Nurse cell-derived small RNAs define paternal epigenetic inheritance inArabidopsis

Abstract

The plant male germline undergoes DNA methylation reprogramming, which methylates genes de novo and thereby alters gene expression and facilitates meiosis. Why reprogramming is limited to the germline and how specific genes are chosen is unknown. Here, we demonstrate that genic methylation in the male germline, from meiocytes to sperm, is established by germline-specific siRNAs transcribed from transposons with imperfect sequence homology. These siRNAs are synthesized by meiocyte nurse cells (tapetum) via activity of the tapetum-specific chromatin remodeler CLASSY3. Remarkably, tapetal siRNAs govern germline methylation throughout the genome, including the inherited methylation patterns in sperm. Finally, we demonstrate that these nurse cell-derived siRNAs (niRNAs) silence germline transposons, thereby safeguarding genome integrity. Our results reveal that tapetal niRNAs are sufficient to reconstitute germline methylation patterns and drive extensive, functional methylation reprogramming analogous to piRNA-mediated reprogramming in animal germlines.

Ovule siRNAs methylate protein-coding genes in trans

“…Siren-like loci that produce highly abundant 24-nt siRNAs were recently described in Arabidopsis tapetum, somatic cells surrounding the male germline (Long et al, 2021). It is not reported whether these loci carry gene fragments, however siRNAs produced from these sites function in trans to trigger methylation and silencing of protein coding transcripts.…”

“…However, exogenous 24-nt siRNAs are capable of triggering DNA methylation and transcriptional silencing with up to 2 mismatches between the siRNA and target locus (Fei et al, 2021), indicating that Pol IV-derived siRNAs might also function in trans. Widespread “surveillance” transcription by Pol V (Tsuzuki et al, 2020) suggests that much of the genome may be poised for trans -acting siRNAs and it was recently demonstrated that 24-nt siRNAs trans -methylate genes during pollen development (Long et al, 2021). However, the extent of trans -acting RdDM is not understood.…”

License to Regulate: Noncoding RNA Special Agents in Plant Meiosis and Reproduction

“…Interestingly, nearly 1,300 loci were found to be hypermethylated in Arabidopsis meiocytes when compared to somatic tissues, and this DNA methylation was shown to be RdDM dependent ( Walker et al, 2017 ). Hypermethylated loci occur not only in TEs (approximately 800 loci) but also in genes (nearly 500 loci; Long et al, 2021 ). In both cases, methylation is triggered by germline-specific 24-nt siRNAs, which are transcribed from TEs; however, genic methylation is established with imperfect sequence homology ( Long et al, 2021 ).…”

“…Hypermethylated loci occur not only in TEs (approximately 800 loci) but also in genes (nearly 500 loci; Long et al, 2021 ). In both cases, methylation is triggered by germline-specific 24-nt siRNAs, which are transcribed from TEs; however, genic methylation is established with imperfect sequence homology ( Long et al, 2021 ). These siRNAs are produced in tapetum cells (nurse cells for PMCs; hence called nurse cell-derived siRNAs, niRNAs) with the help of the generative tissue-specific chromatin remodeler CLASSY3 ( Zhou et al, 2021 ) and further transported to meiocytes via plasmodesmata ( Figure 1 ; Long et al, 2021 ).…”

“…The fact that tapetum-derived siRNAs arise from transposons and show only imperfect matches with genic sequences suggests that this type of regulation of meiotic gene expression evolved from the original RdDM task of preventing transposon expansion ( Long et al, 2021 ). Although classical RdDM in somatic cells is sufficient to silence most transposons in Arabidopsis, some groups of transposons, e.g., those from the Gypsy family, are expressed specifically in the germline ( Long et al, 2021 ). This explains why new targets of RdDM need to be established in meiocytes that establish germline lineages.…”