The rapid evolution of signal peptides is mainly caused by relaxed selection on non-synonymous and synonymous sites

Li, Yudong; Xie, Zhongyu; Du, Yi‐Ling; Zhou, Zhan; Mao, Xu‐Ming; Lv, Longxian; Li, Yongquan

doi:10.1016/j.gene.2009.01.015

Cited by 38 publications

(26 citation statements)

References 32 publications

(31 reference statements)

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“…In many cases, the Ka/Ks values of signal peptides were found to be 2–7 times higher than those of the mature proteins. Similar results for an increased rate of evolution of signal peptides were reported for yeast [48] and avian growth hormone genes [49]. Although there might be a tendency, we failed to find a strong correlation between Ka/Ks values of the mature and signal peptides.…”

Section: Resultssupporting

confidence: 82%

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Contrasted evolutionary constraints on secreted and non-secreted proteomes of selected Actinobacteria

et al. 2013

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BackgroundActinobacteria have adapted to contrasted ecological niches such as the soil, and among others to plants or animals as pathogens or symbionts. Mycobacterium genus contains mostly pathogens that cause a variety of mammalian diseases, among which the well-known leprosy and tuberculosis, it also has saprophytic relatives. Streptomyces genus is mostly a soil microbe known for its secondary metabolites, it contains also plant pathogens, animal pathogens and symbionts. Frankia, a nitrogen-fixing actinobacterium establishes a root symbiosis with dicotyledonous pionneer plants. Pathogens and symbionts live inside eukaryotic cells and tissues and interact with their cellular environment through secreted proteins and effectors transported through transmembrane systems; nevertheless they also need to avoid triggering host defense reactions. A comparative genome analysis of the secretomes of symbionts and pathogens allows a thorough investigation of selective pressures shaping their evolution. In the present study, the rates of silent mutations to non-silent mutations in secretory proteins were assessed in different strains of Frankia, Streptomyces and Mycobacterium, of which several genomes have recently become publicly available.ResultsIt was found that secreted proteins as a whole have a stronger purifying evolutionary rate (non-synonymous to synonymous substitutions or Ka/Ks ratio) than the non-secretory proteins in most of the studied genomes. This difference becomes statistically significant in cases involving obligate symbionts and pathogens. Amongst the Frankia, secretomes of symbiotic strains were found to have undergone evolutionary trends different from those of the mainly saprophytic strains. Even within the secretory proteins, the signal peptide part has a higher Ka/Ks ratio than the mature part. Two contrasting trends were noticed amongst the Frankia genomes regarding the relation between selection strength (i.e. Ka/Ks ratio) and the codon adaptation index (CAI), a predictor of the expression rate, in all the genes belonging to the core genome as well as the core secretory protein genes. The genomes of pathogenic Mycobacterium and Streptomyces also had reduced secretomes relative to saprophytes, as well as in general significant pairwise Ka/Ks ratios in their secretomes.ConclusionIn marginally free-living facultative symbionts or pathogenic organisms under consideration, secretory protein genes as a whole evolve at a faster rate than the rest and this process may be an adaptive life-strategy to counter the host selection pressure. The higher evolutionary rate of signal peptide part compared to mature protein provides an indication that signal peptide parts may be under relaxed purifying selection, indicative of the signal peptides not being secreted into host cells. Codon usage analysis suggests that in actinobacterial strains under host selection pressure such as symbiotic Frankia, ACN, FD and the pathogenic Mycobacterium, codon usage bias was negatively correlated to the selective pressure exerted o...

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Section: Resultssupporting

confidence: 82%

“…the Ka/Ks ratio was positively correlated to CAI, with R values ranging from 0.188 to 0.262). This kind of unusual relationship between evolutionary rate and CAI value in signal-peptide-bearing genes was reported earlier for Streptomyces [48]. They have proposed that intensity of purifying selection was significantly relaxed in such genes.…”

Section: Resultssupporting

confidence: 68%

Contrasted evolutionary constraints on secreted and non-secreted proteomes of selected Actinobacteria

et al. 2013

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“…There are two possible explanations for this observation. First, the first exons, which usually contain N-terminal signal peptides, appear to be under more relaxed selection pressure than other exons (34). This relaxed selection pressure may cause the mutagenic effect of DNA methylation to be more evident, leading to higher d S and d N in this exon group.…”

Section: Discussionmentioning

confidence: 99%

Position-dependent correlations between DNA methylation and the evolutionary rates of mammalian coding exons

Chuang

Chen

2012

Proc. Natl. Acad. Sci. U.S.A.

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DNA cytosine methylation is a central epigenetic marker that is usually mutagenic and may increase the level of sequence divergence. However, methylated genes have been reported to evolve more slowly than unmethylated genes. Hence, there is a controversy on whether DNA methylation is correlated with increased or decreased protein evolutionary rates. We hypothesize that this controversy has resulted from the differential correlations between DNA methylation and the evolutionary rates of coding exons in different genic positions. To test this hypothesis, we compare human-mouse and human-macaque exonic evolutionary rates against experimentally determined single-base resolution DNA methylation data derived from multiple human cell types. We show that DNA methylation is significantly related to within-gene variations in evolutionary rates. First, DNA methylation level is more strongly correlated with C-to-T mutations at CpG dinucleotides in the first coding exons than in the internal and last exons, although it is positively correlated with the synonymous substitution rate in all exon positions. Second, for the first exons, DNA methylation level is negatively correlated with exonic expression level, but positively correlated with both nonsynonymous substitution rate and the sample specificity of DNA methylation level. For the internal and last exons, however, we observe the opposite correlations. Our results imply that DNA methylation level is differentially correlated with the biological (and evolutionary) features of coding exons in different genic positions. The first exons appear more prone to the mutagenic effects, whereas the other exons are more influenced by the regulatory effects of DNA methylation.methylation-associated mutation | exon evolution | genomics | deep sequencing | bioinformatics D NA methylation is a common form of epigenetic modification that is important for a variety of biological functions, including transcriptional silencing (1), genomic imprinting (2), X-chromosome inactivation (3), the silencing of transposons (4), tumorigenesis (5), and the differentiation of pluripotent cells (6). DNA methylation is unevenly distributed in the human genome. For example, the CpG islands near the promoter regions of active genes tend to be unmethylated (7-10), because methylation in these regions is strongly correlated with transcriptional suppression (8). It has also been reported that exons tend to be more methylated than introns, and that sharp transitions of methylation occur at exonintron boundaries in human (6). Moreover, the level of DNA methylation also varies among exonic regions. The levels of DNA methylation in the first exons were reported to be lower than in downstream exons, and tightly linked to transcriptional silencing (11). In addition, the level of DNA methylation exhibits a slight but sharp step-down at the transcriptional terminal sites (6).In terms of molecular evolution, DNA methylation is relevant in two aspects. First, DNA methylation can significantly increase the rate of spontan...

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“…These orthologs were curated based on gene positional synteny and sequence similarity. For those genes without ortholog annotation, their orthologs were identified based on the Reciprocal BLAST best hits between S. cerevisiae and other species, with an E -value cutoff of 10 -6 , an identity = 40% and at least 75% alignable region [31]. All sequence alignments are available on request.…”

Section: Methodsmentioning

confidence: 99%

The evolutionary rate variation among genes of HOG-signaling pathway in yeast genomes

Chi

Wang

et al. 2010

Biol Direct

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BackgroundResponses to extracellular stress are required for microbes to survive in changing environments. Although the stress response mechanisms have been characterized extensively, the evolution of stress response pathway remains poorly understood. Here, we studied the evolution of High Osmolarity Glycerol (HOG) pathway, one of the important osmotic stress response pathways, across 10 yeast species and underpinned the evolutionary forces acting on the pathway evolution.ResultsAlthough the HOG pathway is well conserved across the surveyed yeast species, the evolutionary rate of the genes in this pathway varied substantially among or within different lineages. The fast divergence of MSB2 gene indicates that this gene is subjected to positive selection. Moreover, transcription factors in HOG pathway tend to evolve more rapidly, but the genes in conserved MAPK cascade underwent stronger functional selection. Remarkably, the dN/dS values are negatively correlated with pathway position along HOG pathway from Sln1 (Sho1) to Hog1 for transmitting external signal into nuclear. The increased gradient of selective constraints from upstream to downstream genes suggested that the downstream genes are more pleiotropic, being required for a wider range of pathways. In addition, protein length, codon usage, gene expression, and protein interaction appear to be important factors to determine the evolution of genes in HOG pathway.ConclusionsTaken together, our results suggest that functional constraints play a large role in the evolutionary rate variation in HOG pathway, but the genetic variation was influenced by quite complicated factors, such as pathway position, protein length and so on. These findings provide some insights into how HOG pathway genes evolved rapidly for responding to environmental osmotic stress changes.ReviewersThis article was reviewed by Han Liang (nominated by Laura Landweber), Georgy Bazykin (nominated by Mikhail Gelfand) and Zhenguo Lin (nominated by John Logsdon).

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The rapid evolution of signal peptides is mainly caused by relaxed selection on non-synonymous and synonymous sites

Cited by 38 publications

References 32 publications

Contrasted evolutionary constraints on secreted and non-secreted proteomes of selected Actinobacteria

Contrasted evolutionary constraints on secreted and non-secreted proteomes of selected Actinobacteria

Position-dependent correlations between DNA methylation and the evolutionary rates of mammalian coding exons

The evolutionary rate variation among genes of HOG-signaling pathway in yeast genomes

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