Ovule siRNAs methylate protein-coding genes in trans

Abstract

Twenty-four-nt small interfering RNAs (siRNAs) maintain asymmetric DNA methylation at thousands of euchromatic transposable elements in plant genomes in a process called RNA-directed DNA methylation (RdDM). RdDM is dispensable for growth and development in Arabidopsis thaliana, but is required for reproduction in other plants, such as Brassica rapa. The 24-nt siRNAs are abundant in maternal reproductive tissue, due largely to overwhelming expression from a few loci in the ovule and developing seed coat, termed siren loci. A recent study showed that 24-nt siRNAs produced in the anther tapetal tissue can methylate male meiocyte genes in trans. Here we show that in B. rapa, a similar process takes place in female tissue. siRNAs are produced from gene fragments embedded in some siren loci, and these siRNAs can trigger methylation in trans at related protein-coding genes. This trans-methylation is associated with silencing of some target genes and may be responsible for seed abortion in RdDM mutants. Furthermore, we demonstrate that a consensus sequence in at least two families of DNA transposons is associated with abundant siren expression, most likely through recruitment of CLASSY3, a putative chromatin remodeller. This research describes a mechanism whereby RdDM influences gene expression and sheds light on the role of RdDM during plant reproduction.

Shaping inheritance: how distinct reproductive strategies influence DNA methylation memory in plants

“…Notably, most of these TEs gain CHH methylation during embryo development [6,18,25] in association with increased siRNAs levels in seeds [6,26]. Similar methylation dynamics were observed in soybean, chickpea, and rice [18,24,27], suggesting that incremental RdDM activity during embryogenesis likely evolved before the radiation of flowering plants.…”

A null allele of the pol IV second subunit impacts stature and reproductive development in Oryza sativa

“…There was a good correlation between wild‐type sRNA accumulation in leaf and seedling tissues (Figure 2a). Because there is 24‐nt siRNA depletion in both nrpd2 and nrpd1 mutants, we wanted to understand if this loss was distributed across many genomic loci, or if it came from a small subset of abundantly expressed loci (Burgess et al., 2021). To examine this, we assessed sRNA accumulation in 300‐bp windows.…”

The Rise and Fall of Billionaire siRNAs during Reproductive Development in Rice

“…Although bill-siRNAs may have little effect on gene expression of the bill-siRNA cluster-adjacent genes, our results indicate that they have a significant role in DNA methylation and that they may have important roles in tissue development. According to recent research, highly expressed siRNAs in ovary [ 18 ] and tapetum cells [ 19 ] might function in directing DNA methylation in trans. The mechanisms and functions of bill-siRNAs warrant further research.…”