Chromosome mobility during meiotic prophase in Saccharomyces cerevisiae

In many organisms, a synaptonemal complex (SC) intimately connects each pair of homologous chromosomes during much of the first meiotic prophase and is thought to play a role in regulating recombination. In the yeast Saccharomyces cerevisiae, the central element of each SC contains Zip1, a protein orthologous to mammalian SYCP1. To study the dynamics of SCs in living meiotic cells, a functional ZIP1::GFP fusion was introduced into yeast and analyzed by fluorescence video microscopy. During pachytene, SCs exhibited dramatic and continuous movement throughout the nucleus, traversing relatively large distances while twisting, folding, and unfolding. Chromosomal movements were accompanied by changes in the shape of the nucleus, and all movements were reversibly inhibited by the actin antagonist Latrunculin B. Normal movement required the NDJ1 gene, which encodes a meiosis-specific telomere protein needed for the attachment of telomeres to the nuclear periphery and for normal kinetics of recombination and meiosis. These results show that SC movements involve telomere attachment to the nuclear periphery and are actin-dependent and suggest these movements could facilitate completion of meiotic recombination.

[1]  S. Keeney,et al.  Synaptonemal complex formation: where does it start? , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[2]  U. Aebi,et al.  Nuclear actin extends, with no contraction in sight. , 2005, Molecular biology of the cell.

[3]  D. Kaback,et al.  In Vivo Analysis of Synaptonemal Complex Formation During Yeast Meiosis , 2004, Genetics.

[4]  N. Kleckner,et al.  Crossover/Noncrossover Differentiation, Synaptonemal Complex Formation, and Regulatory Surveillance at the Leptotene/Zygotene Transition of Meiosis , 2004, Cell.

[5]  K. Miura,et al.  Dynamic Organization of the Actin Cytoskeleton During Meiosis and Spore Formation in Budding Yeast , 2006, Traffic.

[6]  D. Zickler,et al.  The synaptonemal complex and the spindle plaque during meiosis in yeast , 2004, Chromosoma.

[7]  R. Padmore,et al.  Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae , 1991, Cell.

[8]  G. Roeder,et al.  ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis , 1993, Cell.

[9]  N. Kleckner,et al.  The leptotene-zygotene transition of meiosis. , 1998, Annual review of genetics.

[10]  N. Kleckner,et al.  γ-H2AX illuminates meiosis , 2001, Nature Genetics.

[11]  T. Allers,et al.  Differential Timing and Control of Noncrossover and Crossover Recombination during Meiosis , 2001, Cell.

[12]  Michael E Dresser,et al.  MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae , 2007, Proceedings of the National Academy of Sciences.

[13]  H. Scherthan,et al.  Bouquet formation in budding yeast: initiation of recombination is not required for meiotic telomere clustering. , 1999, Journal of cell science.

[14]  H. Scherthan,et al.  Homologous pairing is reduced but not abolished in asynaptic mutants of yeast , 1994, The Journal of cell biology.

[15]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[16]  N. Kleckner,et al.  Meiotic chromosomes: integrating structure and function. , 1999, Annual review of genetics.

[17]  R. Mortimer,et al.  A polymerization model of chiasma interference and corresponding computer simulation. , 1990, Genetics.

[18]  M. Primig,et al.  Novel Response to Microtubule Perturbation in Meiosis , 2005, Molecular and Cellular Biology.

[19]  G. Fink,et al.  Methods in yeast genetics , 1979 .

[20]  M. Parvinen,et al.  Chromosome rotation and formation of synapsis , 1976, Nature.

[21]  R. Rosenfeld.  Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[22]  C. Heyting,et al.  A coiled‐coil related protein specific for synapsed regions of meiotic prophase chromosomes. , 1992, The EMBO journal.

[23]  M. Conrad,et al.  Ndj1p, a meiotic telomere protein required for normal chromosome synapsis and segregation in yeast. , 1997, Science.

[24]  M. Moses,et al.  Synaptonemal complex analysis of mouse chromosomal rearrangements , 2004, Chromosoma.

[25]  R. Sikorski,et al.  A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. , 1989, Genetics.

[26]  B. Bainbridge,et al.  Genetics , 1981, Experientia.

[27]  J. Brune,et al.  Structural features in a brittle–ductile wax model of continental extension , 1997, nature.

[28]  S. Dwight,et al.  Genetic and physical maps of Saccharomyces cerevisiae. , 1997, Methods in enzymology.

[29]  Josef Loidl,et al.  Meiotic telomere clustering requires actin for its formation and cohesin for its resolution , 2005, The Journal of cell biology.

[30]  Y. Hiraoka,et al.  Meiotic Proteins Bqt1 and Bqt2 Tether Telomeres to Form the Bouquet Arrangement of Chromosomes , 2006, Cell.

[31]  B. Byers,et al.  Electron microscopic observations on the meiotic karyotype of diploid and tetraploid Saccharomyces cerevisiae. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[32]  R. W. Davis,et al.  Replacement of chromosome segments with altered DNA sequences constructed in vitro. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[33]  S. Burgess,et al.  Multiple branches of the meiotic recombination pathway contribute independently to homolog pairing and stable juxtaposition during meiosis in budding yeast. , 2005, Genes & development.

[34]  K. Murata,et al.  Transformation of intact yeast cells treated with alkali cations , 1983 .

[35]  B. Liebe,et al.  Telomere attachment, meiotic chromosome condensation, pairing, and bouquet stage duration are modified in spermatocytes lacking axial elements. , 2003, Molecular biology of the cell.

[36]  H. Scherthan.  Factors directing telomere dynamics in synaptic meiosis. , 2006, Biochemical Society transactions.

[37]  S M Kane,et al.  Carbohydrate Metabolism During Ascospore Development in Yeast , 1974, Journal of bacteriology.

[38]  P. Esponda,et al.  The attachment of the synaptonemal complex to the nuclear envelope , 1972, Chromosoma.

[39]  K. Nairz,et al.  Meiotic chromosome synapsis in a haploid yeast , 1991, Chromosoma.

[40]  Harry Scherthan,et al.  Meiotic Telomere Protein Ndj1p Is Required for Meiosis-Specific Telomere Distribution, Bouquet Formation and Efficient Homologue Pairing , 2000, The Journal of cell biology.

[41]  M. Yanagida,et al.  Telomere-led premeiotic chromosome movement in fission yeast. , 1994, Science.

[42]  G. Roeder,et al.  Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. , 1997, Genes & development.

[43]  B. S. Baker,et al.  The genetic control of meiosis. , 1976, Annual review of genetics.