In the mutant of Decreased DNA methylation 1 (DDM1), a gene encoding ATP-dependent chromatin remodeler in Arabidopsis, global DNA methylation level is dramatically reduced, thereby numerous TEs are reactivated (Vongs et al., 1993; Creasey et al., 2014). A large fraction of those reactivated TEs are accompanied with the production of 21 or 22 nt-siRNAs, known as epigenetically activated siRNAs (easiRNAs) (Creasey et al., 2014). The easiRNAs target TE transcripts for cleavage ensuring the silencing of TEs at the post-transcriptional step. Interestingly, a subset of the easiRNAs in ddm1 mutants can interact with genic mRNAs reducing their expression levels. For example, siRNA854 is one of the easiRNAs generated in ddm1 mutant and produced from Athila6A TE. It targets 3′ UTR of UBP1 transcript which encodes a stress granule protein (Figure 1A; McCue et al., 2012). Using the multiple reporter gene constructs containing the 3′ UTR of UBP1, it was demonstrated that siRNA854 represses non-TE targets as well. The expression levels of Athila6A and siRNA854 are increasingly upregulated in multiple generations of ddm1 mutation. For example, the plants with ddm1 homozygous mutation for six generations (ddm1 F6) have higher levels of siRNA854 compared to ddm1 F2. The ubp1 mutants show strong susceptibility to osmotic stress and similar phenotype was also observed in ddm1 F6 but not in ddm1 F2 plants. Therefore, the targeting of Athila6A-derived siRNA854 to UBP1 transcript and alteration of resistance to abiotic stresses provides insight into how TEs adapted to changing environment in plants. In addition to UBP1, Athila6A-derived easiRNAs can target other genic mRNAs including AMS and HHP2 (McCue et al., 2013). Several of those targets were experimentally validated for the easiRNA-mediated repression by the short tandem target mimic (STTM) transgenic approach, however, the biological relevance of this regulation is yet to be answered.

A more recent paper by Zhang et al. (2016) suggested that TE-siRNA815 in rice can induce de novo DNA methylation in the target gene loci through RdDM pathway (Figure 1A). Two allelic transcription factor genes, WRKY45-1 and WRKY45-2, were previously shown to have opposing effects in the resistance to Xanthomonas oryzae pv. oryzae (Xoo). WRKY45-1 allele produces TE-siRNA815 from WANDERER_OS-type DNA TE located in the intron. TE-siRNA815 then recognizes the complementary sequence and deposits DNA methylation through RdDM pathway in the intron of ST1 locus, which is critical in the resistance against Xoo. On the other hand, WRKY45-2 allele lacks such siRNA producing region that ensures stable ST1 expression contributing to the pathogen resistance.

Since easiRNAs are mainly produced in the epigenetic mutants, it has been questioned if easiRNAs have a function in natural conditions. Two recent studies answered this question by demonstrating the roles of easiRNAs in the hybridization barrier in Arabidopsis (Borges et al., 2018; Martinez et al., 2018). The vegetative nuclei of pollen grains have reduced activity of DDM1 and numerous TEs are reactivated (Slotkin et al., 2009). Pollen-specific miRNA845b recognizes the conserved sequence [primer-binding site (PBS)] in the LTR retrotransposons activated in pollen and triggers the initial cleavage of LTR-TE mRNAs followed by the production of easiRNAs (Borges et al., 2018). Higher dosage of the paternal genome brings higher amount of easiRNAs in fertilization which gives rise to the unbalanced gametic siRNAs and ultimately seed failure (triploid block, Martinez et al., 2018). When the paternal easiRNA levels were suppressed by poliv mutation, the triploid blockage phenotype was partly restored, indicating a critical role of the paternal easiRNAs in the hybridization barrier (Martinez et al., 2018). The exact mechanism for the easiRNA-mediated triploid block is still unclear, however, it was suggested that the excess paternal easiRNAs might interfere with DNA methylation establishment around the paternally expressed imprinted genes by hijacking PolV-transcribed nascent transcripts (Figure 1A).

Transposable elements have often domesticated to miRNA genes in plants (Li et al., 2011). One example is miRNA820 of rice. miRNA820 is 22 or 24 nt in size and is originated from the internal region of CACTA DNA TE (Nosaka et al., 2012). Interestingly, miRNA820 targets the transcripts of DRM2 that encodes a de novo DNA methyltransferase (Figure 1A). The targeting of miRNA820 to DRM2 is evolutionarily conserved in the Oryza genus and the repression of DRM2 gene results in strong reduction in DNA methylation and transcriptional upregulation of many TEs. Therefore, miRNA820 can be seen as an anti-silencing factor encoded within a TE that works at the post-transcriptional level. Similarly, UBP1 is the Arabidopsis homolog of TIA-1 in mammals which is known to suppress the viral translation of Tick-Borne Encephalitis Virus (Albornoz et al., 2014). McCue et al. (2013) have also shown that UBP1 protein forms the cytoplasmic stress granules in abiotic stress condition or when heterochromatic TE silencing is released, for instance in ddm1 mutant. As is the case in mammals that TIA-1 inhibits the viral translation, the level of GAG protein encoded in Athila6A was elevated in ddm1 rdr6 ubp1 triple mutants (McCue et al., 2013). This data supports the notion that UBP1 acts on the activated TE mRNAs to suppress their translation and therefore TE-siRNAs are the repressors of the host TE silencing mechanism.

Since many TEs in plants possess stress-responsive cis-acting elements within them (Paszkowski, 2015), TE-lncRNAs often appear in specific stress conditions (Liu et al., 2012; Quattro et al., 2017; Wang et al., 2017). In a recent report, Wang et al. (2017) interrogated the lncRNAs in Arabidopsis, rice and maize under various abiotic stresses. There was a large discrepancy in TE families that TE-lncRNAs are originated from; RC/Helitron in Arabidopsis, MITEs in rice and LTR retrotransposons in maize were predominantly overrepresented in TE-lncRNAs (Wang et al., 2017). Particularly, TE-lncRNA11195 in Arabidopsis contains an LTR-type retrotransposon and is activated after abiotic stresses or ABA treatment. The deletion of the LTR sequence compromised the ABA responsiveness, suggesting that LTR sequence conferred the stress responsiveness to TE-lncRNA11195 (Wang et al., 2017). TE-lncRNA11195 was tested for its role in stress response using T-DNA insertional mutants. Interestingly, two independent mutant lines showed marked increase in resistance to abscisic acid (ABA) in root elongation and shoot fresh weight (Wang et al., 2017). TE-lncRNAs in tomato were also described to be responsive for both abiotic and biotic stresses (Wang et al., 2015), however, the biological function has not been investigated as yet.

In mammals, the majority of lncRNAs are derived from TEs and exhibit strong tissue-specific expression pattern (Kelley and Rinn, 2012; Kapusta et al., 2013). Similarly, TE activation in plants is associated with specific development stages potentiating the emergence of tissue-specific TE-lncRNA (Hsieh et al., 2009; Slotkin et al., 2009; Baubec et al., 2014; Cho and Paszkowski, 2017). Recently, Cho and Paszkowski (2017) have investigated the expression pattern of TEs in various rice tissues and identified a retrotransposon-derived transcript called MIKKI which is specifically transcribed in rice roots. MIKKI contains multiple introns and has low coding potential, which is a strong sign of domestication to lncRNA. Intriguingly, the fourth intron of MIKKI is derived from an independent family of retrotransposon and the splicing of this intron generates a binding site for miR171 in the exon–exon junction. Despite the miR171-binding sequence, MIKKI mRNAs are not cleaved by miR171. The miR171-binding site of MIKKI does not perfectly base-pair with its cognate miRNA but has two mismatches at the positions where the cleavage is supposed to occur. It is very well-known that mismatches in the cleavage positions attenuate the cleavage activity of miRNA and is regarded as the signature of miRNA target mimic (Franco-Zorrilla et al., 2007; Yan et al., 2012; Reichel et al., 2015). Indeed, the knock-out mutants of MIKKI that had lost the target mimicking sequence showed higher levels of miR171, while overexpression of MIKKI resulted in the downregulation of miR171. miR171 targets the mRNAs encoding SCARECROW-Like (SCL) transcription factors which are critical regulators of root development (Wang et al., 2010). Therefore, MIKKI evolved from retrotransposons in rice and was positively selected to suppress miR171 in root. This in turn stabilizes the mRNAs of SCLs which are essential in the root development. Similarly, Quattro et al., 2017 also identified multiple TE-derived lncRNAs from Brachypodium genome that are able to interact with miRNAs, however, their target mimicry activities are yet to be confirmed.