Miniature inverted-repeat transposable elements drive rapid microRNA diversification in angiosperms

MicroRNAs (miRNAs) are rapidly evolving endogenous small RNAs programing organism function and behavior. Although models for miRNA origination have been proposed based on sporadic cases, the genomic mechanisms driving swift diversification of the miRNA repertoires in plants remain elusive. Here, by comprehensively analyzing 20 phylogenetically representative plant species, we identified miniature inverted-repeat transposable elements (MITEs) as the predominant genomic sources for de novo miRNAs in angiosperms. Our data illustrated a transposition-transcription process whereby properly sized MITEs transposed into active genic regions could be converted into new miRNAs, termed MITE-miRNAs, in as few as 20 generations. We showed that this molecular domestication mechanism leads to a possible evolutionary arms race between the MITEs and the host genomes that rapidly and continuously changes the miRNA repertoires. We found that the MITE-miRNAs are selected for targeting genes associated with plant adaptation and habitat expansion, thereby constituting a genomic innovation potentially underlying angiosperm megadiversity.