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Heat shock response in yeast involves changes in both transcription rates and mRNA stabilities.

Castells-Roca L, García-Martínez J, Moreno J, Herrero E, Bellí G, Pérez-Ortín JE - PLoS ONE (2011)

Bottom Line: This study indicates that the yeast response to heat shock is not only due to changes in transcription rates, but also to changes in the mRNA stabilities. mRNA stability is affected in 62% of the yeast genes and it is particularly important in shaping the mRNA profile of the genes belonging to the environmental stress response.In most cases, changes in transcription rates and mRNA stabilities are homodirectional for both parameters, although some interesting cases of antagonist behavior are found.The statistical analysis of gene targets and sequence motifs within the clusters of genes with similar behaviors shows that both transcriptional and post-transcriptional regulons apparently contribute to the general heat stress response by means of transcriptional factors and RNA binding proteins.

View Article: PubMed Central - PubMed

Affiliation: Departament de Ciències Mèdiques Bàsiques and IRBLleida, Universitat de Lleida, Lleida, Catalunya, Spain.

ABSTRACT
We have analyzed the heat stress response in the yeast Saccharomyces cerevisiae by determining mRNA levels and transcription rates for the whole transcriptome after a shift from 25 °C to 37 °C. Using an established mathematical algorithm, theoretical mRNA decay rates have also been calculated from the experimental data. We have verified the mathematical predictions for selected genes by determining their mRNA decay rates at different times during heat stress response using the regulatable tetO promoter. This study indicates that the yeast response to heat shock is not only due to changes in transcription rates, but also to changes in the mRNA stabilities. mRNA stability is affected in 62% of the yeast genes and it is particularly important in shaping the mRNA profile of the genes belonging to the environmental stress response. In most cases, changes in transcription rates and mRNA stabilities are homodirectional for both parameters, although some interesting cases of antagonist behavior are found. The statistical analysis of gene targets and sequence motifs within the clusters of genes with similar behaviors shows that both transcriptional and post-transcriptional regulons apparently contribute to the general heat stress response by means of transcriptional factors and RNA binding proteins.

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mRNA kinetics of the genes in the 16 clusters upon heat shock.RA values are represented in the y axis as a function of time (min) (shift from 25°C to 37°C at time 0). Experimental RA values (continuous lines) were determined as indicated in the text. Theoretical RA values (dashed lines) were determined from the experimental TR values by assuming a constant kD identical to that of time 0. Graphics represent the mean values corresponding to all the genes in the indicated cluster in relative units, referring to the mean value at time 0. Note that different scales are employed for the y axis depending on the cluster.
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pone-0017272-g004: mRNA kinetics of the genes in the 16 clusters upon heat shock.RA values are represented in the y axis as a function of time (min) (shift from 25°C to 37°C at time 0). Experimental RA values (continuous lines) were determined as indicated in the text. Theoretical RA values (dashed lines) were determined from the experimental TR values by assuming a constant kD identical to that of time 0. Graphics represent the mean values corresponding to all the genes in the indicated cluster in relative units, referring to the mean value at time 0. Note that different scales are employed for the y axis depending on the cluster.

Mentions: An alternative way to visualize the importance of the changes in mRNA stability in the transcriptional response to heat stress is by comparing the experimentally determined RA kinetics over time with the theoretical one (see equation [1] in M & M) obtained from TR values and the initial RA by assuming no changes in mRNA stability (ΔkD = 0). Fig. 4 represents the mean real and theoretical kinetics of the genes in each individual cluster. When comparing both kinetics profiles, it is clear that the actual kinetics from clusters 3–10 runs below the theoretical one, which is indicative of destabilization effects. Therefore, the ribosome biogenesis genes especially enriched in clusters 3 and 4 are downregulated through both the decrease in TA and the destabilization of mRNA. On the contrary, the actual RA kinetics from clusters 12–16 is above the theoretical one, indicating stabilization effects. Cluster 11, which includes the largest number of genes among the 16 clusters, as well as clusters 1 and 2, show very similar actual and theoretical kinetics, which therefore indicate modest, if any, mRNA stabilization effects modulating of the stress response in these genes. This kind of representation is, thus, particularly suited to show that some groups of genes strongly deviate from the behavior predicted from the TR changes, evidencing that either decreased mRNA stability is used to rapidly diminish mRNA levels (clusters 3–6), or that the stabilization of mRNA is used to cooperate with a TR increase to raise mRNA levels (clusters 12–14). Therefore, we can conclude that about 62% of the yeast genes undergo significant mRNA stability regulation during the heat shock response. There is a decrease in stability for downregulated genes (clusters 3–6) that cooperates with decreases in TR. Most upregulated genes (clusters 12–16) have an mRNA stabilization that cooperates with a TR increase. Thus, 36% of the genes experience homodirectional changes in TR and mRNA stability and 26% (clusters 7–10) do not. Finally, the general analysis of the correlation coefficients between the theoretical and the experimental RA data shows that generally there is a good positive correlation (see Fig. S2), meaning that TR change is the main determinant of the transcriptional response to heat stress.


Heat shock response in yeast involves changes in both transcription rates and mRNA stabilities.

Castells-Roca L, García-Martínez J, Moreno J, Herrero E, Bellí G, Pérez-Ortín JE - PLoS ONE (2011)

mRNA kinetics of the genes in the 16 clusters upon heat shock.RA values are represented in the y axis as a function of time (min) (shift from 25°C to 37°C at time 0). Experimental RA values (continuous lines) were determined as indicated in the text. Theoretical RA values (dashed lines) were determined from the experimental TR values by assuming a constant kD identical to that of time 0. Graphics represent the mean values corresponding to all the genes in the indicated cluster in relative units, referring to the mean value at time 0. Note that different scales are employed for the y axis depending on the cluster.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3045430&req=5

pone-0017272-g004: mRNA kinetics of the genes in the 16 clusters upon heat shock.RA values are represented in the y axis as a function of time (min) (shift from 25°C to 37°C at time 0). Experimental RA values (continuous lines) were determined as indicated in the text. Theoretical RA values (dashed lines) were determined from the experimental TR values by assuming a constant kD identical to that of time 0. Graphics represent the mean values corresponding to all the genes in the indicated cluster in relative units, referring to the mean value at time 0. Note that different scales are employed for the y axis depending on the cluster.
Mentions: An alternative way to visualize the importance of the changes in mRNA stability in the transcriptional response to heat stress is by comparing the experimentally determined RA kinetics over time with the theoretical one (see equation [1] in M & M) obtained from TR values and the initial RA by assuming no changes in mRNA stability (ΔkD = 0). Fig. 4 represents the mean real and theoretical kinetics of the genes in each individual cluster. When comparing both kinetics profiles, it is clear that the actual kinetics from clusters 3–10 runs below the theoretical one, which is indicative of destabilization effects. Therefore, the ribosome biogenesis genes especially enriched in clusters 3 and 4 are downregulated through both the decrease in TA and the destabilization of mRNA. On the contrary, the actual RA kinetics from clusters 12–16 is above the theoretical one, indicating stabilization effects. Cluster 11, which includes the largest number of genes among the 16 clusters, as well as clusters 1 and 2, show very similar actual and theoretical kinetics, which therefore indicate modest, if any, mRNA stabilization effects modulating of the stress response in these genes. This kind of representation is, thus, particularly suited to show that some groups of genes strongly deviate from the behavior predicted from the TR changes, evidencing that either decreased mRNA stability is used to rapidly diminish mRNA levels (clusters 3–6), or that the stabilization of mRNA is used to cooperate with a TR increase to raise mRNA levels (clusters 12–14). Therefore, we can conclude that about 62% of the yeast genes undergo significant mRNA stability regulation during the heat shock response. There is a decrease in stability for downregulated genes (clusters 3–6) that cooperates with decreases in TR. Most upregulated genes (clusters 12–16) have an mRNA stabilization that cooperates with a TR increase. Thus, 36% of the genes experience homodirectional changes in TR and mRNA stability and 26% (clusters 7–10) do not. Finally, the general analysis of the correlation coefficients between the theoretical and the experimental RA data shows that generally there is a good positive correlation (see Fig. S2), meaning that TR change is the main determinant of the transcriptional response to heat stress.

Bottom Line: This study indicates that the yeast response to heat shock is not only due to changes in transcription rates, but also to changes in the mRNA stabilities. mRNA stability is affected in 62% of the yeast genes and it is particularly important in shaping the mRNA profile of the genes belonging to the environmental stress response.In most cases, changes in transcription rates and mRNA stabilities are homodirectional for both parameters, although some interesting cases of antagonist behavior are found.The statistical analysis of gene targets and sequence motifs within the clusters of genes with similar behaviors shows that both transcriptional and post-transcriptional regulons apparently contribute to the general heat stress response by means of transcriptional factors and RNA binding proteins.

View Article: PubMed Central - PubMed

Affiliation: Departament de Ciències Mèdiques Bàsiques and IRBLleida, Universitat de Lleida, Lleida, Catalunya, Spain.

ABSTRACT
We have analyzed the heat stress response in the yeast Saccharomyces cerevisiae by determining mRNA levels and transcription rates for the whole transcriptome after a shift from 25 °C to 37 °C. Using an established mathematical algorithm, theoretical mRNA decay rates have also been calculated from the experimental data. We have verified the mathematical predictions for selected genes by determining their mRNA decay rates at different times during heat stress response using the regulatable tetO promoter. This study indicates that the yeast response to heat shock is not only due to changes in transcription rates, but also to changes in the mRNA stabilities. mRNA stability is affected in 62% of the yeast genes and it is particularly important in shaping the mRNA profile of the genes belonging to the environmental stress response. In most cases, changes in transcription rates and mRNA stabilities are homodirectional for both parameters, although some interesting cases of antagonist behavior are found. The statistical analysis of gene targets and sequence motifs within the clusters of genes with similar behaviors shows that both transcriptional and post-transcriptional regulons apparently contribute to the general heat stress response by means of transcriptional factors and RNA binding proteins.

Show MeSH
Related in: MedlinePlus