Eukaryotic genomes consist to a significant extent of retrotransposons that are suppressed by host epigenetic mechanisms, preventing their uncontrolled propagation. However, it is not clear how this is achieved. Here we show that in Arabidopsis seedlings subjected to heat stress, a copia-type retrotransposon named ONSEN (Japanese 'hot spring') not only became transcriptionally active but also synthesized extrachromosomal DNA copies. Heat-induced ONSEN accumulation was stimulated in mutants impaired in the biogenesis of small interfering RNAs (siRNAs); however, there was no evidence of transposition occurring in vegetative tissues. After stress, both ONSEN transcripts and extrachromosomal DNA gradually decayed and were no longer detected after 20-30 days. Surprisingly, a high frequency of new ONSEN insertions was observed in the progeny of stressed plants deficient in siRNAs. Insertion patterns revealed that this transgenerational retrotransposition occurred during flower development and before gametogenesis. Therefore in plants with compromised siRNA biogenesis, memory of stress was maintained throughout development, priming ONSEN to transpose during differentiation of generative organs. Retrotransposition was not observed in the progeny of wild-type plants subjected to stress or in non-stressed mutant controls, pointing to a crucial role of the siRNA pathway in restricting retrotransposition triggered by environmental stress. Finally, we found that natural and experimentally induced variants in ONSEN insertions confer heat responsiveness to nearby genes, and therefore mobility bursts may generate novel, stress-responsive regulatory gene networks.

BackgroundThe mobilization of transposable elements (TEs) is suppressed by host genome defense mechanisms. Recent studies showed that the cis-regulatory region of Arabidopsis thaliana COPIA78/ONSEN retrotransposons contains heat-responsive elements (HREs), which cause their activation during heat stress. However, it remains unknown whether this is a common and potentially conserved trait and how it has evolved.ResultsWe show that ONSEN, COPIA37, TERESTRA, and ROMANIAT5 are the major families of heat-responsive TEs in A. lyrata and A. thaliana. Heat-responsiveness of COPIA families is correlated with the presence of putative high affinity heat shock factor binding HREs within their long terminal repeats in seven Brassicaceae species. The strong HRE of ONSEN is conserved over millions of years and has evolved by duplication of a proto-HRE sequence, which was already present early in the evolution of the Brassicaceae. However, HREs of most families are species-specific, and in Boechera stricta, the ONSEN HRE accumulated mutations and lost heat-responsiveness.ConclusionsGain of HREs does not always provide an ultimate selective advantage for TEs, but may increase the probability of their long-term survival during the co-evolution of hosts and genomic parasites.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1072-3) contains supplementary material, which is available to authorized users.

Retrotransposons containing long terminal repeats (LTRs) form a substantial fraction of eukaryotic genomes. The timing of past transposition can be estimated by quantifying the accumulation of mutations in initially identical LTRs. This way, retrotransposons are divided into young, potentially mobile elements, and old that moved thousands or even millions of years ago. Both types are found within a single retrotransposon family and it is assumed that the old members will remain immobile and degenerate further. Here, we provide evidence in Arabidopsis that old members enter into replication/transposition cycles through high rates of intra-family recombination. The recombination occurs pairwise, resembling the formation of recombinant retroviruses. Thus, each transposition burst generates a novel progeny population of chromosomally integrated LTR retrotransposons consisting of pairwise recombination products produced in a process comparable the sexual exchange of genetic information. Our observations provide an explanation for the reported high rates of sequence diversification in retrotransposons.

Retrotransposons (RTs) can rapidly increase in copy number due to periodic bursts of transposition. Such bursts are mutagenic and thus potentially deleterious. However, certain transposition-induced gain-of-function or regulatory mutations may be of selective advantage. How an optimal balance between these opposing effects arises is not well characterized. Here, we studied transposition bursts of a heat-activated retrotransposon family in Arabidopsis. We recorded a high inter and intraplant variation in the number and chromosomal position of new insertions, which usually did not affect plant fertility and were equally well transmitted through male and female gametes, even though 90% of them were within active genes. We found that a highly heterogeneous distribution of these new retroelement copies result from a combination of two mechanisms, of which the first prevents multiple transposition bursts in a given somatic cell lineage that later contributes to differentiation of gametes, and the second restricts the regulatory influence of new insertions toward neighboring chromosomal DNA. As a whole, such regulatory characteristics of this family of RTs ensure its rapid but stepwise accumulation in plant populations experiencing transposition bursts accompanied by high diversity of chromosomal sites harboring new RT insertions.

Summary Transposable elements (TEs) are ubiquitous genomic features. ‘Copy‐and‐paste’ long‐terminal‐repeat (LTR) retrotransposons have been particularly successful during evolution of the plant kingdom, representing a substantial proportion of genomes. For survival in copious numbers, these TEs may have evolved replicative mobilization strategies that circumvented hosts’ epigenetic silencing. Stressful circumstances are known to trigger the majority of known mobilizing plant retrotransposons, leading to the idea that most are activated by environmental signals. However, previous research revealed that plant developmental programs include steps of silencing relaxation, suggesting that developmental signals may also be of importance for thriving parasitic elements. Here, we uncover an unusual family of giant LTR retrotransposons from the Solanum clade, named MESSI, with transcriptional competence in shoot apical meristems of tomato. Despite being recognized and targeted by the host epigenetic surveillance, this family is activated in specific meristematic areas fundamental for plant shoot development, which are involved in meristem formation and maintenance. Our work provides initial evidence that some retrotransposons may evolve developmentally associated escape strategies to overcome transcriptional gene silencing in vegetative tissues contributing to the host's next generation. This implies that not only environmental but also developmental signals could be exploited by selfish elements for survival within the plant kingdom.