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Spatio-temporal dynamics of yeast mitochondrial biogenesis: transcriptional and post-transcriptional mRNA oscillatory modules.

Lelandais G, Saint-Georges Y, Geneix C, Al-Shikhley L, Dujardin G, Jacq C - PLoS Comput. Biol. (2009)

Bottom Line: This last spatio-temporal module concerns mostly mRNAs coding for basic elements of mitochondrial construction: assembly and regulatory factors.Prediction that unknown genes from this module code for important elements of mitochondrial biogenesis is supported by experimental evidence.More generally, these observations underscore the importance of post-transcriptional processes in mitochondrial biogenesis, highlighting close connections between nuclear transcription and cytoplasmic site-specific translation.

View Article: PubMed Central - PubMed

Affiliation: Dynamique des Structures et Interactions des Macromolécules Biologiques (DSIMB), INSERM UMR-S 665, Université Paris Diderot, Paris, France. gaelle.lelandais@univ-paris-diderot.fr

ABSTRACT
Examples of metabolic rhythms have recently emerged from studies of budding yeast. High density microarray analyses have produced a remarkably detailed picture of cycling gene expression that could be clustered according to metabolic functions. We developed a model-based approach for the decomposition of expression to analyze these data and to identify functional modules which, expressed sequentially and periodically, contribute to the complex and intricate mitochondrial architecture. This approach revealed that mitochondrial spatio-temporal modules are expressed during periodic spikes and specific cellular localizations, which cover the entire oscillatory period. For instance, assembly factors (32 genes) and translation regulators (47 genes) are expressed earlier than the components of the amino-acid synthesis pathways (31 genes). In addition, we could correlate the expression modules identified with particular post-transcriptional properties. Thus, mRNAs of modules expressed "early" are mostly translated in the vicinity of mitochondria under the control of the Puf3p mRNA-binding protein. This last spatio-temporal module concerns mostly mRNAs coding for basic elements of mitochondrial construction: assembly and regulatory factors. Prediction that unknown genes from this module code for important elements of mitochondrial biogenesis is supported by experimental evidence. More generally, these observations underscore the importance of post-transcriptional processes in mitochondrial biogenesis, highlighting close connections between nuclear transcription and cytoplasmic site-specific translation.

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Cluster analysis of nuclear genes involved in mitochondrialbiogenesis.Periodic gene expression data for yeast grown under continuous,nutrient-limited conditions [3] wereanalyzed using the EDPM algorithm. Theω-footprints (orω-values) were calculated for each of the626 gene expression profiles and used for hierarchical clusteranalysis (left). Six clusters, A to F, account for the time courseof periodic expression. They are represented along a time scale fromthe top (cluster A) to the bottom (cluster F). A meanω-footprint is represented for eachcluster (middle) and maximal values are indicated by vertical arrowstogether with the number of the associated model pattern.Correspondences between maximalω-values and timepoints in the metabolic cycle are indicated by vertical arrows.Clusters A to F correspond to distinct phases during the metaboliccycle [3]: clusters A and B correspond toreductive-building (R/B); clusters C and D, to reductive-charging(R/C); and clusters E and F to oxidative activity (Ox). For each ofthe 6 clusters, a set of 10 typical genes is represented (left),together with their expression variations.
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pcbi-1000409-g003: Cluster analysis of nuclear genes involved in mitochondrialbiogenesis.Periodic gene expression data for yeast grown under continuous,nutrient-limited conditions [3] wereanalyzed using the EDPM algorithm. Theω-footprints (orω-values) were calculated for each of the626 gene expression profiles and used for hierarchical clusteranalysis (left). Six clusters, A to F, account for the time courseof periodic expression. They are represented along a time scale fromthe top (cluster A) to the bottom (cluster F). A meanω-footprint is represented for eachcluster (middle) and maximal values are indicated by vertical arrowstogether with the number of the associated model pattern.Correspondences between maximalω-values and timepoints in the metabolic cycle are indicated by vertical arrows.Clusters A to F correspond to distinct phases during the metaboliccycle [3]: clusters A and B correspond toreductive-building (R/B); clusters C and D, to reductive-charging(R/C); and clusters E and F to oxidative activity (Ox). For each ofthe 6 clusters, a set of 10 typical genes is represented (left),together with their expression variations.

Mentions: The gene clusters presented in the previous section can be distinguished bythe model patterns that contribute the most to the EDPM decompositions (seevertical arrows, middle panel Figure 3). The 15 model patterns differ by the time at whichthey reach their maximal values, so there is a direct relationship betweenclusters A to F and the temporal phases during metabolic cycle (Figure 4A). For instance,cluster A (262 genes) and B (77 genes) comprised genes whose EDPMdecomposition preferentially followed model patterns n°1 andn°2, respectively. The mRNAs of these genes peak at the verybeginning of the metabolic cycle (between 0 and 75 minutes). Genes inclusters C (123 genes) and D (27 genes) mainly conformed to model patternsn°5 and 8 and are expressed in the middle of the metabolic cycle(between 75 and 200 minutes). Finally, clusters E (30 genes) and F (107genes) followed model patterns n°11 and 13 and comprised genes thatare expressed at the end of the metabolic cycle (between 200 and 300minutes).


Spatio-temporal dynamics of yeast mitochondrial biogenesis: transcriptional and post-transcriptional mRNA oscillatory modules.

Lelandais G, Saint-Georges Y, Geneix C, Al-Shikhley L, Dujardin G, Jacq C - PLoS Comput. Biol. (2009)

Cluster analysis of nuclear genes involved in mitochondrialbiogenesis.Periodic gene expression data for yeast grown under continuous,nutrient-limited conditions [3] wereanalyzed using the EDPM algorithm. Theω-footprints (orω-values) were calculated for each of the626 gene expression profiles and used for hierarchical clusteranalysis (left). Six clusters, A to F, account for the time courseof periodic expression. They are represented along a time scale fromthe top (cluster A) to the bottom (cluster F). A meanω-footprint is represented for eachcluster (middle) and maximal values are indicated by vertical arrowstogether with the number of the associated model pattern.Correspondences between maximalω-values and timepoints in the metabolic cycle are indicated by vertical arrows.Clusters A to F correspond to distinct phases during the metaboliccycle [3]: clusters A and B correspond toreductive-building (R/B); clusters C and D, to reductive-charging(R/C); and clusters E and F to oxidative activity (Ox). For each ofthe 6 clusters, a set of 10 typical genes is represented (left),together with their expression variations.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2690403&req=5

pcbi-1000409-g003: Cluster analysis of nuclear genes involved in mitochondrialbiogenesis.Periodic gene expression data for yeast grown under continuous,nutrient-limited conditions [3] wereanalyzed using the EDPM algorithm. Theω-footprints (orω-values) were calculated for each of the626 gene expression profiles and used for hierarchical clusteranalysis (left). Six clusters, A to F, account for the time courseof periodic expression. They are represented along a time scale fromthe top (cluster A) to the bottom (cluster F). A meanω-footprint is represented for eachcluster (middle) and maximal values are indicated by vertical arrowstogether with the number of the associated model pattern.Correspondences between maximalω-values and timepoints in the metabolic cycle are indicated by vertical arrows.Clusters A to F correspond to distinct phases during the metaboliccycle [3]: clusters A and B correspond toreductive-building (R/B); clusters C and D, to reductive-charging(R/C); and clusters E and F to oxidative activity (Ox). For each ofthe 6 clusters, a set of 10 typical genes is represented (left),together with their expression variations.
Mentions: The gene clusters presented in the previous section can be distinguished bythe model patterns that contribute the most to the EDPM decompositions (seevertical arrows, middle panel Figure 3). The 15 model patterns differ by the time at whichthey reach their maximal values, so there is a direct relationship betweenclusters A to F and the temporal phases during metabolic cycle (Figure 4A). For instance,cluster A (262 genes) and B (77 genes) comprised genes whose EDPMdecomposition preferentially followed model patterns n°1 andn°2, respectively. The mRNAs of these genes peak at the verybeginning of the metabolic cycle (between 0 and 75 minutes). Genes inclusters C (123 genes) and D (27 genes) mainly conformed to model patternsn°5 and 8 and are expressed in the middle of the metabolic cycle(between 75 and 200 minutes). Finally, clusters E (30 genes) and F (107genes) followed model patterns n°11 and 13 and comprised genes thatare expressed at the end of the metabolic cycle (between 200 and 300minutes).

Bottom Line: This last spatio-temporal module concerns mostly mRNAs coding for basic elements of mitochondrial construction: assembly and regulatory factors.Prediction that unknown genes from this module code for important elements of mitochondrial biogenesis is supported by experimental evidence.More generally, these observations underscore the importance of post-transcriptional processes in mitochondrial biogenesis, highlighting close connections between nuclear transcription and cytoplasmic site-specific translation.

View Article: PubMed Central - PubMed

Affiliation: Dynamique des Structures et Interactions des Macromolécules Biologiques (DSIMB), INSERM UMR-S 665, Université Paris Diderot, Paris, France. gaelle.lelandais@univ-paris-diderot.fr

ABSTRACT
Examples of metabolic rhythms have recently emerged from studies of budding yeast. High density microarray analyses have produced a remarkably detailed picture of cycling gene expression that could be clustered according to metabolic functions. We developed a model-based approach for the decomposition of expression to analyze these data and to identify functional modules which, expressed sequentially and periodically, contribute to the complex and intricate mitochondrial architecture. This approach revealed that mitochondrial spatio-temporal modules are expressed during periodic spikes and specific cellular localizations, which cover the entire oscillatory period. For instance, assembly factors (32 genes) and translation regulators (47 genes) are expressed earlier than the components of the amino-acid synthesis pathways (31 genes). In addition, we could correlate the expression modules identified with particular post-transcriptional properties. Thus, mRNAs of modules expressed "early" are mostly translated in the vicinity of mitochondria under the control of the Puf3p mRNA-binding protein. This last spatio-temporal module concerns mostly mRNAs coding for basic elements of mitochondrial construction: assembly and regulatory factors. Prediction that unknown genes from this module code for important elements of mitochondrial biogenesis is supported by experimental evidence. More generally, these observations underscore the importance of post-transcriptional processes in mitochondrial biogenesis, highlighting close connections between nuclear transcription and cytoplasmic site-specific translation.

Show MeSH
Related in: MedlinePlus