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Heat stress enhances the accumulation of polyadenylated mitochondrial transcripts in Arabidopsis thaliana.

Adamo A, Pinney JW, Kunova A, Westhead DR, Meyer P - PLoS ONE (2008)

Bottom Line: We followed up a surprising observation that a large number of mitochondrial transcripts are detectable in microarray experiments that used poly(A)-specific RNA probes, and that these transcript levels are significantly enhanced after heat treatment.We found that the affected transcripts were uncapped transcripts of mitochondrial origin, which were polyadenylated at multiple sites within their 3'region.As many microarrays contain mitochondrial probes, due to the frequent transfer of mitochondrial genes into the genome, these effects need to be considered when interpreting microarray data.

View Article: PubMed Central - PubMed

Affiliation: Center for Plant Sciences, University of Leeds, Leeds, United Kingdom.

ABSTRACT

Background: Polyadenylation of RNA has a decisive influence on RNA stability. Depending on the organisms or subcellular compartment, it either enhances transcript stability or targets RNAs for degradation. In plant mitochondria, polyadenylation promotes RNA degradation, and polyadenylated mitochondrial transcripts are therefore widely considered to be rare and unstable. We followed up a surprising observation that a large number of mitochondrial transcripts are detectable in microarray experiments that used poly(A)-specific RNA probes, and that these transcript levels are significantly enhanced after heat treatment.

Methodology/principal findings: As the Columbia genome contains a complete set of mitochondrial genes, we had to identify polymorphisms to differentiate between nuclear and mitochondrial copies of a mitochondrial transcript. We found that the affected transcripts were uncapped transcripts of mitochondrial origin, which were polyadenylated at multiple sites within their 3'region. Heat-induced enhancement of these transcripts was quickly restored during a short recovery period.

Conclusions/significance: Our results show that polyadenylated transcripts of mitochondrial origin are more stable than previously suggested, and that their steady-state levels can even be significantly enhanced under certain conditions. As many microarrays contain mitochondrial probes, due to the frequent transfer of mitochondrial genes into the genome, these effects need to be considered when interpreting microarray data.

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Related in: MedlinePlus

Coordinate increase of numt transcripts after heat treatment.Log2 fold change in gene expression between heat treatment and time-matched controls plotted over a 24 hour time course (3h 38°C) heat treatment followed by 21 hours recovery) for the numt insertion genes (black lines) and the heat shock transcription factor (At2g26150, dashed line). 0h marks the beginning of the heat treatment.
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pone-0002889-g001: Coordinate increase of numt transcripts after heat treatment.Log2 fold change in gene expression between heat treatment and time-matched controls plotted over a 24 hour time course (3h 38°C) heat treatment followed by 21 hours recovery) for the numt insertion genes (black lines) and the heat shock transcription factor (At2g26150, dashed line). 0h marks the beginning of the heat treatment.

Mentions: As part of a general study of gene co-expression and transcriptional regulation, genes showing co-expression with the heat shock transcription factor At2g26150 were investigated in the Arabidopsis co-expression tool (ACT). These genes were further clustered with the CliqueFinder tool, and this revealed two main clusters. The first contained a variety of heat and general stress response genes, as would have been expected. Intriguingly, the second comprised 20 genes from the numt insertion. Within this second cluster, transcript levels showed an average pair-wise Pearson correlation of 0.80, and an average correlation of 0.70 with the transcription factor. Full details of the ACT clique clustering analysis are available as supplementary material (Fig. S1). Heat induction of the transcript signals from these genes on the Affymetrix ATH1 microarray was then investigated in a 38°C heat stress time series experiment. Figure 1 shows the fold change in expression signal in heat stressed plants (shoot tissues) compared to controls over the time course, for the genes of the numt insertion. Many of the genes show a signal that peaks strongly at the 3h time point, subsequently decaying back to normal levels. Of the 53 genes within the insertion for which the ATH1 array has probes, 48 show statistically significant (as judged by a Benjamini-Hochberg corrected p value for differential expression of <0.0001) fold changes at this time point.


Heat stress enhances the accumulation of polyadenylated mitochondrial transcripts in Arabidopsis thaliana.

Adamo A, Pinney JW, Kunova A, Westhead DR, Meyer P - PLoS ONE (2008)

Coordinate increase of numt transcripts after heat treatment.Log2 fold change in gene expression between heat treatment and time-matched controls plotted over a 24 hour time course (3h 38°C) heat treatment followed by 21 hours recovery) for the numt insertion genes (black lines) and the heat shock transcription factor (At2g26150, dashed line). 0h marks the beginning of the heat treatment.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2483354&req=5

pone-0002889-g001: Coordinate increase of numt transcripts after heat treatment.Log2 fold change in gene expression between heat treatment and time-matched controls plotted over a 24 hour time course (3h 38°C) heat treatment followed by 21 hours recovery) for the numt insertion genes (black lines) and the heat shock transcription factor (At2g26150, dashed line). 0h marks the beginning of the heat treatment.
Mentions: As part of a general study of gene co-expression and transcriptional regulation, genes showing co-expression with the heat shock transcription factor At2g26150 were investigated in the Arabidopsis co-expression tool (ACT). These genes were further clustered with the CliqueFinder tool, and this revealed two main clusters. The first contained a variety of heat and general stress response genes, as would have been expected. Intriguingly, the second comprised 20 genes from the numt insertion. Within this second cluster, transcript levels showed an average pair-wise Pearson correlation of 0.80, and an average correlation of 0.70 with the transcription factor. Full details of the ACT clique clustering analysis are available as supplementary material (Fig. S1). Heat induction of the transcript signals from these genes on the Affymetrix ATH1 microarray was then investigated in a 38°C heat stress time series experiment. Figure 1 shows the fold change in expression signal in heat stressed plants (shoot tissues) compared to controls over the time course, for the genes of the numt insertion. Many of the genes show a signal that peaks strongly at the 3h time point, subsequently decaying back to normal levels. Of the 53 genes within the insertion for which the ATH1 array has probes, 48 show statistically significant (as judged by a Benjamini-Hochberg corrected p value for differential expression of <0.0001) fold changes at this time point.

Bottom Line: We followed up a surprising observation that a large number of mitochondrial transcripts are detectable in microarray experiments that used poly(A)-specific RNA probes, and that these transcript levels are significantly enhanced after heat treatment.We found that the affected transcripts were uncapped transcripts of mitochondrial origin, which were polyadenylated at multiple sites within their 3'region.As many microarrays contain mitochondrial probes, due to the frequent transfer of mitochondrial genes into the genome, these effects need to be considered when interpreting microarray data.

View Article: PubMed Central - PubMed

Affiliation: Center for Plant Sciences, University of Leeds, Leeds, United Kingdom.

ABSTRACT

Background: Polyadenylation of RNA has a decisive influence on RNA stability. Depending on the organisms or subcellular compartment, it either enhances transcript stability or targets RNAs for degradation. In plant mitochondria, polyadenylation promotes RNA degradation, and polyadenylated mitochondrial transcripts are therefore widely considered to be rare and unstable. We followed up a surprising observation that a large number of mitochondrial transcripts are detectable in microarray experiments that used poly(A)-specific RNA probes, and that these transcript levels are significantly enhanced after heat treatment.

Methodology/principal findings: As the Columbia genome contains a complete set of mitochondrial genes, we had to identify polymorphisms to differentiate between nuclear and mitochondrial copies of a mitochondrial transcript. We found that the affected transcripts were uncapped transcripts of mitochondrial origin, which were polyadenylated at multiple sites within their 3'region. Heat-induced enhancement of these transcripts was quickly restored during a short recovery period.

Conclusions/significance: Our results show that polyadenylated transcripts of mitochondrial origin are more stable than previously suggested, and that their steady-state levels can even be significantly enhanced under certain conditions. As many microarrays contain mitochondrial probes, due to the frequent transfer of mitochondrial genes into the genome, these effects need to be considered when interpreting microarray data.

Show MeSH
Related in: MedlinePlus