Abstract
BackgroundMutator-like transposable elements, a class of DNA transposons, exist pervasively in both prokaryotic and eukaryotic genomes, with more than 10,000 copies identified in the rice genome. These elements can capture ectopic genomic sequences that lead to the formation of new gene structures. Here, based on whole-genome comparative analyses, we comprehensively investigated processes and mechanisms of the evolution of putative genes derived from Mutator-like transposable elements in ten Oryza species and the outgroup Leersia perieri, bridging ~20 million years of evolutionary history.ResultsOur analysis identified thousands of putative genes in each of the Oryza species, a large proportion of which have evidence of expression and contain chimeric structures. Consistent with previous reports, we observe that the putative Mutator-like transposable element-derived genes are generally GC-rich and mainly derive from GC-rich parental sequences. Furthermore, we determine that Mutator-like transposable elements capture parental sequences preferentially from genomic regions with low methylation levels and high recombination rates. We explicitly show that methylation levels in the internal and terminated inverted repeat regions of these elements, which might be directed by the 24-nucleotide small RNA-mediated pathway, are different and change dynamically over evolutionary time. Lastly, we demonstrate that putative genes derived from Mutator-like transposable elements tend to be expressed in mature pollen, which have undergone de-methylation programming, thereby providing a permissive expression environment for newly formed/transposable element-derived genes.ConclusionsOur results suggest that DNA methylation may be a primary mechanism to facilitate the origination, survival, and regulation of genes derived from Mutator-like transposable elements, thus contributing to the evolution of gene innovation and novelty in plant genomes.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-0954-8) contains supplementary material, which is available to authorized users.
Highlights
Mutator-like transposable elements, a class of DNA transposons, exist pervasively in both prokaryotic and eukaryotic genomes, with more than 10,000 copies identified in the rice genome
Between ~7000 and 10,000 elements were detected in each AA and BB genome assembly, which is similar to the number of Mutator-like element (MULE) previously identified in the O. sativa ssp. japonica RefSeq [7], and ~4000 and 5000 in the basal Oryza species O. brachyantha and the outgroup L. perrieri (Fig. 1)
We found that fewer MULEs were present in the internal branches, which were referred as the ancestors of multiple Oryza species (Fig. 2)
Summary
Mutator-like transposable elements, a class of DNA transposons, exist pervasively in both prokaryotic and eukaryotic genomes, with more than 10,000 copies identified in the rice genome. These elements can capture ectopic genomic sequences that lead to the formation of new gene structures. Mutators are class II DNA transposable elements (TEs) and have propagated widely across both prokaryotic and eukaryotic genomes through a “cut-and-paste” mechanism. Mutator-like transposable elements (MULEs) are especially pervasive in higher plant genomes such as rice (Oryza sativa), in which more than 10,000 copies have been identified [6,7,8,9].
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