Neural BC1 RNA as an evolutionary marker: guinea pig remains a rodent.

Abstract

The traditional morphologicaily grounded placement of South American guinea pig-like rodents (Caviomorpha) within one of the two rodent suborders, Hystricognathi, has been disputed by recent analysis of protein and nucleic acid sequence data. The Caviomorpha and possibly all Hystricognathi would be considered a separate order, distinct from the other rodent suborder, Sciurognathi, and thus of the order Rodentia, and would be placed closer phylogenetically to other mammals [Graur, D., Hide, W. A. & Li, W.-H. (1991) Nature (London) 351,[649][650][651][652]. To address the discrepancy between morphological comparisons and sequence analyses, we have applied an alternative form of molecular analysis. We demonstrate that BC1 RNA, a neural-specific small cytoplasmic RNA that is the product of a retropositionally generated gene (a gene derived by reverse transcription of RNA followed by insertion of the DNA copy into the genome), is present in Sciurognathi and guinea pig but not in other mammalian orders including Lagomorpha, Artiodactyla, and Primates.The species:confined, tissue-specific expression of a retroposed sequence therefore supports the morphological evidence for monophyly of Rodentia inclusive of guinea pig and demonstrates the usefulness of such molecular genetic markers. Furthermore, the conservation and tissue-specific expression of the BC1 RNA gene in the two divergent rodent suborders suggests that this macromolecule has been exapted into a functional role (i.e., coopted into a variant or novel function) in the rodent nervous system. Based on a large body of morphological evidence, the order Rodentia, containing approximately half of all mammalian species (1), has been subdivided into two suborders (2). The Sciurognathi include true rats, mice, hamsters, and squirrellike rodents, while the Hystricognathi, also representing a group of Old and New World rodent families, are now primarily restricted to Africa and South America. Examples of this diverse suborder include guinea pig, chinchilla, and porcupine. However, challenging this morphologically established phylogenetic scheme of Rodentia is an apparent "molecular paradox"-namely, most guinea pig protein and nucleic acid sequences exhibit an unusually high level of dissimilarity when compared with their rodent orthologues (refs. 3-5, but also see ref. 6).A recently proposed solution (7, 8) would define Caviomorpha and possibly the entire suborder Hystricognathi as a separate mammalian order distinct from Rodentia. Unfortunately, the proposal of a separate order addresses the molecular data but leads to incongruence with paleontological information and anatomical data (9). Thus, well-established morphological synapomorphies between Sciurognathi and Hystricognathi would be reinterpreted as homoplasies (10). Furthermore, the molecular evidence underlying this exThe publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to ...

Role of a neuronal small non-messenger RNA: behavioural alterations in BC1 RNA-deleted mice

“…This conclusion is in line with phylogenetic considerations that argue for an indispensable modulatory role of this RNA. The gene for BC1 RNA appeared comparatively late in evolution, probably not more than 110 million years ago [22,30]. It is nonetheless found in all rodents, with highly conserved spatiotemporal neuronal expression patterns and somatodendritic subcellular localisation [10,11,45].…”

“…It is nonetheless found in all rodents, with highly conserved spatiotemporal neuronal expression patterns and somatodendritic subcellular localisation [10,11,45]. Within the BC1 RNA gene, moreover, the RNA coding region-but not the flanking regions-exhibits a high degree of sequence similarity among rodent species ( [30], C. Raabe, B.V. Skryabin and J. Brosius, unpublished observations). Such sequence conservation implies that the BC1 RNA gene conveys a selective advantage.…”

The Persistent Contributions of RNA to Eukaryotic Gen(om)e Architecture and Cellular Function

“…Unfortunately, these claims did not stand the test of time (Owens et al 1985;Sapienza and St-Jacques 1986;Goldman et al 2014). 6 For sure, any seemingly insig-nificant novelty could have far-reaching consequences for future lineages (Martignetti and Brosius 1993;Kapitonov and Jurka 2005), but in their infancy, the functional significance, if not potential of novelties, is not easy to assess and often might be transitory. And what is true for regulatory elements and protein-coding genes and their exonic modules should also apply to functions of non-protein-coding RNAs.…”

“…Snora35 gene-depleted mice do not appear to display a phenotype different from their wild-type siblings, thus far (BV Skryabin and J Brosius, unpubl.). In another example of an RNA knockout, it took several years of work to tease out a reduced exploratory behavior in mice when small cytoplasmic BC1 RNA, phylogenetically restricted to rodents and expressed in neurons where it is delivered to dendritic processes, was deleted (Tiedge et al 1991;Martignetti and Brosius 1993;Lewejohann et al 2004). In a further mouse snoRNA knockout, the entire cluster encoding Snord116 RNA isoforms (earlier termed MBII-85 snoRNA) was deleted from a locus associated with Prader-Willi syndrome, a neurodevelopmental disorder in humans.…”

Species-specific amplification of tRNA-derived short interspersed repetitive elements (SINEs) by retroposition: a process of parasitization of entire genomes during the evolution of salmonids.

“…However, the data do not preclude the possibility that SINEs developed a functional role later in evolution as a result of symbiotic relationships with the hosts (38,39), or that SINEs may play a role in speciation by changing genomic organization or gene expression. A role in speciation might provide an explanation at the molecular level for some phenotypic changes accrued in a punctuated manner (40).…”