Evolutionary Mechanisms Involved in Development of Fungal Secondary Metabolite Gene Clusters

Moore, Geromy G.; Collemare, Jérôme; Lebrun, Marc; Bradshaw, Rosie E.

doi:10.1002/9781118794623.ch18

Cited by 7 publications

(8 citation statements)

References 44 publications

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“…Although HGT and LGT occur in the majority of cases by transfer of single genes only (for review see [9, 50], the transfer of multiple genes or gene clusters has also been shown [11, 19, 50–52], particularly for genes encoding proteins for secondary metabolite synthesis [18, 20, 53–59]. In contrast, our data show that the fungal sorbicillin biosynthesis cluster evolved by complementing symplesiomorphous genes by LGT from other fungal donors, which in P. rubens occurred in at least two steps.…”

Section: Discussionmentioning

confidence: 99%

Several steps of lateral gene transfer followed by events of ‘birth-and-death’ evolution shaped a fungal sorbicillinoid biosynthetic gene cluster

Druzhinina

Kubicek

2016

BMC Evol Biol

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BackgroundSorbicillinoids are a family of complex cyclic polyketides produced by only a small number of distantly related ascomycete fungi such as Trichoderma (Sordariomycetes) and Penicillium (Eurotiomycetes). In T. reesei, they are synthesized by a gene cluster consisting of eight genes including two polyketide synthases (PKS). To reconstruct the evolutionary origin of this gene cluster, we examined the occurrence of these eight genes in ascomycetes.ResultsA cluster comprising at least six of them was only found in Hypocreales (Acremonium chrysogenum, Ustilaginoidea virens, Trichoderma species from section Longibrachiatum) and in Penicillium rubens (Eurotiales). In addition, Colletotrichum graminicola contained the two pks (sor1 and sor2), but not the other sor genes. A. chrysogenum was the evolutionary eldest species in which sor1, sor2, sor3, sor4 and sor6 were present. Sor5 was gained by lateral gene transfer (LGT) from P. rubens. In the younger Hypocreales (U. virens, Trichoderma spp.), the cluster evolved by vertical transfer, but sor2 was lost and regained by LGT from C. graminicola. SorB (=sor2) and sorD (=sor4) were symplesiomorphic in P. rubens, whereas sorA, sorC and sorF were obtained by LGT from A. chrysogenum, and sorE by LGT from Pestalotiopsis fici (Xylariales). The sorbicillinoid gene cluster in Trichoderma section Longibrachiatum is under strong purifying selection. The T. reesei sor genes are expressed during fast vegetative growth, during antagonism of other fungi and regulated by the secondary metabolism regulator LAE1.ConclusionsOur findings pinpoint the evolution of the fungal sorbicillinoid biosynthesis gene cluster. The core cluster arose in early Hypocreales, and was complemented by LGT. During further speciation in the Hypocreales, it became subject to birth and death evolution in selected lineages. In P. rubrens (Eurotiales), two cluster genes were symplesiomorphic, and the whole cluster formed by LGT from at least two different fungal donors.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0834-6) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Several steps of lateral gene transfer followed by events of ‘birth-and-death’ evolution shaped a fungal sorbicillinoid biosynthetic gene cluster

Druzhinina

Kubicek

2016

BMC Evol Biol

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“… b Number of MCG genes, where column D is the number of genes in the existing MGC in the donor lineage, R is the number of genes in the existing MGC in the recipient lineage, T is the number of gene trees supporting MGC-HGT reported by the original reference, and C is the number of gene trees supporting MGC-HGT confirmed by Richards et al ( 2011 ) . c See also Moore et al ( 2014 ) which argues that extensive gene duplication and loss could also explain the ACE1 gene phylogenies . d Genes are not clustered in some fungal lineages .…”

Section: Metabolic Caravans—gene Clustering Can Facilitate the Transfmentioning

confidence: 98%

“… c See also Moore et al ( 2014 ) which argues that extensive gene duplication and loss could also explain the ACE1 gene phylogenies . …”

Section: Metabolic Caravans—gene Clustering Can Facilitate the Transfmentioning

confidence: 98%

Fungal metabolic gene clustersâ€”caravans traveling across genomes and environments

2015

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Metabolic gene clusters (MGCs), physically co-localized genes participating in the same metabolic pathway, are signature features of fungal genomes. MGCs are most often observed in specialized metabolism, having evolved in individual fungal lineages in response to specific ecological needs, such as the utilization of uncommon nutrients (e.g., galactose and allantoin) or the production of secondary metabolic antimicrobial compounds and virulence factors (e.g., aflatoxin and melanin). A flurry of recent studies has shown that several MGCs, whose functions are often associated with fungal virulence as well as with the evolutionary arms race between fungi and their competitors, have experienced horizontal gene transfer (HGT). In this review, after briefly introducing HGT as a source of gene innovation, we examine the evidence for HGT's involvement on the evolution of MGCs and, more generally of fungal metabolism, enumerate the molecular mechanisms that mediate such transfers and the ecological circumstances that favor them, as well as discuss the types of evidence required for inferring the presence of HGT in MGCs. The currently available examples indicate that transfers of entire MGCs have taken place between closely related fungal species as well as distant ones and that they sometimes involve large chromosomal segments. These results suggest that the HGT-mediated acquisition of novel metabolism is an ongoing and successful ecological strategy for many fungal species.

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“…Often, missing orthologs and discontinuous distributions of homologs are also used to infer potential LGT events ( Ambrose et al 2014 ; Moore et al 2014 ; Fitzpatrick et al 2008 ; Temporini and Van Etten 2004 ), but these assumptions tend to change as more genomes are sequenced and intermediate genes are found ( Khaldi et al 2008 ). Finally, many of the tools developed to detect LGT events are based on phylogenetic methods that have been developed for bacteria, but in practice, fungal phylogenies are much harder to reconstruct than bacterial phylogenies due to the presence of cryptic intronic sequences and other sequence complexities.…”

Section: Discussionmentioning

confidence: 99%

Genomic Data Quality Impacts Automated Detection of Lateral Gene Transfer in Fungi

Dupont

Cox

2017

G3 Genes|Genomes|Genetics

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Lateral gene transfer (LGT, also known as horizontal gene transfer), an atypical mechanism of transferring genes between species, has almost become the default explanation for genes that display an unexpected composition or phylogeny. Numerous methods of detecting LGT events all rely on two fundamental strategies: primary structure composition or gene tree/species tree comparisons. Discouragingly, the results of these different approaches rarely coincide. With the wealth of genome data now available, detection of laterally transferred genes is increasingly being attempted in large uncurated eukaryotic datasets. However, detection methods depend greatly on the quality of the underlying genomic data, which are typically complex for eukaryotes. Furthermore, given the automated nature of genomic data collection, it is typically impractical to manually verify all protein or gene models, orthology predictions, and multiple sequence alignments, requiring researchers to accept a substantial margin of error in their datasets. Using a test case comprising plant-associated genomes across the fungal kingdom, this study reveals that composition- and phylogeny-based methods have little statistical power to detect laterally transferred genes. In particular, phylogenetic methods reveal extreme levels of topological variation in fungal gene trees, the vast majority of which show departures from the canonical species tree. Therefore, it is inherently challenging to detect LGT events in typical eukaryotic genomes. This finding is in striking contrast to the large number of claims for laterally transferred genes in eukaryotic species that routinely appear in the literature, and questions how many of these proposed examples are statistically well supported.

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Evolutionary Mechanisms Involved in Development of Fungal Secondary Metabolite Gene Clusters

Cited by 7 publications

References 44 publications

Several steps of lateral gene transfer followed by events of ‘birth-and-death’ evolution shaped a fungal sorbicillinoid biosynthetic gene cluster

Several steps of lateral gene transfer followed by events of ‘birth-and-death’ evolution shaped a fungal sorbicillinoid biosynthetic gene cluster

Fungal metabolic gene clustersâ€”caravans traveling across genomes and environments

Genomic Data Quality Impacts Automated Detection of Lateral Gene Transfer in Fungi

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