Evolution of microRNA genes in Oryza sativa and Arabidopsis thaliana: an update of the inverted duplication model

Abstract

The origin and evolution of microRNA (miRNA) genes, which are of significance in tuning and buffering gene expressions in a number of critical cellular processes, have long attracted evolutionary biologists. However, genome-wide perspectives on their origins, potential mechanisms of their de novo generation and subsequent evolution remain largely unsolved in flowering plants. Here, genome-wide analyses of Oryza sativa and Arabidopsis thaliana revealed apparently divergent patterns of miRNA gene origins. A large proportion of miRNA genes in O. sativa were TE-related and MITE-related miRNAs in particular, whereas the fraction of these miRNA genes much decreased in A. thaliana. Our results show that the majority of TE-related and pseudogene-related miRNA genes have originated through inverted duplication instead of segmental or tandem duplication events. Based on the presented findings, we hypothesize and illustrate the four likely molecular mechanisms to de novo generate novel miRNA genes from TEs and pseudogenes. Our rice genome analysis demonstrates that non-MITEs and MITEs mediated inverted duplications have played different roles in de novo generating miRNA genes. It is confirmed that the previously proposed inverted duplication model may give explanations for non-MITEs mediated duplication events. However, many other miRNA genes, known from the earlier proposed model, were rather arisen from MITE transpositions into target genes to yield binding sites. We further investigated evolutionary processes spawned from de novo generated to maturely-formed miRNA genes and their regulatory systems. We found that miRNAs increase the tunability of some gene regulatory systems with low gene copy numbers. The results also suggest that gene balance effects may have largely contributed to the evolution of miRNA regulatory systems.

Figure 1. Quantitative contributions of different miRNA gene origin modes in O. sativa and A. thaliana genomes.

Horizontal axis indicates origin modes of miRNA genes, TR represents TE-related, PR represents pseudogene-related, ID represents inverted duplication, TD represents tandem duplication, SD represents segmental duplication, and OT represents other miRNA genes could not fit any above-mentioned categories. Vertical axis indicates miRNA gene number. Mistyrose bars represent O. sativa specific miRNA genes. Red bars represent conserved miRNA genes (both present in O. sativa and A. thaliana) in O. sativa genome. Lightblue bars represent A. thaliana specific miRNA genes. Blue bars represent conserved miRNA genes (both present in O. sativa and A. thaliana) in A. thaliana genome.

Figure 2. Relationships among different origin modes of miRNA genes.

(A) and (B) are for O. sativa, while (C) and (D) are for A. thaliana. TR represents TE-related, PR represents pseudogene-related, ID represents inverted duplication, TD represents tandem duplication, and SD represents segmental duplication. (A) and (C) are intersection number of miRNA gene sets with different origin modes. Number in the center of each lattice represents intersection number of miRNA gene sets with different origin modes represented by vertical and horizontal axes, and number in parentheses is values of random state deduced from 100,000 Monte Carlo simulations. Lattice color represents P-value between real and simulation values, red lattice represents that real value is larger than simulation value, and blue lattice represents that real value is smaller than simulation value. (B) and (D) are classification accuracy of miRNA gene sets with different origin modes.

Figure 3. Schematic illustrations of the proposed de novo origin mechanisms of miRNA genes.

(A) Mechanism of miRNA gene de novo originated from non-MITE transposable element. (B) Mechanism of miRNA gene de novo originated from MITE. (C) Mechanism of miRNA gene de novo originated from pseudogenes arose from one parent gene. (D) Mechanism of miRNA gene do novo originated from pseudogenes arose from one parent gene and its paralogous gene.