Abstract
BackgroundMicroRNAs (miRNAs) posttranscriptionally down-regulate gene expression by binding target mRNAs. Analysis of the evolution of miRNA binding sites is helpful in understanding the co-evolution between miRNAs and their targets. To understand this process in plants a comparative analysis of miRNA-targeted duplicated gene pairs derived from a well-documented whole genome duplication (WGD) event in combination with a population genetics study of six experimentally validated miRNA binding sites in rice (O. sativa) was carried out.ResultsOf the 1,331 pairs of duplicate genes from the WGD, 41 genes (29 pairs) were computationally predicted to be miRNA targets. Sequence substitution analysis indicated that the synonymous substitution rate was significantly lower in the miRNA binding sites than their 5' and 3' flanking regions. Of the 29 duplicated gene pairs, 17 have only one paralog been targeted by a miRNA. This could be due to either gain of a miRNA binding site after the WGD or because one of the duplicated genes has escaped from being a miRNA target after the WGD (loss of miRNA binding site). These possibilities were distinguished by separating miRNAs conserved in both dicots and monocot plants from rice-specific miRNAs and by phylogenetic analysis of miRNA target gene families. The gain/loss rate of miRNA binding sites was estimated to be 3.0 × 10-9 gain/loss per year. Most (70.6%) of the gains/losses were due to nucleotide mutation. By analysis of cultivated (O. sativa; n = 30) and wild (O. rufipogon; n = 15) rice populations, no segregating site was observed in six miRNA binding sites whereas 0.12–0.20 SNPs per 21-nt or 1.53–1.80 × 10-3 of the average pairwise nucleotide diversity (π) were found in their flanking regions.ConclusionBoth molecular evolution and population genetics support the hypothesis that conservation of miRNA binding sites is maintained by purifying selection through elimination of deleterious alleles. Nucleotide mutations play a major role in the gain/loss of miRNA binding sites during evolution.
Highlights
IntroductionMicroRNAs (miRNAs) posttranscriptionally down-regulate gene expression by binding target mRNAs
MicroRNAs posttranscriptionally down-regulate gene expression by binding target mRNAs
Prediction of miRNA targets located on whole genome duplication (WGD) genes At least nine duplicated blocks from an ancient WGD with retained syntenic duplicate gene copies have been reported [16,17,18,19,20]
Summary
MicroRNAs (miRNAs) posttranscriptionally down-regulate gene expression by binding target mRNAs. The basis of the estimation of selective constraint is the comparison of the relative divergence of putatively constrained segments of the genome with that of linked, putatively neutrally evolving sequences. It is assumed that homologous segments that show significant similarity are under strong selective constraints, while other sequences lacking similarity are evolving free from selective constraints. Based on this assumption, several methods for estimation of selective constraint have been proposed and applied to the coding and non-coding DNAs in invertebrates and mammals By comparing recent segmentally duplicated genes we found that strong purifying selection applies to non-coding sequences in rice [12]. Analysis of the distribution of fitness effects on new mutations in the conserved non-coding sequences in mammals has revealed weak purifying selection [15], whereas in humans, purifying selection is stronger in the conserved miRNA binding sites than in other conserved sequence motifs in the 3' UTRs [13]
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