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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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Regulation of mitochondrial genes by Puf3p regulon.(A) Expression change of mitochondrial genes in fermentative conditions. The ratio for the number of down- to up-regulated (1.5 fold difference) gene from the reference to the fermentative condition was shown. P-value was obtained by the Fisher's exact test where the numbers of down- and up-regulated genes with P3E were compared to those genes without P3E. (B) The distribution for the pair-wise correlation coefficients of gene expression. The grey line denotes the distribution for the mitochondrial genes with P3E. The dashed line denotes the distribution for the mitochondrial genes without P3E. The black line denotes the distribution between mitochondrial gene pairs one of which has P3E and the other does not have P3E. The student t-test was used to compare different distributions.
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pgen-1001030-g004: Regulation of mitochondrial genes by Puf3p regulon.(A) Expression change of mitochondrial genes in fermentative conditions. The ratio for the number of down- to up-regulated (1.5 fold difference) gene from the reference to the fermentative condition was shown. P-value was obtained by the Fisher's exact test where the numbers of down- and up-regulated genes with P3E were compared to those genes without P3E. (B) The distribution for the pair-wise correlation coefficients of gene expression. The grey line denotes the distribution for the mitochondrial genes with P3E. The dashed line denotes the distribution for the mitochondrial genes without P3E. The black line denotes the distribution between mitochondrial gene pairs one of which has P3E and the other does not have P3E. The student t-test was used to compare different distributions.

Mentions: Due to the importance of Puf3p regulation in mitochondrial gene degradation, we further investigated expression of its target mitochondrial genes under the fermentative condition. Using gene-expression profiling measured by microarray data [43], we discovered that significantly more mitochondrial genes with P3E were down-regulated in the fermentative medium (YPD) than those without P3E (Figure 4A, Fisher's exact test, P = 1.2×10−4). Furthermore, we found that mitochondrial genes with P3E tend to be co-regulated because the average correlation coefficients of gene expression among mitochondrial genes with P3E in different conditions is significantly higher than that of genes without P3E (Figure 4B, student t test, P = 0). Therefore Puf3p regulon plays an important role in regulating mitochondrial genes in different conditions.


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

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

Regulation of mitochondrial genes by Puf3p regulon.(A) Expression change of mitochondrial genes in fermentative conditions. The ratio for the number of down- to up-regulated (1.5 fold difference) gene from the reference to the fermentative condition was shown. P-value was obtained by the Fisher's exact test where the numbers of down- and up-regulated genes with P3E were compared to those genes without P3E. (B) The distribution for the pair-wise correlation coefficients of gene expression. The grey line denotes the distribution for the mitochondrial genes with P3E. The dashed line denotes the distribution for the mitochondrial genes without P3E. The black line denotes the distribution between mitochondrial gene pairs one of which has P3E and the other does not have P3E. The student t-test was used to compare different distributions.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1001030-g004: Regulation of mitochondrial genes by Puf3p regulon.(A) Expression change of mitochondrial genes in fermentative conditions. The ratio for the number of down- to up-regulated (1.5 fold difference) gene from the reference to the fermentative condition was shown. P-value was obtained by the Fisher's exact test where the numbers of down- and up-regulated genes with P3E were compared to those genes without P3E. (B) The distribution for the pair-wise correlation coefficients of gene expression. The grey line denotes the distribution for the mitochondrial genes with P3E. The dashed line denotes the distribution for the mitochondrial genes without P3E. The black line denotes the distribution between mitochondrial gene pairs one of which has P3E and the other does not have P3E. The student t-test was used to compare different distributions.
Mentions: Due to the importance of Puf3p regulation in mitochondrial gene degradation, we further investigated expression of its target mitochondrial genes under the fermentative condition. Using gene-expression profiling measured by microarray data [43], we discovered that significantly more mitochondrial genes with P3E were down-regulated in the fermentative medium (YPD) than those without P3E (Figure 4A, Fisher's exact test, P = 1.2×10−4). Furthermore, we found that mitochondrial genes with P3E tend to be co-regulated because the average correlation coefficients of gene expression among mitochondrial genes with P3E in different conditions is significantly higher than that of genes without P3E (Figure 4B, student t test, P = 0). Therefore Puf3p regulon plays an important role in regulating mitochondrial genes in different 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