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. 1984 Mar 1;98(3):859–869. doi: 10.1083/jcb.98.3.859

Malorientation in half-bivalents at anaphase: analysis of autosomal laggards in untreated, cold-treated, and cold-recovering crane fly spermatocytes

PMCID: PMC2113135  PMID: 6699088

Abstract

Exposing crane fly larvae to 6 degrees C or returning them to 22 degrees C after exposure to 6, 2, or 0.2 degrees C can induce any number of autosomes in their primary spermatocytes to lag near the spindle equator at anaphase. Autosomal laggards in cold-recovering cells are contained in bivalents until anaphase (Janicke, M. A., and J. R. LaFountain, 1982, Chromosoma, 85:619-631). We report here documentation that lagging autosomes in cold-treated and cold- recovering cells are maloriented. During meiosis I, half-bivalents usually associate with only one pole via kinetochore fibers, with sister chromatids being oriented to the same pole. In contrast, laggards had kinetochore microtubules (kMTs) extending from them toward both poles: one sister was oriented to one pole and the other had some or all of its kMTs extending toward the opposite pole. Bipolar malorientation of autosomal laggards also was observed in one untreated cell. The number of kMTs per half-bivalent was similar in lagging and non-lagging autosomes, and those kMTs were contained in long birefringent kinetochore fibers. The overall spindle structure in cold- recovering cells was similar to that observed in untreated anaphase cells. Giemsa-stained centromeric dots of sister chromatids were contiguous in non-laggards and separated in laggards at anaphase. We conclude that bipolar malorientations can exist at anaphase in chromosomes that remain paired until anaphase, that cold recovery increases the frequency of that anomaly, and that such malorientations may be one cause of anaphase lag.

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Selected References

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

  1. Begg D. A., Ellis G. W. Micromanipulation studies of chromosome movement. II. Birefringent chromosomal fibers and the mechanical attachment of chromosomes to the spindle. J Cell Biol. 1979 Aug;82(2):542–554. doi: 10.1083/jcb.82.2.542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Church K., Lin H. P. Meiosis in Drosophila melanogaster. II. The prometaphase-I kinetochore microtubule bundle and kinetochore orientation in males. J Cell Biol. 1982 May;93(2):365–373. doi: 10.1083/jcb.93.2.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dietz R. Bau ud Fnktion des Spindelapparats. Naturwissenschaften. 1969 May;56(5):237–248. doi: 10.1007/BF00633917. [DOI] [PubMed] [Google Scholar]
  4. Forer A., Koch C. Influence of autosome movements and of sex-chromosome movements on sex-chromosome segregation in crane fly spermatocytes. Chromosoma. 1973;40(4):417–442. doi: 10.1007/BF00399432. [DOI] [PubMed] [Google Scholar]
  5. Fuge H. Anaphase transport of akinetochoric fragments in tipulid spermatocytes. Electron microscopic observations on fragment-spindle interactions. Chromosoma. 1975 Sep 26;52(2):149–158. doi: 10.1007/BF00326264. [DOI] [PubMed] [Google Scholar]
  6. Fuge H. Morphological studies on the structure of univalent sex chromosomes during anaphase movement in spermatocytes of the crane fly Pales ferruginea. Chromosoma. 1972;39(4):403–417. doi: 10.1007/BF00326175. [DOI] [PubMed] [Google Scholar]
  7. Fuge H. The arrangement of microtubules and the attachment of chromosomes to the spindle during anaphase in tipulid spermatocytes. Chromosoma. 1974 Apr 9;45(3):245–260. doi: 10.1007/BF00283409. [DOI] [PubMed] [Google Scholar]
  8. Hays T. S., Wise D., Salmon E. D. Traction force on a kinetochore at metaphase acts as a linear function of kinetochore fiber length. J Cell Biol. 1982 May;93(2):374–389. doi: 10.1083/jcb.93.2.374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Henderson S. A., Nicklas R. B., Koch C. A. Temperature-induced orientation instability during meiosis: an experimental analysis. J Cell Sci. 1970 Mar;6(2):323–350. doi: 10.1242/jcs.6.2.323. [DOI] [PubMed] [Google Scholar]
  10. Janicke M. A., LaFountain J. R., Jr Chromosome segregation in crane-fly spermatocytes: cold treatment and cold recovery induce anaphase lag. Chromosoma. 1982;85(5):619–631. doi: 10.1007/BF00330776. [DOI] [PubMed] [Google Scholar]
  11. Jensen C. G. Dynamics of spindle microtubule organization: kinetochore fiber microtubules of plant endosperm. J Cell Biol. 1982 Feb;92(2):540–558. doi: 10.1083/jcb.92.2.540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kubai D. F., Wise D. Nonrandom chromosome segregation in Neocurtilla (Gryllotalpa) hexadactyla: an ultrastructural study. J Cell Biol. 1981 Feb;88(2):281–293. doi: 10.1083/jcb.88.2.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. La Fountain J. R., Jr An association between microtubules and aligned mitochondria in Nephrotoma spermatocytes. Exp Cell Res. 1972;71(2):325–328. doi: 10.1016/0014-4827(72)90300-x. [DOI] [PubMed] [Google Scholar]
  14. LaFountain J. R., Jr Analysis of birefringence and ultrastructure of spindles in primary spermatocytes of Nephrotoma suturalis during anaphase. J Ultrastruct Res. 1976 Mar;54(3):333–346. doi: 10.1016/s0022-5320(76)80020-2. [DOI] [PubMed] [Google Scholar]
  15. LaFountain J. R., Jr Birefringence and fine structure of spindles in spermatocytes of Nephrotoma suturalis at metaphase of first meiotic division. J Ultrastruct Res. 1974 Feb;46(2):268–278. doi: 10.1016/s0022-5320(74)80061-4. [DOI] [PubMed] [Google Scholar]
  16. Marks G. E. The Giemsa-staining centromeres of Nigella damascena. J Cell Sci. 1975 Jun;18(1):19–25. doi: 10.1242/jcs.18.1.19. [DOI] [PubMed] [Google Scholar]
  17. Nicklas R. B. Chromosome micromanipulation. II. Induced reorientation and the experimental control of segregation in meiosis. Chromosoma. 1967;21(1):17–50. doi: 10.1007/BF00330545. [DOI] [PubMed] [Google Scholar]
  18. Nicklas R. B. Mitosis. Adv Cell Biol. 1971;2:225–297. doi: 10.1007/978-1-4615-9588-5_5. [DOI] [PubMed] [Google Scholar]
  19. Sugawara S., Mikamo K. An experimental approach to the analysis of mechanisms of meiotic nondisjunction and anaphase lagging in primary oocytes. Cytogenet Cell Genet. 1980;28(4):251–264. doi: 10.1159/000131538. [DOI] [PubMed] [Google Scholar]
  20. Sumner A. T. A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res. 1972 Nov;75(1):304–306. doi: 10.1016/0014-4827(72)90558-7. [DOI] [PubMed] [Google Scholar]

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