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Tinkering evolution of post-transcriptional RNA regulons: puf3p in fungi as an example.

Jiang H, Guan W, Gu Z - PLoS Genet. (2010)

Bottom Line: The evolution of the Puf3p regulon remains unclear because previous studies have shown functional divergence of Puf3p regulon targets among yeast, fruit fly, and humans.By analyzing evolutionary patterns of Puf3p and its targeted genes in forty-two sequenced fungi, we demonstrated that, although the Puf3p regulon is conserved among all of the studied fungi, the dedicated regulation of mitochondrial biogenesis by Puf3p emerged only in the Saccharomycotina clade.Our results provide a scenario for how evolution like a tinker exploits pre-existing materials of a conserved post-transcriptional regulon to regulate gene expression for novel functional roles.

View Article: PubMed Central - PubMed

Affiliation: Division of Nutritional Sciences, Cornell University, Ithaca, New York, United States of America.

ABSTRACT
Genome-wide studies of post-transcriptional mRNA regulation in model organisms indicate a "post-transcriptional RNA regulon" model, in which a set of functionally related genes is regulated by mRNA-binding RNAs or proteins. One well-studied post-transcriptional regulon by Puf3p functions in mitochondrial biogenesis in budding yeast. The evolution of the Puf3p regulon remains unclear because previous studies have shown functional divergence of Puf3p regulon targets among yeast, fruit fly, and humans. By analyzing evolutionary patterns of Puf3p and its targeted genes in forty-two sequenced fungi, we demonstrated that, although the Puf3p regulon is conserved among all of the studied fungi, the dedicated regulation of mitochondrial biogenesis by Puf3p emerged only in the Saccharomycotina clade. Moreover, the evolution of the Puf3p regulon was coupled with evolution of codon usage bias in down-regulating expression of genes that function in mitochondria in yeast species after genome duplication. Our results provide a scenario for how evolution like a tinker exploits pre-existing materials of a conserved post-transcriptional regulon to regulate gene expression for novel functional roles.

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Function of the Puf3p regulon under different conditions.(A) The expression level of PUF3 gene in the fermentative (YPD) and respiratory (YPE) growth conditions. The ACT1 gene was used as a control in the real-time PCR experiments. (B) The average growth rate of gene deletion mutants for the mitochondrial genes with and without P3E in the two conditions. The student t-test was used to compare gene expression (in A) and average growth rate of gene deletion mutants (in B). (C) The growth of PUF3 gene deletion mutant and the wide-type (WT) strains in the two conditions.
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pgen-1001030-g005: Function of the Puf3p regulon under different conditions.(A) The expression level of PUF3 gene in the fermentative (YPD) and respiratory (YPE) growth conditions. The ACT1 gene was used as a control in the real-time PCR experiments. (B) The average growth rate of gene deletion mutants for the mitochondrial genes with and without P3E in the two conditions. The student t-test was used to compare gene expression (in A) and average growth rate of gene deletion mutants (in B). (C) The growth of PUF3 gene deletion mutant and the wide-type (WT) strains in the two conditions.

Mentions: PUF protein was first characterized in Drosophila as an mRNA-binding factor that recruits other proteins to inhibit the translation of the bound mRNA [21]. Subsequently, many studies in yeast revealed that the PUF family regulates specific mRNA degeneration by their RNA-binding domains [17], [31], [44], [45]. It was shown that the function of targeting mRNA for degeneration by Puf3p is much more efficient in 2% glucose (YPD, fermentative) than in 3% ethanol (YPE, non-fermentative) [17], [46]. Furthermore, it was shown that Puf3p is crucial for mitochondrial biogenesis and motility under non-fermentative conditions in budding yeast [43]. Saint-Georges and his colleagues reported that Puf3p can transfer its target mRNAs to the peripheral mitochondria in the non-fermentative growth medium [37]. The expression of PUF3 gene is significantly higher in yeast growing in YPE than in YPD (Figure 5A, P-value<0.05). We speculate that this is true because the positive regulation of mitochondrial biogenesis might not be as important for Puf3p in fermentative conditions as that in respiratory conditions: First, based on gene deletion data, the mitochondrial genes with P3E are significantly more important (having more severe growth defects after gene deletion) than those genes without P3E (P = 4×10−6) under non-fermentative conditions, but these two gene groups do not show obvious difference in deletion phenotype under fermentative conditions (Figure 5B). Second, severe growth defect after PUF3 gene deletion was observed in YPE, but not in YPD (Figure 5C). Therefore in non-fermentative condition Puf3p regulates both mitochondrial biogenesis and mRNA degradation, but in fermentative condition, it might only regulate mRNA degradation, albeit more efficiently in this condition. The expression difference of PUF3 in two growth conditions can also be explained by the fact that mitochondrial biogenesis in non-fermentative conditions is extremely important for yeast because the organism relies on respiration, and therefore mitochondria, to generate cellular energy in these conditions. In contrast, the function of mRNA degradation might not be as essential to the organism under fermentative conditions.


Tinkering evolution of post-transcriptional RNA regulons: puf3p in fungi as an example.

Jiang H, Guan W, Gu Z - PLoS Genet. (2010)

Function of the Puf3p regulon under different conditions.(A) The expression level of PUF3 gene in the fermentative (YPD) and respiratory (YPE) growth conditions. The ACT1 gene was used as a control in the real-time PCR experiments. (B) The average growth rate of gene deletion mutants for the mitochondrial genes with and without P3E in the two conditions. The student t-test was used to compare gene expression (in A) and average growth rate of gene deletion mutants (in B). (C) The growth of PUF3 gene deletion mutant and the wide-type (WT) strains in the two conditions.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2908677&req=5

pgen-1001030-g005: Function of the Puf3p regulon under different conditions.(A) The expression level of PUF3 gene in the fermentative (YPD) and respiratory (YPE) growth conditions. The ACT1 gene was used as a control in the real-time PCR experiments. (B) The average growth rate of gene deletion mutants for the mitochondrial genes with and without P3E in the two conditions. The student t-test was used to compare gene expression (in A) and average growth rate of gene deletion mutants (in B). (C) The growth of PUF3 gene deletion mutant and the wide-type (WT) strains in the two conditions.
Mentions: PUF protein was first characterized in Drosophila as an mRNA-binding factor that recruits other proteins to inhibit the translation of the bound mRNA [21]. Subsequently, many studies in yeast revealed that the PUF family regulates specific mRNA degeneration by their RNA-binding domains [17], [31], [44], [45]. It was shown that the function of targeting mRNA for degeneration by Puf3p is much more efficient in 2% glucose (YPD, fermentative) than in 3% ethanol (YPE, non-fermentative) [17], [46]. Furthermore, it was shown that Puf3p is crucial for mitochondrial biogenesis and motility under non-fermentative conditions in budding yeast [43]. Saint-Georges and his colleagues reported that Puf3p can transfer its target mRNAs to the peripheral mitochondria in the non-fermentative growth medium [37]. The expression of PUF3 gene is significantly higher in yeast growing in YPE than in YPD (Figure 5A, P-value<0.05). We speculate that this is true because the positive regulation of mitochondrial biogenesis might not be as important for Puf3p in fermentative conditions as that in respiratory conditions: First, based on gene deletion data, the mitochondrial genes with P3E are significantly more important (having more severe growth defects after gene deletion) than those genes without P3E (P = 4×10−6) under non-fermentative conditions, but these two gene groups do not show obvious difference in deletion phenotype under fermentative conditions (Figure 5B). Second, severe growth defect after PUF3 gene deletion was observed in YPE, but not in YPD (Figure 5C). Therefore in non-fermentative condition Puf3p regulates both mitochondrial biogenesis and mRNA degradation, but in fermentative condition, it might only regulate mRNA degradation, albeit more efficiently in this condition. The expression difference of PUF3 in two growth conditions can also be explained by the fact that mitochondrial biogenesis in non-fermentative conditions is extremely important for yeast because the organism relies on respiration, and therefore mitochondria, to generate cellular energy in these conditions. In contrast, the function of mRNA degradation might not be as essential to the organism under fermentative conditions.

Bottom Line: The evolution of the Puf3p regulon remains unclear because previous studies have shown functional divergence of Puf3p regulon targets among yeast, fruit fly, and humans.By analyzing evolutionary patterns of Puf3p and its targeted genes in forty-two sequenced fungi, we demonstrated that, although the Puf3p regulon is conserved among all of the studied fungi, the dedicated regulation of mitochondrial biogenesis by Puf3p emerged only in the Saccharomycotina clade.Our results provide a scenario for how evolution like a tinker exploits pre-existing materials of a conserved post-transcriptional regulon to regulate gene expression for novel functional roles.

View Article: PubMed Central - PubMed

Affiliation: Division of Nutritional Sciences, Cornell University, Ithaca, New York, United States of America.

ABSTRACT
Genome-wide studies of post-transcriptional mRNA regulation in model organisms indicate a "post-transcriptional RNA regulon" model, in which a set of functionally related genes is regulated by mRNA-binding RNAs or proteins. One well-studied post-transcriptional regulon by Puf3p functions in mitochondrial biogenesis in budding yeast. The evolution of the Puf3p regulon remains unclear because previous studies have shown functional divergence of Puf3p regulon targets among yeast, fruit fly, and humans. By analyzing evolutionary patterns of Puf3p and its targeted genes in forty-two sequenced fungi, we demonstrated that, although the Puf3p regulon is conserved among all of the studied fungi, the dedicated regulation of mitochondrial biogenesis by Puf3p emerged only in the Saccharomycotina clade. Moreover, the evolution of the Puf3p regulon was coupled with evolution of codon usage bias in down-regulating expression of genes that function in mitochondria in yeast species after genome duplication. Our results provide a scenario for how evolution like a tinker exploits pre-existing materials of a conserved post-transcriptional regulon to regulate gene expression for novel functional roles.

Show MeSH