miRNA-like secondary structures in maize (Zea mays) genes and transposable elements correlate with small RNAs, methylation, and expression

Abstract

RNA molecules carry information in their primary sequence and also their secondary structure. Secondary structure can confer important functional information, but it is also a signal for an RNAi-like host epigenetic response mediated by small RNAs (smRNAs). In this study, we used two bioinformatic methods to predict local secondary structures across features of the maize genome, focusing on small regions that had similar folding properties to pre-miRNA loci. We found miRNA-like secondary structures to be common in genes and most, but not all, superfamilies of RNA and DNA transposable elements (TEs). The miRNA-like regions map to a higher diversity of smRNAs than regions without miRNA-like structure, explaining up to 27% of variation in smRNA mapping for some TE superfamilies. This mapping bias is more pronounced among putatively autonomous TEs relative to nonautonomous TEs. Genome-wide, miRNA-like regions are also associated with elevated methylation levels, particularly in the CHH context. Among genes, those with miRNA-like secondary structure are 1.5-fold more highly expressed, on average, than other genes. However, these genes are also more variably expressed across the 26 nested association mapping founder lines, and this variability positively correlates with the number of mapping smRNAs. We conclude that local miRNA-like structures are a nearly ubiquitous feature of expressed regions of the maize genome, that they correlate with higher smRNA mapping and methylation, and that they may represent a trade-off between functional requirements and the potentially negative consequences of smRNA production.