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DNA methylation changes facilitated evolution of genes derived from Mutator-like transposable elements.

ABSTRACT: 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. 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.Our 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.Our 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.

SUBMITTER: Wang J

PROVIDER: S-EPMC4858842 | biostudies-literature | 2016 May

REPOSITORIES: biostudies-literature

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DNA methylation changes facilitated evolution of genes derived from Mutator-like transposable elements.

Wang Jun J Yu Yeisoo Y Tao Feng F Zhang Jianwei J Copetti Dario D Kudrna Dave D Talag Jayson J Lee Seunghee S Wing Rod A RA Fan Chuanzhu C

Genome biology 20160506 1

<h4>Background</h4>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. 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 i ...[more]

PMID: 27154274

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Project description:BackgroundMutator-like elements (MULEs) are a significant superfamily of DNA transposons on account of their: (i) great transpositional activity and propensity for insertion in or near gene sequences, (ii) their consequent high mutagenic capacity, and, (iii) their tendency to acquire host gene fragments. Consequently, MULEs are important genetic tools and represent a key study system for research into host-transposon interactions. Yet, while several studies have focused on the impacts of MULEs on crop and fungus genomes, their evolution remains poorly explored.ResultsWe perform comprehensive bioinformatic and phylogenetic analyses to address currently available MULE diversity and reconstruct evolution for the group. For this, we mine MULEs from online databases, and combine search results with available transposase sequences retrieved from previously published studies. Our analyses uncover two entirely new MULE clades that contain elements almost entirely restricted to arthropod hosts, considerably expanding the set of MULEs known from this group, suggesting that many additional MULEs may await discovery from further arthropod genomes. In several cases, close relationships occur between MULEs recovered from distantly related host organisms, suggesting that horizontal transfer events may have played an important role in the evolution of the group. However, it is apparent that MULEs from plants remain separate from MULEs identified from other host groups. MULE structure varies considerably across phylogeny, and TIR length is shown to vary greatly both within and between MULE groups. Our phylogeny suggests that MULE diversity is clustered in well-supported groups, typically according to host taxonomy. With reference to this, we make suggestions on how MULE diversity can be partitioned to provide a robust taxonomic framework.ConclusionsOur study represents a considerable advance in the understanding of MULE diversity, host range and evolution, and provides a taxonomic framework for the classification of further MULE elements that await discovery. Our findings also raise a number of questions relating to MULE biology, suggesting that this group will provide a rich avenue for future study.

Project description:BACKGROUND: More than 80% of the wheat genome is composed of transposable elements (TEs). Since active TEs can move to different locations and potentially impose a significant mutational load, their expression is suppressed in the genome via small non-coding RNAs (sRNAs). sRNAs guide silencing of TEs at the transcriptional (mainly 24-nt sRNAs) and post-transcriptional (mainly 21-nt sRNAs) levels. In this study, we report the distribution of these two types of sRNAs among the different classes of wheat TEs, the regions targeted within the TEs, and their impact on the methylation patterns of the targeted regions. RESULTS: We constructed an sRNA library from hexaploid wheat and developed a database that included our library and three other publicly available sRNA libraries from wheat. For five completely-sequenced wheat BAC contigs, most perfectly matching sRNAs represented TE sequences, suggesting that a large fraction of the wheat sRNAs originated from TEs. An analysis of all wheat TEs present in the Triticeae Repeat Sequence database showed that sRNA abundance was correlated with the estimated number of TEs within each class. Most of the sRNAs perfectly matching miniature inverted repeat transposable elements (MITEs) belonged to the 21-nt class and were mainly targeted to the terminal inverted repeats (TIRs). In contrast, most of the sRNAs matching class I and class II TEs belonged to the 24-nt class and were mainly targeted to the long terminal repeats (LTRs) in the class I TEs and to the terminal repeats in CACTA transposons. An analysis of the mutation frequency in potentially methylated sites revealed a three-fold increase in TE mutation frequency relative to intron and untranslated genic regions. This increase is consistent with wheat TEs being preferentially methylated, likely by sRNA targeting. CONCLUSIONS: Our study examines the wheat epigenome in relation to known TEs. sRNA-directed transcriptional and post-transcriptional silencing plays important roles in the short-term suppression of TEs in the wheat genome, whereas DNA methylation and increased mutation rates may provide a long-term mechanism to inactivate TEs.

Dataset Information

DNA methylation changes facilitated evolution of genes derived from Mutator-like transposable elements.

Publications

DNA methylation changes facilitated evolution of genes derived from Mutator-like transposable elements.

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