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Uncovering genes with divergent mRNA-protein dynamics in Streptomyces coelicolor.

Jayapal KP, Philp RJ, Kok YJ, Yap MG, Sherman DH, Griffin TJ, Hu WS - PLoS ONE (2008)

Bottom Line: Many biological processes are intrinsically dynamic, incurring profound changes at both molecular and physiological levels.Despite this overall correlation, by employing a systematic concordance analysis, we estimated that over 30% of the analyzed genes likely exhibited significantly divergent patterns, of which nearly one-third displayed even opposing trends.Our observations suggest that differences between mRNA and protein synthesis/degradation mechanisms are prominent in microbes while reaffirming the plausibility of such mechanisms acting in a concerted fashion at a protein complex or sub-pathway level.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemical Engineering and Materials Science, University of Minnesota, Minneapolis, Minnesota, United States of America.

ABSTRACT
Many biological processes are intrinsically dynamic, incurring profound changes at both molecular and physiological levels. Systems analyses of such processes incorporating large-scale transcriptome or proteome profiling can be quite revealing. Although consistency between mRNA and proteins is often implicitly assumed in many studies, examples of divergent trends are frequently observed. Here, we present a comparative transcriptome and proteome analysis of growth and stationary phase adaptation in Streptomyces coelicolor, taking the time-dynamics of process into consideration. These processes are of immense interest in microbiology as they pertain to the physiological transformations eliciting biosynthesis of many naturally occurring therapeutic agents. A shotgun proteomics approach based on mass spectrometric analysis of isobaric stable isotope labeled peptides (iTRAQ) enabled identification and rapid quantification of approximately 14% of the theoretical proteome of S. coelicolor. Independent principal component analyses of this and DNA microarray-derived transcriptome data revealed that the prominent patterns in both protein and mRNA domains are surprisingly well correlated. Despite this overall correlation, by employing a systematic concordance analysis, we estimated that over 30% of the analyzed genes likely exhibited significantly divergent patterns, of which nearly one-third displayed even opposing trends. Integrating this data with biological information, we discovered that certain groups of functionally related genes exhibit mRNA-protein discordance in a similar fashion. Our observations suggest that differences between mRNA and protein synthesis/degradation mechanisms are prominent in microbes while reaffirming the plausibility of such mechanisms acting in a concerted fashion at a protein complex or sub-pathway level.

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Integrated transcriptome and proteome data mapped onto a simplified metabolic network.Proteome data (red lines) and transcriptome data (blue lines) are plotted in the same graph. The horizontal axis of each plot represents time ranging from 7 h to 38 h. The fold-change ratios of genes in the vertical axis span a value of 6 in log2 scale, except for actinorhodin, undecylprodigiosin, type I polyketide biosynthesis and phosphate starvation response genes where the vertical axis spans a value of 8 in log2 scale. Each plot begins with log ratio  =  0 at 7 h. Single peptide protein identifications are indicated with an asterisk (⋆), and their MS/MS spectra are provided Figure S4. Pathways and corresponding enzymes were identified from KEGG database [34]. Only major reactions in each pathway are shown. Gene names and SCO numbers are provided in Tables S2 and S3.
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pone-0002097-g005: Integrated transcriptome and proteome data mapped onto a simplified metabolic network.Proteome data (red lines) and transcriptome data (blue lines) are plotted in the same graph. The horizontal axis of each plot represents time ranging from 7 h to 38 h. The fold-change ratios of genes in the vertical axis span a value of 6 in log2 scale, except for actinorhodin, undecylprodigiosin, type I polyketide biosynthesis and phosphate starvation response genes where the vertical axis spans a value of 8 in log2 scale. Each plot begins with log ratio  =  0 at 7 h. Single peptide protein identifications are indicated with an asterisk (⋆), and their MS/MS spectra are provided Figure S4. Pathways and corresponding enzymes were identified from KEGG database [34]. Only major reactions in each pathway are shown. Gene names and SCO numbers are provided in Tables S2 and S3.

Mentions: Genes in major functional classes were examined for their correlations with the principal eigen-genes and eigen-proteins shown in Figure 4A. In the following discussion, presence of a gene in the top or bottom 10 percentile of PC-1, PC-2 values are considered as indications for positive or negative correlation with that particular eigen-gene or protein. To facilitate identification of patterns among functional classes in a metabolic context, the transcriptomic and proteomic data were also plotted on a simplified metabolic reaction network using gene annotations taken from KEGG pathway database (Figure 5).


Uncovering genes with divergent mRNA-protein dynamics in Streptomyces coelicolor.

Jayapal KP, Philp RJ, Kok YJ, Yap MG, Sherman DH, Griffin TJ, Hu WS - PLoS ONE (2008)

Integrated transcriptome and proteome data mapped onto a simplified metabolic network.Proteome data (red lines) and transcriptome data (blue lines) are plotted in the same graph. The horizontal axis of each plot represents time ranging from 7 h to 38 h. The fold-change ratios of genes in the vertical axis span a value of 6 in log2 scale, except for actinorhodin, undecylprodigiosin, type I polyketide biosynthesis and phosphate starvation response genes where the vertical axis spans a value of 8 in log2 scale. Each plot begins with log ratio  =  0 at 7 h. Single peptide protein identifications are indicated with an asterisk (⋆), and their MS/MS spectra are provided Figure S4. Pathways and corresponding enzymes were identified from KEGG database [34]. Only major reactions in each pathway are shown. Gene names and SCO numbers are provided in Tables S2 and S3.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2367054&req=5

pone-0002097-g005: Integrated transcriptome and proteome data mapped onto a simplified metabolic network.Proteome data (red lines) and transcriptome data (blue lines) are plotted in the same graph. The horizontal axis of each plot represents time ranging from 7 h to 38 h. The fold-change ratios of genes in the vertical axis span a value of 6 in log2 scale, except for actinorhodin, undecylprodigiosin, type I polyketide biosynthesis and phosphate starvation response genes where the vertical axis spans a value of 8 in log2 scale. Each plot begins with log ratio  =  0 at 7 h. Single peptide protein identifications are indicated with an asterisk (⋆), and their MS/MS spectra are provided Figure S4. Pathways and corresponding enzymes were identified from KEGG database [34]. Only major reactions in each pathway are shown. Gene names and SCO numbers are provided in Tables S2 and S3.
Mentions: Genes in major functional classes were examined for their correlations with the principal eigen-genes and eigen-proteins shown in Figure 4A. In the following discussion, presence of a gene in the top or bottom 10 percentile of PC-1, PC-2 values are considered as indications for positive or negative correlation with that particular eigen-gene or protein. To facilitate identification of patterns among functional classes in a metabolic context, the transcriptomic and proteomic data were also plotted on a simplified metabolic reaction network using gene annotations taken from KEGG pathway database (Figure 5).

Bottom Line: Many biological processes are intrinsically dynamic, incurring profound changes at both molecular and physiological levels.Despite this overall correlation, by employing a systematic concordance analysis, we estimated that over 30% of the analyzed genes likely exhibited significantly divergent patterns, of which nearly one-third displayed even opposing trends.Our observations suggest that differences between mRNA and protein synthesis/degradation mechanisms are prominent in microbes while reaffirming the plausibility of such mechanisms acting in a concerted fashion at a protein complex or sub-pathway level.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemical Engineering and Materials Science, University of Minnesota, Minneapolis, Minnesota, United States of America.

ABSTRACT
Many biological processes are intrinsically dynamic, incurring profound changes at both molecular and physiological levels. Systems analyses of such processes incorporating large-scale transcriptome or proteome profiling can be quite revealing. Although consistency between mRNA and proteins is often implicitly assumed in many studies, examples of divergent trends are frequently observed. Here, we present a comparative transcriptome and proteome analysis of growth and stationary phase adaptation in Streptomyces coelicolor, taking the time-dynamics of process into consideration. These processes are of immense interest in microbiology as they pertain to the physiological transformations eliciting biosynthesis of many naturally occurring therapeutic agents. A shotgun proteomics approach based on mass spectrometric analysis of isobaric stable isotope labeled peptides (iTRAQ) enabled identification and rapid quantification of approximately 14% of the theoretical proteome of S. coelicolor. Independent principal component analyses of this and DNA microarray-derived transcriptome data revealed that the prominent patterns in both protein and mRNA domains are surprisingly well correlated. Despite this overall correlation, by employing a systematic concordance analysis, we estimated that over 30% of the analyzed genes likely exhibited significantly divergent patterns, of which nearly one-third displayed even opposing trends. Integrating this data with biological information, we discovered that certain groups of functionally related genes exhibit mRNA-protein discordance in a similar fashion. Our observations suggest that differences between mRNA and protein synthesis/degradation mechanisms are prominent in microbes while reaffirming the plausibility of such mechanisms acting in a concerted fashion at a protein complex or sub-pathway level.

Show MeSH
Related in: MedlinePlus