Abstract
BackgroundRetrotransposons play a central role in plant evolution and could be a powerful endogenous source of genetic and epigenetic variability for crop breeding. To ensure genome integrity several silencing mechanisms have evolved to repress retrotransposon mobility. Even though retrotransposons fully depend on transcriptional activity of the host RNA polymerase II (Pol II) for their mobility, it was so far unclear whether Pol II is directly involved in repressing their activity.ResultsHere we show that plants defective in Pol II activity lose DNA methylation at repeat sequences and produce more extrachromosomal retrotransposon DNA upon stress in Arabidopsis and rice. We demonstrate that combined inhibition of both DNA methylation and Pol II activity leads to a strong stress-dependent mobilization of the heat responsive ONSEN retrotransposon in Arabidopsis seedlings. The progenies of these treated plants contain up to 75 new ONSEN insertions in their genome which are stably inherited over three generations of selfing. Repeated application of heat stress in progeny plants containing increased numbers of ONSEN copies does not result in increased activation of this transposon compared to control lines. Progenies with additional ONSEN copies show a broad panel of environment-dependent phenotypic diversity.ConclusionsWe demonstrate that Pol II acts at the root of transposon silencing. This is important because it suggests that Pol II can regulate the speed of plant evolution by fine-tuning the amplitude of transposon mobility. Our findings show that it is now possible to study induced transposon bursts in plants and unlock their use to induce epigenetic and genetic diversity for crop breeding.
Highlights
Retrotransposons play a central role in plant evolution and could be a powerful endogenous source of genetic and epigenetic variability for crop breeding
Using quantitative real-time PCR, we determined that challenging nrpb2-3 seedlings by heat stress (HS) led to a mild increase in total ONSEN copy number relative to control stress (CS) and compared to the wild type (WT) (Fig. 1a)
In order to test the interaction between polymerase II (Pol II)-mediated repression of transposable elements (TEs) activation and DNA methylation, we grew WT and nrpb2-3 plants on media supplemented with zebularine (Z), an inhibitor of DNA methyltransferases active in plants [19], and subjected them to HS
Summary
Retrotransposons play a central role in plant evolution and could be a powerful endogenous source of genetic and epigenetic variability for crop breeding. Long terminal repeat (LTR) retrotransposons (class I elements), which represent the most abundant class of transposable elements (TEs) in eukaryotes, transpose via a copy and paste mechanism. This process requires the conversion of a full length RNA polymerase II (Pol II) transcript into extrachromosomal complementary DNA (ecDNA) by reverse transcription [1]. Recent work suggests a new “non-canonical” branch of RdDM that specializes in targeting transcriptionally active full-length TEs [16] This pathway functions independently of RDRs via Pol II transcripts that are directly processed by DCL3 into small interfering RNAs (siRNAs)
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