Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana

Abstract

MicroRNAs (miRNAs) in plants and animals function as post-transcriptional regulators of target genes, many of which are involved in multicellular development. miRNAs guide effector complexes to target mRNAs through base-pair complementarity, facilitating site-specific cleavage or translational repression. Biogenesis of miRNAs involves nucleolytic processing of a precursor transcript with extensive foldback structure. Here, we provide evidence that genes encoding miRNAs in plants originated by inverted duplication of target gene sequences. Several recently evolved genes encoding miRNAs in Arabidopsis thaliana and other small RNA-generating loci possess the hallmarks of inverted duplication events that formed the arms on each side of their respective foldback precursors. We propose a model for miRNA evolution that suggests a mechanism for de novo generation of new miRNA genes with unique target specificities.

Evolution of plant microRNA gene families

“…The special stem-loop structure and the functional mode by which miRNAs pair with their target genes support the hypothesis that the de novo generation of miRNA genes was related to their target genes [40]. In spite of this, cases of similarities between miRNAs and their target genes remain rare and have only been observed in the non-conserved miRNA genes, such as the Arabidopsis miR161 and miR163.…”

“…Significant similarity to their target genes was found at the regions outside the mature miRNA and its pairing sequence (miRNA*) of these two genes. A putative mechanism was put forward for the arising and evolution of miRNA genes with unique target specificities [40]. The hypothesis proposed that head-to-head or tail-to-tail gene configuration was generated by inverted gene duplication events from one founder gene with or without the founder gene's promoter.…”

On the origin and functions of RNA-mediated silencing: from protists to man

“…In addition, the regulation of gene expression by miRNAs may be a relatively easy innovation, particularly when triggering transcript cleavage as in plants. As recently proposed (Allen et al 2004;Smalheiser and Torvik 2005), at least some miRNA genes may arise from inverted duplications of target gene sequences and the initially produced double stranded foldback transcripts may operate as regulators via the degradative RNAi pathway. Progressive sequence degradation, under selective pressure, may eventually result in the bulged structure typical of miRNA precursors.…”

Fine tuning of auxin signaling by miRNAs

“…A majority of the conserved plant miRNA targets constitute the transcripts of crucial transcription factors or other regulatory proteins that play an important role in basic organogenesis or signal transduction, (Allen et al, 2004;Bartel, 2004;Jones-Rhoades et al, 2004;Mallory et al, 2004b;Kidner and Martienssen, 2005). In addition, non-conserved miRNAs may function in the specialized processes like biosynthesis of cell wall metabolites (Lu et al, 2005) or cotton fiber development .…”