MicroRNA Gene Evolution in Arabidopsis lyrata and Arabidopsis thaliana    

Abstract

MicroRNAs (miRNAs) are short regulatory RNAs processed from partially self-complementary foldbacks within longer MIRNA primary transcripts. Several MIRNA families are conserved deeply through land plants, but many are present only in closely related species or are species specific. The finding of numerous evolutionarily young MIRNA, many with low expression and few if any targets, supports a rapid birth-death model for MIRNA evolution. A systematic analysis of MIRNA genes and families in the close relatives, Arabidopsis thaliana and Arabidopsis lyrata, was conducted using both wholegenome comparisons and high-throughput sequencing of small RNAs. Orthologs of 143 A. thaliana MIRNA genes were identified in A. lyrata, with nine having significant sequence or processing changes that likely alter function. In addition, at least 13% of MIRNA genes in each species are unique, despite their relatively recent speciation (;10 million years ago). Alignment of MIRNA foldbacks to the Arabidopsis genomes revealed evidence for recent origins of 32 families by inverted or direct duplication of mostly protein-coding gene sequences, but less than half of these yield miRNA that are predicted to target transcripts from the originating gene family. miRNA nucleotide divergence between A. lyrata and A. thaliana orthologs was higher for young MIRNA genes, consistent with reduced purifying selection compared with deeply conserved MIRNA genes. Additionally, target sites of younger miRNA were lost more frequently than for deeply conserved families. In summary, our systematic analyses emphasize the dynamic nature of the MIRNA complement of plant genomes.

Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs

“…In addition, the low overlap between our identified miRNA sequences and the sequences present in miRBase version 19 suggests that most miRNA sequences are species specific, which is in line with our observation that the majority of miRNA sequences are present in a single species (Fig. 8b), and consistent both with previous reports 3,5,39 , and with the observation that even the closely related species A. thaliana and A. lyrata have each specific miRNAs 6 .…”

“…Functionally, plant miRNAs are involved in many fundamental biological processes, and their conservation across the plant kingdom suggests that these molecules have been active in the regulation of gene expression and have played key roles in plant developmental processes since the earliest stages of their evolution 8,9 . Nevertheless, the majority of miRNA sequences are only present in one to a few species 3,[10][11][12] , and a comparison between Arabidopsis thaliana and A. lyrata shows that even closely related species do not have highly overlapping miRNomes 6 . This suggests that many miRNA loci have emerged recently, and that miRNA loci in plant genomes are in a constant dynamic evolutionary state 6,11,12 .…”

“…Nevertheless, the majority of miRNA sequences are only present in one to a few species 3,[10][11][12] , and a comparison between Arabidopsis thaliana and A. lyrata shows that even closely related species do not have highly overlapping miRNomes 6 . This suggests that many miRNA loci have emerged recently, and that miRNA loci in plant genomes are in a constant dynamic evolutionary state 6,11,12 .…”

“…Studies of plant miRNAs have historically focused on sequence conservation and, more recently, miRNA loci sequence variability across species 5,6 . Several of these studies have shown that only a small number of miRNA families are present across phylogenetically distant species 3,5 .…”

microRNAs in a multicellular green alga Volvox carteri

“…Mature Vca-miR94 and Cre-miR1167 are both located in the 5′ arm of the precursors ( Figure 5B). In plants, the precursors of orthologous miRNAs and their flanking sequences are very often located in relatively collinear regions with little rearrangement [21]. We thus plotted the alignments of genomic sequences (~40 kb) surrounding the Vca-miR94 and Cre-miR1167 to evaluate the conservation and divergence in the two species ( Figure 5C).…”