Skip to main content
Genetics logoLink to Genetics
. 1998 Mar;148(3):1285–1294. doi: 10.1093/genetics/148.3.1285

Effect of the pairing gene Ph1 on centromere misdivision in common wheat.

J M Vega 1, M Feldman 1
PMCID: PMC1460028  PMID: 9539442

Abstract

The cytologically diploid-like meiotic behavior of hexaploid wheat (i.e., exclusive bivalent pairing of homologues) is largely controlled by the pairing homoeologous gene Ph1. This gene suppresses pairing between homoeologous (partially homologous) chromosomes of the three closely related genomes that compose the hexaploid wheat complement. It has been previously proposed that Ph1 regulates meiotic pairing by determining the pattern of premeiotic arrangement of homologous and homoeologous chromosomes. We therefore assume that Ph1 action may be targeted at the interaction of centromeres with spindle microtubules--an interaction that is critical for movement of chromosomes to their specific interphase positions. Using monosomic lines of common wheat, we studied the effect of this gene on types and rates of centromere division of univalents at meiosis. In the presence of the normal two doses of Ph1, the frequency of transverse breakage (misdivision) of the centromere of univalent chromosomes was high in both first and second meiotic divisions; whereas with zero dose of the gene, this frequency was drastically reduced. The results suggest that Ph1 is a trans-acting gene affecting centromere-microtubules interaction. The findings are discussed in the context of the effect of Ph1 on interphase chromosome arrangement.

Full Text

The Full Text of this article is available as a PDF (190.8 KB).

Selected References

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

  1. 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]
  2. Avivi L., Feldman M. Arrangement of chromosomes in the interphase nucleus of plants. Hum Genet. 1980;55(3):281–295. doi: 10.1007/BF00290206. [DOI] [PubMed] [Google Scholar]
  3. Avivi L., Feldman M., Bushuk W. The Mechanism of Somatic Association in Common Wheat, TRITICUM AESTIVUM L. II. Differential Affinity for Colchicine of Spindle Microtubules of Plants Having Different Doses of the Somatic-Association Suppressor. Genetics. 1970 Aug;65(4):585–592. doi: 10.1093/genetics/65.4.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Avivi L., Feldman M. The Mechanism of Somatic Association in Common Wheat, TRITICUM AESTIVUM L. IV. Further Evidence for Modification of Spindle Tubulin through the Somatic-Association Genes as Measured by Vinblastine Binding. Genetics. 1973 Mar;73(3):379–385. doi: 10.1093/genetics/73.3.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cassimeris L., Inoué S., Salmon E. D. Microtubule dynamics in the chromosomal spindle fiber: analysis by fluorescence and high-resolution polarization microscopy. Cell Motil Cytoskeleton. 1988;10(1-2):185–196. doi: 10.1002/cm.970100123. [DOI] [PubMed] [Google Scholar]
  6. Cassimeris L., Rieder C. L., Rupp G., Salmon E. D. Stability of microtubule attachment to metaphase kinetochores in PtK1 cells. J Cell Sci. 1990 May;96(Pt 1):9–15. doi: 10.1242/jcs.96.1.9. [DOI] [PubMed] [Google Scholar]
  7. Doheny K. F., Sorger P. K., Hyman A. A., Tugendreich S., Spencer F., Hieter P. Identification of essential components of the S. cerevisiae kinetochore. Cell. 1993 May 21;73(4):761–774. doi: 10.1016/0092-8674(93)90255-O. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dubcovsky J., Luo M., Dvorak J. Differentiation between homoeologous chromosomes 1A of wheat and 1Am of Triticum monococcum and its recognition by the wheat Ph1 locus. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6645–6649. doi: 10.1073/pnas.92.14.6645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Feldman M., Liu B., Segal G., Abbo S., Levy A. A., Vega J. M. Rapid elimination of low-copy DNA sequences in polyploid wheat: a possible mechanism for differentiation of homoeologous chromosomes. Genetics. 1997 Nov;147(3):1381–1387. doi: 10.1093/genetics/147.3.1381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Feldman M., Mello-Sampayo T., Sears E. R. Somatic association in Triticum aestivum. Proc Natl Acad Sci U S A. 1966 Oct;56(4):1192–1199. doi: 10.1073/pnas.56.4.1192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Feldman M. The effect of chromosomes 5B, 5D, and 5A on chromosomal pairing in triticum aestivum. Proc Natl Acad Sci U S A. 1966 Jun;55(6):1447–1453. doi: 10.1073/pnas.55.6.1447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gill K. S., Gill B. S. A DNA fragment mapped within the submicroscopic deletion of Ph1, a chromosome pairing regulator gene in polyploid wheat. Genetics. 1991 Sep;129(1):257–259. doi: 10.1093/genetics/129.1.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gill K. S., Gill B. S., Endo T. R., Mukai Y. Fine physical mapping of Ph1, a chromosome pairing regulator gene in polyploid wheat. Genetics. 1993 Aug;134(4):1231–1236. doi: 10.1093/genetics/134.4.1231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Haber J. E., Thorburn P. C. Healing of broken linear dicentric chromosomes in yeast. Genetics. 1984 Feb;106(2):207–226. doi: 10.1093/genetics/106.2.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hadlaczky G., Went M., Ringertz N. R. Direct evidence for the non-random localization of mammalian chromosomes in the interphase nucleus. Exp Cell Res. 1986 Nov;167(1):1–15. doi: 10.1016/0014-4827(86)90199-0. [DOI] [PubMed] [Google Scholar]
  16. Hawley R. S., Arbel T. Yeast genetics and the fall of the classical view of meiosis. Cell. 1993 Feb 12;72(3):301–303. doi: 10.1016/0092-8674(93)90108-3. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Jauhar P. P. Genetic control of diploid-like meiosis in hexaploid tall fescue. Nature. 1975 Apr 17;254(5501):595–597. doi: 10.1038/254595a0. [DOI] [PubMed] [Google Scholar]
  19. Kaszás E., Birchler J. A. Misdivision analysis of centromere structure in maize. EMBO J. 1996 Oct 1;15(19):5246–5255. [PMC free article] [PubMed] [Google Scholar]
  20. Kleckner N. Meiosis: how could it work? Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8167–8174. doi: 10.1073/pnas.93.16.8167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kleckner N., Weiner B. M. Potential advantages of unstable interactions for pairing of chromosomes in meiotic, somatic, and premeiotic cells. Cold Spring Harb Symp Quant Biol. 1993;58:553–565. doi: 10.1101/sqb.1993.058.01.062. [DOI] [PubMed] [Google Scholar]
  22. Loidl J. The initiation of meiotic chromosome pairing: the cytological view. Genome. 1990 Dec;33(6):759–778. doi: 10.1139/g90-115. [DOI] [PubMed] [Google Scholar]
  23. Mitchison T., Evans L., Schulze E., Kirschner M. Sites of microtubule assembly and disassembly in the mitotic spindle. Cell. 1986 May 23;45(4):515–527. doi: 10.1016/0092-8674(86)90283-7. [DOI] [PubMed] [Google Scholar]
  24. Mitchison T., Kirschner M. Dynamic instability of microtubule growth. Nature. 1984 Nov 15;312(5991):237–242. doi: 10.1038/312237a0. [DOI] [PubMed] [Google Scholar]
  25. Nagele R., Freeman T., McMorrow L., Lee H. Y. Precise spatial positioning of chromosomes during prometaphase: evidence for chromosomal order. Science. 1995 Dec 15;270(5243):1831–1835. doi: 10.1126/science.270.5243.1831. [DOI] [PubMed] [Google Scholar]
  26. Rajhathy T., Thomas H. Genetic control of chromosome pairing in hexaploid oats. Nat New Biol. 1972 Oct 18;239(94):217–219. doi: 10.1038/newbio239217a0. [DOI] [PubMed] [Google Scholar]
  27. SEARS E. R. Misdivision of univalents in common wheat. Chromosoma. 1952;4(6):535–550. doi: 10.1007/BF00325789. [DOI] [PubMed] [Google Scholar]
  28. Scherthan H., Weich S., Schwegler H., Heyting C., Härle M., Cremer T. Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J Cell Biol. 1996 Sep;134(5):1109–1125. doi: 10.1083/jcb.134.5.1109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Steinitz-Sears L. M. Somatic instability of telocentric chromosomes in wheat and the nature of the centromere. Genetics. 1966 Jul;54(1):241–248. doi: 10.1093/genetics/54.1.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Weiner B. M., Kleckner N. Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell. 1994 Jul 1;77(7):977–991. doi: 10.1016/0092-8674(94)90438-3. [DOI] [PubMed] [Google Scholar]
  31. Willard H. F. Evolution of alpha satellite. Curr Opin Genet Dev. 1991 Dec;1(4):509–514. doi: 10.1016/s0959-437x(05)80200-x. [DOI] [PubMed] [Google Scholar]
  32. Willard H. F., Waye J. S. Chromosome-specific subsets of human alpha satellite DNA: analysis of sequence divergence within and between chromosomal subsets and evidence for an ancestral pentameric repeat. J Mol Evol. 1987;25(3):207–214. doi: 10.1007/BF02100014. [DOI] [PubMed] [Google Scholar]
  33. Wise D., Cassimeris L., Rieder C. L., Wadsworth P., Salmon E. D. Chromosome fiber dynamics and congression oscillations in metaphase PtK2 cells at 23 degrees C. Cell Motil Cytoskeleton. 1991;18(2):131–142. doi: 10.1002/cm.970180208. [DOI] [PubMed] [Google Scholar]
  34. Zhai Y., Kronebusch P. J., Borisy G. G. Kinetochore microtubule dynamics and the metaphase-anaphase transition. J Cell Biol. 1995 Nov;131(3):721–734. doi: 10.1083/jcb.131.3.721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Zinkowski R. P., Meyne J., Brinkley B. R. The centromere-kinetochore complex: a repeat subunit model. J Cell Biol. 1991 Jun;113(5):1091–1110. doi: 10.1083/jcb.113.5.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES