Mu Transposon Insertion Sites and Meiotic Recombination Events Co-Localize with Epigenetic Marks for Open Chromatin across the Maize Genome

Abstract

The Mu transposon system of maize is highly active, with each of the ∼50–100 copies transposing on average once each generation. The approximately one dozen distinct Mu transposons contain highly similar ∼215 bp terminal inverted repeats (TIRs) and generate 9-bp target site duplications (TSDs) upon insertion. Using a novel genome walking strategy that uses these conserved TIRs as primer binding sites, Mu insertion sites were amplified from Mu stocks and sequenced via 454 technology. 94% of ∼965,000 reads carried Mu TIRs, demonstrating the specificity of this strategy. Among these TIRs, 21 novel Mu TIRs were discovered, revealing additional complexity of the Mu transposon system. The distribution of >40,000 non-redundant Mu insertion sites was strikingly non-uniform, such that rates increased in proportion to distance from the centromere. An identified putative Mu transposase binding consensus site does not explain this non-uniformity. An integrated genetic map containing more than 10,000 genetic markers was constructed and aligned to the sequence of the maize reference genome. Recombination rates (cM/Mb) are also strikingly non-uniform, with rates increasing in proportion to distance from the centromere. Mu insertion site frequencies are strongly correlated with recombination rates. Gene density does not fully explain the chromosomal distribution of Mu insertion and recombination sites, because pronounced preferences for the distal portion of chromosome are still observed even after accounting for gene density. The similarity of the distributions of Mu insertions and meiotic recombination sites suggests that common features, such as chromatin structure, are involved in site selection for both Mu insertion and meiotic recombination. The finding that Mu insertions and meiotic recombination sites both concentrate in genomic regions marked with epigenetic marks of open chromatin provides support for the hypothesis that open chromatin enhances rates of both Mu insertion and meiotic recombination.

High-Resolution Mapping of Crossover Events in the Hexaploid Wheat Genome Suggests a Universal Recombination Mechanism

“…New wheat-genomic tools allow more resolute analysis of recombination pattern Whole-genome, fine-scale recombination studies in plants have only been conducted in species for which the genome sequence was available (Wu et al 2003;Liu et al 2009;Paape et al 2012;Rodgers-Melnick et al 2015;Shilo et al 2015). However, this mainly restricted such analyses to species with small and compact genomes with low rates of TEs.…”

“…However, this mainly restricted such analyses to species with small and compact genomes with low rates of TEs. Only maize had a large genome and data showed a correlation between Mu TE insertion sites and CO localization (Liu et al 2009). Bread wheat has a six-times-larger genome than maize and recombination at the chromosome scale is low and occurs preferentially in distal regions.…”

“…CO distribution is largely modified in Arabidopsis met1 and ddm1 mutants, which show an increase of proximal recombination events and a simultaneous decrease in pericentromeric and distal regions (Colome-Tatche et al 2012;Melamed-Bessudo and Levy 2012;Mirouze et al 2012;Yelina et al 2012). Since H3K4me3 and H2A.Z landmarks are important for promotion of gene transcription (Liu et al 2009;Yelina et al 2012;Choi et al 2013) and are associated with high recombination rates in Arabidopsis (Yelina et al 2012) as well as in barley (Aliyeva-Schnorr et al 2015;Baker et al 2015), this suggests that both recombination and DNA-transposon insertion benefit from low compaction of DNA to occur within the genome. …”

“…Repeated sequences and recombination rate are correlated positively in Caenorhabditis elegans (Duret et al 2000) and negatively in the Drosophila melanogaster genome (Rizzon et al 2002). Even in the same species, in maize, insertion sites of the Mu transposon concentrate in the same regions as meiotic recombination (Liu et al 2009), while fine-scale studies at the bronze locus revealed a reduction of recombination in regions containing TEs, suggesting that retrotransposons are probably inert with regard to recombination because of methylation and the likely associated condensed chromatin (Dooner and Martínez-Férez 1997;He and Dooner 2009;Rodgers-Melnick et al 2015). In Arabidopsis, DNA methylation can silence CO hotspots and plays an essential role in forming domains of meiotic recombination along chromosomes (Yelina et al 2015).…”

A blessing in disguise: Transposable elements are more than parasites

“…Besides such genome invasion, discrete transposition (and the potential consecutive epigenetic or genetic regulations) may also account for generating new stress-inducible gene expression. A similar site insertion preference is true for the Mu transposable element in maize: using a novel strategy combining genome walking and deep-sequencing, Liu and colleagues 25 demonstrate that Mu preferentially integrates into sequences with open chromatin marks, therefore most often in the 5' flanking regions of genes.…”