) (18-21), suggesting that the natural substrates of fungi have likely provided ample opportunity for populations to evolve niche-dependent adaptations for galactose utilization.The protein products of three GAL genes (GAL1, GAL7, and GAL10) are involved in four enzymatic steps (22). In the first s...

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“…The only other PKS/NRPS that is known to be involved in plant-fungus interactions is Ace1 of M. grisea. Ace1 putatively encodes an unidentified secondary metabolite that acts as an avirulence factor during interactions with rice cultivars harbouring the Pi33 'R' gene triggering a hypersensitive response in a gene-for-gene fashion (Böhnert et al, 2004;Collemare et al, 2008a, b;Fudal et al, 2007;Khaldi et al, 2008;Vergne et al, 2007). This gene is expressed specifically in the appressoria of M. grisea, and the metabolite produced by this gene cluster has not yet been identified.…”

Section: Discussionmentioning

confidence: 99%

“…These phytotoxins act as virulence factors (Walton et al, 2004;Hoffmeister & Keller, 2007;Walton, 2006;Johnson et al, 2000;Elliott et al, 2007). Additionally, a PKS/NRPS hybrid enzyme (Ace1) of Magnaporthe grisea acts as an avirulence factor, triggering resistance in selective rice cultivars harbouring the corresponding resistance gene Pi33 (Böhnert et al, 2004;Collemare et al, 2008a, b;Fudal et al, 2007;Khaldi et al, 2008;Vergne et al, 2007). A recent comparative genomics study revealed that the genomes of the two biocontrol species T. virens and Trichoderma atroviride harbour a large number of NRPS and PKS genes, and the genome of T. virens contains more NRPSs than any other filamentous fungi studied so far (Kubicek et al, 2011 …”

Section: Introductionmentioning

confidence: 99%

Functional analysis of non-ribosomal peptide synthetases (NRPSs) in Trichoderma virens reveals a polyketide synthase (PKS)/NRPS hybrid enzyme involved in the induced systemic resistance response in maize

et al. 2012

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Trichoderma virens genome harbours genes encoding 22 non-ribosomal peptide synthetases (NRPSs) with at least one complete module (containing adenylation, thiolation and condensation domains) and four PKS/NRPS (polyketide synthase/NRPS) hybrid enzymes. After a primary screen for expression of these 26 genes when mycelia of T. virens are in contact with maize roots, seven genes that are upregulated were selected for further study. Using homologous recombination, loss-of-function mutants in six of these were obtained (the seventh, tex2, was acquired from our previous studies). Plant assays in a hydroponics system revealed that all seven mutants retained the ability to internally colonize maize roots. However, a mutation in one of the PKS/NRPS hybrid genes impaired the ability of T. virens to induce the defence response gene pal (phenylalanine ammonia lyase), suggesting a putative role for the associated metabolite product in induced systemic resistance. Interestingly, the mutant retained its ability to induce another defence response gene aos (allene oxide synthase). We thus provide evidence that a PKS/NRPS hybrid enzyme is involved in Trichoderma-plant interactions resulting in induction of defence responses.

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Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi

Cited by 208 publications

References 50 publications

Evolution of Chemical Diversity in Echinocandin Lipopeptide Antifungal Metabolites

Evolution of Chemical Diversity in Echinocandin Lipopeptide Antifungal Metabolites

Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi

Functional analysis of non-ribosomal peptide synthetases (NRPSs) in Trichoderma virens reveals a polyketide synthase (PKS)/NRPS hybrid enzyme involved in the induced systemic resistance response in maize

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