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 (Evadé, French for 'fugitive') evaded suppression of its movement during inbreeding of hybrid epigenomes consisting of met1- and wild-type-derived chromosomes. Evadé (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.

Ribosomal protein L24 (RPL24) is implicated in translation reinitiation of polycistronic genes. A newly isolated Arabidopsis thaliana short valve1 (stv1) mutant, in which one of the RPL24-encoding genes, RPL24B, is deleted, shows specific defects in the apical-basal patterning of the gynoecium, in addition to phenotypes induced by ribosome deficiency. A similar gynoecium phenotype is caused by mutations in the auxin response factor (ARF) genes ETTIN (ETT) and MONOPTEROS (MP), which have upstream open reading frames (uORFs) in their 59-transcript leader sequences. Gynoecia of a double mutant of stv1 and a weak ett mutant allele are similar to those of a strong ett allele, and transformation with a uORFeliminated ETT construct partially suppressed the stv1 gynoecium phenotype, implying that STV1 could influence ETT translation through its uORFs. Analyses of 59-leader-reporter gene fusions showed that the uORFs of ETT and MP negatively regulate the translation of the downstream major ORFs, indicating that translation reinitiation is an important step for the expression of these proteins. Taken together, we propose that perturbation of translation reinitiation of the ARF transcripts causes the defects in gynoecium patterning observed in the stv1 mutant.

DNA methylation is a type of epigenetic marking that strongly influences chromatin structure and gene expression in plants and mammals. Over the past decade, DNA methylation has been intensively investigated in order to elucidate its control mechanisms. These studies have shown that small RNAs are involved in the induction of DNA methylation, that there is a relationship between DNA methylation and histone methylation, and that the base excision repair pathway has an important role in DNA demethylation. Some aspects of DNA methylation have also been shown to be shared with mammals, suggesting that the regulatory pathways are, in part at least, evolutionarily conserved. Considerable progress has been made in elucidating the mechanisms that control DNA methylation; however, many aspects of the mechanisms that read the information encoded by DNA methylation and mediate this into downstream regulation remain uncertain, although some candidate proteins have been identified. DNA methylation has a vital role in the inactivation of transposons, suggesting that DNA methylation is a key factor in the evolution and adaptation of plants.