Skip to main content
Genetics logoLink to Genetics
. 2004 Apr;166(4):1923–1933. doi: 10.1534/genetics.166.4.1923

Integrating genetic linkage maps with pachytene chromosome structure in maize.

Lorinda K Anderson 1, Naser Salameh 1, Hank W Bass 1, Lisa C Harper 1, W Z Cande 1, Gerd Weber 1, Stephen M Stack 1
PMCID: PMC1470829  PMID: 15126409

Abstract

Genetic linkage maps reveal the order of markers based on the frequency of recombination between markers during meiosis. Because the rate of recombination varies along chromosomes, it has been difficult to relate linkage maps to chromosome structure. Here we use cytological maps of crossing over based on recombination nodules (RNs) to predict the physical position of genetic markers on each of the 10 chromosomes of maize. This is possible because (1). all 10 maize chromosomes can be individually identified from spreads of synaptonemal complexes, (2). each RN corresponds to one crossover, and (3). the frequency of RNs on defined chromosomal segments can be converted to centimorgan values. We tested our predictions for chromosome 9 using seven genetically mapped, single-copy markers that were independently mapped on pachytene chromosomes using in situ hybridization. The correlation between predicted and observed locations was very strong (r(2) = 0.996), indicating a virtual 1:1 correspondence. Thus, this new, high-resolution, cytogenetic map enables one to predict the chromosomal location of any genetically mapped marker in maize with a high degree of accuracy. This novel approach can be applied to other organisms as well.

Full Text

The Full Text of this article is available as a PDF (144.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson Lorinda K., Doyle Gregory G., Brigham Brian, Carter Jenna, Hooker Kristina D., Lai Ann, Rice Mindy, Stack Stephen M. High-resolution crossover maps for each bivalent of Zea mays using recombination nodules. Genetics. 2003 Oct;165(2):849–865. doi: 10.1093/genetics/165.2.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bridges C B. Non-Disjunction as Proof of the Chromosome Theory of Heredity. Genetics. 1916 Jan;1(1):1–52. doi: 10.1093/genetics/1.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Carpenter A. T. Synaptonemal complex and recombination nodules in wild-type Drosophila melanogaster females. Genetics. 1979 Jun;92(2):511–541. doi: 10.1093/genetics/92.2.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cheng Z., Presting G. G., Buell C. R., Wing R. A., Jiang J. High-resolution pachytene chromosome mapping of bacterial artificial chromosomes anchored by genetic markers reveals the centromere location and the distribution of genetic recombination along chromosome 10 of rice. Genetics. 2001 Apr;157(4):1749–1757. doi: 10.1093/genetics/157.4.1749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Civardi L., Xia Y., Edwards K. J., Schnable P. S., Nikolau B. J. The relationship between genetic and physical distances in the cloned a1-sh2 interval of the Zea mays L. genome. Proc Natl Acad Sci U S A. 1994 Aug 16;91(17):8268–8272. doi: 10.1073/pnas.91.17.8268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Davis G. L., McMullen M. D., Baysdorfer C., Musket T., Grant D., Staebell M., Xu G., Polacco M., Koster L., Melia-Hancock S. A maize map standard with sequenced core markers, grass genome reference points and 932 expressed sequence tagged sites (ESTs) in a 1736-locus map. Genetics. 1999 Jul;152(3):1137–1172. doi: 10.1093/genetics/152.3.1137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Froenicke Lutz, Anderson Lorinda K., Wienberg Johannes, Ashley Terry. Male mouse recombination maps for each autosome identified by chromosome painting. Am J Hum Genet. 2002 Nov 12;71(6):1353–1368. doi: 10.1086/344714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fu H., Park W., Yan X., Zheng Z., Shen B., Dooner H. K. The highly recombinogenic bz locus lies in an unusually gene-rich region of the maize genome. Proc Natl Acad Sci U S A. 2001 Jul 3;98(15):8903–8908. doi: 10.1073/pnas.141221898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fu Huihua, Zheng Zhenwei, Dooner Hugo K. Recombination rates between adjacent genic and retrotransposon regions in maize vary by 2 orders of magnitude. Proc Natl Acad Sci U S A. 2002 Jan 15;99(2):1082–1087. doi: 10.1073/pnas.022635499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gill K. S., Gill B. S., Endo T. R., Boyko E. V. Identification and high-density mapping of gene-rich regions in chromosome group 5 of wheat. Genetics. 1996 Jun;143(2):1001–1012. doi: 10.1093/genetics/143.2.1001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Harper L. C., Cande W. Z. Mapping a new frontier; development of integrated cytogenetic maps in plants. Funct Integr Genomics. 2000 Sep;1(2):89–98. doi: 10.1007/s101420000013. [DOI] [PubMed] [Google Scholar]
  12. King J., Roberts L. A., Kearsey M. J., Thomas H. M., Jones R. N., Huang L., Armstead I. P., Morgan W. G., King I. P. A demonstration of a 1:1 correspondence between chiasma frequency and recombination using a Lolium perenne/Festuca pratensis substitution. Genetics. 2002 May;161(1):307–314. doi: 10.1093/genetics/161.1.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Korenberg J. R., Chen X. N., Sun Z., Shi Z. Y., Ma S., Vataru E., Yimlamai D., Weissenbach J. S., Shizuya H., Simon M. I. Human genome anatomy: BACs integrating the genetic and cytogenetic maps for bridging genome and biomedicine. Genome Res. 1999 Oct;9(10):994–1001. doi: 10.1101/gr.9.10.994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Koumbaris George L., Bass Hank W. A new single-locus cytogenetic mapping system for maize (Zea mays L.): overcoming FISH detection limits with marker-selected sorghum (S. propinquum L.) BAC clones. Plant J. 2003 Sep;35(5):647–659. doi: 10.1046/j.1365-313x.2003.01829.x. [DOI] [PubMed] [Google Scholar]
  15. Künzel G., Korzun L., Meister A. Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics. 2000 Jan;154(1):397–412. doi: 10.1093/genetics/154.1.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lee Michael, Sharopova Natalya, Beavis William D., Grant David, Katt Maria, Blair Deborah, Hallauer Arnel. Expanding the genetic map of maize with the intermated B73 x Mo17 (IBM) population. Plant Mol Biol. 2002 Mar-Apr;48(5-6):453–461. doi: 10.1023/a:1014893521186. [DOI] [PubMed] [Google Scholar]
  17. Lynn Audrey, Koehler Kara E., Judis LuAnn, Chan Ernest R., Cherry Jonathan P., Schwartz Stuart, Seftel Allen, Hunt Patricia A., Hassold Terry J. Covariation of synaptonemal complex length and mammalian meiotic exchange rates. Science. 2002 Jun 6;296(5576):2222–2225. doi: 10.1126/science.1071220. [DOI] [PubMed] [Google Scholar]
  18. Marcon Edyta, Moens Peter. MLH1p and MLH3p localize to precociously induced chiasmata of okadaic-acid-treated mouse spermatocytes. Genetics. 2003 Dec;165(4):2283–2287. doi: 10.1093/genetics/165.4.2283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Moens Peter B., Kolas Nadine K., Tarsounas Madalena, Marcon Edyta, Cohen Paula E., Spyropoulos Barbara. The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J Cell Sci. 2002 Apr 15;115(Pt 8):1611–1622. doi: 10.1242/jcs.115.8.1611. [DOI] [PubMed] [Google Scholar]
  20. Peterson D. G., Lapitan N. L., Stack S. M. Localization of single- and low-copy sequences on tomato synaptonemal complex spreads using fluorescence in situ hybridization (FISH). Genetics. 1999 May;152(1):427–439. doi: 10.1093/genetics/152.1.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Peterson D. G., Stack S. M., Price H. J., Johnston J. S. DNA content of heterochromatin and euchromatin in tomato (Lycopersicon esculentum) pachytene chromosomes. Genome. 1996 Feb;39(1):77–82. doi: 10.1139/g96-011. [DOI] [PubMed] [Google Scholar]
  22. Ramakrishna Wusirika, Ma Jianxin, Sanmiguel Phillip, Emberton John, Dubcovsky Jorge, Shiloff Bryan A., Jiang Zeyu, Rostoks Nils, Busso Carlos S., Ogden Matthew, Linton Eric, Kleinhofs Andris, Devos Katrien M., Messing Joachim, Bennetzen Jeffrey L. Frequent genic rearrangements in two regions of grass genomes identified by comparative sequence analysis. Comp Funct Genomics. 2002;3(2):165–166. doi: 10.1002/cfg.164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Riera-Lizarazu O., Vales M. I., Ananiev E. V., Rines H. W., Phillips R. L. Production and characterization of maize chromosome 9 radiation hybrids derived from an oat-maize addition line. Genetics. 2000 Sep;156(1):327–339. doi: 10.1093/genetics/156.1.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sadder T., Weber G. Comparison between genetic and physical maps in Zea mays L. of molecular markers linked to resistance against Diatraea spp. Theor Appl Genet. 2002 Mar 27;104(6-7):908–915. doi: 10.1007/s00122-001-0797-9. [DOI] [PubMed] [Google Scholar]
  25. Schnable P. S., Hsia A. P., Nikolau B. J. Genetic recombination in plants. Curr Opin Plant Biol. 1998 Apr;1(2):123–129. doi: 10.1016/s1369-5266(98)80013-7. [DOI] [PubMed] [Google Scholar]
  26. Sharopova Natalya, McMullen Michael D., Schultz Linda, Schroeder Steve, Sanchez-Villeda Hector, Gardiner Jack, Bergstrom Dean, Houchins Katherine, Melia-Hancock Susan, Musket Theresa. Development and mapping of SSR markers for maize. Plant Mol Biol. 2002 Mar-Apr;48(5-6):463–481. doi: 10.1023/a:1014868625533. [DOI] [PubMed] [Google Scholar]
  27. Sherman J. D., Stack S. M. Two-dimensional spreads of synaptonemal complexes from solanaceous plants. VI. High-resolution recombination nodule map for tomato (Lycopersicon esculentum). Genetics. 1995 Oct;141(2):683–708. doi: 10.1093/genetics/141.2.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Stack S. M. Heterochromatin, the synaptonemal complex and crossing over. J Cell Sci. 1984 Oct;71:159–176. doi: 10.1242/jcs.71.1.159. [DOI] [PubMed] [Google Scholar]
  29. Stephan W., Langley C. H. DNA polymorphism in lycopersicon and crossing-over per physical length. Genetics. 1998 Dec;150(4):1585–1593. doi: 10.1093/genetics/150.4.1585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tenaillon Maud I., Sawkins Mark C., Anderson Lorinda K., Stack Stephen M., Doebley John, Gaut Brandon S. Patterns of diversity and recombination along chromosome 1 of maize (Zea mays ssp. mays L.). Genetics. 2002 Nov;162(3):1401–1413. doi: 10.1093/genetics/162.3.1401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Weber D., Helentjaris T. Mapping RFLP loci in maize using B-A translocations. Genetics. 1989 Mar;121(3):583–590. doi: 10.1093/genetics/121.3.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Williams C. G., Goodman M. M., Stuber C. W. Comparative recombination distances among Zea mays L. inbreds, wide crosses and interspecific hybrids. Genetics. 1995 Dec;141(4):1573–1581. doi: 10.1093/genetics/141.4.1573. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES