Meiosis-I in Mesostoma ehrenbergii spermatocytes includes distance segregation and inter-polar movements of univalents, and vigorous oscillations of bivalents

Abstract

In this article, we describe meiosis-I in spermatocytes of the free-living freshwater flatworm Mesostoma ehrenbergii. The original observations of Oakley (1983, 1985) and Fuge (Eur J Cell Biol 44:294-298, 1987, Cell Motil Cytoskeleton 13:212-220, 1989, Protoplasma 160:39-48, 1991), the first to describe these cells, challenge our understanding of cell division, and we have expanded on these descriptions with the aim of laying the framework for further experimental work. These cells contain three bivalents and four univalent chromosomes (two pairs). Bivalent kinetochores oscillate vigorously and regularly throughout prometaphase, for up to several hours, until anaphase. Anaphase onset usually begins in the middle of the kinetochore oscillation cycle. Precocious cleavage furrows form at the start of prometaphase, ingress and then remain arrested until the end of anaphase. The four univalents do not pair, yet by anaphase there is one of each kind at each pole, an example of "distance segregation" (Hughes-Schrader in Chromosoma 27:109-129, 1969). Until proper segregation is achieved, univalents move between spindle poles up to seven times in an individual cell; they move with velocities averaging 9 μm/min, which is faster than the oscillatory motions of the bivalent kinetochores (5-6 μm/min), and much faster than the anaphase movements of the segregating half-bivalents (1 μm/min). Bipolar bivalents periodically reorient, most often resulting in the partner kinetochores exchanging poles. We suggest that the large numbers of inter-polar movements of univalents, and the reorientations of bivalents that lead to partners exchanging poles, might be because there is non-random segregation of chromosomes, as in some other cell types.

Chromosome interaction over a distance in meiosis

“…with each bivalent having a bipolar attachment and each pole associated with one of each type of univalent) suggests that Mesostoma might have non-random segregation of chromosomes. There may be both coordinated positioning of partner chromosomes, and coordinated positioning of non-partner chromosomes [ 11 , 34 ]. Additionally, univalents and half-bivalents prior to anaphase I will move away from and then back to the same pole, apparently detaching from the pole with which they were associated and then reattaching to that same pole [ 11 , 30 ].…”

“…Additionally, univalents and half-bivalents prior to anaphase I will move away from and then back to the same pole, apparently detaching from the pole with which they were associated and then reattaching to that same pole [ 11 , 30 ]. Anaphase movements ( figure 6 c ) start in the middle of oscillations, with no apparent stable metaphase prior to anaphase I [ 30 , 34 ]. The trigger that leads to onset of anaphase I is unknown, but it seems to be associated with a euploid distribution of chromosomes.…”

Evidence of Non-microtubule Spindle Forces in Mesostoma ehrenbergii Spermatocytes

“…The univalent chromosomes are never paired: there are only 3 synaptonemal complexes in pre-division nuclei, corresponding to each of the 3 bivalents ( Oakley and Jones, 1982 ). Throughout prometaphase the three bivalent chromosomes oscillate toward and away from the two poles with excursion distances averaging 4 μm and at speeds averaging 5–6 μm/min (e.g., Ferraro-Gideon et al, 2014 ). The chromosomes never form a metaphase plate: oscillations continue until anaphase.…”

“…The chromosomes never form a metaphase plate: oscillations continue until anaphase. At anaphase the bivalent oscillations end abruptly and the segregating chromosomes move toward the two poles at speeds of approximately 1 μm/min ( Fuge, 1987 , 1989 ; Ferraro-Gideon et al, 2013 , 2014 ). For clarity, we must describe several other unusual behaviors in these cells.…”

“…In early prometaphase there often are “faulty” distributions of univalents at the two poles but by anaphase there is one of each kind at each pole ( Oakley, 1983, 1985 ). Univalents move between poles in living cells ( Oakley, 1985 ; Forer and Pickett-Heaps, 2010 ; Ferraro-Gideon et al, 2014 ). Proper distribution of univalents seems to arise from their movements between the poles because early in prometaphase the univalents often are distributed wrongly ( Oakley, 1983, 1985 ), such as 3 or 4 at one pole and one or none at the other, or two of one kind at one pole and two of the other kind at the other pole.…”