Pancreatic-Type Ribonuclease 1 Gene Duplications in Rat Species

Abstract

Mammalian pancreatic-type ribonucleases (RNases) 1 represent single-copy genes in the genome of most investigated mammalian species, including Mus musculus and other murid rodents. However, in six species belonging to the genus Rattus and closely related taxa, several paralogous gene products were identified by Southern blotting and PCR amplifications of genomic sequences. Phylogenies of nucleotide and derived amino acid sequences were reconstructed by several procedures, with three Mus species as outgroup. Duplications of the RNase 1 occurred after the divergence of Niviventer cremoriventer and Leopoldamys edwardsi from the other investigated species. Four groups of paralogous genes could be identified from specific amino acid sequence features in each of them. Low ratios of nonsynonymous-to-synonymous substitutions and the paucity of pseudogene features suggest functional gene products. One of the RNase 1 genes of R. norvegicus is expressed in the pancreas. RNases 1 were isolated from pancreatic tissues of R. rattus and R. exulans and submitted to N-terminal amino acid sequence analysis. In R. rattus, the orthologue of the expressed gene of R. norvegicus was identified, but in R. exulans, two paralogous gene products were found. The gene encoding for one of these had not yet been found by PCR amplification of genomic DNA. A well-defined group of orthologous sequences found in five investigated species codes for very basic RNases. Northern blot analysis showed expression of messenger RNA for this RNase in the spleen of R. norvegicus, but the protein product could not be identified. Evolutionary rates of RNase 1, expressed as nucleotide substitutions per site per 10(3) million years (Myr), vary between 5 and 9 in the lines leading to Mus, Niviventer, and Lepoldamys (on the basis of an ancestral date of mouse/rat divergence of 12.2 Myr) and between 20 and 50 in the lines to the other sequences after divergence from Niviventer and Leopoldamys (5.5 Myr).

Recent Segmental Duplications in the Working Draft Assembly of the Brown Norway Rat

“…; Atchison and Adesnik 1986;Pages et al 1990;Yan et al 1995;McFadyen et al 1999;Ioannidu et al 2001;Oldfield et al 2001;Rolstad et al 2001) were validated during our analysis, not all were detected. For example, the pancreatic type ribonuclease I represents a single-copy gene within most mammalian lineages that has expanded specifically within the genus Rattus (Dubois et al 2002). It was not detected as a duplicated gene within rat genome assembly v. 3.1 by our criteria.…”

Duplication and functional diversification of pancreatic ribonuclease (RNASE1) gene

“…However, the study of the adaptive evolution of RNASE superfamily in rats and mice found that a group of eight genes in this superfamily in rat is evolving under positive selection, suggesting that numerous gene duplications and functional diversification events have occurred at these loci [60]. Subsequently, Dubois et al [26] investigated pancreatic RNASE1 gene of Rattus species and several their sister taxa. Surprisingly, they observed a "birth (gene duplication)-and-death (gene deactivation)" process for the evolution of pancreatic RNASE1 genes in R. norvegicus, while other species had only one RNASE1 gene [1].…”

“…Surprisingly, they observed a "birth (gene duplication)-and-death (gene deactivation)" process for the evolution of pancreatic RNASE1 genes in R. norvegicus, while other species had only one RNASE1 gene [1]. In addition, the duplicated genes were found to undergo rapid evolution [26,61]. Isolation and purification of proteins further suggest that one of these genes is expressed with a high level in pancreas, while the other genes are expressed in other tissues [26].…”

“…RNASE1 gene thus becomes one of the most important candidate genetic markers to study the molecular mechanism of adaptation of animals to feeding habits. Interestingly, RNASE1 gene duplication has also been found in some species of rodents and carnivores, which have a relatively simple digestive system and lack the microbial digestion in rumen or cecum typical of most herbivores, suggesting that RNASE1 gene may have produced novel tissue specificity or functions in these species [26,31]. In this review, we summarize the advancements of research on RNASE1 gene and its implications in adaptive evolution of animals.…”

“…It is expressed at high levels in the pancreas of ruminants with ruminant digestion and also a number of species with ruminant-like or cecal digestion to degrade large amounts of RNA released by symbiotic bacteria from herbivorous stomach or cecum in order to gain nutrients [17][18][19][20]. While most mammals have only one RNASE1 gene, ruminants and ruminant-like animals were found to have multiple RNASE1 genes resulting from gene duplications, including ox, sheep, camel, rat, guinea pig and elephant [21][22][23][24][25][26][27]. Using both molecular analyses and functional assays, Zhang et al [28][29][30] have revealed that the duplicated RNASE1 genes in two colobines, Asian Pygathrix nemaeus and African Colobus guereza, evolved rapidly under positive selection for enhanced digestive efficiencies, as an adaptive response to the increased demands for the enzyme for digesting bacterial RNA.…”