Skip to main content
Genetics logoLink to Genetics
. 1993 Dec;135(4):1151–1166. doi: 10.1093/genetics/135.4.1151

The Role of the Ameiotic1 Gene in the Initiation of Meiosis and in Subsequent Meiotic Events in Maize

I Golubovskaya 1, Z K Grebennikova 1, N A Avalkina 1, W F Sheridan 1
PMCID: PMC1205746  PMID: 8307330

Abstract

Understanding the initiation of meiosis and the relationship of this event with other key cytogenetic processes are major goals in studying the genetic control of meiosis in higher plants. Our genetic and structural analysis of two mutant alleles of the ameiotic1 gene (am1 and am1-praI) suggest that this locus plays an essential role in the initiation of meiosis in maize. The product of the ameiotic1 gene affects an earlier stage in the meiotic sequence than any other known gene in maize and is important for the irreversible commitment of cells to meiosis and for crucial events marking the passage from premeiotic interphase into prophase I including chromosome synapsis. It appears that the period of ameiotic1 gene function in meiosis at a minimum covers the interval from some point during premeiotic interphase until the early zygotene stage of meiosis. To study the interaction of genes in the progression of meiosis, several double meiotic mutants were constructed. In these double mutants (i) the ameiotic1 mutant allele was brought together with the meiotic mutation (afd1) responsible for the fixation of centromeres in meiosis; and with the mutant alleles of the three meiotic genes that control homologous chromosome segregation (dv1, ms43 and ms28), which impair microtubule organizing center organization, the orientation of the spindle fiber apparatus, and the depolymerization of spindle filaments after the first meiotic division, respectively; (ii) the afd1 mutation was combined with two mutations (dsy1 and as1) affecting homologous pairing; (iii) the ms43 mutation was combined with the as1, the ms28 and the dv1 mutations; and (iv) the ms28 mutation was combined with the dv1 mutation and the ms4 (polymitotic1) mutations. An analysis of gene interaction in the double mutants led us to conclude that the ameiotic1 gene is epistatic over the afd1, the dv1, the ms43 and the ms28 genes but the significance of this relationship requires further analysis. The afd gene appears to function from premeiotic interphase throughout the first meiotic division, but it is likely that its function begins after the start of the ameiotic1 gene expression. The afd1 gene is epistatic over the two synaptic mutations dsy1 and as1 and also over the dv1 mutation. The new ameiotic*-485 and leptotene arrest*-487 mutations isolated from an active ROBERTSON's Mutator stocks take part in the control of the initiation of meiosis.

Full Text

The Full Text of this article is available as a PDF (10.9 MB).

Selected References

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

  1. Baker B. S., Carpenter A. T., Esposito M. S., Esposito R. E., Sandler L. The genetic control of meiosis. Annu Rev Genet. 1976;10:53–134. doi: 10.1146/annurev.ge.10.120176.000413. [DOI] [PubMed] [Google Scholar]
  2. Byers B., Goetsch L. Reversible pachytene arrest of Saccharomyces cerevisiae at elevated temperature. Mol Gen Genet. 1982;187(1):47–53. doi: 10.1007/BF00384382. [DOI] [PubMed] [Google Scholar]
  3. Dorée M., Peaucellier G., Picard A. Activity of the maturation-promoting factor and the extent of protein phosphorylation oscillate simultaneously during meiotic maturation of starfish oocytes. Dev Biol. 1983 Oct;99(2):489–501. doi: 10.1016/0012-1606(83)90298-1. [DOI] [PubMed] [Google Scholar]
  4. Golubovskaya I. N. Genetic control of meiosis. Int Rev Cytol. 1979;58:247–290. doi: 10.1016/s0074-7696(08)61477-1. [DOI] [PubMed] [Google Scholar]
  5. Honigberg S. M., Conicella C., Espositio R. E. Commitment to meiosis in Saccharomyces cerevisiae: involvement of the SPO14 gene. Genetics. 1992 Apr;130(4):703–716. doi: 10.1093/genetics/130.4.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Jacobs T. Control of the cell cycle. Dev Biol. 1992 Sep;153(1):1–15. doi: 10.1016/0012-1606(92)90087-w. [DOI] [PubMed] [Google Scholar]
  7. Kassir Y., Granot D., Simchen G. IME1, a positive regulator gene of meiosis in S. cerevisiae. Cell. 1988 Mar 25;52(6):853–862. doi: 10.1016/0092-8674(88)90427-8. [DOI] [PubMed] [Google Scholar]
  8. Kleckner N., Padmore R., Bishop D. K. Meiotic chromosome metabolism: one view. Cold Spring Harb Symp Quant Biol. 1991;56:729–743. doi: 10.1101/sqb.1991.056.01.082. [DOI] [PubMed] [Google Scholar]
  9. Loidl J. Coming to grips with a complex matter. A multidisciplinary approach to the synaptonemal complex. Chromosoma. 1991 Jun;100(5):289–292. doi: 10.1007/BF00360526. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Malone R. E. Dual regulation of meiosis in yeast. Cell. 1990 May 4;61(3):375–378. doi: 10.1016/0092-8674(90)90517-i. [DOI] [PubMed] [Google Scholar]
  12. Mitchell A. P. Two switches govern entry into meiosis in yeast. Prog Clin Biol Res. 1988;267:47–66. [PubMed] [Google Scholar]
  13. Pelech S. L., Sanghera J. S., Daya-Makin M. Protein kinase cascades in meiotic and mitotic cell cycle control. Biochem Cell Biol. 1990 Dec;68(12):1297–1330. doi: 10.1139/o90-194. [DOI] [PubMed] [Google Scholar]
  14. RHOADES M. M. Meiosis in maize. J Hered. 1950 Mar;41(3):59–67. doi: 10.1093/oxfordjournals.jhered.a106089. [DOI] [PubMed] [Google Scholar]
  15. Shah J. C., Clancy M. J. IME4, a gene that mediates MAT and nutritional control of meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 1992 Mar;12(3):1078–1086. doi: 10.1128/mcb.12.3.1078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Simchen G., Kassir Y. Genetic regulation of differentiation towards meiosis in the yeast Saccharomyces cerevisiae. Genome. 1989;31(1):95–99. doi: 10.1139/g89-018. [DOI] [PubMed] [Google Scholar]
  17. Simchen G., Kassir Y., Horesh-Cabilly O., Friedmann A. Elevated recombination and pairing structures during meiotic arrest in yeast of the nuclear division mutant cdc5. Mol Gen Genet. 1981;184(1):46–51. doi: 10.1007/BF00271193. [DOI] [PubMed] [Google Scholar]
  18. Staiger C. J., Cande W. Z. Ameiotic, a gene that controls meiotic chromosome and cytoskeletal behavior in maize. Dev Biol. 1992 Nov;154(1):226–230. doi: 10.1016/0012-1606(92)90063-m. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. von Wettstein D., Rasmussen S. W., Holm P. B. The synaptonemal complex in genetic segregation. Annu Rev Genet. 1984;18:331–413. doi: 10.1146/annurev.ge.18.120184.001555. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES