, Volume 121, Issue 2, pp 201–208 | Cite as

Inversions of chromosome arms 4AL and 2BS in wheat invert the patterns of chiasma distribution

  • Adam J. LukaszewskiEmail author
  • David Kopecky
  • Gabriella Linc
Research Article


In many species, including wheat, crossing over is distal, and the proximal regions of chromosome arms contribute little to genetic maps. This was thought to be a consequence of terminal initiation of synapsis favoring distal crossing over. However, in an inverted rye chromosome arm, the pattern of metaphase I chiasmata was also inverted, suggesting that crossover frequencies were specific to chromosome segments. Here, wheat chromosome arms 2BS and 4AL, with essentially entire arms inverted in reverse tandem duplications (rtd), were studied in the MI of meiosis. Inversion–duplication placed the recombining segments in the middle of the arms. While the overall pairing frequencies of the inverted–duplicated arms were considerably reduced relative to normal arms, chiasmata, if present, were always located in the same regions as in structurally normal arms, and relative chiasma frequencies remained the same. The frequencies of fragment or fragment + bridge configurations in AI and AII indicated that of the two tandemly arranged copies of segments in rtds, the more distal inverted segments were more likely to cross over than the segments in their original orientations. These observations show that also in wheat, relative crossover frequencies along chromosome arms are predetermined and independent of the segment location. The segments normally not licensed to cross over do not do so even when placed in seemingly most favorable positions for it.


Normal Chromosome Crossover Frequency Inverted Segment Chiasma Distribution Telomere Bouquet 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



DK was supported by the Ministry of Education, Youth and Sports of the Czech Republic and the European Regional Development Fund (Operational Programme Research and Development for Innovations No. CZ.1.05/2.1.00/01.0007). GL was supported by the Hungarian National Research Fund (K67808) and the Js Bolyai Research Scholarship of the Hungarian Academy of Sciences.


  1. Bass HW, Marshall WF, Sedat JW, Agard DA, Cande WZ (1997) Telomeres cluster de novo before the initiation of synapsis: a three dimensional spatial analysis of telomere positions before and during meiotic prophase. J Cell Biol 137:5–18PubMedCrossRefGoogle Scholar
  2. Bass HW, Riera-Lizarazu O, Ananiev EV, Bordolo SJ, Rines HW, Phillips RL, Sedat JW, Agard DA, Cande WZ (2000) Evidence for the coincident initiation of homolog pairing and synapsis during the telomere clustering (bouquet) stage of meiotic prophase. J Cell Sci 113:1033–1042PubMedGoogle Scholar
  3. Chikashige Y, Ding DQ, Funabiki H, Haraguchi T, Mashiko S, Yanagida M, Hiraoka Y (1994) Telomere-led premeiotic chromosome movement in fission yeast. Science 264:270–273PubMedCrossRefGoogle Scholar
  4. Close TJ, Bhat PR, Lonardi S, Wu Y, Rostoks N, Ramsay L, Druka A, Stein N, Svensson JT, Wanamaker S, Bozdag S, Roose ML, Moscou MJ, Chao S, Varshney RK, Szűcs P, Sato K, Hayes PM, Matthews DE, Kleinhofs A, Muehlbauer GJ, DeYoung J, Marshall DF, Madishetty K, Fenton RD, Condamine P, Graner A, Waugh R (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics 10:582–595PubMedCrossRefGoogle Scholar
  5. Corredor E, Lukaszewski AJ, Pachón P, Allen DC, Naranjo T (2007) Terminal regions of wheat chromosomes select their pairing partners in meiosis. Genetics 177:699–706PubMedCrossRefGoogle Scholar
  6. Curtis CA, Lukaszewski AJ, Chrzastek M (1991) Metaphase I pairing of deficient chromosomes and genetic mapping of deficiency breakpoints in common wheat. Genome 34:553–560CrossRefGoogle Scholar
  7. Dernburg AF, Sedat JW, Hawley RS (1996) Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86:135–146PubMedCrossRefGoogle Scholar
  8. Francki M (2001) Identification of Bilby, a diverged centromeric Ty1-copia retrotransposon family from cereal rye (Secale cereale L.). Genome 44:266–274PubMedGoogle Scholar
  9. Fussel CP (1987) The Rabl orientation: a prelude to synapsis. In: Moens PB (ed) Meiosis. Academic Press, Orlando, pp 275–299Google Scholar
  10. Gill BC, Friebe B, Endo TR (1991) Standard karyotype and nomenclature system for description of chromosome bands and structural aberrations in wheat (Triticum aestivum). Genome 34:830–839CrossRefGoogle Scholar
  11. Gill KS, Gill BS, Endo TR, Boyko EV (1996) Identification and high density mapping of gene-rich regions in chromosome group-1 of wheat. Genetics 143:1001–1012PubMedGoogle Scholar
  12. Harper L, Golubovskaya I, Cande WZ (2004) A bouquet of chromosomes. J Cell Sci 117:4025–4032PubMedCrossRefGoogle Scholar
  13. Hughes SE, Gilliland WD, Cotitta JO, Takeo S, Collins KA, Hawley RS (2009) Heterochromatic threads connect oscillating chromosomes during prometaphase I in Drosophila oocytes. PLoS Genetics 5(1):e1000348PubMedCrossRefGoogle Scholar
  14. John B (1990) Meiosis. Cambridge Univ Press, CambridgeCrossRefGoogle Scholar
  15. Jones GH (1967) The control of chiasma distribution in rye. Chromosoma 22:69–90CrossRefGoogle Scholar
  16. Jones LE, Rybka K, Lukaszewski AJ (2002) The effect of a deficiency and a deletion on recombination in chromosome 1BL in wheat. Theor Appl Genet 104:1204–1208PubMedCrossRefGoogle Scholar
  17. Khrustaleva LI, Kik C (1998) Cytogenetical studies in the bridge cross Allium cepa × (A. fistulosum × A. roylei). Theor Appl Genet 96:8–14CrossRefGoogle Scholar
  18. Kopecky D, Havrankova M, Loureiro J, Castro S, Lukaszewski AJ, Bartos J, Kopecka J, Dolezel J (2010) Physical distribution of homoeologous recombination in individual chromosomes of Festuca pratensis in Lolium multiflorum. Cytogenet Genome Res 129:162–172PubMedCrossRefGoogle Scholar
  19. Kubalakova M, Lysak MA, Vrana J, Simková H, Cíhalíkova J, Dolezel J (2000) Rapid identification and determination of purity of flow-sorted plant chromosomes using C-PRINS. Cytometry 41:102–108PubMedCrossRefGoogle Scholar
  20. Kunzel G, Korzun L, Meister A (2000) Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics 154:397–412PubMedGoogle Scholar
  21. Lukaszewski AJ (1992) A comparison of physical distribution of recombination in chromosome 1R in diploid rye and in hexaploid triticale. Theor Appl Genet 83:1048–1053CrossRefGoogle Scholar
  22. Lukaszewski AJ (1995) Chromatid and chromosome type breakage–fusion–bridge cycles in wheat (Triticum aestivum L.). Genetics 140:1069–1085PubMedGoogle Scholar
  23. Lukaszewski AJ (1997) The development and meiotic behavior of asymmetrical isochromosomes in wheat. Genetics 145:1155–1160PubMedGoogle Scholar
  24. Lukaszewski AJ (2003) Manipulation of recombination in wheat. In: Pogna NE et al. (eds) Proc. 10th Int. Wheat Genet Symp. Paestum, Italy, Sept 2003, pp.73-76Google Scholar
  25. Lukaszewski AJ (2008) Unexpected behavior of an inverted rye chromosome arm in wheat. Chromosoma 117:569–578PubMedCrossRefGoogle Scholar
  26. Lukaszewski AJ, Curtis CA (1993) Physical distribution of recombination in B-genome chromosomes of tetraploid wheat. Theor Appl Genet 86:121–127CrossRefGoogle Scholar
  27. Lukaszewski AJ, Rybka K, Korzun V, Malyshev SV, Lapinski B, Whitkus R (2004) Genetic and physical mapping of homoeologous recombination points involving wheat chromosome 2B and rye chromosome 2R. Genome 47:36–45PubMedCrossRefGoogle Scholar
  28. Luo MC, Deal KR, Akhunova ED, Akhunova AR, Anderson OD, Anderson JA, Blake N, Clegg MT, Coleman-Derr D, Conley EJ, Crossman CC, Dubcovsky J, Gill BS, Gub YQ, Hadam J, Heo HY, Huo N, Lazo G, Ma Y, Matthews DE, McGuire PE, Morrell PL, Qualset CO, Renfro J, Tabanao D, Talbert LE, Tiana C, Toleno DM, Warburton ML, Youb FM, Zhang W, Dvorak J (2009) Genome comparisons reveal a dominant mechanism of chromosome number reduction in grasses and accelerated genome evolution in Triticeae. Proc Natl Acad Sci USA 106:15780–15785PubMedCrossRefGoogle Scholar
  29. Massoudi-Nejad A, Nasuda S, McIntosh RA, Endo TR (2002) Transfer of rye chromosome segments to wheat by gametocidal system. Chromosome Res 10:349–357CrossRefGoogle Scholar
  30. Mayer KFX, Martis M, Hedley PE, Simkova H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, Kubalakova M, Suchankova P, Murat F, Felder M, Nussbaumer T, Graner A, Salse J, Endo T, Sakai H, Tanaka T, Itoh T, Sato K, Platzer M, Matsumoto M, Scholz U, Dolezel J, Waugh R, Stein N (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23:1249–1263PubMedCrossRefGoogle Scholar
  31. Moens PB, Bernelot-Moens C, Spyropulous B (1989) Chromosome core attachment to the meiotic nuclear envelope regulates synapsis in Chloealtis (Orthoptera). Genome 32:601–610CrossRefGoogle Scholar
  32. Naranjo T, Valenzuela N, Perera E (2010) Chiasma frequency is region-specific and chromosome conformation-dependent in a rye chromosome added to wheat. Cytogenet Genome Res 129:133–142PubMedCrossRefGoogle Scholar
  33. Pawlowski WP, Cande WZ (2005) Coordinating the events of the meiotic prophase. Trends Cell Biol 15:664–681CrossRefGoogle Scholar
  34. Qi LL, Friebe B, Gill BS (2002) A strategy for enhancing recombination in proximal regions of chromosomes. Chromosome Res 10:645–654PubMedCrossRefGoogle Scholar
  35. Ross LO, Zenvirth D, Jardim AR, Dawson D (2000) Double-strand breaks on artificial chromosomes in yeast. Chromosoma 109:226–234PubMedCrossRefGoogle Scholar
  36. Sallee PJ, Kimber G (1978) An analysis of the pairing of wheat telocentric chromosomes. In: Ramanujan S (ed) Proc. 5th Int. Wheat Genet. Symp. New Dehli, India, pp. 408–419Google Scholar
  37. Sheehan MJ, Pawlowski WP (2009) Live imaging of rapid chromosome movements in meiotic prophase I in maize. Proc Natl Ac Sci USA 106:20989–20994CrossRefGoogle Scholar
  38. Tsai J, McKee BD (2011) Homologous pairing and the role of pairing centers in meiosis. J Cell Sci 124:1955–1963PubMedCrossRefGoogle Scholar
  39. Werner JE, Endo TR, Gill BS (1992) Towards a cytogenetically based physical map of the wheat genome. Proc Natl Acad Sci USA 89:11307–11311PubMedCrossRefGoogle Scholar
  40. Zhang P, Friebe B, Lukaszewski AJ, Gill BS (2001) The centromere structure in Robertsonian translocation chromosomes indicates that centric breakage-fusion can occur at various locations within the primary constriction. Chromosoma 110:335–344PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Adam J. Lukaszewski
    • 1
    Email author
  • David Kopecky
    • 2
  • Gabriella Linc
    • 3
  1. 1.Department of Botany and Plant SciencesUniversity of CaliforniaRiversideUSA
  2. 2.Centre of the Region Hana for Biotechnological and Agricultural ResearchInstitute of Experimental BotanyOlomoucCzech Republic
  3. 3.Agricultural Research Institute of the Hungarian Academy of SciencesMartonvásárHungary

Personalised recommendations