Abstract
In meiosis I, two chromatids move to each spindle pole. Then, in meiosis II, the two are distributed, one to each future gamete. This requires that meiosis I chromosomes attach to the spindle differently than meiosis II chromosomes and that they regulate chromosome cohesion differently. We investigated whether the information that dictates the division type of the chromosome comes from the whole cell, the spindle, or the chromosome itself. Also, we determined when chromosomes can switch from meiosis I behavior to meiosis II behavior. We used a micromanipulation needle to fuse grasshopper spermatocytes in meiosis I to spermatocytes in meiosis II, and to move chromosomes from one spindle to the other. Chromosomes placed on spindles of a different meiotic division always behaved as they would have on their native spindle; e.g., a meiosis I chromosome attached to a meiosis II spindle in its normal fashion and sister chromatids moved together to the same spindle pole. We also showed that meiosis I chromosomes become competent meiosis II chromosomes in anaphase of meiosis I, but not before. The patterns for attachment to the spindle and regulation of cohesion are built into the chromosome itself. These results suggest that regulation of chromosome cohesion may be linked to differences in the arrangement of kinetochores in the two meiotic divisions.
MeSH Terms
Anaphase/physiology
Animals
Cells, Cultured
Chromosomes/physiology
Grasshoppers
Kinetochores/physiology
Male
Meiosis/genetics
Spermatocytes/cytology,physiology
Spindle Apparatus/physiology
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Paliulis L V
Department of Biology, Duke University, Durham, North Carolina 27708, USA.
[email protected]
Nicklas R B
References (23)
23 references, click to expand
-
A comparative study of orientation at behavior of univalent in living grasshopper spermatocytes.
Chromosoma. 1995 Oct;104(1):56-67
PMID: 7587595
-
Involvement of chromatid cohesiveness at the centromere and chromosome arms in meiotic chromosome segregation: a cytological approach.
Chromosoma. 1992 Jun;101(8):493-501
PMID: 1424993
-
Holding chromatids together to ensure they go their separate ways.
Bioessays. 1996 Apr;18(4):293-300
PMID: 8967897
-
Chromosome segregation during meiosis: building an unambivalent bivalent.
Curr Top Dev Biol. 1998;37:263-99
PMID: 9352189
-
The role of sister chromatid cohesiveness and structure in meiotic behaviour.
Chromosoma. 1997 Dec;106(7):422-34
PMID: 9391215
-
Sister-chromatid cohesion in mitosis and meiosis.
Annu Rev Genet. 1994;28:167-87
PMID: 7893122
-
The cohesion protein MEI-S332 localizes to condensed meiotic and mitotic centromeres until sister chromatids separate.
J Cell Biol. 1998 Mar 9;140(5):1003-12
PMID: 9490715
-
Genetic interactions between mei-S332 and ord in the control of sister-chromatid cohesion.
Genetics. 1998 Dec;150(4):1467-76
PMID: 9832524
-
Maintenance of sister-chromatid cohesion at the centromere by the Drosophila MEI-S332 protein.
Genes Dev. 1998 Dec 15;12(24):3843-56
PMID: 9869638
-
A functional assay for centromere-associated sister chromatid cohesion.
Science. 1999 Jul 9;285(5425):254-7
PMID: 10398602
-
A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis.
Cell. 1999 Jul 9;98(1):91-103
PMID: 10412984
-
Cohesin Rec8 is required for reductional chromosome segregation at meiosis.
Nature. 1999 Jul 29;400(6743):461-4
PMID: 10440376
-
Identification of cohesin association sites at centromeres and along chromosome arms.
Cell. 1999 Sep 17;98(6):847-58
PMID: 10499801
-
The centromeric sister chromatid cohesion site directs Mcd1p binding to adjacent sequences.
Mol Cell. 1999 Sep;4(3):445-50
PMID: 10518226
-
The ties that bind: localization of the sister-chromatid cohesin complex on yeast chromosomes.
Cell. 1999 Oct 1;99(1):1-4
PMID: 10520987
-
[Electron microscopic studies on the form change of kinetochores during spermatocyte divisions in Pales ferruginea (Nematocera)].
Chromosoma. 1972;38(2):139-72
PMID: 5066446
-
Chromosome distribution: experiments on cell hybrids and in vitro.
Philos Trans R Soc Lond B Biol Sci. 1977 Mar 21;277(955):267-76
PMID: 16290
-
Kinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster.
Cell. 1981 Sep;25(3):591-602
PMID: 6793236
-
Spindle microtubules and their mechanical associations after micromanipulation in anaphase.
J Cell Biol. 1982 Oct;95(1):91-104
PMID: 6890559
-
Meiosis in Drosophila melanogaster, III. The effect of orientation disruptor (ord) on gonial mitotic and the meiotic divisions in males.
Genetics. 1982 Dec;102(4):751-70
PMID: 6821250
-
Microtubules, chromosome movement, and reorientation after chromosomes are detached from the spindle by micromanipulation.
Chromosoma. 1985;92(4):313-24
PMID: 4042772
-
The Drosophila mei-S332 gene promotes sister-chromatid cohesion in meiosis following kinetochore differentiation.
Genetics. 1992 Apr;130(4):827-41
PMID: 1582560
-
Mei-S332, a Drosophila protein required for sister-chromatid cohesion, can localize to meiotic centromere regions.
Cell. 1995 Oct 20;83(2):247-56
PMID: 7585942