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Positional dependence of transcriptional inhibition by DNA torsional stress in yeast chromosomes.

Joshi RS, Piña B, Roca J - EMBO J. (2010)

Bottom Line: The results revealed that, whereas the overwinding of DNA produced a general impairment of transcription initiation, genes situated at <100 kb from the chromosomal ends gradually escaped from the transcription stall.This novel positional effect seemed to be a simple function of the gene distance to the telomere: It occurred evenly in all 32 chromosome extremities and was independent of the atypical structure and transcription activity of subtelomeric chromatin.These results suggest that DNA helical tension dissipates at chromosomal ends and, therefore, provides a functional indication that yeast chromosome extremities are topologically open.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Diagnóstico Ambiental y Estudios del Agua (IDAEA), Instituto de Biologia Molecular de Barcelona-CSIC, Baldiri Reixac, Barcelona, Spain.

ABSTRACT
How DNA helical tension is constrained along the linear chromosomes of eukaryotic cells is poorly understood. In this study, we induced the accumulation of DNA (+) helical tension in Saccharomyces cerevisiae cells and examined how DNA transcription was affected along yeast chromosomes. The results revealed that, whereas the overwinding of DNA produced a general impairment of transcription initiation, genes situated at <100 kb from the chromosomal ends gradually escaped from the transcription stall. This novel positional effect seemed to be a simple function of the gene distance to the telomere: It occurred evenly in all 32 chromosome extremities and was independent of the atypical structure and transcription activity of subtelomeric chromatin. These results suggest that DNA helical tension dissipates at chromosomal ends and, therefore, provides a functional indication that yeast chromosome extremities are topologically open. The gradual escape from the transcription stall along the chromosomal flanks also indicates that friction restrictions to DNA twist diffusion, rather than tight topological boundaries, might suffice to confine DNA helical tension along eukaryotic chromatin.

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Positional response to DNA helical stress occurs similarly in all chromosomal flanks and independently of chromosome length, transcript length, and transcript direction. (A) The variation of transcript levels (log2) on the accumulation of DNA (+) helical stress is plotted in each of the 32 yeast chromosomal arms against the corresponding gene distance (bp) from the telomere. Coloured splines average values for nine consecutive genes. Distances from telomeres correspond to the central gene. (B) The relative variation of individual transcript levels (log2) is plotted along the physical length of yeast chromosomes I (225 kb) and XIII (915 kb). Polynomial tendency lanes are shown. (C) The relative variation of inwards and outwards transcripts plotted against their gene distance (kb) from the corresponding telomere. Values are calculated as in Figure 2B. (D) The relative variations of transcript level (log2) of the genes located at <100 kb from the telomere is plotted against their respective transcript length (kb).
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f3: Positional response to DNA helical stress occurs similarly in all chromosomal flanks and independently of chromosome length, transcript length, and transcript direction. (A) The variation of transcript levels (log2) on the accumulation of DNA (+) helical stress is plotted in each of the 32 yeast chromosomal arms against the corresponding gene distance (bp) from the telomere. Coloured splines average values for nine consecutive genes. Distances from telomeres correspond to the central gene. (B) The relative variation of individual transcript levels (log2) is plotted along the physical length of yeast chromosomes I (225 kb) and XIII (915 kb). Polynomial tendency lanes are shown. (C) The relative variation of inwards and outwards transcripts plotted against their gene distance (kb) from the corresponding telomere. Values are calculated as in Figure 2B. (D) The relative variations of transcript level (log2) of the genes located at <100 kb from the telomere is plotted against their respective transcript length (kb).

Mentions: Next, we inspected whether the differential response of chromosome flanking genes to DNA helical stress was consistent in all yeast chromosomes. We plotted the relative transcript variations versus the gene distances from the telomere for the individual 32 chromosomal arms (Figure 3A). In all cases, relative transcript levels gradually increased, as genes got closer to the chromosomal end. Moreover, regardless of the respective chromosomal length, all flanks followed similar slopes starting around 100 kb from the telomere. By this circumstance, in short chromosomes (such as Chr. I, 225 kb) the positional effect covered nearly the entire chromosome (Figure 3B). In longer chromosomes (such as Chr. XIII, 915kb), only the flanks exposed the differential response, without similar deviations of the transcript levels at more internal or core regions (Figure 3B). We also observed that the positional effect equally affected genes transcribed in the direction towards and away from the chromosomal end (Figure 3C), and that the different response of chromosome flanking genes to DNA helical stress was independent of their respective transcript length (Figure 3D).


Positional dependence of transcriptional inhibition by DNA torsional stress in yeast chromosomes.

Joshi RS, Piña B, Roca J - EMBO J. (2010)

Positional response to DNA helical stress occurs similarly in all chromosomal flanks and independently of chromosome length, transcript length, and transcript direction. (A) The variation of transcript levels (log2) on the accumulation of DNA (+) helical stress is plotted in each of the 32 yeast chromosomal arms against the corresponding gene distance (bp) from the telomere. Coloured splines average values for nine consecutive genes. Distances from telomeres correspond to the central gene. (B) The relative variation of individual transcript levels (log2) is plotted along the physical length of yeast chromosomes I (225 kb) and XIII (915 kb). Polynomial tendency lanes are shown. (C) The relative variation of inwards and outwards transcripts plotted against their gene distance (kb) from the corresponding telomere. Values are calculated as in Figure 2B. (D) The relative variations of transcript level (log2) of the genes located at <100 kb from the telomere is plotted against their respective transcript length (kb).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2805846&req=5

f3: Positional response to DNA helical stress occurs similarly in all chromosomal flanks and independently of chromosome length, transcript length, and transcript direction. (A) The variation of transcript levels (log2) on the accumulation of DNA (+) helical stress is plotted in each of the 32 yeast chromosomal arms against the corresponding gene distance (bp) from the telomere. Coloured splines average values for nine consecutive genes. Distances from telomeres correspond to the central gene. (B) The relative variation of individual transcript levels (log2) is plotted along the physical length of yeast chromosomes I (225 kb) and XIII (915 kb). Polynomial tendency lanes are shown. (C) The relative variation of inwards and outwards transcripts plotted against their gene distance (kb) from the corresponding telomere. Values are calculated as in Figure 2B. (D) The relative variations of transcript level (log2) of the genes located at <100 kb from the telomere is plotted against their respective transcript length (kb).
Mentions: Next, we inspected whether the differential response of chromosome flanking genes to DNA helical stress was consistent in all yeast chromosomes. We plotted the relative transcript variations versus the gene distances from the telomere for the individual 32 chromosomal arms (Figure 3A). In all cases, relative transcript levels gradually increased, as genes got closer to the chromosomal end. Moreover, regardless of the respective chromosomal length, all flanks followed similar slopes starting around 100 kb from the telomere. By this circumstance, in short chromosomes (such as Chr. I, 225 kb) the positional effect covered nearly the entire chromosome (Figure 3B). In longer chromosomes (such as Chr. XIII, 915kb), only the flanks exposed the differential response, without similar deviations of the transcript levels at more internal or core regions (Figure 3B). We also observed that the positional effect equally affected genes transcribed in the direction towards and away from the chromosomal end (Figure 3C), and that the different response of chromosome flanking genes to DNA helical stress was independent of their respective transcript length (Figure 3D).

Bottom Line: The results revealed that, whereas the overwinding of DNA produced a general impairment of transcription initiation, genes situated at <100 kb from the chromosomal ends gradually escaped from the transcription stall.This novel positional effect seemed to be a simple function of the gene distance to the telomere: It occurred evenly in all 32 chromosome extremities and was independent of the atypical structure and transcription activity of subtelomeric chromatin.These results suggest that DNA helical tension dissipates at chromosomal ends and, therefore, provides a functional indication that yeast chromosome extremities are topologically open.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Diagnóstico Ambiental y Estudios del Agua (IDAEA), Instituto de Biologia Molecular de Barcelona-CSIC, Baldiri Reixac, Barcelona, Spain.

ABSTRACT
How DNA helical tension is constrained along the linear chromosomes of eukaryotic cells is poorly understood. In this study, we induced the accumulation of DNA (+) helical tension in Saccharomyces cerevisiae cells and examined how DNA transcription was affected along yeast chromosomes. The results revealed that, whereas the overwinding of DNA produced a general impairment of transcription initiation, genes situated at <100 kb from the chromosomal ends gradually escaped from the transcription stall. This novel positional effect seemed to be a simple function of the gene distance to the telomere: It occurred evenly in all 32 chromosome extremities and was independent of the atypical structure and transcription activity of subtelomeric chromatin. These results suggest that DNA helical tension dissipates at chromosomal ends and, therefore, provides a functional indication that yeast chromosome extremities are topologically open. The gradual escape from the transcription stall along the chromosomal flanks also indicates that friction restrictions to DNA twist diffusion, rather than tight topological boundaries, might suffice to confine DNA helical tension along eukaryotic chromatin.

Show MeSH
Related in: MedlinePlus