Marie Mirouze

An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress

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.

Epigenetic contribution to stress adaptation in plants

Plant epigenetics has recently gained unprecedented interest, not only as a subject of basic research but also as a possible new source of beneficial traits for plant breeding. We discuss here mechanisms of epigenetic regulation that should be considered when undertaking the latter. Since these mechanisms are responsible for the formation of heritable epigenetic gene variants (epialleles) and also regulate transposons mobility, both aspects could be exploited to broaden plant phenotypic and genetic variation, which could improve long-term plant adaptation to environmental challenges and, thus, increase productivity.

Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes

Transgenerational epigenetic inheritance has been defined by the study of relatively few loci. We examined a population of recombinant inbred lines with epigenetically mosaic chromosomes consisting of wild-type and CG methylation-depleted segments (epiRILs). Surprisingly, transposons that were immobile in the parental lines displayed stochastic movement in 28% of the epiRILs. Although analysis after eight generations of inbreeding, supported by genome-wide DNA methylation profiling, identified recombined parental chromosomal segments, these were interspersed with unexpectedly high frequencies of nonparental methylation polymorphism. Hence, epigenetic inheritance in hybrids derived from parents with divergent epigenomes permits long-lasting epi-allelic interactions that violate Mendelian expectations. Such persistently unstable epigenetic states complicate linkage-based epigenomic mapping. Thus, future epigenomic analyses should consider possible genetic instabilities and alternative mapping strategies.

Selective epigenetic control of retrotransposition in Arabidopsis

Retrotransposons are mobile genetic elements that populate chromosomes, where the host largely controls their activities. In plants and mammals, retrotransposons are transcriptionally silenced by DNA methylation, which in Arabidopsis is propagated at CG dinucleotides by METHYLTRANSFERASE 1 (MET1). In met1 mutants, however, mobilization of retrotransposons is not observed, despite their transcriptional activation. A post-transcriptional mechanism therefore seems to be preventing retrotransposition. Here we show that a copia-type retrotransposon (Évadé, French for ‘fugitive’) evaded suppression of its movement during inbreeding of hybrid epigenomes consisting of met1- and wild-type-derived chromosomes. Évadé (EVD) reinsertions caused a series of developmental mutations that allowed its identification. Genetic testing of host control of the EVD life cycle showed that transcriptional suppression occurred by CG methylation supported by RNA-directed DNA methylation. On transcriptional reactivation, subsequent steps of the EVD cycle were inhibited by plant-specific RNA polymerase IV/V and the histone methyltransferase KRYPTONITE (KYP). Moreover, genome resequencing demonstrated retrotransposition of EVD but no other potentially active retroelements when this combination of epigenetic mechanisms was compromised. Our results demonstrate that epigenetic control of retrotransposons extends beyond transcriptional suppression and can be individualized for particular elements.

Epigenetic regulation of adaptive responses of forest tree species to the environment

Epigenetic variation is likely to contribute to the phenotypic plasticity and adaptative capacity of plant species, and may be especially important for long-lived organisms with complex life cycles, including forest trees. Diverse environmental stresses and hybridization/polyploidization events can create reversible heritable epigenetic marks that can be transmitted to subsequent generations as a form of molecular “memory”. Epigenetic changes might also contribute to the ability of plants to colonize or persist in variable environments. In this review, we provide an overview of recent data on epigenetic mechanisms involved in developmental processes and responses to environmental cues in plant, with a focus on forest tree species. We consider the possible role of forest tree epigenetics as a new source of adaptive traits in plant breeding, biotechnology, and ecosystem conservation under rapid climate change.

Loss of DNA methylation affects the recombination landscape in Arabidopsis

During sexual reproduction, one-half of the genetic material is deposited in gametes, and a complete set of chromosomes is restored upon fertilization. Reduction of the genetic information before gametogenesis occurs in meiosis, when cross-overs (COs) between homologous chromosomes secure an exchange of their genetic information. COs are not evenly distributed along chromosomes and are suppressed in chromosomal regions encompassing compact, hypermethylated centromeric and pericentromeric DNA. Therefore, it was postulated that DNA hypermethylation is inhibitory to COs. Here, when analyzing meiotic recombination in mutant plants with hypomethylated DNA, we observed unexpected and counterintuitive effects of DNA methylation losses on CO distribution. Recombination was further promoted in the hypomethylated chromosome arms while it was inhibited in heterochromatic regions encompassing pericentromeric DNA. Importantly, the total number of COs was not affected, implying that loss of DNA methylation led to a global redistribution of COs along chromosomes. To determine by which mechanisms altered levels of DNA methylation influence recombination—whether directly in cis or indirectly in trans by changing expression of genes encoding recombination components—we analyzed CO distribution in wild-type lines with randomly scattered and well-mapped hypomethylated chromosomal segments. The results of these experiments, supported by expression profiling data, suggest that DNA methylation affects meiotic recombination in cis. Because DNA methylation exhibits significant variation even within a single species, our results imply that it may influence the evolution of plant genomes through the control of meiotic recombination.

Widespread and frequent horizontal transfers of transposable elements in plants

Vertical, transgenerational transmission of genetic material occurs through reproduction of living organisms. In addition to vertical inheritance, horizontal gene transfer between reproductively isolated species has recently been shown to be an important, if not dominant, mechanism in the evolution of prokaryotic genomes. In contrast, only a few horizontal transfer (HT) events have been characterized so far in eukaryotes and mainly concern transposable elements (TEs). Whether these are frequent and have a significant impact on genome evolution remains largely unknown. We performed a computational search for highly conserved LTR retrotransposons among 40 sequenced eukaryotic genomes representing the major plant families. We found that 26 genomes (65%) harbor at least one case of horizontal TE transfer (HTT). These transfers concern species as distantly related as palm and grapevine, tomato and bean, or poplar and peach. In total, we identified 32 cases of HTTs, which could translate into more than 2 million among the 13,551 monocot and dicot genera. Moreover, we show that these TEs have remained functional after their transfer, occasionally causing a transpositional burst. This suggests that plants can frequently exchange genetic material through horizontal transfers and that this mechanism may be important in TE-driven genome evolution.

Epigenetic control of transposon transcription and mobility in Arabidopsis

The mobility of genetic elements called transposable elements (TEs) was discovered half a century ago by Barbara McClintock. Although she had recognized them as chromosomal controlling elements, for much of the consequent time TEs were primarily considered as parasites of the host genome. However the recent explosion of discoveries in the fields of genomics and epigenetics have unambiguously shown the importance of TEs in genome function and evolution. Bursts of endogenous TEs have been reported in plants with epigenetic misregulation, revealing the molecular mechanisms underlying their control. We review here the different steps in TE invasion of the host genome involving epigenetic control and environmental stress responses. As TEs propagate in plant genomes and attract epigenetic marks, their neo-insertions can lead to the formation of new, heritable epigenetic variants (epialleles) of genes in their vicinity and impact on host gene regulatory networks. The epigenetic interplay between TE and genes thus plays a crucial role in the TE-host co-evolution.

Adaptation to Global Change: A Transposable Element–Epigenetics Perspective

Understanding how organisms cope with global change is a major scientific challenge. The molecular pathways underlying rapid adaptive phenotypic responses to global change remain poorly understood. Here, we highlight the relevance of two environment-sensitive molecular elements: transposable elements (TEs) and epigenetic components (ECs). We first outline the sensitivity of these elements to global change stressors and review how they interact with each other. We then propose an integrative molecular engine coupling TEs and ECs and allowing organisms to fine-tune phenotypes in a real-time fashion, adjust the production of phenotypic and genetic variation, and produce heritable phenotypes with different levels of transmission fidelity. We finally discuss the implications of this molecular engine in the context of global change.

Transposable elements, a treasure trove to decipher epigenetic variation: insights from Arabidopsis and crop epigenomes

In the past decade, plant biologists and breeders have developed a growing interest in the field of epigenetics, which is defined as the study of heritable changes in gene expression that cannot be explained by changes in the DNA sequence. Epigenetic marks can be responsive to the environment, and evolve faster than genetic changes. Therefore, epigenetic diversity may represent an unexplored resource of natural variation that could be used in plant breeding programmes. On the other hand, crop genomes are largely populated with transposable elements (TEs) that are efficiently targeted by epigenetic marks, and part of the epigenetic diversity observed might be explained by TE polymorphisms. Characterizing the degree to which TEs influence epigenetic variation in crops is therefore a major goal to better use epigenetic variation. To date, epigenetic analyses have been mainly focused on the model plant Arabidopsis thaliana, and have provided clues on epigenome features, components that silence pathways, and effects of silencing impairment. But to what extent can Arabidopsis be used as a model for the epigenomics of crops? In this review, we discuss the similarities and differences between the epigenomes of Arabidopsis and crops. We explore the relationship between TEs and epigenomes, focusing on TE silencing control and escape, and the impact of TE mobility on epigenomic variation. Finally, we provide insights into challenges to tackle, and future directions to take in the route towards using epigenetic diversity in plant breeding programmes.