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Transcription dynamically patterns the meiotic chromosome-axis interface.

Sun X, Huang L, Markowitz TE, Blitzblau HG, Chen D, Klein F, Hochwagen A - Elife (2015)

Bottom Line: We found that the axial element proteins of budding yeast are flexibly anchored to chromatin by the ring-like cohesin complex.Importantly, axis anchoring by cohesin is adjustable and readily displaced in the direction of transcription by the transcriptional machinery.We propose that such robust but flexible tethering allows the axial element to promote recombination while easily adapting to changes in chromosome activity.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, New York University, New York, United States.

ABSTRACT
Meiotic chromosomes are highly compacted yet remain transcriptionally active. To understand how chromosome folding accommodates transcription, we investigated the assembly of the axial element, the proteinaceous structure that compacts meiotic chromosomes and promotes recombination and fertility. We found that the axial element proteins of budding yeast are flexibly anchored to chromatin by the ring-like cohesin complex. The ubiquitous presence of cohesin at sites of convergent transcription provides well-dispersed points for axis attachment and thus chromosome compaction. Axis protein enrichment at these sites directly correlates with the propensity for recombination initiation nearby. A separate modulating mechanism that requires the conserved axial-element component Hop1 biases axis protein binding towards small chromosomes. Importantly, axis anchoring by cohesin is adjustable and readily displaced in the direction of transcription by the transcriptional machinery. We propose that such robust but flexible tethering allows the axial element to promote recombination while easily adapting to changes in chromosome activity.

No MeSH data available.


Related in: MedlinePlus

Red1 accumulates next to transcript ends of convergent gene pairs.(A) Example of overlapping transcripts from a convergent gene pair. ORFs and transcripts of YKL077W and YKL075C were plotted with respect to their positions on chromosome XI. (B) Two-peak pattern of Red1 binding at convergent gene pairs correlates with the amount of transcript overlap. Convergent gene pairs were ranked by the extent of transcript overlap (Brar et al., 2012a). Red1 signals (red) were plotted within 1-kb regions centered at the midpoints between of transcript ends. Nucleosome occupancy signals (blue) (Pan et al., 2011a) were also plotted as described above. The two blue curves represent the positions of transcript ends of each gene (dark blue = forward direction, light blue = reverse direction; see schematic to the left). (C) Enrichment of cohesin subunits and axis proteins was averaged for all convergent transcript ends and plotted as a function of distance from the transcript ends.DOI:http://dx.doi.org/10.7554/eLife.07424.005
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fig2: Red1 accumulates next to transcript ends of convergent gene pairs.(A) Example of overlapping transcripts from a convergent gene pair. ORFs and transcripts of YKL077W and YKL075C were plotted with respect to their positions on chromosome XI. (B) Two-peak pattern of Red1 binding at convergent gene pairs correlates with the amount of transcript overlap. Convergent gene pairs were ranked by the extent of transcript overlap (Brar et al., 2012a). Red1 signals (red) were plotted within 1-kb regions centered at the midpoints between of transcript ends. Nucleosome occupancy signals (blue) (Pan et al., 2011a) were also plotted as described above. The two blue curves represent the positions of transcript ends of each gene (dark blue = forward direction, light blue = reverse direction; see schematic to the left). (C) Enrichment of cohesin subunits and axis proteins was averaged for all convergent transcript ends and plotted as a function of distance from the transcript ends.DOI:http://dx.doi.org/10.7554/eLife.07424.005

Mentions: (A) Red1 distribution was plotted as an average across all genes on each of the 16 chromosomes as well as for the whole genome. The coding regions of genes were normalized to lengths of 1 kb (500 bp–1500 bp on x-axis). 500 bp upstream of the start codon and downstream of the stop codon were included in the plot. (B) Comparison of Red1 binding between convergent and tandem gene pairs. Average signals of Red1 binding were plotted within a 1 kb region from the midpoints of the intergenic regions. Signals were averaged at each bp among all the convergent (red) and tandem (blue) gene pairs across the genome. (C) qPCR analysis of Red1 binding at the YKL077W/YKL075C convergent gene pair before and after insertion of a URA3 transcription unit. Schematic shows the insertion of URA3 in two orientations between YKL077W and YKL075C. ChIP signals were normalized against input and an internal control; the control primer was chosen at the promoter region of YKL077W. Failure to detect a peak doublet upon URA3 insertion may be due to primer positions or because the URA3 transcript does not lead to overlapping transcription (see Figure 2).


Transcription dynamically patterns the meiotic chromosome-axis interface.

Sun X, Huang L, Markowitz TE, Blitzblau HG, Chen D, Klein F, Hochwagen A - Elife (2015)

Red1 accumulates next to transcript ends of convergent gene pairs.(A) Example of overlapping transcripts from a convergent gene pair. ORFs and transcripts of YKL077W and YKL075C were plotted with respect to their positions on chromosome XI. (B) Two-peak pattern of Red1 binding at convergent gene pairs correlates with the amount of transcript overlap. Convergent gene pairs were ranked by the extent of transcript overlap (Brar et al., 2012a). Red1 signals (red) were plotted within 1-kb regions centered at the midpoints between of transcript ends. Nucleosome occupancy signals (blue) (Pan et al., 2011a) were also plotted as described above. The two blue curves represent the positions of transcript ends of each gene (dark blue = forward direction, light blue = reverse direction; see schematic to the left). (C) Enrichment of cohesin subunits and axis proteins was averaged for all convergent transcript ends and plotted as a function of distance from the transcript ends.DOI:http://dx.doi.org/10.7554/eLife.07424.005
© Copyright Policy
Related In: Results  -  Collection

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fig2: Red1 accumulates next to transcript ends of convergent gene pairs.(A) Example of overlapping transcripts from a convergent gene pair. ORFs and transcripts of YKL077W and YKL075C were plotted with respect to their positions on chromosome XI. (B) Two-peak pattern of Red1 binding at convergent gene pairs correlates with the amount of transcript overlap. Convergent gene pairs were ranked by the extent of transcript overlap (Brar et al., 2012a). Red1 signals (red) were plotted within 1-kb regions centered at the midpoints between of transcript ends. Nucleosome occupancy signals (blue) (Pan et al., 2011a) were also plotted as described above. The two blue curves represent the positions of transcript ends of each gene (dark blue = forward direction, light blue = reverse direction; see schematic to the left). (C) Enrichment of cohesin subunits and axis proteins was averaged for all convergent transcript ends and plotted as a function of distance from the transcript ends.DOI:http://dx.doi.org/10.7554/eLife.07424.005
Mentions: (A) Red1 distribution was plotted as an average across all genes on each of the 16 chromosomes as well as for the whole genome. The coding regions of genes were normalized to lengths of 1 kb (500 bp–1500 bp on x-axis). 500 bp upstream of the start codon and downstream of the stop codon were included in the plot. (B) Comparison of Red1 binding between convergent and tandem gene pairs. Average signals of Red1 binding were plotted within a 1 kb region from the midpoints of the intergenic regions. Signals were averaged at each bp among all the convergent (red) and tandem (blue) gene pairs across the genome. (C) qPCR analysis of Red1 binding at the YKL077W/YKL075C convergent gene pair before and after insertion of a URA3 transcription unit. Schematic shows the insertion of URA3 in two orientations between YKL077W and YKL075C. ChIP signals were normalized against input and an internal control; the control primer was chosen at the promoter region of YKL077W. Failure to detect a peak doublet upon URA3 insertion may be due to primer positions or because the URA3 transcript does not lead to overlapping transcription (see Figure 2).

Bottom Line: We found that the axial element proteins of budding yeast are flexibly anchored to chromatin by the ring-like cohesin complex.Importantly, axis anchoring by cohesin is adjustable and readily displaced in the direction of transcription by the transcriptional machinery.We propose that such robust but flexible tethering allows the axial element to promote recombination while easily adapting to changes in chromosome activity.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, New York University, New York, United States.

ABSTRACT
Meiotic chromosomes are highly compacted yet remain transcriptionally active. To understand how chromosome folding accommodates transcription, we investigated the assembly of the axial element, the proteinaceous structure that compacts meiotic chromosomes and promotes recombination and fertility. We found that the axial element proteins of budding yeast are flexibly anchored to chromatin by the ring-like cohesin complex. The ubiquitous presence of cohesin at sites of convergent transcription provides well-dispersed points for axis attachment and thus chromosome compaction. Axis protein enrichment at these sites directly correlates with the propensity for recombination initiation nearby. A separate modulating mechanism that requires the conserved axial-element component Hop1 biases axis protein binding towards small chromosomes. Importantly, axis anchoring by cohesin is adjustable and readily displaced in the direction of transcription by the transcriptional machinery. We propose that such robust but flexible tethering allows the axial element to promote recombination while easily adapting to changes in chromosome activity.

No MeSH data available.


Related in: MedlinePlus