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.

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Figure 1: Flowchart for identification of miRNA foldbacks and endogenous small RNA loci with properties that are consistent with derivation by inverted duplication from protein coding genes.
Figure 2: Computational analysis of miRNA and endogenous small RNA–generating foldback sequences.
Figure 3: Genomic regions corresponding to A. thaliana MIR161, MIR163 and the small RNA–generating locus ASRP1729.
Figure 4: Similarity between foldback arms and protein-coding genes.
Figure 5: Biogenesis and function of A. thaliana miR161, miR163 and ASRP1729.
Figure 6: Phylogenetic analysis of MIR161 and MIR163 foldback arms and target families and of ASRP1729 foldback arms and DC1 domain–containing genes.
Figure 7: Inverted duplication model for miRNA gene evolution in plants.

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Acknowledgements

We thank S. Givan, D. Smith and C. Sullivan for assistance and advice with computational resources; L. Johansen for initial propagation of the rdr6-15 mutant; and S. Poethig and H. Vaucheret for discussions about trans-acting siRNAs and the suggestion to analyze miR161 in multiple dcl1 mutated alleles. This work was supported by grants from the US National Science Foundation, the US National Institutes of Health and the United States Department of Agriculture.

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Correspondence to James C Carrington.

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Supplementary information

Supplementary Fig. 1

Predicted foldback structures for small RNA generating loci containing inverted repeats with similarity to protein coding genes. (PDF 48 kb)

Supplementary Table 1

MIRNA genes and small RNA-generating loci used for FASTA searches presented in Figure 2. (XLS 39 kb)

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Allen, E., Xie, Z., Gustafson, A. et al. Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet 36, 1282–1290 (2004). https://doi.org/10.1038/ng1478

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