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New transposon insertions are deleterious to genome stability. The RNA-directed DNA methylation (RdDM) pathway evolved to regulate transposon activity via DNA methylation. However, current studies have not yet clearly described the transposition regulation. ONSEN is a heat-activated retrotransposon that is activated at 37°C. The plant-specific SUPPRESSOR OF VARIEGATION 3–9 HOMOLOG (SUVH) family proteins function downstream of the RdDM pathway. The SUVH protein families are linked to TE silencing by two pathways, one through DNA methylation and the other through chromatin remodeling. In this study, we analyzed the regulation of ONSEN activity by SUVH2. We observed that ONSEN transcripts were increased; however, there was no transpositional activity in Arabidopsis suvh2 mutant. The suvh2 mutant produced siRNAs from the ONSEN locus under heat stress, suggesting that siRNAs are involved in suppressing transposition. These results provide new insights into the regulatory mechanisms of retrotransposons that involve siRNA in the RdDM pathway.

The RNA-directed DNA methylation (RdDM) pathway plays an essential role in the transposon silencing mechanism; the DDR complex, consisting of DRD1, DMS3, and RDM1, is an essential component of the RdDM pathway. ONSEN, identified in Arabidopsis, is a retrotransposon activated by heat stress at 37°C; however, studies on the regulation of ONSEN are limited. In this study, we analyzed the regulation of ONSEN activity by the DDR complex in Arabidopsis. We elucidated that loss of any component of the DDR complex increased ONSEN transcript levels. Transgenerational transposition of ONSEN was observed in the DDR-complex mutants treated with heat stress for 48 h. Furthermore, the DDR complex components DRD1, DMS3, and RDM1 played independent roles in suppressing ONSEN transcription and transposition. Moreover, we found that the duration of heat stress affects ONSEN activity. Therefore, the results of this study provide new insights into the retrotransposon regulatory mechanisms of the DDR complex in the RdDM pathway.

Transposable elements are present in a wide variety of organisms; however, our understanding of the diversity of mechanisms involved in their activation is incomplete. In this study, we analyzed the transcriptional activation of the ONSEN retrotransposon, which is activated by high-temperature stress in Arabidopsis thaliana. We found that its transcription is significantly higher in the Japanese ecotype Kyoto. Considering that transposons are epigenetically regulated, DNA methylation levels were analyzed, revealing that CHH methylation was reduced in Kyoto compared to the standard ecotype, Col-0. A mutation was also detected in the Kyoto CMT2 gene, encoding a CHH methyltransferase, suggesting that it may be responsible for increased expression of ONSEN. CHH methylation is controlled by histone modifications through a self-reinforcing loop between DNA methyltransferase and histone methyltransferase. Analysis of these modifications revealed that the level of H3K9me2, a repressive histone marker for gene expression, was lower in Kyoto than in Col-0. The level of another repressive histone marker, H3K27me1, was decreased in Kyoto; however, it was not impacted in a Col-0 cmt2 mutant. Therefore, in addition to the CMT2 mutation, other factors may reduce repressive histone modifications in Kyoto.