Abstract
BackgroundHorizontal gene transfer (HGT) plays an important role in the adaptation of lineages to changing environments. The extent of this process in eukaryotes, however, remains controversial. The most well-known and dramatic form of HGT represents intracellular gene transfer from endosymbionts to the host nuclear genome. Such episodes of transfer typically involve hundreds of genes and are thought to be possible only in the case of endosymbiosis.ResultsUsing a conservative phylogenomic approach, we analyzed genomic data from the fungal pathogen Magnaporthiopsis incrustans in the order Magnaporthales and identified two instances of exclusive sharing of HGT-derived gene markers between Magnaporthales and another lineage of plant-pathogenic fungi in the genus Colletotrichum. Surprisingly, inspection of these data demonstrated that HGT is far more widespread than anticipated, with more than 90 genes (including 33 highly supported candidates) being putatively transferred between Magnaporthales and Colletotrichum. These gene transfers are often physically linked in the genome and show more than two-fold functional enrichment in carbohydrate activating enzymes associated with plant cell wall degradation.ConclusionsOur work provides a novel perspective on the scale of HGT between eukaryotes. These results challenge the notion that recognized HGT plays a minor role in the evolution of fungal lineages, and in the case we describe, is likely implicated in the evolution of plant pathogenesis. More generally, we suggest that the expanding database of closely related eukaryotic genomes and the application of novel analytic methods will further underline the significant impact of foreign gene acquisition across the tree of life. Major lifestyle transitions such as those accompanying the origin of extremophily or pathogenesis are expected to be ideal candidates for studying the mode and tempo of HGT.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0264-3) contains supplementary material, which is available to authorized users.
Highlights
Horizontal gene transfer (HGT) plays an important role in the adaptation of lineages to changing environments
The same topology and maximum likelihood (ML) bootstrap support values were obtained when using the 583 (40 %) genes with the strongest phylogenetic signal and when using the full set of 1453 genes, with decreasing genesupport frequencies (GSF) and Internode certainty (IC) values (Additional file 1). These results show that Magnaporthales and Colletotrichum are distinct lineages separated in the tree by multiple, well-defined Sordariomycetes lineages
We identified three instances in which M. incrustans genes and their Magnaporthales orthologs were derived from non-Pezizomycotina (NP) sources via HGT (Additional file 3) with 85 % or more SH-like branch support [24] and 85 % or more ultrafast bootstrap (UFboot) support [25]
Summary
Horizontal gene transfer (HGT) plays an important role in the adaptation of lineages to changing environments. Qiu et al BMC Biology (2016) 14:41 following simple guiding principle: generally, fungi (including Magnaporthales) contain limited amounts of foreign genes derived from distantly related sources (e.g., [10,11,12]), whereas gene transfer highways exist that allow massive gene exchanges between fungal lineages (e.g., [13,14,15]). In this context, we hypothesized that two unrelated fungal species are unlikely to acquire the same HGT gene marker from the same (or closely related) donor species via independent events. The framework for this study is a recently generated comprehensive Magnaporthales genome database generated by our group [16]
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