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The reduction of chromosome number in meiosis is determined by properties built into the chromosomes.

Paliulis LV, Nicklas RB - J. Cell Biol. (2000)

Bottom Line: Also, we determined when chromosomes can switch from meiosis I behavior to meiosis II behavior.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Duke University, Durham, North Carolina 27708, USA. lvp@acpub.duke.edu

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.

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Determinants for the pattern of chromosome attachment to the spindle and release of chromosome cohesion are built into the chromosome. A metaphase I grasshopper spermatocyte was fused to a metaphase II spermatocyte. Spindle poles are indicated by asterisks, manipulated meiosis I chromosomes by straight arrows, unmanipulated meiosis I chromosomes by curved arrows, manipulated meiosis II chromosomes by filled arrowheads, and unmanipulated meiosis II chromosomes by open arrowheads. The fused cell contains two spindles. A bivalent was detached from the meiosis I spindle and placed near the meiosis II spindle (0 and 8 min, straight arrows). The bivalent attached to the meiosis II spindle with a pair of sister kinetochores facing each pole (48 min, straight arrows). Pairs of sister chromatids segregated to each pole (69 min, straight arrows). Unmanipulated bivalents on the meiosis I spindle had a pair of sister kinetochores facing each pole (48 min, curved arrows). In anaphase in unmanipulated bivalents, pairs of sister chromatids separated from one another (69 min, curved arrows). A meiosis II chromosome (12 min, filled arrowhead) was detached from the meiosis II spindle and placed near the meiosis I spindle (36 min, filled arrowhead). The meiosis II chromosome attached to the meiosis I spindle with a single sister kinetochore facing each pole (48 min, filled arrowhead), and single sister chromatids moved to opposite poles in anaphase (69 min, filled arrowheads). Unmanipulated meiosis II chromosomes attached with a single sister kinetochore facing each pole (48 min, open arrowheads) and moved to opposite poles in anaphase (69 min, open arrowheads). Bar, 10 μm.
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Figure 2: Determinants for the pattern of chromosome attachment to the spindle and release of chromosome cohesion are built into the chromosome. A metaphase I grasshopper spermatocyte was fused to a metaphase II spermatocyte. Spindle poles are indicated by asterisks, manipulated meiosis I chromosomes by straight arrows, unmanipulated meiosis I chromosomes by curved arrows, manipulated meiosis II chromosomes by filled arrowheads, and unmanipulated meiosis II chromosomes by open arrowheads. The fused cell contains two spindles. A bivalent was detached from the meiosis I spindle and placed near the meiosis II spindle (0 and 8 min, straight arrows). The bivalent attached to the meiosis II spindle with a pair of sister kinetochores facing each pole (48 min, straight arrows). Pairs of sister chromatids segregated to each pole (69 min, straight arrows). Unmanipulated bivalents on the meiosis I spindle had a pair of sister kinetochores facing each pole (48 min, curved arrows). In anaphase in unmanipulated bivalents, pairs of sister chromatids separated from one another (69 min, curved arrows). A meiosis II chromosome (12 min, filled arrowhead) was detached from the meiosis II spindle and placed near the meiosis I spindle (36 min, filled arrowhead). The meiosis II chromosome attached to the meiosis I spindle with a single sister kinetochore facing each pole (48 min, filled arrowhead), and single sister chromatids moved to opposite poles in anaphase (69 min, filled arrowheads). Unmanipulated meiosis II chromosomes attached with a single sister kinetochore facing each pole (48 min, open arrowheads) and moved to opposite poles in anaphase (69 min, open arrowheads). Bar, 10 μm.

Mentions: A total of six metaphase I/metaphase II fusions were studied. Fusion did not cause cell death, showing that the physiological differences between meiosis I and meiosis II cells do not make the two different cell types incompatible. The cells retained both a meiosis I and a meiosis II spindle in the same cell (Fig. 2, 0 min). We detached a bivalent from the meiosis I spindle. Such detachment is genuine—the old kinetochore microtubules are lost, so the chromosome must start fresh in forming microtubule attachments (Nicklas and Kubai 1985). The detached chromosome was then moved to the side of the meiosis II spindle farthest from the meiosis I spindle so that it would have no option but to attach to the meiosis II spindle. The bivalent promptly attached to the meiosis II spindle (Fig. 2, 8 min, straight arrows) and congressed to the spindle equator (Fig. 2, 48 min, straight arrows). In anaphase, sister chromatids behaved in the normal meiosis I fashion and moved together to their associated pole (Fig. 2, 69 min, straight arrows); meanwhile, the other chromosomes on that spindle behaved in their normal way with sister chromatids moving to opposite poles (Fig. 2 and 69 min, open arrowheads). Cohesion behavior was also chromosome intrinsic. Meiosis I chromosomes on meiosis II spindles lost cohesion only between chromatid arms (Fig. 2, 69 min, straight arrows), while the nearby meiosis II chromosomes lost cohesion between centromeres (Fig. 2, 69 min, open arrowheads).


The reduction of chromosome number in meiosis is determined by properties built into the chromosomes.

Paliulis LV, Nicklas RB - J. Cell Biol. (2000)

Determinants for the pattern of chromosome attachment to the spindle and release of chromosome cohesion are built into the chromosome. A metaphase I grasshopper spermatocyte was fused to a metaphase II spermatocyte. Spindle poles are indicated by asterisks, manipulated meiosis I chromosomes by straight arrows, unmanipulated meiosis I chromosomes by curved arrows, manipulated meiosis II chromosomes by filled arrowheads, and unmanipulated meiosis II chromosomes by open arrowheads. The fused cell contains two spindles. A bivalent was detached from the meiosis I spindle and placed near the meiosis II spindle (0 and 8 min, straight arrows). The bivalent attached to the meiosis II spindle with a pair of sister kinetochores facing each pole (48 min, straight arrows). Pairs of sister chromatids segregated to each pole (69 min, straight arrows). Unmanipulated bivalents on the meiosis I spindle had a pair of sister kinetochores facing each pole (48 min, curved arrows). In anaphase in unmanipulated bivalents, pairs of sister chromatids separated from one another (69 min, curved arrows). A meiosis II chromosome (12 min, filled arrowhead) was detached from the meiosis II spindle and placed near the meiosis I spindle (36 min, filled arrowhead). The meiosis II chromosome attached to the meiosis I spindle with a single sister kinetochore facing each pole (48 min, filled arrowhead), and single sister chromatids moved to opposite poles in anaphase (69 min, filled arrowheads). Unmanipulated meiosis II chromosomes attached with a single sister kinetochore facing each pole (48 min, open arrowheads) and moved to opposite poles in anaphase (69 min, open arrowheads). Bar, 10 μm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2150703&req=5

Figure 2: Determinants for the pattern of chromosome attachment to the spindle and release of chromosome cohesion are built into the chromosome. A metaphase I grasshopper spermatocyte was fused to a metaphase II spermatocyte. Spindle poles are indicated by asterisks, manipulated meiosis I chromosomes by straight arrows, unmanipulated meiosis I chromosomes by curved arrows, manipulated meiosis II chromosomes by filled arrowheads, and unmanipulated meiosis II chromosomes by open arrowheads. The fused cell contains two spindles. A bivalent was detached from the meiosis I spindle and placed near the meiosis II spindle (0 and 8 min, straight arrows). The bivalent attached to the meiosis II spindle with a pair of sister kinetochores facing each pole (48 min, straight arrows). Pairs of sister chromatids segregated to each pole (69 min, straight arrows). Unmanipulated bivalents on the meiosis I spindle had a pair of sister kinetochores facing each pole (48 min, curved arrows). In anaphase in unmanipulated bivalents, pairs of sister chromatids separated from one another (69 min, curved arrows). A meiosis II chromosome (12 min, filled arrowhead) was detached from the meiosis II spindle and placed near the meiosis I spindle (36 min, filled arrowhead). The meiosis II chromosome attached to the meiosis I spindle with a single sister kinetochore facing each pole (48 min, filled arrowhead), and single sister chromatids moved to opposite poles in anaphase (69 min, filled arrowheads). Unmanipulated meiosis II chromosomes attached with a single sister kinetochore facing each pole (48 min, open arrowheads) and moved to opposite poles in anaphase (69 min, open arrowheads). Bar, 10 μm.
Mentions: A total of six metaphase I/metaphase II fusions were studied. Fusion did not cause cell death, showing that the physiological differences between meiosis I and meiosis II cells do not make the two different cell types incompatible. The cells retained both a meiosis I and a meiosis II spindle in the same cell (Fig. 2, 0 min). We detached a bivalent from the meiosis I spindle. Such detachment is genuine—the old kinetochore microtubules are lost, so the chromosome must start fresh in forming microtubule attachments (Nicklas and Kubai 1985). The detached chromosome was then moved to the side of the meiosis II spindle farthest from the meiosis I spindle so that it would have no option but to attach to the meiosis II spindle. The bivalent promptly attached to the meiosis II spindle (Fig. 2, 8 min, straight arrows) and congressed to the spindle equator (Fig. 2, 48 min, straight arrows). In anaphase, sister chromatids behaved in the normal meiosis I fashion and moved together to their associated pole (Fig. 2, 69 min, straight arrows); meanwhile, the other chromosomes on that spindle behaved in their normal way with sister chromatids moving to opposite poles (Fig. 2 and 69 min, open arrowheads). Cohesion behavior was also chromosome intrinsic. Meiosis I chromosomes on meiosis II spindles lost cohesion only between chromatid arms (Fig. 2, 69 min, straight arrows), while the nearby meiosis II chromosomes lost cohesion between centromeres (Fig. 2, 69 min, open arrowheads).

Bottom Line: Also, we determined when chromosomes can switch from meiosis I behavior to meiosis II behavior.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Duke University, Durham, North Carolina 27708, USA. lvp@acpub.duke.edu

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.

Show MeSH
Related in: MedlinePlus