Tempo and Mode of Gene Duplication in Mammalian Ribosomal Protein Evolution

Abstract

Gene duplication has been widely recognized as a major driver of evolutionary change and organismal complexity through the generation of multi-gene families. Therefore, understanding the forces that govern the evolution of gene families through the retention or loss of duplicated genes is fundamentally important in our efforts to study genome evolution. Previous work from our lab has shown that ribosomal protein (RP) genes constitute one of the largest classes of conserved duplicated genes in mammals. This result was surprising due to the fact that ribosomal protein genes evolve slowly and transcript levels are very tightly regulated. In our present study, we identified and characterized all RP duplicates in eight mammalian genomes in order to investigate the tempo and mode of ribosomal protein family evolution. We show that a sizable number of duplicates are transcriptionally active and are very highly conserved. Furthermore, we conclude that existing gene duplication models do not readily account for the preservation of a very large number of intact retroduplicated ribosomal protein (RT-RP) genes observed in mammalian genomes. We suggest that selection against dominant-negative mutations may underlie the unexpected retention and conservation of duplicated RP genes, and may shape the fate of newly duplicated genes, regardless of duplication mechanism.

Expression of Muscle‐Specific Ribosomal Protein L3‐Like Impairs Myotube Growth

“…Studies on genome evolution, and the development of gene families, revealed that, unlike almost every other ribosomal protein gene duplicate, Rpl3l arose as the result of a DNA‐mediated duplication event (Jun et al, ). The muscle‐specific expression of Rpl3l is consistent with the finding that genes derived by such a duplication mechanism are often subject to more complex regulation because upstream regulatory sequences tend to be copied along with the protein coding region (Dharia et al, ). A recent analysis of human RNA‐seq data by Gupta and Warner confirmed the muscle‐specific expression of Rpl3l and further showed Rpl3l to be one of only a few ribosomal proteins with tissue‐specific expression (Gupta and Warner, ).…”

Regulation of ribosomal protein genes: An ordered anarchy

“…Despite the high conservation of RPs, the number of RPGs coding for these proteins varies greatly between different kingdoms of life and even between closely related species like Saccharomyces cerevisiae and Candida glabrata (Mullis et al, 2020). Most RPs in plants and fungi are encoded by more than one gene, while protists and animal genomes contain only a few verified duplicated RPGs (dRPGs; Dharia, Obla, Gajdosik, Simon, & Nelson, 2014; Nakao et al, 2004; Wapinski et al, 2010). These duplicated genes are believed to have risen from genome duplication, genome hybridization, retroduplication, or in some cases from polyploidy (Dharia et al, 2014; Nakao et al, 2004; Wapinski et al, 2010).…”

Parallel Concerted Evolution of Ribosomal Protein Genes in Fungi and Its Adaptive Significance

“…In general, the gene retention rate of SSDs is much lower than ohnologs (half-life of 4 million years vs 33 million years) (Hakes, et al 2007), it is even lower in genes encoding macromolecular complexes due tp evolutionary constraints imposed by gene dosage balance (Li, et al 1996; Conant and Wolfe 2008). Similar to the fission yeasts, 99.8% of RP duplicates in mammals were found to be generated by retroposition (Dharia, et al 2014). However, almost all RP retroduplicates in mammals become pseudogenes (Dharia, et al 2014).…”

“…Similar to the fission yeasts, 99.8% of RP duplicates in mammals were found to be generated by retroposition (Dharia, et al 2014). However, almost all RP retroduplicates in mammals become pseudogenes (Dharia, et al 2014). Therefore, the high retention rates of functional RP duplicates generated by SSDs in each fission yeasts are indeed unexpected.…”