Skip to main content
Log in

Differential mechanisms governing segregation of a univalent in oocytes and spermatocytes of Drosophila melanogaster

  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

In tricomplex heterozygotes in Drosophila melanogaster three metacentric autosomes (the TRI chromosomes) appear as a trivalent in meiosis while one autosome consisting of two homologous arms attached to the same centromere (a compound) behaves as an obligatory univalent. Cytological analysis of meiosis of tricomplex heterozygotes indicates that in oocytes the univalent compound behaves non-independently in relation to segregation of the trivalent. The compound is distributed preferentially to the same pole as one TRI chromosome. In spermatocytes the compound is distributed at random. In some oocytes the directed segregation is shown to be due to a disjunctional interaction between the compound and one partner of the trivalent at the same time as the other two chromosomes of the trivalent are separating from each other. The basic difference between the segregational mechanisms in the two sexes is discussed with a review of evidence indicating that in males segregation is determined by physical linkage that produces a stable orientation of the homologues at metaphase I. On the other hand, both genetic and cytological evidence indicate that in females a physical linkage (a chiasma) is non-essential for maintenance of co-orientation and stability after the onset of prometaphase. Genetic and cytological evidence support the hypothesis that disjunction is predetermined by non-random arrangement of the centromeric regions of chromosomes in the chromocentre — a suprachromosomal organization characteristic of maturing oocytes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ault JG (1984) Unipolar orientation stability of the sex univalent in the grasshopper (Melanoplus sanguinipes). Chromosoma 89:201–205

    Google Scholar 

  • Ault JG, Lin H-PP, Church K (1982) Meiosis in Drosophila melanogaster IV. The conjunctive mechanism of the XY bivalent. Chromosoma 86:309–317

    Google Scholar 

  • Carpenter ATC (1973) A meiotic mutant defective in distributive disjunction in Drosophila melanogaster. Genetics 73:393–428

    Google Scholar 

  • Chadov BF, Chadova EV, Khotskina EA, Kopil CA (1988) Crossing-over and co-orientation of two nonhomologous chromosomes in meiosis of Drosophila females. Genet (Life Sci Adv) 7:71–76

    Google Scholar 

  • Chubykin VL, Chadov BF (1987) The chromocenter in meiotic cells of Drosophila melanogaster females with XY-compounds. (In Russian with an English summary) Tsitologia 29:168–173

    Google Scholar 

  • Church K, Lin H-PP (1982) Meiosis in Drosophila melanogaster. II. The prometaphase-I kinetochore microtubule bundle and kinetochore orientation in males. J Cell Biol 93:365–373

    Google Scholar 

  • Church K, Lin H-PP (1985) Kinetochore microtubules and chromosome movement during prometaphase in Drosophila melanogaster spermatocytes studied in life and with the electron microscope. Chromosoma 92:273–282

    Google Scholar 

  • Church K, Lin H-PP (1988) Drosophila: a model for the study of aneuploidy. In: Vig BK, Sandberg AA (eds) Aneuploidy, part B: Induction and test systems. Alan R Liss, New York, pp 227–255

    Google Scholar 

  • Cooper KW (1945) Normal segregation without chiasmata in female Drosophila melanogaster. Genetics 30:472–484

    Google Scholar 

  • Cooper KW (1950) Normal spermatogenesis in Drosophila. In: Demerec M (ed) Biology of Drosophila. John Wiley & Sons, New York, pp 1–61

    Google Scholar 

  • Cooper KW (1964) Meiotic conjunctive elements not involving chiasmata. Proc Natl Acad Sci USA 52:1248–1255

    Google Scholar 

  • Dävring L, Sunner M (1973) Female meiosis and embryonic mitosis in Drosophila melanogaster. I. Meiosis and fertilization. Hereditas 73:51–64

    Google Scholar 

  • Dävring L, Sunner M (1979) Cytological evidence for procentric synapsis of meiotic chromosomes in female Drosophila melanogaster. The behaviour of an extra Y chromosome. Hereditas 91:53–64

    Google Scholar 

  • Dietz R (1969) Bau und Function des Spindelapparats. Naturwissenschaften 56:237–248

    Google Scholar 

  • Goldstein LSB (1981) Kinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster. Cell 25:591–602

    Google Scholar 

  • Grell RF (1962) A new hypothesis on the nature and sequence of meiotic events in the female of Drosophila melanogaster. Proc Natl Acad Sci USA 48:165–172

    Google Scholar 

  • Grell RF (1965) Chromosome pairing, crossing-over, and segregation in Drosophila melanogaster. Natl Cancer Inst Monogr 18:215–242

    Google Scholar 

  • Grell RF (1976) Distributive pairing. In: Ashburner M, Novitski E (eds) The genetics and biology of Drosophila, vol 1a. Academic Press, London, pp 435–486

    Google Scholar 

  • Hawley RS (1989) Genetic and molecular analysis of a simple disjunctional system in Drosophila melanogaster. Prog Clin Biol Res 311:277–302

    Google Scholar 

  • Henderson SA, Koch CA (1970) Co-orientation stability by physical tension: a demonstration with experimentally interlocked bivalents. Chromosoma 29:207–216

    Google Scholar 

  • Hughes-Schrader S (1969) Distance segregation and compound sex chromosomes in Mantispids (Neuroptera: Mantispidae). Chromosoma 27:109–129

    Google Scholar 

  • John B (1990) Meiosis. (Developmental and cell biology series 22.) Cambridge University Press, Cambridge, p 396

    Google Scholar 

  • John B, Lewis KR (1965) The meiotic system. Springer-Verlag, Wien, p 335

    Google Scholar 

  • King RC, Rubinson AC, Smith RF (1956) Oogenesis in adult Drosophila melanogaster. Growth 20:121–157

    Google Scholar 

  • Kozhevnikov B (1940) Preferential autosome disjunction in triploids. Bull Biol Med Exp USSR 9:13–14

    Google Scholar 

  • Lin H-PP, Ault JG, Kimble M, Church K (1984) Meiosis in Drosophila melanogaster. V. Univalent behavior in In(1)sc4Lsc8R/BSY males. Can J Genet Cytol 26:445–458

    Google Scholar 

  • Lindsley D, Zimm G (1987) The genome of Drosophila melanogaster. Part 3: rearrangements. Drosophila Inf Serv 65:1–224

    Google Scholar 

  • Lüning KG (1982a) Genetics of inbred Drosophila melanogaster VI. Crossing-over in secondary non-disjunction exceptionals. Hereditas 96:161–174

    Google Scholar 

  • Lüning KG (1982b) Genetics of inbred Drosophila melanogaster VII. Evidence of normal chromosome pairing in the distal ends of X-chromosomes in secondary non-disjunction. Hereditas 96:287–290

    Google Scholar 

  • Merriam JR, Frost JN (1964) Exchange and nondisjunction of the X-chromosome in female Drosophila melanogaster. Genetics 49:109–122

    Google Scholar 

  • Nicklas RB (1961) Recurrent pole-to-pole movements of the sex chromosome during prometaphase I in Melanoplus differentialis spermatocytes. Chromosoma 12:97–115

    Google Scholar 

  • Nicklas RB (1971) Mitosis. Adv Cell Biol 2:225–297

    Google Scholar 

  • Niclas RB (1974) Chromosome segregation mechanisms. Genetics 78:205–213

    Google Scholar 

  • Nicklas RB, Koch CA (1969) Chromosome micromanipulation. III. Spindle fiber tension and the reorientation of mal-oriented chromosomes. J Cell Biol 43:40–50

    Google Scholar 

  • Nokkala S, Puro J (1976) Cytological evidence for a chromocenter in Drosophila melanogaster oocytes. Hereditas 83:265–268

    Google Scholar 

  • Novitski E (1964) An alternative to the distributive pairing hypothesis in Drosophila. Genetics 50:1449–1451

    Google Scholar 

  • Novitski E, Puro J (1978) A critique of theories of meiosis in the female of Drosophila melanogaster. Hereditas 89:51–67

    Google Scholar 

  • Peacock WJ (1965) Nonrandom segregation of chromosomes in Drosophila males. Genetics 51:573–583

    Google Scholar 

  • Puro J (1973) Tricomplex, a new type of autosome complement in Drosophila melanogaster. Hereditas 75:140–143

    Google Scholar 

  • Puro J (1985) Meiotic behaviour of compound chromosomes in tricomplex heterozygotes in Drosophila melanogaster. Genet Res 46:287–307

    Google Scholar 

  • Puro J, Nokkala S (1977) Meiotic segregation of chromosomes in Drosophila melanogaster oocytes. A cytological approach. Chromosoma 63:273–286

    Google Scholar 

  • Rasmussen IE (1960) New mutants. Drosophila Inf Serv 34:53

    Google Scholar 

  • Sandler L, Novitski E (1956) Evidence for genetic homology between chromosomes I and IV in Drosophila melanogaster, with a proposed explanation for the crowding effect in triploids. Genetics 41:189–193

    Google Scholar 

  • Weinstein A (1936) The theory of multiple-strand crossing over. Genetics 21:155–199

    Google Scholar 

  • Yamamoto M (1979) Cytological studies of heterochromatin function in the Drosophila melanogaster male: Autosomal meiotic pairing. Chromosoma 72:293–328

    Google Scholar 

  • Zhang P, Knowles BA, Goldstein LSB, Hawley RS (1990) A kinesin-like protein required for distributive chromosome segregation in Drosophila. Cell 62:1053–1062

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

by D. Schweizer

Rights and permissions

Reprints and permissions

About this article

Cite this article

Puro, J. Differential mechanisms governing segregation of a univalent in oocytes and spermatocytes of Drosophila melanogaster . Chromosoma 100, 305–314 (1991). https://doi.org/10.1007/BF00360529

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00360529

Keywords

Navigation