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PMID: 16532354 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

S. pombe linear elements: the modest cousins of synaptonemal complexes.

Chromosoma ·Vol. 115 ·No. 3 ·2006-06-00 ·Pages 260-71

Loidl J

Abstract

Synaptonemal complexes (SCs) are not formed during meiotic prophase in the fission yeast, Schizosaccharomyces pombe. Instead, so-called linear elements (LinEs) are formed at the corresponding stages. LinEs are remarkable in that their number does not correspond to the number of chromosomes or bivalents and that the changes in their organisation during prophase do not evidently reflect the pairing of chromosomes. Yet, LinEs are necessary for full meiotic pairing levels and for meiotic recombination. In this review, the composition of LinEs, their evolutionary relationship to SCs and their possible functions are discussed.

MeSH Terms
Cell Cycle Proteins/genetics,metabolism,ultrastructure Cell Nucleus Structures/physiology Meiosis Recombination, Genetic Schizosaccharomyces Schizosaccharomyces pombe Proteins/genetics,physiology Synaptonemal Complex/genetics,physiology
Chemicals
Cell Cycle Proteins Schizosaccharomyces pombe Proteins
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Loidl Josef
Department of Chromosome Biology, University of Vienna, Rennweg 14, 1030, Vienna, Austria. [email protected]
References (87)
87 references, click to expand
  1. Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1.
    Mol Biol Cell. 2005 Dec;16(12):5804-18 PMID: 16221890
  2. The yeast Red1 protein localizes to the cores of meiotic chromosomes.
    J Cell Biol. 1997 Mar 10;136(5):957-67 PMID: 9060462
  3. Telomere-led bouquet formation facilitates homologous chromosome pairing and restricts ectopic interaction in fission yeast meiosis.
    EMBO J. 2000 Jul 17;19(14):3831-40 PMID: 10899136
  4. c(3)G encodes a Drosophila synaptonemal complex protein.
    Genes Dev. 2001 Dec 1;15(23):3130-43 PMID: 11731477
  5. The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing.
    J Cell Sci. 2003 Jul 15;116(Pt 14):2999-3007 PMID: 12783989
  6. [Comparative genomics and proteomics of Drosophila, Brenner's nematode, and Arabidopsis: identification of functionally similar genes and proteins of meiotic chromosome synapsis].
    Genetika. 2002 Aug;38(8):1078-89 PMID: 12244692
  7. Fission yeast Pds5 is required for accurate chromosome segregation and for survival after DNA damage or metaphase arrest.
    J Cell Sci. 2002 Feb 1;115(Pt 3):587-98 PMID: 11861765
  8. Unusual nuclear structures in meiotic prophase of fission yeast: a cytological analysis.
    J Cell Biol. 1993 Apr;121(2):241-56 PMID: 8468345
  9. Cohesins are required for meiotic DNA breakage and recombination in Schizosaccharomyces pombe.
    Proc Natl Acad Sci U S A. 2005 Aug 2;102(31):10952-7 PMID: 16043696
  10. Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation.
    Cell. 2002 Dec 13;111(6):791-802 PMID: 12526806
  11. Meiotic chromosomes: integrating structure and function.
    Annu Rev Genet. 1999;33:603-754 PMID: 10690419
  12. Meiotic recombination remote from prominent DNA break sites in S. pombe.
    Mol Cell. 2002 Feb;9(2):253-63 PMID: 11864600
  13. Red1p, a MEK1-dependent phosphoprotein that physically interacts with Hop1p during meiosis in yeast.
    J Biol Chem. 1999 Jan 15;274(3):1783-90 PMID: 9880561
  14. Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast.
    Dev Cell. 2004 Mar;6(3):329-41 PMID: 15030757
  15. The evolution of meiosis: recruitment and modification of somatic DNA-repair proteins.
    Bioessays. 2005 Aug;27(8):795-808 PMID: 16015600
  16. Recombination protein Tid1p controls resolution of cohesin-dependent linkages in meiosis in Saccharomyces cerevisiae.
    J Cell Biol. 2005 Oct 24;171(2):241-53 PMID: 16230461
  17. Dynamic behavior of microtubules during dynein-dependent nuclear migrations of meiotic prophase in fission yeast.
    Mol Biol Cell. 2001 Dec;12(12):3933-46 PMID: 11739791
  18. Meiotic DNA breaks at the S. pombe recombination hot spot M26.
    Mol Cell. 2002 Apr;9(4):847-55 PMID: 11983175
  19. Roles of RecA homologues Rad51 and Dmc1 during meiotic recombination.
    Cytogenet Genome Res. 2004;107(3-4):201-7 PMID: 15467365
  20. A meiosis-specific protein kinase homolog required for chromosome synapsis and recombination.
    Genes Dev. 1991 Dec;5(12B):2392-404 PMID: 1752435
  21. Multiple branches of the meiotic recombination pathway contribute independently to homolog pairing and stable juxtaposition during meiosis in budding yeast.
    Genes Dev. 2005 Apr 1;19(7):863-74 PMID: 15805472
  22. Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1beta and SMC3.
    J Cell Biol. 2003 Mar 3;160(5):657-70 PMID: 12615909
  23. Synaptonemal complex morphogenesis and sister-chromatid cohesion require Mek1-dependent phosphorylation of a meiotic chromosomal protein.
    Genes Dev. 1998 Nov 15;12(22):3551-63 PMID: 9832507
  24. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis.
    Cell. 1999 Jul 9;98(1):91-103 PMID: 10412984
  25. Crossover site determination and interference.
    J Theor Biol. 1988 Oct 21;134(4):565-70 PMID: 3255012
  26. Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes.
    Cell. 2004 Mar 19;116(6):795-802 PMID: 15035982
  27. Telomere-led premeiotic chromosome movement in fission yeast.
    Science. 1994 Apr 8;264(5156):270-3 PMID: 8146661
  28. The meiotic recombination checkpoint is regulated by checkpoint rad+ genes in fission yeast.
    EMBO J. 2002 Jun 3;21(11):2807-18 PMID: 12032093
  29. The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing and sister-chromatid cohesion during meiosis.
    Genetics. 1995 Sep;141(1):61-73 PMID: 8536990
  30. Linear element formation and their role in meiotic sister chromatid cohesion and chromosome pairing.
    J Cell Sci. 2003 May 1;116(Pt 9):1719-31 PMID: 12665553
  31. Microtubule-driven nuclear movements and linear elements as meiosis-specific characteristics of the fission yeasts Schizosaccharomyces versatilis and Schizosaccharomyces pombe.
    Chromosoma. 1995 Nov;104(3):203-14 PMID: 8529460
  32. RED1: a yeast gene required for the segregation of chromosomes during the reductional division of meiosis.
    Proc Natl Acad Sci U S A. 1988 Aug;85(16):6057-61 PMID: 3413075
  33. Meiotic chromosomes: it takes two to tango.
    Genes Dev. 1997 Oct 15;11(20):2600-21 PMID: 9334324
  34. Organization and pairing of meiotic chromosomes in the ciliate Tetrahymena thermophila.
    J Cell Sci. 2004 Nov 15;117(Pt 24):5791-801 PMID: 15522890
  35. Mcp6, a meiosis-specific coiled-coil protein of Schizosaccharomyces pombe, localizes to the spindle pole body and is required for horsetail movement and recombination.
    J Cell Sci. 2005 Jan 15;118(Pt 2):447-59 PMID: 15654021
  36. The Saccharomyces cerevisiae MUM2 gene interacts with the DNA replication machinery and is required for meiotic levels of double strand breaks.
    Genetics. 2001 Mar;157(3):1179-89 PMID: 11238403
  37. BimD/SPO76 is at the interface of cell cycle progression, chromosome morphogenesis, and recombination.
    Proc Natl Acad Sci U S A. 2001 May 22;98(11):6267-72 PMID: 11353817
  38. Meiotic recombination proteins localize to linear elements in Schizosaccharomyces pombe.
    Chromosoma. 2006 Aug;115(4):330-40 PMID: 16532353
  39. A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction.
    Genes Dev. 2001 Jun 1;15(11):1349-60 PMID: 11390355
  40. Regulation of meiotic progression by the meiosis-specific checkpoint kinase Mek1 in fission yeast.
    J Cell Sci. 2003 Jan 15;116(Pt 2):259-71 PMID: 12482912
  41. Hrs1p/Mcp6p on the meiotic SPB organizes astral microtubule arrays for oscillatory nuclear movement.
    Curr Biol. 2005 Aug 23;15(16):1479-86 PMID: 16111942
  42. Genetic interactions between HOP1, RED1 and MEK1 suggest that MEK1 regulates assembly of axial element components during meiosis in the yeast Saccharomyces cerevisiae.
    Genetics. 1997 Sep;147(1):33-42 PMID: 9286666
  43. Meiosis induced by inactivation of Pat1 kinase proceeds with aberrant nuclear positioning of centromeres in the fission yeast Schizosaccharomyces pombe.
    Genes Cells. 2004 Aug;9(8):671-84 PMID: 15298676
  44. Meiotic nuclear reorganization: switching the position of centromeres and telomeres in the fission yeast Schizosaccharomyces pombe.
    EMBO J. 1997 Jan 2;16(1):193-202 PMID: 9009280
  45. Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe.
    Nature. 1998 Apr 23;392(6678):825-8 PMID: 9572142
  46. Monopolar spindle attachment of sister chromatids is ensured by two distinct mechanisms at the first meiotic division in fission yeast.
    EMBO J. 2003 May 1;22(9):2284-96 PMID: 12727894
  47. Chromosome-wide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes.
    Genetics. 2004 Nov;168(3):1275-92 PMID: 15579685
  48. Equal sister chromatid exchange is a major mechanism of double-strand break repair in yeast.
    Mol Cell. 2003 Jun;11(6):1661-71 PMID: 12820977
  49. A cytological study of micronuclear elongation during conjugation in Tetrahymena.
    Chromosoma. 1976 Jun 23;55(4):289-308 PMID: 824106
  50. The synaptonemal complex in genetic segregation.
    Annu Rev Genet. 1984;18:331-413 PMID: 6241453
  51. Conserved and nonconserved proteins for meiotic DNA breakage and repair in yeasts.
    Genetics. 2004 Jun;167(2):593-605 PMID: 15238514
  52. Meiotic DNA breaks associated with recombination in S. pombe.
    Mol Cell. 2000 May;5(5):883-8 PMID: 10882124
  53. MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair.
    Genes Dev. 1995 Jul 15;9(14):1728-39 PMID: 7622037
  54. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis.
    Cell. 2004 Apr 2;117(1):29-45 PMID: 15066280
  55. Juxtaposition of C(2)M and the transverse filament protein C(3)G within the central region of Drosophila synaptonemal complex.
    Proc Natl Acad Sci U S A. 2005 Mar 22;102(12):4482-7 PMID: 15767569
  56. Multiple synaptonemal complexes (polycomplexes): origin, structure and function.
    Cell Biol Int Rep. 1987 Nov;11(11):759-96 PMID: 3319195
  57. A search for synaptonemal complexes in Ustilago maydis.
    J Cell Sci. 1981 Aug;50:171-80 PMID: 7320065
  58. Mammalian protein SCP1 forms synaptonemal complex-like structures in the absence of meiotic chromosomes.
    Mol Biol Cell. 2005 Jan;16(1):212-7 PMID: 15496453
  59. Gene conversions and their relation to homologous chromosome pairing.
    Philos Trans R Soc Lond B Biol Sci. 1986 Jan 29;312(1154):291-302 PMID: 2421362
  60. Dynamics of chromosome organization and pairing during meiotic prophase in fission yeast.
    J Cell Biol. 1994 Oct;127(2):273-85 PMID: 7929575
  61. The genetics and molecular biology of the synaptonemal complex.
    Annu Rev Cell Dev Biol. 2004;20:525-58 PMID: 15473851
  62. Three-dimensional microscopy of the Rad51 recombination protein during meiotic prophase.
    Plant Cell. 1999 May;11(5):809-24 PMID: 10330467
  63. Rad51 recombinase and recombination mediators.
    J Biol Chem. 2003 Oct 31;278(44):42729-32 PMID: 12912992
  64. Fission yeast Taz1 protein is required for meiotic telomere clustering and recombination.
    Nature. 1998 Apr 23;392(6678):828-31 PMID: 9572143
  65. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes.
    Cell. 1990 Apr 6;61(1):73-84 PMID: 2107981
  66. Characterization of rec7, an early meiotic recombination gene in Schizosaccharomyces pombe.
    Genetics. 2001 Feb;157(2):519-32 PMID: 11156975
  67. Un ménage à quatre: the molecular biology of chromosome segregation in meiosis.
    Cell. 2003 Feb 21;112(4):423-40 PMID: 12600308
  68. Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae.
    Genetics. 1992 Oct;132(2):387-402 PMID: 1427035
  69. Whence meiosis?
    Cell. 2001 Sep 21;106(6):647-50 PMID: 11572770
  70. Early decision; meiotic crossover interference prior to stable strand exchange and synapsis.
    Cell. 2004 Apr 2;117(1):9-15 PMID: 15066278
  71. Heterodimeric complexes of Hop2 and Mnd1 function with Dmc1 to promote meiotic homolog juxtaposition and strand assimilation.
    Proc Natl Acad Sci U S A. 2004 Jul 20;101(29):10572-7 PMID: 15249670
  72. Novel genes required for meiotic chromosome segregation are identified by a high-throughput knockout screen in fission yeast.
    Curr Biol. 2005 Sep 20;15(18):1663-9 PMID: 16169489
  73. Cohesin Rec8 is required for reductional chromosome segregation at meiosis.
    Nature. 1999 Jul 29;400(6743):461-4 PMID: 10440376
  74. S. pombe meiotic linear elements contain proteins related to synaptonemal complex components.
    J Cell Sci. 2004 Jul 1;117(Pt 15):3343-51 PMID: 15226405
  75. Cohesins determine the attachment manner of kinetochores to spindle microtubules at meiosis I in fission yeast.
    Mol Cell Biol. 2003 Jun;23(11):3965-73 PMID: 12748297
  76. Homologous recombination in fission yeast: absence of crossover interference and synaptonemal complex.
    Experientia. 1994 Mar 15;50(3):295-306 PMID: 8143803
  77. A novel meiosis-specific protein of fission yeast, Meu13p, promotes homologous pairing independently of homologous recombination.
    EMBO J. 2001 Jul 16;20(14):3871-81 PMID: 11447128
  78. Homologous pairing is reduced but not abolished in asynaptic mutants of yeast.
    J Cell Biol. 1994 Jun;125(6):1191-200 PMID: 8207053
  79. Distinct cohesin complexes organize meiotic chromosome domains.
    Science. 2003 May 16;300(5622):1152-5 PMID: 12750522
  80. A cytoplasmic dynein heavy chain is required for oscillatory nuclear movement of meiotic prophase and efficient meiotic recombination in fission yeast.
    J Cell Biol. 1999 Jun 14;145(6):1233-49 PMID: 10366596
  81. An analysis of interference in the fission yeast Schizosaccharomyces pombe.
    Genetics. 1994 Jul;137(3):701-7 PMID: 8088515
  82. Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans.
    Mol Cell Biol. 1999 May;19(5):3515-28 PMID: 10207075
  83. How do meiotic chromosomes meet their homologous partners?: lessons from fission yeast.
    Bioessays. 2001 Jun;23(6):526-33 PMID: 11385632
  84. Examination of the intron in the meiosis-specific recombination gene REC114 in Saccharomyces.
    Mol Gen Genet. 1997 Jul;255(4):410-9 PMID: 9267437
  85. A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis.
    Curr Biol. 2005 Jan 26;15(2):185-91 PMID: 15668177
  86. Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism.
    EMBO J. 2001 Oct 15;20(20):5779-90 PMID: 11598020
  87. Meiosis in Aspergillus nidulans: another example for lacking synaptonemal complexes in the absence of crossover interference.
    Hereditas. 1982;97(2):179-87 PMID: 6761318
Article Info
Journal
Chromosoma
Abbr.
Chromosoma
ISSN
0009-5915
DOI
10.1007/s00412-006-0047-7
Email
[email protected]
Published
2006-06-00
Epub
2006-00-11
Pages
260-71
Language
English
Region
Austria
NLM ID
2985138R
Subset
IM
External Links
PubMed source DOI: 10.1007/s00412-006-0047-7 View journal details
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