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Phylogenetic and Genomic Analyses Resolve the Origin of Important Plant Genes Derived from Transposable Elements.

ABSTRACT: Once perceived as merely selfish, transposable elements (TEs) are now recognized as potent agents of adaptation. One way TEs contribute to evolution is through TE exaptation, a process whereby TEs, which persist by replicating in the genome, transform into novel host genes, which persist by conferring phenotypic benefits. Known exapted TEs (ETEs) contribute diverse and vital functions, and may facilitate punctuated equilibrium, yet little is known about this process. To better understand TE exaptation, we designed an approach to resolve the phylogenetic context and timing of exaptation events and subsequent patterns of ETE diversification. Starting with known ETEs, we search in diverse genomes for basal ETEs and closely related TEs, carefully curate the numerous candidate sequences, and infer detailed phylogenies. To distinguish TEs from ETEs, we also weigh several key genomic characteristics including repetitiveness, terminal repeats, pseudogenic features, and conserved domains. Applying this approach to the well-characterized plant ETEs MUG and FHY3, we show that each group is paraphyletic and we argue that this pattern demonstrates that each originated in not one but multiple exaptation events. These exaptations and subsequent ETE diversification occurred throughout angiosperm evolution including the crown group expansion, the angiosperm radiation, and the primitive evolution of angiosperms. In addition, we detect evidence of several putative novel ETE families. Our findings support the hypothesis that TE exaptation generates novel genes more frequently than is currently thought, often coinciding with key periods of evolution.

SUBMITTER: Joly-Lopez Z

PROVIDER: S-EPMC4948706 | biostudies-literature | 2016 Aug

REPOSITORIES: biostudies-literature

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Phylogenetic and Genomic Analyses Resolve the Origin of Important Plant Genes Derived from Transposable Elements.

Joly-Lopez Zoé Z Hoen Douglas R DR Blanchette Mathieu M Bureau Thomas E TE

Molecular biology and evolution 20160428 8

Once perceived as merely selfish, transposable elements (TEs) are now recognized as potent agents of adaptation. One way TEs contribute to evolution is through TE exaptation, a process whereby TEs, which persist by replicating in the genome, transform into novel host genes, which persist by conferring phenotypic benefits. Known exapted TEs (ETEs) contribute diverse and vital functions, and may facilitate punctuated equilibrium, yet little is known about this process. To better understand TE exap ...[more]

PMID: 27189548

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Project description:Background:Miniature inverted repeat transposable elements (MITEs) are small non-autonomous DNA transposons that are ubiquitous in plant genomes, and are mobilised by their autonomous relatives. Stowaway MITEs are derived from and mobilised by elements from the mariner superfamily. Those elements constitute a significant portion of the carrot genome; however the variation caused by Daucus carota Stowaway MITEs (DcStos), their association with genes and their putative impact on genome evolution has not been comprehensively analysed. Results:Fourteen families of Stowaway elements DcStos occupy about 0.5% of the carrot genome. We systematically analysed 31 genomes of wild and cultivated Daucus carota, yielding 18.5 thousand copies of these elements, showing remarkable insertion site polymorphism. DcSto element demography differed based on the origin of the host populations, and corresponded with the four major groups of D. carota, wild European, wild Asian, eastern cultivated and western cultivated. The DcStos elements were associated with genes, and most frequently occurred in 5' and 3' untranslated regions (UTRs). Individual families differed in their propensity to reside in particular segments of genes. Most importantly, DcSto copies in the 2?kb regions up- and downstream of genes were more frequently associated with open reading frames encoding transcription factors, suggesting their possible functional impact. More than 1.5% of all DcSto insertion sites in different host genomes contained different copies in exactly the same position, indicating the existence of insertional hotspots. The DcSto7b family was much more polymorphic than the other families in cultivated carrot. A line of evidence pointed at its activity in the course of carrot domestication, and identified Dcmar1 as an active carrot mariner element and a possible source of the transposition machinery for DcSto7b. Conclusion:Stowaway MITEs have made a substantial contribution to the structural and functional variability of the carrot genome.

Project description:BackgroundWith the expansion of high throughput sequencing, we now have access to a larger number of genome-wide studies analyzing the Transposable elements (TEs) composition in a wide variety of organisms. However, genomic analyses often remain too limited in number and diversity of species investigated to study in depth the dynamics and evolutionary success of the different types of TEs among metazoans. Therefore, we chose to investigate the use of transcriptomes to describe the diversity of TEs in phylogenetically related species by conducting the first comparative analysis of TEs in two groups of polychaetes and evaluate the diversity of TEs that might impact genomic evolution as a result of their mobility.ResultsWe present a detailed analysis of TEs distribution in transcriptomes extracted from 15 polychaetes depending on the number of reads used during assembly, and also compare these results with additional TE scans on associated low-coverage genomes. We then characterized the clades defined by 1021 LTR-retrotransposon families identified in 26 species. Clade richness was highly dependent on the considered superfamily. Copia elements appear rare and are equally distributed in only three clades, GalEa, Hydra and CoMol. Among the eight BEL/Pao clades identified in annelids, two small clades within the Sailor lineage are new for science. We characterized 17 Gypsy clades of which only 4 are new; the C-clade largely dominates with a quarter of the families. Finally, all species also expressed for the majority two distinct transcripts encoding PIWI proteins, known to be involved in control of TEs mobilities.ConclusionsThis study shows that the use of transcriptomes assembled from 40 million reads was sufficient to access to the diversity and proportion of the transposable elements compared to those obtained by low coverage sequencing. Among LTR-retrotransposons Gypsy elements were unequivocally dominant but results suggest that the number of Gypsy clades, although high, may be more limited than previously thought in metazoans. For BEL/Pao elements, the organization of clades within the Sailor lineage appears more difficult to establish clearly. The Copia elements remain rare and result from the evolutionary consistent success of the same three clades.

Dataset Information

Phylogenetic and Genomic Analyses Resolve the Origin of Important Plant Genes Derived from Transposable Elements.

Publications

Phylogenetic and Genomic Analyses Resolve the Origin of Important Plant Genes Derived from Transposable Elements.

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