Abstract
The role of the conserved meiotic telomere bouquet has been enigmatic for over a century. We showed previously that disruption of the fission yeast bouquet impairs spindle formation in approximately half of meiotic cells. Surprisingly, bouquet-deficient meiocytes with functional spindles harbour chromosomes that fail to achieve spindle attachment. Kinetochore proteins and the centromeric histone H3 variant Cnp1 fail to localize to those centromeres that exhibit spindle attachment defects in the bouquet’s absence. The HP1 orthologue Swi6 also fails to bind these centromeres, suggesting that compromised pericentromeric heterochromatin underlies the kinetochore defects. We find that centromeres are prone to disassembly during meiosis, but this is reversed by localization of centromeres to the telomere-proximal microenvironment, which is conducive to heterochromatin formation and centromere reassembly. Accordingly, artificially tethering a centromere to a telomere rescues the tethered centromere but not other centromeres. These results reveal an unanticipated level of control of centromeres by telomeres.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Klutstein, M. & Cooper, J. P. The Chromosomal Courtship Dance-homolog pairing in early meiosis. Curr. Opin. Cell Biol. 26, 123–131 (2014).
Yoshida, M. et al. Microtubule-organizing center formation at telomeres induces meiotic telomere clustering. J. Cell Biol. 200, 385–395 (2013).
Ding, D. Q., Yamamoto, A., Haraguchi, T. & Hiraoka, Y. Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev. Cell 6, 329–341 (2004).
Cooper, J. P., Watanabe, Y. & Nurse, P. Fission yeast Taz1 protein is required for meiotic telomere clustering and recombination. Nature 392, 828–831 (1998).
Chikashige, Y. et al. Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125, 59–69 (2006).
Ding, X. et al. SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev. Cell 12, 863–872 (2007).
Conrad, M. N. et al. Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination. Cell 133, 1175–1187 (2008).
Chua, P. R. & Roeder, G. S. Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. Genes Dev. 11, 1786–1800 (1997).
Davis, L. & Smith, G. R. The meiotic bouquet promotes homolog interactions and restricts ectopic recombination in Schizosaccharomyces pombe. Genetics 174, 167–177 (2006).
Nimmo, E. R., Pidoux, A. L., Perry, P. E. & Allshire, R. C. Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe. Nature 392, 825–828 (1998).
Niwa, O., Shimanuki, M. & Miki, F. Telomere-led bouquet formation facilitates homologous chromosome pairing and restricts ectopic interaction in fission yeast meiosis. EMBO J. 19, 3831–3840 (2000).
Tomita, K. & Cooper, J. P. The telomere bouquet controls the meiotic spindle. Cell 130, 113–126 (2007).
Jain, D., Hebden, A. K., Nakamura, T. M., Miller, K. M. & Cooper, J. P. HAATI survivors replace canonical telomeres with blocks of generic heterochromatin. Nature 467, 223–227 (2010).
O’ Sullivan, R. J. et al. Rapid induction of alternative lengthening of telomeres by depletion of the histone chaperone ASF1. Nat. Struct. Mol. Biol. 21, 167–174 (2014).
Heaphy, C. M. et al. Altered telomeres in tumors with ATRX and DAXX mutations. Science 333, 425 (2011).
Kawashima, S. A. et al. Shugoshin enables tension-generating attachment of kinetochores by loading Aurora to centromeres. Genes Dev. 21, 420–435 (2007).
Bernard, P. et al. Requirement of heterochromatin for cohesion at centromeres. Science 294, 2539–2542 (2001).
Folco, H. D., Pidoux, A. L., Urano, T. & Allshire, R. C. Heterochromatin and RNAi are required to establish CENP-A chromatin at centromeres. Science 319, 94–97 (2008).
Yokobayashi, S. & Watanabe, Y. The kinetochore protein Moa1 enables cohesion-mediated monopolar attachment at meiosis I. Cell 123, 803–817 (2005).
Kitajima, T. S., Kawashima, S. A. & Watanabe, Y. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427, 510–517 (2004).
Tomita, K., Bez, C., Fennell, A. & Cooper, J. P. A single internal telomere tract ensures meiotic spindle formation. EMBO Rep. 14, 252–260 (2013).
Fennell, A., Fernandez-Alvarez, A., Tomita, K. & Cooper, J. P. Telomeres and centromeres have interchangeable roles in promoting meiotic spindle formation. J. Cell Biol. 208, 415–428 (2015).
Sakuno, T., Tada, K. & Watanabe, Y. Kinetochore geometry defined by cohesion within the centromere. Nature 458, 852–858 (2009).
Takahashi, K., Chen, E. S. & Yanagida, M. Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast. Science 288, 2215–2219 (2000).
Palmer, D. K., O’Day, K., Wener, M. H., Andrews, B. S. & Margolis, R. L. A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones. J. Cell Biol. 104, 805–815 (1987).
Vafa, O. & Sullivan, K. F. Chromatin containing CENP-A and α-satellite DNA is a major component of the inner kinetochore plate. Curr. Biol. 7, 897–900 (1997).
Blower, M. D. & Karpen, G. H. The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nat. Cell Biol. 3, 730–739 (2001).
Hayashi, A., Asakawa, H., Haraguchi, T. & Hiraoka, Y. Reconstruction of the kinetochore during meiosis in fission yeast Schizosaccharomyces pombe. Mol. Biol. Cell 17, 5173–5184 (2006).
Sanchez-Perez, I. et al. The DASH complex and Klp5/Klp6 kinesin coordinate bipolar chromosome attachment in fission yeast. EMBO J. 24, 2931–2943 (2005).
Liu, X., McLeod, I., Anderson, S., Yates, J. R. III & He, X. Molecular analysis of kinetochore architecture in fission yeast. EMBO J. 24, 2919–2930 (2005).
Smith, K. M., Phatale, P. A., Sullivan, C. M., Pomraning, K. R. & Freitag, M. Heterochromatin is required for normal distribution of Neurospora crassa CenH3. Mol. Cell. Biol. 31, 2528–2542 (2011).
Nakashima, H. et al. Assembly of additional heterochromatin distinct from centromere-kinetochore chromatin is required for de novo formation of human artificial chromosome. J. Cell Sci. 118, 5885–5898 (2005).
Ekwall, K. et al. The chromodomain protein Swi6: a key component at fission yeast centromeres. Science 269, 1429–1431 (1995).
Ekwall, K. et al. Mutations in the fission yeast silencing factors clr4+ and rik1+ disrupt the localisation of the chromo domain protein Swi6p and impair centromere function. J. Cell Sci. 109, 2637–2648 (1996).
Volpe, T. et al. RNA interference is required for normal centromere function in fission yeast. Chromosome Res. 11, 137–146 (2003).
Kitajima, T. S., Yokobayashi, S., Yamamoto, M. & Watanabe, Y. Distinct cohesin complexes organize meiotic chromosome domains. Science 300, 1152–1155 (2003).
Yamamoto, A., West, R. R., McIntosh, J. R. & Hiraoka, Y. A cytoplasmic dynein heavy chain is required for oscillatory nuclear movement of meiotic prophase and efficient meiotic recombination in fission yeast. J. Cell Biol. 145, 1233–1249 (1999).
Hiraoka, Y., Ding, D. Q., Yamamoto, A., Tsutsumi, C. & Chikashige, Y. Characterization of fission yeast meiotic mutants based on live observation of meiotic prophase nuclear movement. Chromosoma 109, 103–109 (2000).
Chikashige, Y. et al. Chromosomes rein back the spindle pole body during horsetail movement in fission yeast meiosis. Cell Struct. Funct. 39, 93–100 (2014).
Chikashige, Y. et al. Meiotic nuclear reorganization: switching the position of centromeres and telomeres in the fission yeast Schizosaccharomyces pombe. EMBO J. 16, 193–202 (1997).
Naito, T., Matsuura, A. & Ishikawa, F. Circular chromosome formation in a fission yeast mutant defective in two ATM homologues. Nat. Genet. 20, 203–206 (1998).
Sadaie, M., Naito, T. & Ishikawa, F. Stable inheritance of telomere chromatin structure and function in the absence of telomeric repeats. Genes Dev. 17, 2271–2282 (2003).
Nakamura, T. M., Cooper, J. P. & Cech, T. R. Two modes of survival of fission yeast without telomerase. Science 282, 493–496 (1998).
Dodgson, J. et al. Spatial segregation of polarity factors into distinct cortical clusters is required for cell polarity control. Nat. Commun. 4, 1834 (2013).
Schober, H., Ferreira, H., Kalck, V., Gehlen, L. R. & Gasser, S. M. Yeast telomerase and the SUN domain protein Mps3 anchor telomeres and repress subtelomeric recombination. Genes Dev. 23, 928–938 (2009).
Taddei, A. et al. The functional importance of telomere clustering: global changes in gene expression result from SIR factor dispersion. Genome Res. 19, 611–625 (2009).
Asakawa, H., Hayashi, A., Haraguchi, T. & Hiraoka, Y. Dissociation of the Nuf2-Ndc80 complex releases centromeres from the spindle-pole body during meiotic prophase in fission yeast. Mol. Biol. Cell 16, 2325–2338 (2005).
Liu, L., Blasco, M. A. & Keefe, D. L. Requirement of functional telomeres for metaphase chromosome alignments and integrity of meiotic spindles. EMBO Rep. 3, 230–234 (2002).
Moreno, S., Klar, A. & Nurse, P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795–823 (1991).
Bahler, J. et al. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943–951 (1998).
Hentges, P., Van Driessche, B., Tafforeau, L., Vandenhaute, J. & Carr, A. M. Three novel antibiotic marker cassettes for gene disruption and marker switching in Schizosaccharomyces pombe. Yeast 22, 1013–1019 (2005).
Sato, M., Dhut, S. & Toda, T. New drug-resistant cassettes for gene disruption and epitope tagging in Schizosaccharomyces pombe. Yeast 22, 583–591 (2005).
Grimm, C., Kohli, J., Murray, J. & Maundrell, K. Genetic engineering of Schizosaccharomyces pombe: a system for gene disruption and replacement using the ura4 gene as a selectable marker. Mol. Gen. Genet. 215, 81–86 (1988).
Lorentz, A., Ostermann, K., Fleck, O. & Schmidt, H. Switching gene swi6, involved in repression of silent mating-type loci in fission yeast, encodes a homologue of chromatin-associated proteins from Drosophila and mammals. Gene 143, 139–143 (1994).
Bannister, A. J. et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120–124 (2001).
Acknowledgements
We thank our current and former laboratory members for discussions and advice, and R. Allshire (Wellcome Trust, University of Edinburgh, UK), M. Sato (University of Tokyo, Japan), T. Toda (Cancer Research UK, UK) and Y. Watanabe (University of Tokyo, Japan) for strains and reagents. We thank M. Lichten, S. Grewal and their laboratory members for discussion and help with reagents and equipment during our recent move. This work was supported by the National Institutes of Health, Cancer Research UK, the European Research Council, and a Marie Curie fellowship to M.K.
Author information
Authors and Affiliations
Contributions
J.P.C., M.K. and A.F. designed the study. M.K. performed experiments for nearly all figures. A.F. performed the experiments in Fig. 5a and helped with experiments in Figs 3 and 6 as well as strain construction and data analysis throughout. A.F-A. performed the experiments in Figs 6c and 8 and analysis of cells with nuclear membrane markers (Supplementary Videos 3 and 4), and helped with strain construction and data analysis. J.P.C. supervised the study. J.P.C. and M.K. wrote the manuscript and all authors edited it.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Integrated supplementary information
Supplementary Figure 1 Bouquet deficient meiocytes show failure of chromosome attachment to correctly formed spindles.
(A–C) Examples of bouquet-deficient cells undergoing meiosis. Tubulin and histone H3 are observed via ectopically expressed GFP-Atb2 (green) and endogenous mRFP tagging of one of the two alleles encoding Hht1 (red), respectively. Numbers below frames represent minutes before or after metaphase I. Scale bars represent 5 μm. (D,E) Tubulin and histone H3 are observed via endogenously tagged Atb2-mRFP (red) and endogenous CFP tagging of one of the two alleles encoding Hht1 (blue), respectively. Labels as in A. (A,B,D,E) bqt1Δ meiosis. The spindle forms correctly but some chromosomes (arrows) fail to attach to those spindles and remain unsegregated. (C) rap1Δ meiosis. The spindle forms correctly but some chromosomes (arrows) fail to attach to those spindles and remain unsegregated. (F) Bouquet deficient cells form spindles with normal elongation rates. The time from anaphase I onset to the moment of maximal spindle length was measured. Red dots represent values for each individual cell; black lines represent the mean +/− standard error. Wt and bqt1Δ cells with good spindles have identical maximal spindle lengths and rates of spindle elongation.
Supplementary Figure 2 Bouquet deficient meiocytes show incomplete recruitment of Dad1 and Mis6 to centromeres.
(A,B) Series of frames from films of cells undergoing meiosis. Dad1 is observed via endogenous GFP tagging, and histone H3 via mRFP tagging as in Fig. 1. Numbers below frames represent minutes before or after metaphase I. Scale bars represent 5 μm. (A) wt meiosis. Dad1-GFP appears at all chromatin masses at MI and MII. (B) bqt1Δ meiosis. Some chromosomes (arrows) fail to recruit Dad1 and remain unsegregated. (C,D) Series of frames from films of cells undergoing meiosis. Mis6 is observed via endogenous functional GFP tagging. cenI–TetO/R is observed as in Fig. 2 Numbers below frames represent minutes before or after metaphase I. Scale bars represent 5 μm. (C) wt meiosis. Mis6-GFP is correctly recruited to centromere I. (D) bqt1Δ meiosis. In some cases centromere I fails to recruit Mis6 and remains unsegregated. (E) Quantitation of Dad1 localization. For each genetic background, the percentage of cells harbouring unsegregated chromosomes is plotted; the superimposed colour code specifies the pattern of Dad1-GFP signal in those cells. See Methods for definitions of ‘stable’ and ‘unstable’. Number of cells filmed is indicated above each lane. Asterisks indicate significant difference from wt calculated using Fisher’s exact test (wt-bqt1Δ p = 10−8, wt-rap1Δ p = 2 × 10−5; see Methods). (F) Quantitation of Mis6 localization on centromere I. The percentage of cells harbouring unsegregated centromere I is plotted; the superimposed colour code specifies the pattern of Mis6-GFP signal on those centromeres. Number of cells filmed is indicated above each lane. Asterisk indicates significant difference from wt calculated using Fisher’s exact test (wt-bqt1Δ P = 0.04).
Supplementary Figure 3 Bouquet deficient meiocytes fail to properly assemble outer kinetochores.
(A–C) Nnf1 and chromosomes are observed via endogenously tagged functional Nnf1-GFP and Hht1-mRFP (as in Fig. 1), respectively. Nnf1 disappears from centromeres in early prophase and relocalizes to centromeres 10-40 min before metaphase I. Labels as in Supplementary Fig. 1. (A) wt meiosis. Nnf1-GFP appears on all chromatin masses at MI and MII. (B,C) bqt1Δ meiosis. Some chromosomes fail to recruit Nnf1 and remain unsegregated (arrows). (D) Quantitation of Nnf1 localization. For each genetic background, the percentage of cells harbouring unsegregated chromosomes is plotted; the superimposed colour code specifies the pattern of Nnf1-GFP signal in those cells. See Methods for definitions of ‘stable’ and ‘unstable’. Labels as in Supplementary Fig. 1. (wt-bqt1Δ p = 0.0014).
Supplementary Figure 4 Centromere assembly failure occurs not only in meiocytes with functional spindles, but also in those with dysfunctional spindles.
Series of frames from films of cells undergoing meiosis. Cnp1 and Swi6 are observed as in Fig. 2. Histone H3 is observed by CFP tagging as in Supplementary Fig. 1, and tubulin and SPB by endogenous mCherry tagging of Atb2 and Sid4. Numbers below frames represent minutes before or after metaphase I. Scale bars represent 5 μm. In these three examples, SPBs are scattered far from chromatin and spindles fail to assemble properly. Some chromosomes lacking kinetochore signals (either Cnp1 or Swi6; arrows) can be discerned as they separate from the main chromatin mass.
Supplementary Figure 5 Meiocytes deficient in pericentromeric heterochromatin formation show centromere assembly defects.
(A) Genetic epistasis analysis of mutations that abolish the bouquet or compromise heterochromatin assembly. Cumulative frequencies of non-attachment events in MI and MII are observed via GFP-Atb2, Sid4-GFP and Hht1-mRFP (as in Fig. 1). Asterisks indicate that all mutant backgrounds differ significantly from wt; no significant difference is observed among the various mutant genotypes. Number of cells filmed is indicated above each bar. Significance was calculated using Fisher’s exact test (wt-bqt1Δ p = 5 × 10−5, wt-clr4Δ p = 0.002, wt-clr4Δ bqt1Δ p = 0.0005, wt-dcr1Δ p = 0.01, wt-dcr1Δ bqt1Δ p = 0.0001, see Methods for details). (B) Series of frames of a film of a cell undergoing meiosis. Cnp1, tubulin and chromatin are observed via ectopically expressed Cnp1-GFP (green) atb2-mCherry (red) and Hht1-CFP (blue), respectively. Numbers below frames represent minutes before or after metaphase I. Scale bars represent 5 μm. This film shows an example of clr4Δ meiosis. Some chromosomes (arrows) fail to recruit cohesin and thus missegregate, while maintaining high levels of Cnp1.
Supplementary Figure 6 Impaired kinetochore function in meiocytes harbouring circular chromosomes.
Series of frames of cells undergoing meiosis. Cnp1, tubulin, SPB and chromatin are observed via ectopically expressed Cnp1-GFP, Atb2-mCherry, Sid4-mCherry (red) and Hht1-CFP, respectively. Numbers below frames represent minutes before or after metaphase I. Scale bars represent 5 μm. Circular chromosome-containing meiocytes suffer similar phenotypes to bouquet-deficient linear chromosome-containing meiocytes. In these examples, spindles form properly but some chromosomes (arrows) lack kinetochore signals and fail to attach. The top two series show MI missegregation, and the bottom shows an unsegregated chromatid at MII.
Supplementary Figure 7 Chr III is not inherently protected from centromere assembly defects.
A potential alternative explanation for the attachment of Chr III to the spindle in a ‘circular + internal telo’ background could stem from the unique presence on Chr III of the rDNA repeats, whose heterochromatic nature could conceivably protect the centromere of Chr III from effects of bouquet deficiency. To assess this possibility, we monitored the attachment of Chr III to the spindle in linear chromosome-containing bqt1Δ meiocytes via endogenously GFP-tagged and functional Reb1, a rDNA binding protein. Of 29 cells with functional spindles, 10 had chromosomes remaining in the centre of the cell at anaphase I or II. In 4 of these 10, the unsegregated chromosome harboured Reb1 signal, indicating that the centromere of Chr III does not enjoy singular protection from non-attachment; rather, the internal telomere stretch affords proper kinetochore assembly on circular Chr III. Representative films are shown. Numbers below frames represent time relative to metaphase I. Scale bar represents 5 μm. Chr III resides in the middle of the cell at anaphase I (arrow), indicating failed segregation.
Supplementary information
Supplementary Information
Supplementary Information (PDF 1461 kb)
Supplementary Table 1
Supplementary Information (XLSX 21 kb)
Correct attachment of chromosomes to the spindle in wt meiosis.
Film of a wt cell undergoing meiosis. Tubulin (green) and histone H3 (red) are observed as in Fig. 1. All chromosomes attach correctly to the spindle and segregate correctly in MI and MII. (MOV 360 kb)
Bouquet deficient meiocytes fail in chromosome attachment to correctly formed spindles.
Film of a rap1Δ cell undergoing meiosis. Tubulin (green) and histone H3 (red) are observed as in Fig. 1. Bouquet formation fails, and a chromatin mass fails to associate with the spindle and remains unsegregated in MI and MII. (MOV 580 kb)
Nuclear rupture does not occur in bouquet deficient meiocytes.
Films of bqt1Δ cells undergoing meiosis. Ish1-GFP (a nuclear membrane marker, green), tubulin and SPB (red) and histone H3 (blue) are observed. The nucleus remains as one entity and does not undergo breakage; nonetheless, a chromatin mass fails to associate with the spindle and remains unsegregated at MI and MII. (MOV 1804 kb)
Nuclear rupture does not occur in bouquet deficient meiocytes.
Films of bqt1Δ cells undergoing meiosis. Ish1-GFP (a nuclear membrane marker, green), tubulin and SPB (red) and histone H3 (blue) are observed. The nucleus remains as one entity and does not undergo breakage; nonetheless, a chromatin mass fails to associate with the spindle and remains unsegregated at MI and MII. (MOV 5391 kb)
Correct kinetochore assembly in wt meiosis.
Film of a wt cell undergoing meiosis. Cnp1 (green) and histone H3 (red) are observed as in Fig. 2. Cnp1-GFP appears at all chromatin masses at MI and MII. (MOV 282 kb)
Bouquet deficient meiocytes fail to properly load Cnp1.
Film of a bqt1Δ cell undergoing meiosis. Cnp1 (green) and histones (red) are observed as in Fig. 2. Note that at MI a chromatin mass remains unsegregated. This unsegregated chromatin mass lacks detectable Cnp1-GFP. (MOV 577 kb)
Correct pericentromeric heterochromatin formation in wt meiosis.
Film of a wt cell undergoing meiosis. Swi6 (green) and cenI (red) are observed as in Fig. 3. Swi6-GFP localizes to centromeres and telomeres; the latter are seen moving with the leading edge of the nucleus (where the SPB is located) during the horsetail period. Swi6 is correctly recruited to cenI throughout meiosis. (MOV 141 kb)
Bouquet deficient meiocytes show defects in pericentromeric heterochromatin formation.
Film of a bqt1Δ cell undergoing meiosis. Swi6 (green) and cenI (red) are observed as in Fig. 3. Note that cenI fails to attach to the spindle and remains unsegregated. This cenI lacks detectable Swi6-GFP signal. (MOV 318 kb)
Heterochromatin deficient meiocytes fail to properly assemble kinetochores.
Film of a clr4Δ cell undergoing meiosis. Cnp1 (green), tubulin (red) and histone H3 (blue) are observed. Despite proper bouquet formation, a chromatin mass fails to recruit Cnp1 and remains unsegregated at MI. (MOV 408 kb)
Heterochromatin deficient meiocytes show failure of chromosome attachment to correctly formed spindles.
Film of a clr4Δ cell undergoing meiosis. Tubulin (green) and histone H3 (red) are observed. Despite proper bouquet formation, a chromatin mass fails to associate with the spindle and remains unsegregated at MI. (MOV 1999 kb)
Telomeres and centromeres co-localize at the onset of meiotic prophase.
Film of wt azygotic meiotic prophase. Centromeres (green) and telomeres (red) are observed as in Fig. 5. A subset of centromeres and telomeres co-localize in many frames, until all telomeres localize to the SPB and all centromeres are released on the onset of horsetail nuclear movements. (MOV 1961 kb)
Chromosomes associated with the bouquet are protected from centromere assembly defects.
Film of a ‘circular + internal telo’ cell undergoing meiosis. Tubulin and SPB (red), Taz1 (green) and histone H3 (blue) are observed as in Fig. 5. Note that the chromosome attached to spindle harbours a Taz1-YFP signal, while chromosomes off the spindle lack this signal. (MOV 778 kb)
Centromeres tethered to the bouquet during prophase are protected from centromere assembly defects.
Film of two ‘circular + internal telo’ meiocytes harbouring Bqt1-GBP, cenI-lacO/I (green) and histone H3 (red) as in Fig. 6. In both cells, all cenI-containing chromosomes attach to the spindle. Chromatin collapse immediately following spindle dissolution at MI and MII is typical in ‘circular’ strains due to catenation of their chromosomes. (MOV 7204 kb)
Rights and permissions
About this article
Cite this article
Klutstein, M., Fennell, A., Fernández-Álvarez, A. et al. The telomere bouquet regulates meiotic centromere assembly. Nat Cell Biol 17, 458–469 (2015). https://doi.org/10.1038/ncb3132
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ncb3132
This article is cited by
-
Centromeres are dismantled by foundational meiotic proteins Spo11 and Rec8
Nature (2021)
-
Two telomeric ends of acrocentric chromosome play distinct roles in homologous chromosome synapsis in the fetal mouse oocyte
Chromosoma (2021)
-
The telomere bouquet facilitates meiotic prophase progression and exit in fission yeast
Cell Discovery (2017)
-
Position matters: multiple functions of LINC-dependent chromosome positioning during meiosis
Current Genetics (2017)
-
E-type cyclins modulate telomere integrity in mammalian male meiosis
Chromosoma (2016)
