Secretory ribonucleases in the primitive ruminant chevrotain (Tragulus javanicus)

Abstract

Phylogenetic analyses of secretory ribonucleases or RNases 1 have shown that gene duplication events, giving rise to three paralogous genes (pancreatic, seminal and brain RNase), occurred during the evolution of ancestral ruminants. A higher number of paralogous sequences are present in chevrotain (Tragulus javanicus), the earliest diverged taxon within the ruminants. Two pancreatic RNase sequences were identified, one encoding the pancreatic enzyme, the other encoding a pseudogene. The identity of the pancreatic enzyme was confirmed by isolation of the protein and N‐terminal sequence analysis. It is the most acidic pancreatic ribonuclease identified so far. Formation of the mature enzyme requires cleavage by signal peptidase of a peptide bond between two glutamic acid residues. The seminal‐type RNase gene shows features of a pseudogene, like orthologous genes in other ruminants investigated with the exception of the bovine species. The brain‐type RNase gene of chevrotain is expressed in brain tissue. A hybrid gene with a pancreatic‐type N‐terminal and a brain‐type C‐terminal sequence has been identified but nothing is known about its expression. Phylogenetic analysis of RNase 1 sequences of six ruminant, three other artiodactyl and two whale species support previous findings that two gene duplications occurred in a ruminant ancestor. Three distinct groups of pancreatic, seminal‐type and brain‐type RNases have been identified and within each group the chevrotain sequence it the first to diverge. In taxa with duplications of the RNase gene (ruminants and camels) the gene evolved at twice as fast than in taxa in which only one gene could be demonstrated; in ruminants there was an ≈ fourfold increase directly after the duplications and then a slowing in evolutionary rate.

Evolutionary and Functional Novelty of Pancreatic Ribonuclease: a Study of Musteloidea (order Carnivora)

“…, leaf-eating monkeys), in which two independent RNASE1 gene duplication events have been found in Asian colobine and African colobine subfamilies12131415. In comparison, the RNASE1 gene duplication pattern in the ruminant artiodactyls is different, which has been reported to arise through ancient gene duplication events in the common ancestor of all ruminants627, rather than independent duplications. Furthermore, several other lines of evidence support the independent diversifications of RNASE1 genes in four Musteloidea families discovered here: (1) the alternative tree topology supporting a single-gene duplication event prior to the divergence of the four families of Musteloidea was significantly worse than our presented tree (P < 0.05) under the Kishino-Hasegawa test28 and the Shimodaira-Hasegawa test29; and (2) no signals of gene conversion events, which can lead to spurious independent duplications by homogenizing sequences within species, were found using GENECOVN software30, suggesting that the observed family-specific clusters were not the results of concerted evolution via gene conversion.…”

“…The RNASE1 gene has been thoroughly investigated in many mammalian herbivores having multicompartmentalized stomachs, like ruminants ( e.g. ox, sheep and camel)1234567, and species with ruminant-like or cecal digestions ( e.g. leaf-eating colobines and elephants)89101112131415.…”

“…leaf-eating colobines and elephants)89101112131415. Whereas other mammalian species contain only a single RNASE1 gene, these herbivorous species harbor multiple RNASE1 genes resulting from gene duplication, which are thought to be an adaptive response to increased demands for the enzyme for digesting bacterial RNA from the gut microflora567891314.…”

Evolution of Digestive Enzymes and RNASE1 Provides Insights into Dietary Switch of Cetaceans

“…RNASE1 gene duplication has been found in many mammals with multi-compartmentalized stomachs, such as ruminants (e.g., cows, sheep, and camels) (Kleineidam et al 1999; Breukelman et al 2001), and species with ruminant-like or cecal digestions (e.g., leaf-eating colobines and elephants) (Zhang et al 2002; Yu et al 2010; Goo and Cho 2013; Zhou et al 2014). Gene duplication of RNASE1 is believed to be correlated with the plant-feeding adaptation of foregut-fermenting herbivores (Liu et al 2014), and ruminant artiodactyls have considerably higher concentrations of pancreatic RNASE1 than other mammals (Zhang 2006).…”

Duplication and functional diversification of pancreatic ribonuclease (RNASE1) gene

“…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.…”