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Subfunctionalization of sigma factors during the evolution of land plants based on mutant analysis of liverwort (Marchantia polymorpha L.) MpSIG1.

Ueda M, Takami T, Peng L, Ishizaki K, Kohchi T, Shikanai T, Nishimura Y - Genome Biol Evol (2013)

Bottom Line: The mutant did not show any visible phenotypes, implying that MpSIG1 function is redundant with that of other sigma factors.The transcript levels of genes clustered in the petL, psaA, psbB, psbK, and psbE operons of liverwort were lower than those in the wild type, a result similar to that in the SIG1 defective mutant in rice (Oryza sativa).Our study shows the ancestral function of SIG1 and the process of functional partitioning (subfunctionalization) of sigma factors during the evolution of land plants.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany, Graduate School of Science, Kyoto University, Japan.

ABSTRACT
Sigma factor is a subunit of plastid-encoded RNA polymerase that regulates the transcription of plastid-encoded genes by recognizing a set of promoters. Sigma factors have increased in copy number and have diversified during the evolution of land plants, but details of this process remain unknown. Liverworts represent the basal group of embryophytes and are expected to retain the ancestral features of land plants. In liverwort (Marchantia polymorpha L.), we isolated and characterized a T-DNA-tagged mutant (Mpsig1) of sigma factor 1 (MpSIG1). The mutant did not show any visible phenotypes, implying that MpSIG1 function is redundant with that of other sigma factors. However, quantitative reverse-transcription polymerase chain reaction and RNA gel blot analysis revealed that genes related to photosynthesis were downregulated, resulting in the minor reduction of some protein complexes. The transcript levels of genes clustered in the petL, psaA, psbB, psbK, and psbE operons of liverwort were lower than those in the wild type, a result similar to that in the SIG1 defective mutant in rice (Oryza sativa). Overexpression analysis revealed primitive functional divergence between the SIG1 and SIG2 proteins in bryophytes, whereas these proteins still retain functional redundancy. We also discovered that the predominant sigma factor for ndhF mRNA expression has been diversified in liverwort, Arabidopsis (Arabidopsis thaliana), and rice. Our study shows the ancestral function of SIG1 and the process of functional partitioning (subfunctionalization) of sigma factors during the evolution of land plants.

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The effect of overexpressing liverwort sigma factor 2 (MpSIG2) on plastid transcript abundance in the Mpsig1 mutant. MpSIG2 was overexpressed under the control of the CaMV 35S promoter in the Mpsig1 mutant. Fifteen-day-old plants grown under continuous white light (40 μmol photons m−2 s−1) at 20 °C on agar plates were used. The means are depicted by white, gray, and black bars for the Mpsig1 mutant (Mpsig1), plants overexpressing MpSIG1 (Mpsig1 + P35S:MpSIG1), and plants overexpressing MpSIG2 (Mpsig1 + P35S:MpSIG2), respectively. The standard errors (n = 3, n stands for technical replicates) are indicated by lines extending from the bars. Each mean represents the ratio of the expression level of transcripts in the experimental plants compared with that of WT plants.
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evt137-F5: The effect of overexpressing liverwort sigma factor 2 (MpSIG2) on plastid transcript abundance in the Mpsig1 mutant. MpSIG2 was overexpressed under the control of the CaMV 35S promoter in the Mpsig1 mutant. Fifteen-day-old plants grown under continuous white light (40 μmol photons m−2 s−1) at 20 °C on agar plates were used. The means are depicted by white, gray, and black bars for the Mpsig1 mutant (Mpsig1), plants overexpressing MpSIG1 (Mpsig1 + P35S:MpSIG1), and plants overexpressing MpSIG2 (Mpsig1 + P35S:MpSIG2), respectively. The standard errors (n = 3, n stands for technical replicates) are indicated by lines extending from the bars. Each mean represents the ratio of the expression level of transcripts in the experimental plants compared with that of WT plants.

Mentions: MpSIG2 was overexpressed under the control of the CaMV 35S promoter in the Mpsig1 mutant, and its effects on various transcript levels were analyzed by qRT-PCR. The overexpressing lines accumulated approximately a 3-fold higher level of MpSIG2 transcripts than the WT plants and did not show any visible phenotypic difference. MpSIG2 overexpression resulted in an effect similar to that of MpSIG1 overexpression on the transcript levels of psaA, psbE, psbK, and rps18, suggesting that both sigma factors have roughly the same affinity for these promoters. In contrast, a drastic difference was observed in the effect on the ndhF transcript level. Although MpSIG1 highly up-regulated ndhF transcript accumulation, the effect was subtle in the MpSIG2 overexpression lines (fig. 5), suggesting a different promoter preference between the two sigma factors. Overexpression of MpSIG2 upregulated the expression levels of psbA and rbcL slightly more than that of MpSIG1 (fig. 5). Collectively, these results suggest a slight difference in the promoter preferences between MpSIG1 and MpSIG2; however, the lack of a clear mutant phenotype in the Mpsig1 mutant implies that sigma factors may share many targets in liverwort and that each sigma factor may have acquired more specific functions during the further evolution of land plants.Fig. 5.—


Subfunctionalization of sigma factors during the evolution of land plants based on mutant analysis of liverwort (Marchantia polymorpha L.) MpSIG1.

Ueda M, Takami T, Peng L, Ishizaki K, Kohchi T, Shikanai T, Nishimura Y - Genome Biol Evol (2013)

The effect of overexpressing liverwort sigma factor 2 (MpSIG2) on plastid transcript abundance in the Mpsig1 mutant. MpSIG2 was overexpressed under the control of the CaMV 35S promoter in the Mpsig1 mutant. Fifteen-day-old plants grown under continuous white light (40 μmol photons m−2 s−1) at 20 °C on agar plates were used. The means are depicted by white, gray, and black bars for the Mpsig1 mutant (Mpsig1), plants overexpressing MpSIG1 (Mpsig1 + P35S:MpSIG1), and plants overexpressing MpSIG2 (Mpsig1 + P35S:MpSIG2), respectively. The standard errors (n = 3, n stands for technical replicates) are indicated by lines extending from the bars. Each mean represents the ratio of the expression level of transcripts in the experimental plants compared with that of WT plants.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3814195&req=5

evt137-F5: The effect of overexpressing liverwort sigma factor 2 (MpSIG2) on plastid transcript abundance in the Mpsig1 mutant. MpSIG2 was overexpressed under the control of the CaMV 35S promoter in the Mpsig1 mutant. Fifteen-day-old plants grown under continuous white light (40 μmol photons m−2 s−1) at 20 °C on agar plates were used. The means are depicted by white, gray, and black bars for the Mpsig1 mutant (Mpsig1), plants overexpressing MpSIG1 (Mpsig1 + P35S:MpSIG1), and plants overexpressing MpSIG2 (Mpsig1 + P35S:MpSIG2), respectively. The standard errors (n = 3, n stands for technical replicates) are indicated by lines extending from the bars. Each mean represents the ratio of the expression level of transcripts in the experimental plants compared with that of WT plants.
Mentions: MpSIG2 was overexpressed under the control of the CaMV 35S promoter in the Mpsig1 mutant, and its effects on various transcript levels were analyzed by qRT-PCR. The overexpressing lines accumulated approximately a 3-fold higher level of MpSIG2 transcripts than the WT plants and did not show any visible phenotypic difference. MpSIG2 overexpression resulted in an effect similar to that of MpSIG1 overexpression on the transcript levels of psaA, psbE, psbK, and rps18, suggesting that both sigma factors have roughly the same affinity for these promoters. In contrast, a drastic difference was observed in the effect on the ndhF transcript level. Although MpSIG1 highly up-regulated ndhF transcript accumulation, the effect was subtle in the MpSIG2 overexpression lines (fig. 5), suggesting a different promoter preference between the two sigma factors. Overexpression of MpSIG2 upregulated the expression levels of psbA and rbcL slightly more than that of MpSIG1 (fig. 5). Collectively, these results suggest a slight difference in the promoter preferences between MpSIG1 and MpSIG2; however, the lack of a clear mutant phenotype in the Mpsig1 mutant implies that sigma factors may share many targets in liverwort and that each sigma factor may have acquired more specific functions during the further evolution of land plants.Fig. 5.—

Bottom Line: The mutant did not show any visible phenotypes, implying that MpSIG1 function is redundant with that of other sigma factors.The transcript levels of genes clustered in the petL, psaA, psbB, psbK, and psbE operons of liverwort were lower than those in the wild type, a result similar to that in the SIG1 defective mutant in rice (Oryza sativa).Our study shows the ancestral function of SIG1 and the process of functional partitioning (subfunctionalization) of sigma factors during the evolution of land plants.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany, Graduate School of Science, Kyoto University, Japan.

ABSTRACT
Sigma factor is a subunit of plastid-encoded RNA polymerase that regulates the transcription of plastid-encoded genes by recognizing a set of promoters. Sigma factors have increased in copy number and have diversified during the evolution of land plants, but details of this process remain unknown. Liverworts represent the basal group of embryophytes and are expected to retain the ancestral features of land plants. In liverwort (Marchantia polymorpha L.), we isolated and characterized a T-DNA-tagged mutant (Mpsig1) of sigma factor 1 (MpSIG1). The mutant did not show any visible phenotypes, implying that MpSIG1 function is redundant with that of other sigma factors. However, quantitative reverse-transcription polymerase chain reaction and RNA gel blot analysis revealed that genes related to photosynthesis were downregulated, resulting in the minor reduction of some protein complexes. The transcript levels of genes clustered in the petL, psaA, psbB, psbK, and psbE operons of liverwort were lower than those in the wild type, a result similar to that in the SIG1 defective mutant in rice (Oryza sativa). Overexpression analysis revealed primitive functional divergence between the SIG1 and SIG2 proteins in bryophytes, whereas these proteins still retain functional redundancy. We also discovered that the predominant sigma factor for ndhF mRNA expression has been diversified in liverwort, Arabidopsis (Arabidopsis thaliana), and rice. Our study shows the ancestral function of SIG1 and the process of functional partitioning (subfunctionalization) of sigma factors during the evolution of land plants.

Show MeSH
Related in: MedlinePlus