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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

Model of the interface between axial elements and DNA.Using the topological protein–DNA interaction of cohesin, a robust linkage between a protein rod (the axial element) and a transcriptionally active chromosome can be established. The protein axis forms on top of cohesin, while the elongating RNAPII, likely unable to pass through the cohesin molecule, may pull the DNA through the complex to avoid a premature transcription block. Blue arrows indicate the direction of DNA flow, going in the opposite direction of transcription. Based on the range of transcriptional overlap, loop movements will in most cases not exceed 500 bp and are not drawn to scale.DOI:http://dx.doi.org/10.7554/eLife.07424.015
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fig8: Model of the interface between axial elements and DNA.Using the topological protein–DNA interaction of cohesin, a robust linkage between a protein rod (the axial element) and a transcriptionally active chromosome can be established. The protein axis forms on top of cohesin, while the elongating RNAPII, likely unable to pass through the cohesin molecule, may pull the DNA through the complex to avoid a premature transcription block. Blue arrows indicate the direction of DNA flow, going in the opposite direction of transcription. Based on the range of transcriptional overlap, loop movements will in most cases not exceed 500 bp and are not drawn to scale.DOI:http://dx.doi.org/10.7554/eLife.07424.015

Mentions: Significantly, our findings indicate that anchoring of the axial element is highly flexible. We demonstrate that axis protein accumulation peaks ∼150 bp downstream of transcript ends and is actively driven by differential promoter activity, implying that axis proteins are not stably bound to DNA. For steric reasons, the observed double peaks likely reflect the average distribution of axis proteins within the assayed cell population, rather than the distribution along a single chromatid. Given that the cohesin ring was previously proposed to slide along chromatin in response to transcription (Bausch et al., 2007; Ocampo-Hafalla and Uhlmann, 2011), these data indicate that cohesin sliding controls the sites of axis protein attachment. We note that this system allows DNA to be robustly anchored to the protein axis with enough flexibility to allow dynamic processes such as transcription to proceed undisturbed on the DNA (Figure 8).10.7554/eLife.07424.015Figure 8.Model of the interface between axial elements and DNA.


Transcription dynamically patterns the meiotic chromosome-axis interface.

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

Model of the interface between axial elements and DNA.Using the topological protein–DNA interaction of cohesin, a robust linkage between a protein rod (the axial element) and a transcriptionally active chromosome can be established. The protein axis forms on top of cohesin, while the elongating RNAPII, likely unable to pass through the cohesin molecule, may pull the DNA through the complex to avoid a premature transcription block. Blue arrows indicate the direction of DNA flow, going in the opposite direction of transcription. Based on the range of transcriptional overlap, loop movements will in most cases not exceed 500 bp and are not drawn to scale.DOI:http://dx.doi.org/10.7554/eLife.07424.015
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4530585&req=5

fig8: Model of the interface between axial elements and DNA.Using the topological protein–DNA interaction of cohesin, a robust linkage between a protein rod (the axial element) and a transcriptionally active chromosome can be established. The protein axis forms on top of cohesin, while the elongating RNAPII, likely unable to pass through the cohesin molecule, may pull the DNA through the complex to avoid a premature transcription block. Blue arrows indicate the direction of DNA flow, going in the opposite direction of transcription. Based on the range of transcriptional overlap, loop movements will in most cases not exceed 500 bp and are not drawn to scale.DOI:http://dx.doi.org/10.7554/eLife.07424.015
Mentions: Significantly, our findings indicate that anchoring of the axial element is highly flexible. We demonstrate that axis protein accumulation peaks ∼150 bp downstream of transcript ends and is actively driven by differential promoter activity, implying that axis proteins are not stably bound to DNA. For steric reasons, the observed double peaks likely reflect the average distribution of axis proteins within the assayed cell population, rather than the distribution along a single chromatid. Given that the cohesin ring was previously proposed to slide along chromatin in response to transcription (Bausch et al., 2007; Ocampo-Hafalla and Uhlmann, 2011), these data indicate that cohesin sliding controls the sites of axis protein attachment. We note that this system allows DNA to be robustly anchored to the protein axis with enough flexibility to allow dynamic processes such as transcription to proceed undisturbed on the DNA (Figure 8).10.7554/eLife.07424.015Figure 8.Model of the interface between axial elements and DNA.

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