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PLoS Comput Biol. Jun 2009; 5(6): e1000409.
Published online Jun 12, 2009. doi:  10.1371/journal.pcbi.1000409
PMCID: PMC2690403

Spatio-Temporal Dynamics of Yeast Mitochondrial Biogenesis: Transcriptional and Post-Transcriptional mRNA Oscillatory Modules

Lars Juhl Jensen, Editor

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.

Author Summary

In bacterial and eukaryotic cells, gene expression is regulated at both the transcriptional and translational levels. In eukaryotes these two processes cannot be directly coupled because the nuclear membrane separates the chromosomes from the ribosomes. Although the transcription levels in different cellular conditions have been widely examined, genome-wide post-transcriptional mechanisms are poorly documented and therefore, the connections between the two processes are difficult to explain. In this work, the time-regulated expression of the genes involved in the construction of the mitochondrion, an important organelle present in nearly all the eukaryotic cells, was scrutinized both at transcriptional and post-transcriptional levels. We observed that temporal transcriptional profiles coincide with groups of genes which are translated at specific cellular loci. The description of these relationships is functionally relevant since the genes which are transcribed early in mitochondria cycles are those which are translated to the vicinity of mitochondria. In addition, these early genes code for essential assembling factors or core elements of the protein complexes whereas the peripheral proteins are translated later in the cytoplasm. Also, these observations support the concerted action of important regulatory factors which control either the gene transcription level (transcription factors) or the mRNA localization (mRNA-binding proteins).


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