Skip to main content
SpringerLink
Log in

Diter von Wettstein and The Meiotic Program of Pairing and Recombination

  • Protocol
  • First Online:
Biolistic DNA Delivery in Plants

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2124))

Abstract

Recombination and pairing are prominent features of meiosis where they play an important role in increasing genetic diversity. In most organisms recombination also plays mechanical roles in mediating pairing of homologous chromosomes during prophase and in ensuring regular segregation of homologous pairs at the first meiotic division. The laboratory directed by D. von Wettstein identified six key steps in the meiotic process: (1) Recombination mediated processes occur in physical and functional linkage with the synaptonemal complex (SC), a highly conserved, meiosis-specific structure that links homologous axes along their lengths. (2) The pairing process involves formation and resolution of chromosomal entanglements/interlockings. (3) The SC normally forms specifically between homologous chromosomes, but in unusual situations can form between nonhomologous chromosomes or regions resulting in two-phase SC formation. (4) In hexaploid common wheat, extensive multivalents form with multiple, pairing partner shifts, indicating homology recognition and SC formation among homoeologs as well as homologs. (5) Linkage between recombination and the SC is revealed by crossover-correlated nodules localized in the SC central region. (6) Modified SCs sometimes play a direct role in homolog segregation, providing the required connection between homologs in absence of crossovers/chiasmata.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. von Wettstein D, Rasmussen SW, Holm PB (1984) The synaptonemal complex in genetic segregation. Annu Rev Genet 18:331–413

    Article  Google Scholar 

  2. Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754

    Article  CAS  PubMed  Google Scholar 

  3. Zickler D, Kleckner N (2015) Recombination, pairing, and synapsis of homologs during meiosis. Cold Spring Harb Perspect Biol 7:a016626

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Moses MJ (1956) Chromosome structures in crayfish spermatocytes. J Biophys Biochem Cytol 2:215–218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Fawcett DW (1956) The fine structure of chromosomes in the meiotic prophase of vertebrate spermatocytes. J Biophys Biochem Cytol 2:403–406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Carpenter ATC (1988) Thoughts on recombination nodules, meiotic recombination and chiasmata. In: Kucherlapati R, Smith GR (eds) Genetic recombination. American Society for Microbiology, Washington, DC, pp 549–574

    Google Scholar 

  7. Westergaard M, von Wettstein D (1970) Studies on the mechanism of crossing over. IV. The molecular organization of the synaptinemal complex in Neottiella (Cooke) saccardo (Ascomycetes). C R Trav Lab Carlsberg 37:239–268

    CAS  PubMed  Google Scholar 

  8. Westergaard M, von Wettstein D (1972) The synaptinemal complex. Annu Rev Genet 6:71–110

    Article  CAS  PubMed  Google Scholar 

  9. von Wettstein D (1971) The synaptinemal complex and the four-strand crossing over. Proc Natl Acad Sci U S A 68:851–855

    Article  PubMed Central  Google Scholar 

  10. von Wettstein D (1977) The assembly of the synaptinemal complex. Phil Trans R Soc Lond B 277:235–243

    Article  Google Scholar 

  11. Stern H, Westergaard M, von Wettstein D (1975) Presynaptic events in meiocytes of Lilium longiflorum and their relation to crossing-over: a preselection hypothesis. Proc Natl Acad Sci U S A 72:961–965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Gao J, Colaiácovo MP (2018) Zipping and unzipping: protein modifications regulating Synaptonemal Complex dynamics. Trends Genet 34:232–245

    Article  CAS  PubMed  Google Scholar 

  13. Holm PB, Rasmussen SW, von Wettstein D (1979) The possible contribution of electron microscopy to the understanding of the mechanism of non-disjunction in man. Mutat Res 61:115–119

    Article  CAS  PubMed  Google Scholar 

  14. Holm PB, Rasmussen SW, von Wettstein D (1982) Ultrastructural characterization of the meiotic prophase. A tool in the assessment of radiation damage in man. Mutat Res 95:45–59

    Article  CAS  PubMed  Google Scholar 

  15. Rasmussen SW, Holm PB (1980) Mechanics of meiosis. Hereditas 93:187–216

    Article  CAS  PubMed  Google Scholar 

  16. Rasmussen SW, Holm PB (1984) The synaptonemal complex, recombination nodules and chiasmata in human spermatocytes. Symp Soc Exp Biol 38:271–292

    CAS  PubMed  Google Scholar 

  17. Holm PB (1986) Ultrastructural analysis of meiotic recombination and chiasma formation. Tokai J Exp Clin Med 11:415–436

    CAS  PubMed  Google Scholar 

  18. Moses MJ (1977) Synaptonemal complex karyotyping in spermatocytes of the Chinese hamster (Cricetulus griseus). I. Morphology of the autosomal complement in spread preparations. Chromosoma 60:99–125

    Article  CAS  PubMed  Google Scholar 

  19. Holm PB (1986) Chromosome pairing and chiasma formation in allohexaploid wheat, Triticum aestivum, analyzed by spreading of meiotic nuclei. Carlsberg Res Commun 51:239–294

    Article  Google Scholar 

  20. Holm PB (1988) Chromosome pairing and synaptonemal complex formation in hexaploid wheat, monosomic for chromosome 5B. Carlsberg Res Commun 53:57–89

    Article  Google Scholar 

  21. Holm PB (1988) Chromosome pairing and synaptonemal complex formation in hexaploid wheat, nullisomic for chromosome 5B. Carlsberg Res Commun 53:91–110

    Article  Google Scholar 

  22. Holm PB (1988) Chromosome pairing and synaptonemal complex formation in hexaploid wheat, monoisosomic and diisosomic for the long arm of chromosome 5B. Carlsberg Res Commun 53:111–133

    Article  Google Scholar 

  23. Holm PB, Wang X (1988) The effect of chromosome 5B on synapsis and chiasma formation in wheat, Triticum aestivum cv. Chinese Spring. Carlsberg Res Commun 53:191–208

    Article  Google Scholar 

  24. Wang X (1988) Chromosome pairing analysis in haploid wheat by spreading of meiotic nuclei. Carlsberg Res Commun 53:135–166

    Article  Google Scholar 

  25. Rasmussen SW (1986) Initiation of synapsis and interlocking of chromosomes during zygotene in Bombyx spermatocytes. Carlsberg Res Commun 51:401–432

    Article  Google Scholar 

  26. Rasmussen SW (1986) Chromosome interlocking during synapsis – a transient disorder. Tokai J Exp Clin Med 11:437–451

    CAS  PubMed  Google Scholar 

  27. Wang X, Holm PB (1988) Chromosome pairing and synaptonemal complex formation in wheat-rye hybrids. Carlsberg Res Commun 53:167–190

    Article  Google Scholar 

  28. Rasmussen SW (1973) Ultrastructural studies of spermatogenesis in Drosophila melanogaster. Z Zellforsch 140:125–144

    Article  CAS  PubMed  Google Scholar 

  29. Rasmussen SW (1975) Synaptonemal polycomplexes in Drosophila melanogaster. Chromosoma 49:321–331

    Article  Google Scholar 

  30. Rasmussen SW (1977) The transformation of the synaptonemal complex into the “elimination chromatin” in Bombyx mori oocytes. Chromosoma 60:205–221

    Article  CAS  PubMed  Google Scholar 

  31. Rasmussen SW (1977) Chromosome pairing in triploid females of Bombyx mori analyzed by three dimensional reconstructions of synaptonemal complexes. Carlsberg Res Commun 42:163–197

    Article  Google Scholar 

  32. Rasmussen SW (1977) Meiosis in Bombyx mori females. Philos Trans R Soc Lond B Biol Sci 277:343–350

    Article  CAS  PubMed  Google Scholar 

  33. Rasmussen SW, Holm PB (1979) Chromosome pairing in autotetraploid Bombyx mori females. Mechanism for exclusive bivalent formation. Carlsberg Res Commun 44:101–125

    Article  Google Scholar 

  34. Rasmussen SW (1987) Chromosome pairing in autotetraploid Bombyx males. Inihibition of multivalent correction by crossing over. Carlsberg Res Commun 52:211–242

    Article  Google Scholar 

  35. Holm PB, Rasmussen SW (1980) Chromosome pairing, recombination nodules and chiasma formation in diploid Bombyx males. Carlsberg Res Commun 45:483–548

    Article  Google Scholar 

  36. Rasmussen SW, Holm PB (1978) Human meiosis II: chromosome pairing and recombination nodules in human spermatocytes. Carlsberg Res Commun 42:275–327

    Article  Google Scholar 

  37. Rasmussen SW, Holm PB (1978) Human meiosis IV: the elimination of synaptonemal complex fragments from metaphase I bivalents of human spermatocytes. Carlsberg Res Commun 43:423–438

    Article  Google Scholar 

  38. Holm PB, Rasmussen SW (1977) Human meiosis I. The human pachytene pachytene karyotype analyzed by three dimensional reconstruction of the synaptonemal complex. Carlsberg Res Commun 42:283–323

    Article  Google Scholar 

  39. Holm PB, Rasmussen SW (1978) Human meiosis III. Electron microscopical analysis of chromosome pairing in an individual with a balanced translocation 46,XY,t(5p−;22p+). Carlsberg Res Commun 43:329–350

    Article  Google Scholar 

  40. Holm PB, Rasmussen SW (1983) Human meiosis V. Substages of pachytene in human spermatogenesis. Carlsberg Res Commun 48:351–383

    Article  Google Scholar 

  41. Holm PB, Rasmussen SW (1983) Human meiosis Vl. Crossing over in human spermatocytes. Carlsberg Res Commun 48:385–413

    Article  Google Scholar 

  42. Holm PB, Rasmussen SW (1983) Human meiosis VII. Chiasma formation in human spermatocytes. Carlsberg Res Commun 48:415–456

    Article  Google Scholar 

  43. Berthelsen JG, Holm PB, Rasmussen SW (1980) Three ultrastructure markers on pachytene bivalents of human spermatocytes. Carlsberg Res Commun 45:25–28

    Article  Google Scholar 

  44. Holm PB, Rasmussen SW (1984) The synaptonemal complex in chromosome pairing and disjunction. In: Bennett MD, Gropp A, Wolf U (eds) Chromosomes today, vol 8. Georg Allen & Unwin, Crows Nest, NSW, pp 104–116

    Chapter  Google Scholar 

  45. Bojko M (1983) Human meiosis. VIII. Chromosome pairing and formation of the synaptonemal complex in oocytes. Carlsberg Res Commun 48:457–483

    Article  Google Scholar 

  46. Bojko M (1985) Human meiosis. IX. Crossing over and chiasma formation in oocytes. Carlsberg Res Commun 50:43–72

    Article  Google Scholar 

  47. Glamann J (1986) Crossing over in the male mouse as analysed by recombination nodules and bars. Carlsberg Res Commun 51:143–161

    Article  Google Scholar 

  48. Holm PB (1977) The premeiotic DNA replication of euchromatin and heterochromatin in Lilium longiflorum (Thunb.). Carlsberg Res Commun 42:249–281

    Article  CAS  Google Scholar 

  49. Holm PB (1977) Three-dimensional reconstruction of chromosome pairing during the zygotene stage of meiosis in Lilium longiflorum (Thunb.). Carlsberg Res Commun 42:103–151

    Article  Google Scholar 

  50. Gillies CB (1974) The nature and extent of synaptonemal complex formation in haploid barley. Chromosoma 48:441–453

    Article  Google Scholar 

  51. Mogensen HL (1977) Ultrastructural analysis of female pachynema and the relationship between synaptonemal complex length and crossing-over in Zea mays. Carlsberg Res Commun 42:475–497

    Article  Google Scholar 

  52. Hobolth P (1981) Chromosome pairing in allohexaploid wheat var. Chinese Spring. Transformation of multivalents into bivalents, a mechanism for exclusive bivalent formation. Carlsberg Res Commun 46:129–173

    Article  Google Scholar 

  53. Jenkins G (1983) Chromosome pairing in Triticum aestivum cv. Chinese Spring. Carlsberg Res Commun 48:255–283

    Article  Google Scholar 

  54. Wischmann B (1986) Chromosome pairing and chiasma formation in wheat plants trisomic for the long arm of chromosome 5B. Carlsberg Res Commun 51:1–25

    Article  Google Scholar 

  55. Gillies CB (1972) Reconstruction of the Neurospora crassa pachytene karyotype from serial sections of synaptonemal complexes. Chromosoma 36:119–130

    Article  CAS  PubMed  Google Scholar 

  56. Zickler D, Olson LW (1975) The synaptonemal complex and the spindle plaque during meiosis in yeast. Chromosoma 50:1–23

    Article  CAS  PubMed  Google Scholar 

  57. Petersen JGL, Olson LW, Zickler D (1978) Synchronous sporulation of Saccharomyces cerevisiae at high cell concentrations. Carlsberg Res Commun 43:241–253

    Article  Google Scholar 

  58. Zickler D (1981) Ultrastructure of the yeast nucleus. In: Gull K, Oliver SG (eds) The fungal nucleus, British mycological society symposium 5. Cambridge University Press, Cambridge, pp 63–83

    Google Scholar 

  59. Zickler D, Sage J (1981) Synaptonemal complexes with modified lateral elements in Sordaria humana: development of and relationship to the “recombination nodules”. Chromosoma 84:305–318

    Article  Google Scholar 

  60. Holm PB, Rasmussen SW, Zickler D, Lu BC, Sage J (1981) Chromosome pairing, recombination nodules and chiasma formation in the basidiomycete Coprinus cinereus. Carlsberg Res Commun 46:305–346

    Article  Google Scholar 

  61. Rasmussen SW, Holm PB, Lu BC, Zickler D, Sage J (1981) Synaptonemal complex formation and distribution of recombination nodules in pachytene trivalents of triploid Coprinus cinereus. Carlsberg Res Commun 46:347–360

    Article  Google Scholar 

  62. Carmi P, Holm PB, Koltin Y, Rasmussen SW, Sage J, Zickler D (1978) The karyotype of Schizophyllum commune analyzed by three dimensional reconstruction of synaptonemal complexes. Carlsberg Res Commun 43:117–132

    Article  Google Scholar 

  63. Eisen G (1900) The spermatogenesis of Batrachoseps. J Morphol 17:1–117

    Article  Google Scholar 

  64. Zickler D, Kleckner N (1998) The leptotene-zygotene transition of meiosis. Annu Rev Genet 32:619–697

    Article  CAS  PubMed  Google Scholar 

  65. Gelei J (1921) Weitere Studien über die Oogenese des Dendrocoelum lacteum. II. Die Längskonjungation der Chromosomen. Arch Zellforsch 16:88–169

    Google Scholar 

  66. Storlazzi A, Gargano S, Ruprich-Robert G, Falque M, David M, Kleckner N, Zickler D (2010) Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141:94–106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Martinez-Garcia M, Schubert V, Osman K, Darbyshire A, Sanchez-Moran E, Franklin FCH (2018) TOPII and chromosome movement help remove interlocks between entangled chromosomes during meiosis. J Cell Biol 217:4070–4079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Moses MJ, Poorman PA (1981) Synaptosomal complex analysis of mouse chromosomal rearrangements. II. Synaptic adjustment in a tandem duplication. Chromosoma 81:519–535

    Article  CAS  PubMed  Google Scholar 

  69. Moses MJ, Poorman PA, Roderick TH, Davisson MT (1982) Synaptonemal complex analysis of mouse chromosomal rearrangements. IV. Synapsis and synaptic adjustment in two paracentric inversions. Chromosoma 84:457–474

    Article  CAS  PubMed  Google Scholar 

  70. Rog O, Dernburg AF (2013) Chromosome pairing and synapsis during Caenorhabditis elegans meiosis. Curr Opin Cell Biol 25:349–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Zhang H, Bian Y, Gou X, Zhu B, Xu C, Qi B, Li N, Rustgi S, Zhou H, Han F, Jiang J, von Wettstein D, Liu B (2013) Persistent whole-chromosome aneuploidy is generally associated with nascent allohexaploid wheat. Proc Natl Acad Sci U S A 110:3447–3452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Bomblies K, Jones G, Franklin C, Zickler D, Kleckner N (2016) The challenge of evolving stable polyploidy: could an increase in crossover interference distance play a central role? Chromosoma 125:287–300

    Article  PubMed  PubMed Central  Google Scholar 

  73. Sears ER (1976) Genetic control of chromosome pairing in wheat. Annu Rev Genet 10:31–51

    Article  CAS  PubMed  Google Scholar 

  74. Feldman M (1966) The effect of chromosomes 5B, 5D and 5A on chromosomal pairing in Triticum aestivum. Proc Natl Acad Sci U S A 55:1447–1453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Sidhu GK, Rustgi S, Shafqat MN, von Wettstein D, Gill KS (2008) Fine structure mapping of a gene-rich region of wheat carrying Ph1, a suppressor of crossing over between homoeologous chromosomes. Proc Natl Acad Sci U S A 105:5815–5820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Borts RH, Haber JE (1987) Meiotic recombination in yeast: alteration by multiple heterozygosities. Science 237:1459–1465

    Article  CAS  PubMed  Google Scholar 

  77. Rey MD, Martín AC, Smedley M, Hayta S, Harwood W, Shaw P, Moore G (2018) Magnesium increases homoeologous crossover frequency during meiosis in ZIP4 (Ph1 gene) mutant wheat-wild relative hybrids. Front Plant Sci 9:509

    Article  PubMed  PubMed Central  Google Scholar 

  78. Bhullar R, Nagarajan R, Bennypaul H, Sidhu GK, Sidhu G, Rustgi S, von Wettstein D, Gill KS (2014) Silencing of a metaphase I-specific gene results in a phenotype similar to that of the Pairing homeologous 1 (Ph1) gene mutations. Proc Natl Acad Sci U S A 111:14187–14192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Boden SA, Langridge P, Spangenberg G, Able JA (2009) TaASY1 promotes homologous chromosome interactions and is affected by deletion of Ph1. Plant J 57:487–497

    Article  CAS  PubMed  Google Scholar 

  80. Sanchez-Moran E, Santos JL, Jones GH, Franklin FCH (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev 21:2220–2233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Carpenter ATC (1975) Electron microscopy of meiosis in Drosophila melanogaster females. II. The recombination nodule-a recombination-associated structure at pachytene? Proc Natl Acad Sci U S A 72:3186–3189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Rasmussen SW, Holm PB (1982) The meiotic prophase in Bombyx mori. In: King RC, Akai H (eds) Insect ultrastructure, vol 1. Plenum Publishing Corp, New York, NY, pp 61–85

    Chapter  Google Scholar 

  83. Sturtevant AH (1915) The behavior of the chromosomes as studied through linkage. Z Induct Abstammungs Vererbungsl 13:234–287

    Google Scholar 

  84. Muller HJ (1916) The mechanism of crossing over. Am Nat 50:193–434

    Article  Google Scholar 

  85. von Wettstein D (1984) The synaptonemal complex and genetic segregation. Symp Soc Exp Biol 38:195–231

    Google Scholar 

  86. Gruhn JR, Rubio C, Broman KW, Hunt PA, Hassold T (2013) Cytological studies of human meiosis: sex-specific differences in recombination originate at, or prior to, esaishment of double-strand breaks. PLoS One 8:e85075

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Wang S, Hassold T, Hunt P, White MA, Zickler D, Kleckner N, Zhang L (2017) Inefficient crossover maturation underlies elevated aneuploidy in human female meiosis. Cell 168:977–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Rasmussen SW (1976) The meiotic prophase in Bombyx mori females analyzed by three dimensional reconstructions of synaptonemal complexes. Chromosoma 54:245–293

    Article  CAS  PubMed  Google Scholar 

  89. Holter H, Max Møller K (1976) The Carlsberg Laboratory 1876/1976, Rhodos International Science and Art Publishers, New York, NY 379

    Google Scholar 

Download references

Acknowledgments

I thank Penny von Wettstein-Knowles and Sachin Rustgi for comments that improved the manuscript. I am grateful and much indebted to Preben Holm and Søren Rasmussen for their long-standing warm friendship and for their steady encouragement and critical reading of the manuscript. We all three would like to thank the editors for this opportunity to reflect on ways that Diter von Wettstein affected and enriched our lives.

Author information

Authors and Affiliations

  1. Institute for Integrative Biology of the Cell (I2BC), Centre National de la Recherche Scientifique (CNRS), CEA, Université Paris-Sud, Université Paris-Saclay, Gif-sur-Yvette, France

    Denise Zickler

Authors
  1. Denise Zickler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Denise Zickler .

Editor information

Editors and Affiliations

  1. Department of Plant and Environmental Sciences, School of Health Research, Pee Dee Research and Education Center, Clemson University, Florence, SC, USA

    Sachin Rustgi

  2. Department of Genetics and Biochemistry, Clemson University, Clemson, SC, USA

    Hong Luo

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Zickler, D. (2020). Diter von Wettstein and The Meiotic Program of Pairing and Recombination. In: Rustgi, S., Luo, H. (eds) Biolistic DNA Delivery in Plants. Methods in Molecular Biology, vol 2124. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-0356-7_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-0356-7_2

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-0355-0

  • Online ISBN: 978-1-0716-0356-7

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation