MicroRNAs and the advent of vertebrate morphological complexity

Abstract

The causal basis of vertebrate complexity has been sought in genome duplication events (GDEs) that occurred during the emergence of vertebrates, but evidence beyond coincidence is wanting. MicroRNAs (miRNAs) have recently been identified as a viable causal factor in increasing organismal complexity through the action of these Ϸ22-nt noncoding RNAs in regulating gene expression. Because miRNAs are continuously being added to animalian genomes, and, once integrated into a gene regulatory network, are strongly conserved in primary sequence and rarely secondarily lost, their evolutionary history can be accurately reconstructed. Here, using a combination of Northern analyses and genomic searches, we show that 41 miRNA families evolved at the base of Vertebrata, as they are found and/or detected in lamprey, but not in either ascidians or amphioxus (or any other nonchordate taxon). When placed into temporal context, the rate of miRNA acquisition and the extent of phenotypic evolution are anomalously high early in vertebrate history, far outstripping any other episode in chordate evolution. The genomic position of miRNA paralogues in humans, together with gene trees incorporating lamprey orthologues, indicates that although GDEs can account for an increase in the diversity of miRNA family members, which occurred before the last common ancestor of all living vertebrates, GDEs cannot account for the origin of these novel families themselves. We hypothesize that lying behind the origin of vertebrate complexity is the dramatic expansion of the noncoding RNA inventory including miRNAs, rather than an increase in the protein-encoding inventory caused by GDEs.genome duplication ͉ lamprey ͉ macroevolution ͉ shark ͉ chordate

Additional molecular support for the new chordate phylogeny

“…Rare genomic changes have also provided some evidence in its favor: the domain structure of cadherins (Oda et al, 2002), a unique amino-acid insertion in fibrillar collagen (Wada et al, 2006), and the distribution of micro RNAs (miRNAs) (Heimberg et al, 2008). Finally, the Branchiostoma floridae genome helps confirming the sistergroup relationship between tunicates and vertebrates in offering additional evidence from analyses of intron dynamics (Putnam et al, 2008).…”

“…The comparison of miRNA repertoires in metazoans has also recently unearthed some potential signatures for the sister-group relationship of tunicates and vertebrates (Heimberg et al, 2008). miRNAs are small noncoding RNAs involved in regulation of gene expression in eukaryotes and play an important role in the development of metazoans.…”

Systematic analysis of human microRNA divergence based on evolutionary emergence

“…1B and Table 1), and found that major expansions of the new human miRNA family emergence also coincides with the advent of vertebrates, mammals and primates. Heimberg et al [8] found that a greatly expanded set of miRNAs have occurred in vertebrates as compared with bilaterian invertebrates and also identified 41 miRNA families evolved at the base of vertebrate. However, in our study, we revealed 72 miRNA families emerged from the vertebrate lineages, and further found that the number of the new human miRNA family reached a peak in the mammalian lineage.…”

“…The phylogenetic distribution and evolution of animal and plant miRNAs have been studied in recent reports [2][3][4][5][6][7][8][9][10][11][12]. In animals, the expansion of miRNAs is an ongoing process [5].…”

Diversity, evolution, and therapeutic applications of small RNAs in prokaryotic and eukaryotic immune systems

“…Other ways that new miRNAs can arise include the modification or duplication of pre-existing miRNAs [108]. A rapid increase in the diversity of miRNAs in existing genomes is often correlated to a burst of new morphological diversity, and thus miRNA may be crucial to the development of complex morphologies because of its regulatory activity [71,110,134].…”