Vive la différence: biogenesis and evolution of microRNAs in plants and animals

Abstract

MicroRNAs are pervasive in both plants and animals, but many aspects of their biogenesis, function and evolution differ. We reveal how these differences contribute to characteristic features of microRNA evolution in the two kingdoms.

Global characterization of the Dicer-like protein DrnB roles in miRNA biogenesis in the social amoeba Dictyostelium discoideum

“…Poly-T tracts immediately upstream of TSSs is a common feature for protein coding genes in D. discoideum [51], indicating that also D. discoideum pri-miRNAs are transcribed by RNA pol II. This idea is also supported by a previous study by Kruse et al ., who showed reduction of mir-1176 and mir-1177 upon treatment with α-amanitin [30] and is in agreement with the situation in animals and plants where most pri-miRNAs are transcribed by RNA Pol II [4–6]. Furthermore, mammalian RNA Pol II transcripts preferentially start with a purine preceded by a pyrimidine [53,62], which complies with the T and G at position −1 and +1, respectively, seen for the pri-miRNA associated motif in D. discoideum .…”

“…This strongly suggests that DrnB is dedicated to miRNA production and that the other Dicer-like protein DrnA, present in D. discoideum [48], is required for generating siRNAs. Similar division of functionality between Dicer/Dicer-like proteins is also seen in other organisms such as plants and the two Dicers present in Drosophila where Dicer-1 and Dicer-2 are devoted to miRNA and siRNA maturation, respectively [6,57,58]. However, in the single cell alga C. reinhardtii , one of the three Dicer homologs, DCL-3 is required for both miRNA and siRNA maturation, a situation similar to mammals and worms where a single Dicer protein produce both classes of small RNAs [31,57].…”

“…The origin of miRNA pathways have been discussed many times and the prevailing belief is that miRNAs evolved independently several times during the course of evolution although this idea of convergent evolution has recently been challenged [6,27,70,71]. The phylogenetic position of D. discoideum within the Amoebozoa supergroup, which branched off after plants (Archaeplastida) but before animals (Opisthokonta) [72], gives us glimpses into the evolution of the miRNA machinery.…”

“…Although there are many similarities between miRNA biogenesis and function in plants and animals, there are also distinct differences [6]. In plants, miRNA loci are most often intergenic while in animals, miRNA commonly derive from introns of protein coding genes or long noncoding (lnc)RNAs [7–9].…”

Hitting two birds with one stone: The unforeseen consequences of nested gene knockouts inCaenorhabditis elegans

“…14 The most widely studied ncRNAs, the microRNAs (miRNAs), are particularly abundant in nested arrangements with »30% of plant and animal miRNAs located in introns of protein coding genes. 15 Nested structures pose a challenge for gene knockout studies in which the nested gene may be mistakenly altered along with the focal host gene (or vice versa), making it difficult to ascribe an eventual phenotype to a single gene product. This idea was put into sharp relief by the analysis of gene traps in mouse and the finding that »200 miRNAs may have concomitantly been misregulated.…”