Preservation of Gene Duplication Increases the Regulatory Spectrum of Ribosomal Protein Genes and Enhances Growth under Stress

Abstract

In baker's yeast, the majority of ribosomal protein genes (RPGs) are duplicated, and it was recently proposed that such duplications are preserved via the functional specialization of the duplicated genes. However, the origin and nature of duplicated RPGs' (dRPGs) functional specificity remain unclear. In this study, we show that differences in dRPG functions are generated by variations in the modality of gene expression and, to a lesser extent, by protein sequence. Analysis of the sequence and expression patterns of non-intron-containing RPGs indicates that each dRPG is controlled by specific regulatory sequences modulating its expression levels in response to changing growth conditions. Homogenization of dRPG sequences reduces cell tolerance to growth under stress without changing the number of expressed genes. Together, the data reveal a model where duplicated genes provide a means for modulating the expression of ribosomal proteins in response to stress.

Specialized ribosomes and specific ribosomal protein paralogs control translation of mitochondrial proteins

“…For example, expression may involve different parts of the RP mRNA transcript, such as the UTRs and introns ( Parenteau et al, 2011 ). In parallel, cognate RP paralogs were proposed to regulate the level of the other paralog’s mRNA ( Parenteau et al, 2015 ; Gabunilas and Chanfreau, 2016 ). However, alterations in the transcription of one paralog caused by deletion of the other do not correlate with changes in the level of RP protein ( Parenteau et al, 2015 ; Liu et al, 2016 ).…”

“…In parallel, cognate RP paralogs were proposed to regulate the level of the other paralog’s mRNA ( Parenteau et al, 2015 ; Gabunilas and Chanfreau, 2016 ). However, alterations in the transcription of one paralog caused by deletion of the other do not correlate with changes in the level of RP protein ( Parenteau et al, 2015 ; Liu et al, 2016 ). More importantly, RP paralogs do not show synonymous functional substitution but rather diversification.…”

Introns regulate the production of ribosomal proteins by modulating splicing of duplicated ribosomal protein genes

“…For example, the deletion of RPL7A, RPL12B, RPL22A and RPS18B and not their paralog affected the localized translation of Ash1 mRNA ( 8 ). Indeed, we have recently shown that the deletion of the minor and not the major copy of several dRPGs may affect growth under stress without major effect on the global amount of RP ( 12 , 13 ). Deletions of duplicated genes were also shown to generate different transcription profiles and affect growth in a copy-specific manner, suggesting the dRPGs may serve different functions ( 8 ).…”

Paralog-Specific Functions ofRPL7AandRPL7BMediated by Ribosomal Protein or snoRNA Dosage inSaccharomyces cerevisiae

“…Notably, 59 RPs are encoded by paralogous gene pairs that arose from a whole genome duplication and were selectively retained ( Wolfe and Shields 1997 ). Paralogs may persist in the genome because they encode redundant functions that balance gene dosage, become specialized for different environmental conditions, or acquire distinct functions by subfunctionalization or neofunctionalization ( Innan and Kondrashov 2010 ; Parenteau et al 2015 ). Most RP paralogs are redundant for a ribosome-associated function that is essential for optimal cell growth or viability ( Dean et al 2008 ; Steffen et al 2012 ; Woolford and Baserga 2013 ).…”