DNA transposon activity is associated with increased mutation rates in genes of rice and other grasses.

Thomas Wicker,Steve Rounsley,Mingsheng Chen,Klaus F X Mayer,Yeisoo Yu,Stefan Roffler,Andrea Zuccolo,Olivier Panaud,Georg Haberer,Rod A Wing,Pradeep Reddy Marri

doi:10.1038/ncomms12790

Abstract

DNA (class 2) transposons are mobile genetic elements which move within their ‘host' genome through excising and re-inserting elsewhere. Although the rice genome contains tens of thousands of such elements, their actual role in evolution is still unclear. Analysing over 650 transposon polymorphisms in the rice species Oryza sativa and Oryza glaberrima, we find that DNA repair following transposon excisions is associated with an increased number of mutations in the sequences neighbouring the transposon. Indeed, the 3,000 bp flanking the excised transposons can contain over 10 times more mutations than the genome-wide average. Since DNA transposons preferably insert near genes, this is correlated with increases in mutation rates in coding sequences and regulatory regions. Most importantly, we find this phenomenon also in maize, wheat and barley. Thus, these findings suggest that DNA transposon activity is a major evolutionary force in grasses which provide the basis of most food consumed by humankind.

Highlights

DNA transposons are mobile genetic elements which move within their ‘host’ genome through excising and re-inserting elsewhere
Considering findings on double-strand breaks (DSBs) repair from yeast[12,13,14,15,16,17,18] and Arabidopsis[19,20,21,22], we propose a molecular mechanism that explains the high numbers of mutations flanking transposon excisions in rice (Fig. 2c): in the first step, the transposons excise from the genome, leaving a DSB for the cell to repair
The main contrast to previous studies is that our data show that transposon activity is associated with higher mutation rate and may directly change coding sequences and regulatory regions by introducing nucleotide substitutions and insertions and deletions (InDels) during DNA repair

Summary

Introduction

DNA (class 2) transposons are mobile genetic elements which move within their ‘host’ genome through excising and re-inserting elsewhere. The vast majority of DNA transposons in grasses are non-autonomous, meaning that they rely for their transposition on enzymes encoded by a small number of ‘mother’ elements elsewhere in the genome[3,4] These small non-autonomous transposons were reported to preferably insert near genes[3,5,6]. DSB repair is a highly complex process that involves multiple enzymes and, in some pathways, single-stranded DNA intermediates[12,13,14,15,16,17,18,19,20,21,22] (Supplementary Note 1) Considering these complex processes, we wanted to study if and to what degree DNA transposons excisions affect the sequences surrounding the excision site and whether they have an impact on the evolution of genes. The preference of DNA transposons to insert near genes in grasses accelerates evolution of genes and coding regions

Methods

Results

Conclusion