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Horizontal Acquisition of Toxic Alkaloid Synthesis in a Clade of Plant Associated Fungi

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Horizontal Acquisition of Toxic Alkaloid Synthesis in a Clade of Plant Associated Fungi

Marina Marcet-Houben et al. Fungal Genet Biol.

Abstract

Clavicipitaceae is a fungal group that comprises species that closely interact with plants as pathogens, parasites or symbionts. A key factor in these interactions is the ability of these fungi to synthesize toxic alkaloid compounds that contribute to the protection of the plant host against herbivores. Some of these compounds such as ergot alkaloids are toxic to humans and have caused important epidemics throughout history. The gene clusters encoding the proteins responsible for the synthesis of ergot alkaloids and lolines in Clavicipitaceae have been elucidated. Notably, homologs to these gene clusters can be found in distantly related species such as Aspergillus fumigatus and Penicillium expansum, which diverged from Clavicipitaceae more than 400 million years ago. We here use a phylogenetic approach to analyze the evolution of these gene clusters. We found that the gene clusters conferring the ability to synthesize ergot alkaloids and loline emerged first in Eurotiomycetes and were then likely transferred horizontally to Clavicipitaceae. Horizontal gene transfer is known to play a role in shaping the distribution of secondary metabolism clusters across distantly related fungal species. We propose that HGT events have played an important role in the capability of Clavicipitaceae to produce two key secondary metabolites that have enhanced the ability of these species to protect their plant hosts, therefore favoring their interactions.

Keywords: Clavicipitaceae; Ergot alkaloids; HGT; Loline; Phylogenetics; Phylome.

Figures

Fig. 1
Fig. 1
Schematic species tree depicting the relationships between the main groups considered.
Fig. 2
Fig. 2
Example trees for the genes in the loline cluster. A. lolT tree presents a topology where Clavicipitaceae are grouped with Eurotiomycetes. B. lolM tree which presents a topology congruent with the species tree. For both trees circles represent collapsed nodes of the tree and are sized according to the number of leaves that diverged from the node. Colors belong to the different taxonomic groups: green – Sordariomycetes, yellow – Leotiomycetes, red – Eurotiomycetes, blue – Dothideomycetes and gray – Prokaryotes. Bootstrap supports lower than 75 are indicated on the tree. Nodes with a support below 33 are collapsed. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 3
Fig. 3
Left panel shows a Maximum likelihood phylogeny of 34 species based on the concatenation of 167 genes. Leaves are colored according to the main taxonomic groups within Pezizomycotina: Leotiomycetes (yellow), Sordariomycetes (green), Dothideomycetes (blue) and Eurotiomycetes (red). The two panels on the right detail the composition of the two gene clusters discussed in each species. Each gene in each cluster is represented by a square, a circle or a triangle. Squares represent core genes, circles represent accessory genes, whereas triangles represent genes that are not known to be part of the original gene cluster. Spaces between genes indicate that the two genes have more than three non related genes between them or that they belong to different contigs. Homologous genes have the same color. Genes with an identity below 50% to the original gene from the cluster have been excluded from the image. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 4
Fig. 4
Example trees for the genes in the ergot alkaloid cluster. A. easA tree where the Clavicipitaceae species group with Eurotiomycetes and one Leotiomycetes. B. Tree in which easP clusters within a group of other Sordariomycetes and Leotiomycetes. Tree image follows the same format as Fig. 2.
Fig. 5
Fig. 5
Chronogram showing the divergence times between the different species and inference of the timing of the HGT events discussed. The red star indicates where the ergot alkaloid gene cluster emerged in Clavicipitaceae, the red arrow represents the possible HGT direction. The blue stars and arrows show the two alternative hypothesis considered for the emergence of the loline gene cluster. The light colored arrow shows an initial transference from P. expansum to the base of Epichloe followed by a second transference from Epichloe to A. hypoxylon. The dark colored arrow shows the alternative hypothesis where first P. expansum transferred the loline cluster to A. hypoxylon and from this species it was transferred to the base of Epichloe.

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References

    1. Akaike, H., 1973. Information theory and extension of the maximum likelihood principle. In: Proc. 2nd Int. Symp. Inf. Theory, pp. 267–281.
    1. Ballester A.-R., Marcet-Houben M., Levin E., Sela N., Selma-Lázaro C., Carmona L., Wisniewski M., Droby S., González-Candelas L., Gabaldón T. Genome, transcriptome, and functional analyses of Penicillium expansum provide new insights into secondary metabolism and pathogenicity. Mol. Plant-Microbe Interact. MPMI. 2015;28:232–248. - PubMed
    1. Capella-Gutiérrez S., Silla-Martínez J.M., Gabaldón T. TrimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinform. Oxf. Engl. 2009;25:1972–1973. - PMC - PubMed
    1. Coelho M.A., Gonçalves C., Sampaio J.P., Gonçalves P. Extensive intra-kingdom horizontal gene transfer converging on a fungal fructose transporter gene. PLoS Genet. 2013;9:e1003587. - PMC - PubMed
    1. Coyle C.M., Panaccione D.G. An ergot alkaloid biosynthesis gene and clustered hypothetical genes from Aspergillus fumigatus. Appl. Environ. Microbiol. 2005;71:3112–3118. - PMC - PubMed

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