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Background  Retrotransposons 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.    Results  Here 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.    Conclusions  We 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.    Electronic supplementary material  The online version of this article (doi:10.1186/s13059-017-1265-4) contains supplementary material, which is available to authorized users.

Inhibition of RNA polymerase II allows controlled mobilisation of retrotransposons for plant breeding