The evolution of microRNAs in plants

Abstract

MicroRNAs (miRNAs) are a central player in post-transcriptional regulation of gene expression and are involved in numerous biological processes in eukaryotes. Knowledge of the origins and divergence of miRNAs paves the way for a better understanding of the complexity of the regulatory networks that they participate in. The biogenesis, degradation, and regulatory activities of miRNAs are relatively better understood, but the evolutionary history of miRNAs still needs more exploration. Inverted duplication of target genes, random hairpin sequences and small transposable elements constitute three main models that explain the origination of miRNA genes (MIR). Both inter-species and intra-species divergence of miRNAs exhibits functional adaptation and adaptation to changing environments in evolution. Here we summarize recent progress in studies on the evolution of MIR and related genes.

Figure 1. miRNA families identified in selected plant species

(A) miRNA family distribution in selected plant species. Data are from miRBase v21 and [–24,42,49]. The selected species are basal land plants Physcomitrella patens, Marchantia polymorpha and Pellia endiviifolia, the basal vascular plant Selaginella moellendorffii, the basal angiosperm Amborella trichopoda, monocots Brachypodium distachyum, Oryza sativa and Zea mays, and eudicots Glycine max, Phaseolus vulgaris, Populus trichocarpa, Moringa oleifera, Brassica rapa, Capsella rubella, Arabidopsis lyrata, and Arabidopsis thaliana. Only 78 miRNA families are found in more than 4 species, most miRNA families are present in a smaller number of species. (B, C) Venn diagrams for shared miRNA families in closely related species in Brassicaceae (B) and Poaceae (C). The data sources are the same as those in (A). The number of shared miRNA families in closely related species is smaller than that of species-specific ones, indicating rapid and independent origination of miRNA families.

Figure 2. Origins of plant MIR genes

Three models that explain the de novo origination of miRNAs. (A) MIR genes stem from inverted duplication of target genes. The transcription of inverted duplicated founder genes leads to the emergence of proto MIRs. Proto MIRs often exhibit a long stem-loop structure fitting for the processing by DCL3 and DCL4 to generate siRNAs to suppress target gene expression. Shortening and mutations occur to the inverted repeats during evolution, resulting in the formation of pre-miRNA-like hairpins, which are compatible with processing by DCL1 to generate mature miRNAs. The transcript of the founder gene serves as the target of the mature miRNA. Red spots on the transcript indicate mutations that also accumulate when the founder gene evolves. Occasionally, the target of the miRNA is not the founder gene, which implies divergence in the course of evolution. (B) Small random inverted sequences scattered in the genome provide a source of MIR genes. First, the random inverted repeats obtain a promoter element to enable transcription; then mutations and selections occur during evolution to form the precursor of a miRNA. (C) MITEs contribute to the origination of miRNAs. MITEs, a type of non-autonomous transposons, are composed of terminal inverted repeats (TIRs) and a short open reading frame (ORF), and are roughly 100~500bp in size. MITEs may serve as templates to produce miRNA precursors.