Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1999 Jul;11(7):1227–1238. doi: 10.1105/tpc.11.7.1227

A maize homolog of mammalian CENPC is a constitutive component of the inner kinetochore.

R K Dawe 1, L M Reed 1, H G Yu 1, M G Muszynski 1, E N Hiatt 1
PMCID: PMC144275  PMID: 10402425

Abstract

Genes for three maize homologs (CenpcA, CenpcB, and CenpcC) of the conserved kinetochore assembly protein known as centromere protein C (CENPC) have been identified. The C-terminal portion of maize CENPC shares similarity with mammalian CENPC and its yeast homolog Mif2p over a 23-amino acid region known as region I. Immunolocalization experiments combined with three-dimensional light microscopy demonstrated that CENPC is a component of the kinetochore throughout interphase, mitosis, and meiosis. It is shown that sister kinetochore separation occurs in two discrete phases during meiosis. A partial separation of sister kinetochores occurs in prometaphase I, and a complete separation occurs in prometaphase II. CENPC is absent on structures known as neocentromeres that, in maize, demonstrate poleward movement but lack other important features of centromeres/kinetochores. CENPC and a previously identified centromeric DNA sequence interact closely but do not strictly colocalize on meiotic chromosomes. These and other data indicate that CENPC occupies an inner domain of the maize kinetochore.

Full Text

The Full Text of this article is available as a PDF (460.9 KB).

Selected References

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

  1. Alfenito M. R., Birchler J. A. Molecular characterization of a maize B chromosome centric sequence. Genetics. 1993 Oct;135(2):589–597. doi: 10.1093/genetics/135.2.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allshire R. C. Centromeres, checkpoints and chromatid cohesion. Curr Opin Genet Dev. 1997 Apr;7(2):264–273. doi: 10.1016/s0959-437x(97)80137-2. [DOI] [PubMed] [Google Scholar]
  3. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  4. Ananiev E. V., Phillips R. L., Rines H. W. Complex structure of knob DNA on maize chromosome 9. Retrotransposon invasion into heterochromatin. Genetics. 1998 Aug;149(4):2025–2037. doi: 10.1093/genetics/149.4.2025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Aragón-Alcaide L., Miller T., Schwarzacher T., Reader S., Moore G. A cereal centromeric sequence. Chromosoma. 1996 Dec;105(5):261–268. doi: 10.1007/BF02524643. [DOI] [PubMed] [Google Scholar]
  6. Asai D. J., Brokaw C. J., Thompson W. C., Wilson L. Two different monoclonal antibodies to alpha-tubulin inhibit the bending of reactivated sea urchin spermatozoa. Cell Motil. 1982;2(6):599–614. doi: 10.1002/cm.970020608. [DOI] [PubMed] [Google Scholar]
  7. Binarova P., Cihalikova J., Dolezel J. Localization of MPM-2 recognized phosphoproteins and tubulin during cell cycle progression in synchronized Vicia faba root meristem cells. Cell Biol Int. 1993 Sep;17(9):847–856. doi: 10.1006/cbir.1993.1147. [DOI] [PubMed] [Google Scholar]
  8. Brown M. T., Goetsch L., Hartwell L. H. MIF2 is required for mitotic spindle integrity during anaphase spindle elongation in Saccharomyces cerevisiae. J Cell Biol. 1993 Oct;123(2):387–403. doi: 10.1083/jcb.123.2.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brown M. T. Sequence similarities between the yeast chromosome segregation protein Mif2 and the mammalian centromere protein CENP-C. Gene. 1995 Jul 4;160(1):111–116. doi: 10.1016/0378-1119(95)00163-z. [DOI] [PubMed] [Google Scholar]
  10. Campbell M. S., Gorbsky G. J. Microinjection of mitotic cells with the 3F3/2 anti-phosphoepitope antibody delays the onset of anaphase. J Cell Biol. 1995 Jun;129(5):1195–1204. doi: 10.1083/jcb.129.5.1195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Choo K. H. Centromere DNA dynamics: latent centromeres and neocentromere formation. Am J Hum Genet. 1997 Dec;61(6):1225–1233. doi: 10.1086/301657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cooke C. A., Schaar B., Yen T. J., Earnshaw W. C. Localization of CENP-E in the fibrous corona and outer plate of mammalian kinetochores from prometaphase through anaphase. Chromosoma. 1997 Dec;106(7):446–455. doi: 10.1007/s004120050266. [DOI] [PubMed] [Google Scholar]
  13. Dawe R. K., Cande W. Z. Induction of centromeric activity in maize by suppressor of meiotic drive 1. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8512–8517. doi: 10.1073/pnas.93.16.8512. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dawe R. K., Sedat J. W., Agard D. A., Cande W. Z. Meiotic chromosome pairing in maize is associated with a novel chromatin organization. Cell. 1994 Mar 11;76(5):901–912. doi: 10.1016/0092-8674(94)90364-6. [DOI] [PubMed] [Google Scholar]
  15. Dawe R. Kelly. MEIOTIC CHROMOSOME ORGANIZATION AND SEGREGATION IN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49(NaN):371–395. doi: 10.1146/annurev.arplant.49.1.371. [DOI] [PubMed] [Google Scholar]
  16. Dennis E. S., Peacock W. J. Knob heterochromatin homology in maize and its relatives. J Mol Evol. 1984;20(3-4):341–350. doi: 10.1007/BF02104740. [DOI] [PubMed] [Google Scholar]
  17. Depinet T. W., Zackowski J. L., Earnshaw W. C., Kaffe S., Sekhon G. S., Stallard R., Sullivan B. A., Vance G. H., Van Dyke D. L., Willard H. F. Characterization of neo-centromeres in marker chromosomes lacking detectable alpha-satellite DNA. Hum Mol Genet. 1997 Aug;6(8):1195–1204. doi: 10.1093/hmg/6.8.1195. [DOI] [PubMed] [Google Scholar]
  18. Dong F., Miller J. T., Jackson S. A., Wang G. L., Ronald P. C., Jiang J. Rice (Oryza sativa) centromeric regions consist of complex DNA. Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):8135–8140. doi: 10.1073/pnas.95.14.8135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fukagawa T., Brown W. R. Efficient conditional mutation of the vertebrate CENP-C gene. Hum Mol Genet. 1997 Dec;6(13):2301–2308. doi: 10.1093/hmg/6.13.2301. [DOI] [PubMed] [Google Scholar]
  20. Goldstein L. S. Kinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster. Cell. 1981 Sep;25(3):591–602. doi: 10.1016/0092-8674(81)90167-7. [DOI] [PubMed] [Google Scholar]
  21. Harrington J. J., Van Bokkelen G., Mays R. W., Gustashaw K., Willard H. F. Formation of de novo centromeres and construction of first-generation human artificial microchromosomes. Nat Genet. 1997 Apr;15(4):345–355. doi: 10.1038/ng0497-345. [DOI] [PubMed] [Google Scholar]
  22. Houben A., Guttenbach M., Kress W., Pich U., Schubert I., Schmid M. Immunostaining and interphase arrangement of field bean kinetochores. Chromosome Res. 1995 Jan;3(1):27–31. doi: 10.1007/BF00711158. [DOI] [PubMed] [Google Scholar]
  23. Jiang J., Nasuda S., Dong F., Scherrer C. W., Woo S. S., Wing R. A., Gill B. S., Ward D. C. A conserved repetitive DNA element located in the centromeres of cereal chromosomes. Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):14210–14213. doi: 10.1073/pnas.93.24.14210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kalitsis P., Fowler K. J., Earle E., Hill J., Choo K. H. Targeted disruption of mouse centromere protein C gene leads to mitotic disarray and early embryo death. Proc Natl Acad Sci U S A. 1998 Feb 3;95(3):1136–1141. doi: 10.1073/pnas.95.3.1136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Karpen G. H., Allshire R. C. The case for epigenetic effects on centromere identity and function. Trends Genet. 1997 Dec;13(12):489–496. doi: 10.1016/s0168-9525(97)01298-5. [DOI] [PubMed] [Google Scholar]
  26. Knehr M., Poppe M., Schroeter D., Eickelbaum W., Finze E. M., Kiesewetter U. L., Enulescu M., Arand M., Paweletz N. Cellular expression of human centromere protein C demonstrates a cyclic behavior with highest abundance in the G1 phase. Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10234–10239. doi: 10.1073/pnas.93.19.10234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Meluh P. B., Koshland D. Budding yeast centromere composition and assembly as revealed by in vivo cross-linking. Genes Dev. 1997 Dec 15;11(24):3401–3412. doi: 10.1101/gad.11.24.3401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Meluh P. B., Koshland D. Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the mammalian centromere protein CENP-C. Mol Biol Cell. 1995 Jul;6(7):793–807. doi: 10.1091/mbc.6.7.793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Moens P. B., Spyropoulos B. Immunocytology of chiasmata and chromosomal disjunction at mouse meiosis. Chromosoma. 1995 Nov;104(3):175–182. doi: 10.1007/BF00352182. [DOI] [PubMed] [Google Scholar]
  30. Mole-Bajer J., Bajer A. S., Zinkowski R. P., Balczon R. D., Brinkley B. R. Autoantibodies from a patient with scleroderma CREST recognized kinetochores of the higher plant Haemanthus. Proc Natl Acad Sci U S A. 1990 May;87(9):3599–3603. doi: 10.1073/pnas.87.9.3599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nicklas R. B. How cells get the right chromosomes. Science. 1997 Jan 31;275(5300):632–637. doi: 10.1126/science.275.5300.632. [DOI] [PubMed] [Google Scholar]
  32. Peacock W. J., Dennis E. S., Rhoades M. M., Pryor A. J. Highly repeated DNA sequence limited to knob heterochromatin in maize. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4490–4494. doi: 10.1073/pnas.78.7.4490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pluta A. F., Mackay A. M., Ainsztein A. M., Goldberg I. G., Earnshaw W. C. The centromere: hub of chromosomal activities. Science. 1995 Dec 8;270(5242):1591–1594. doi: 10.1126/science.270.5242.1591. [DOI] [PubMed] [Google Scholar]
  34. Richards E. J., Dawe R. K. Plant centromeres: structure and control. Curr Opin Plant Biol. 1998 Apr;1(2):130–135. doi: 10.1016/s1369-5266(98)80014-9. [DOI] [PubMed] [Google Scholar]
  35. Rieder C. L. The formation, structure, and composition of the mammalian kinetochore and kinetochore fiber. Int Rev Cytol. 1982;79:1–58. doi: 10.1016/s0074-7696(08)61672-1. [DOI] [PubMed] [Google Scholar]
  36. Saitoh H., Tomkiel J., Cooke C. A., Ratrie H., 3rd, Maurer M., Rothfield N. F., Earnshaw W. C. CENP-C, an autoantigen in scleroderma, is a component of the human inner kinetochore plate. Cell. 1992 Jul 10;70(1):115–125. doi: 10.1016/0092-8674(92)90538-n. [DOI] [PubMed] [Google Scholar]
  37. Shah D. M., Hightower R. C., Meagher R. B. Genes encoding actin in higher plants: intron positions are highly conserved but the coding sequences are not. J Mol Appl Genet. 1983;2(1):111–126. [PubMed] [Google Scholar]
  38. Staiger C. J., Cande W. Z. Microtubule distribution in dv, a maize meiotic mutant defective in the prophase to metaphase transition. Dev Biol. 1990 Mar;138(1):231–242. doi: 10.1016/0012-1606(90)90193-m. [DOI] [PubMed] [Google Scholar]
  39. Starr D. A., Williams B. C., Li Z., Etemad-Moghadam B., Dawe R. K., Goldberg M. L. Conservation of the centromere/kinetochore protein ZW10. J Cell Biol. 1997 Sep 22;138(6):1289–1301. doi: 10.1083/jcb.138.6.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sugimoto K., Kuriyama K., Shibata A., Himeno M. Characterization of internal DNA-binding and C-terminal dimerization domains of human centromere/kinetochore autoantigen CENP-C in vitro: role of DNA-binding and self-associating activities in kinetochore organization. Chromosome Res. 1997 Apr;5(2):132–141. doi: 10.1023/a:1018422325569. [DOI] [PubMed] [Google Scholar]
  41. Sugimoto K., Yata H., Muro Y., Himeno M. Human centromere protein C (CENP-C) is a DNA-binding protein which possesses a novel DNA-binding motif. J Biochem. 1994 Oct;116(4):877–881. doi: 10.1093/oxfordjournals.jbchem.a124610. [DOI] [PubMed] [Google Scholar]
  42. Sullivan B. A., Schwartz S. Identification of centromeric antigens in dicentric Robertsonian translocations: CENP-C and CENP-E are necessary components of functional centromeres. Hum Mol Genet. 1995 Dec;4(12):2189–2197. doi: 10.1093/hmg/4.12.2189. [DOI] [PubMed] [Google Scholar]
  43. Suzuki T., Ide N., Tanaka I. Immunocytochemical visualization of the centromeres during male and female meiosis in Lilium longiflorum. Chromosoma. 1997 Dec;106(7):435–445. doi: 10.1007/s004120050265. [DOI] [PubMed] [Google Scholar]
  44. Tomkiel J., Cooke C. A., Saitoh H., Bernat R. L., Earnshaw W. C. CENP-C is required for maintaining proper kinetochore size and for a timely transition to anaphase. J Cell Biol. 1994 May;125(3):531–545. doi: 10.1083/jcb.125.3.531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Warburton P. E., Cooke C. A., Bourassa S., Vafa O., Sullivan B. A., Stetten G., Gimelli G., Warburton D., Tyler-Smith C., Sullivan K. F. Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres. Curr Biol. 1997 Nov 1;7(11):901–904. doi: 10.1016/s0960-9822(06)00382-4. [DOI] [PubMed] [Google Scholar]
  46. Yang C. H., Tomkiel J., Saitoh H., Johnson D. H., Earnshaw W. C. Identification of overlapping DNA-binding and centromere-targeting domains in the human kinetochore protein CENP-C. Mol Cell Biol. 1996 Jul;16(7):3576–3586. doi: 10.1128/mcb.16.7.3576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Yu H. G., Hiatt E. N., Chan A., Sweeney M., Dawe R. K. Neocentromere-mediated chromosome movement in maize. J Cell Biol. 1997 Nov 17;139(4):831–840. doi: 10.1083/jcb.139.4.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Yu H. G., Muszynski M. G., Kelly Dawe R. The maize homologue of the cell cycle checkpoint protein MAD2 reveals kinetochore substructure and contrasting mitotic and meiotic localization patterns. J Cell Biol. 1999 May 3;145(3):425–435. doi: 10.1083/jcb.145.3.425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. du Sart D., Cancilla M. R., Earle E., Mao J. I., Saffery R., Tainton K. M., Kalitsis P., Martyn J., Barry A. E., Choo K. H. A functional neo-centromere formed through activation of a latent human centromere and consisting of non-alpha-satellite DNA. Nat Genet. 1997 Jun;16(2):144–153. doi: 10.1038/ng0697-144. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES