Non-random segregation of chromosomes
Non-random segregation of chromosomes is a deviation from the usual distribution of
This article describes cases where non-random segregation is the normal case for the particular organisms or occurs very frequently. A related phenomenon is called
In addition, there are pathological cases that result in aneuploidy and are almost always lethal.
Background and early history of research
According to the
Also in 1909, a paper was published on the spermatogenesis of
It was only after all these counter-examples that a study by Eleanor Carothers on
The third basic variant of non-random segregation, in which the complete sets of chromosomes of maternal and paternal origin are separated from each other, was studied - among some other peculiarities - in the 1920s and 30s by Charles W. Metz and co-workers in
Single chromosomes or chromosome pairs
We first consider cases where only a single chromosome pair or a single unpaired chromosome (univalent) is affected, in the order of first description in the respective taxon.
Aphids
As mentioned, the first example of non-random segregation described as early as 1908 was the behaviour of the X chromosome during spermatogenesis in aphids. These insects exist for most of the year only as females and reproduce parthenogenetically, i.e. without the participation of males. There is no fertilisation or meiosis, and successive generations are genetically identical. Under certain conditions, mostly due to the decreasing day length towards the end of the vegetation period of the host plants, one generation occurs in which males are also present. This is achieved by the two X chromosomes present in females mating as in meiosis and their number being reduced to 1, resulting in males (X0).[1]
The fact that, after this one bisexual generation, only females are produced again is based, as shown above, on the fact that, during spermatogenesis, the X chromosome is always assigned to the daughter cell from which sperm are produced. Hans Ris described the exact sequence of meiosis in 1942:[8] According to this, the X chromosome does not participate in the movement towards the poles of the spindle apparatus during anaphase, but is stretched between the diverging poles. Also during the subsequent cell division, the chromosome remains in this position. Only at a late stage of furrowing does the furrowing groove shift to one side, and the X chromosome is allocated to the opposite, larger daughter cell. Since only this produces two sperm, all sperm as well as the eggs contain an X chromosome. After fertilisation, eggs are laid, which survive until the beginning of the next growing season and then only produce females (XX), which again reproduce parthenogenetically.
Butterflies
In
Fungus gnats
The
Flowering plants
The first case of non-random segregation of single chromosomes in a plant was described by
A corresponding accumulation of additional chromosome segments has also been described in some other plant species, but has not been studied in detail. Much more numerous are studies on additional chromosomes, the
Since Catcheside only studied male meiosis, which usually gives rise to four fertile daughter cells, it cannot be concluded that non-random segregation contributes to the accumulation in inheritance that is characteristic of B chromosomes in general. The situation is different in female meiosis, where three of the four daughter nuclei degenerate. In 1957, Hiroshi Kayano described the behaviour of a B chromosome in female meiosis in the Japanese
This work by Kayano seems to be the only one so far to demonstrate the accumulation of a B chromosome as a result of non-random segregation during meiosis in the embryo sac mother cell.
Flies
Similar to maize, non-random segregation also occurs in the fruit fly
In Drosophila melanogaster, non-random segregation can also occur during male meiosis. This is the case when the sex chromosomes (X and Y) do not pair during meiosis I. In this case, the unpaired chromosomes usually end up in the same daughter cell. Then the unpaired chromosomes usually end up in the same daughter cell. Accordingly, there are many X0-type males among the offspring, but surprisingly few XXY-type males. The latter is due to the fact that the daughter cells with the XY constitution are disturbed in their development. On the other hand, the X0 males are infertile. The bottom line is that the X chromosome involved is enriched in the inheritance (meiotic drive).[26][27][28]
Mealybugs
B chromosomes are also common in the animal kingdom. In the Mealybug, Uzi Nur described non-random segregation in both sexes in 1962. In oogenesis, the segregation behaviour of the B chromosome depends on the number of Bs present. If two Bs are present, then they mate during reduction division (which is meiosis II here, as it is generally in mealybugs, scale insects and aphids) and segregate in the normal way. However, if only one is present, then in two-thirds of the cases it enters the polar body and only in the remaining third does it enter the ovary. And the unpaired supernumerary B chromosome behaves in the same way if 3 or 5 Bs are present, while the paired ones segregate normally. Overall, therefore, there is a tendency in the female sex to exclude B chromosomes from the inheritance by non-random segregation, which comes into play especially when only one is present. However, this is contrasted in the male sex by a strong tendency to accumulate B chromosomes. This is due to the fact that in this species (as in many other mealybugs and scale insects) half of the meiosis products regularly degenerate. During reduction division (also meiosis II here), all B chromosomes are allocated to the future sperm nucleus with about 90 % probability.[29]
Grasshoppers
Transmission of B chromosomes has also been studied in various
Another chromosomal anomaly that is common in locusts is extra segments on individual chromosomes. Such additional segments can segregate quite randomly, and in fact it was locusts with homologous chromosomes of unequal length in which Carothers first found evidence of random segregation in 1917. In contrast, López-León et al. (1991, 1992) found circumstantial evidence for nonrandom segregation in two locust species: in Eyprepocnemis plorans, an extra segment in the female sex is less likely to be transmitted than the normal homologous chromosome if a B chromosome is also present. Thus, the B chromosome influences the transmission of a regular chromosome pair, while even in this case it follows Mendelian rules. The reduced transmission of the additional segment is most likely due to non-random segregation during oogenesis, because the alternative possibility of differential mortality of zygotes could be excluded.[33] In Chorthippus jacobsi, López-León et al. studied the transmission of different additional segments at three different chromosomes. While all additional segments on chromosomes M5 and M6 are transmitted normally, accumulation consistently occurs in both sexes when an additional segment is located on the small chromosome S8. Even if both S8 chromosomes carry different sized additional segments, they do not follow Mendelian rules, but the shorter segment is preferentially transmitted. Again, non-random segregation during oogenesis can be inferred with high probability. In contrast, how non-Mendelian transmission occurs through the male sex is unclear.[34]
Rodents
The first description of non-random segregation in a mammal appeared in 1977 and dealt with the Wood lemming. In some populations of this species, up to 80% of the animals are female. At the same time, some of the females have the "male" chromosome constitution XY. The fact that these animals develop into females, although they have a Y chromosome, is due to a mutation on the X chromosome. During meiosis, this mutated chromosome (X*) enters the egg nucleus more frequently than the Y chromosome and is therefore more likely to be transmitted to the offspring.[11] A second example concerns a B chromosome in the Siberian collared lemming Dicrostonyx torquatus. In female meiosis I of this species, unpaired B chromosomes are preferentially assigned to the future egg nucleus and thus accumulate in the inheritance.[35]
In Siberian populations of the house mouse, a variant form of chromosome 1 with two insertions occurs. This elongated variant is passed on by heterozygous females with much higher probability than the normal chromosome 1. As it turned out, this occurs by non-random segregation of the homologous chromosomes or chromatids in both meiotic divisions. As a result, up to 85% of the offspring of a heterozygous female can receive the insertions.[36] However, the latter is only the case if the males used in the crossing experiments are not also carriers of these insertions. If instead homozygous carriers of these insertions were used, i.e. each sperm received the insertions, then the non-randomness in female meiosis was reversed: In this case, only about 1/3 of the offspring of a heterozygous mother received the insertions from this mother.[37] This surprising influence of sperm on meiosis in the oocyte is possible because in mice, as in vertebrates in general, female meiosis pauses in metaphase II until fertilization occurs.
It has been known since 1962 that female mice with only one X chromosome (XO) are fertile, but their daughters have predominantly two X chromosomes. How this happens was unclear for a long time, but according to recent studies it is apparently due to the fact that the univalent X chromosome is preferentially allocated to the future egg nucleus during meiosis I.[38]
Coordinated segregation of non-homologous chromosomes
Mechanically coupled univalents
That two non-homologous chromosomes segregate in a coordinated manner during meiosis was first described in 1909 in
Free univalents
In some aphid species, males have two different X chromosomes (X1X20), which are not mechanically linked and yet reach the same spindle pole during meiosis I.
More interesting are those cases in which free univalents of different species segregate in a regulated manner to opposite spindle poles. This is part of the normal course of meiosis in the spermatogenesis of various
Also in the northern mole cricket Neocurtilla hexadactyla already mentioned at the beginning, live observations of meiosis were very informative. There, as in Eneoptera, three sex chromosomes (X1X2Y) are present, but only X1 is present as a univalent. In this case, segregation of sex chromosomes also occurs before that of autosomes, in that the X2Y bivalent is already shifted in metaphase I from the metaphase plate toward one spindle pole in such a way that the Y chromosome is located near it, while the univalent X1 is located at the other pole. Through micromanipulation experiments in which they shifted the bivalent or the univalent in the spindle, René Camenzind and R. Bruce Nicklas (1968) found that X1 is the active element and depends on the orientation of the bivalent. Furthermore, the authors found that there is no mechanical connection between the two.[54] However, an electron microscopic examination revealed some microtubules, which also make up the spindle fibers, and which here appear to form a fine connection between X1 and Y.[4] Targeted irradiation of this microtubule junction with UV microbeams often (in about one-third of cases) resulted in X1 moving to the other half of the spindle. The same effect was surprisingly seen with irradiation of one of the three spindle fibers where the sex chromosomes were located, whereas irradiation of autosomal spindle fibers had no effect. Dwayne Wise et al. concluded that these four microtubule bundles form an "interacting network" that enables the coordinated segregation of sex chromosomes, i.e., the correct allocation of the X1.[55]
Complete sets of chromosomes
Fungus gnats
The behavior of chromosomes in fungus gnat spermatogenesis is very unusual in several respects. A detail of meiosis II was already discussed above; however, meiosis I is far more remarkable. There the otherwise obligatory pairing of homologous chromosomes is completely omitted, and these are segregated from each other according to their origin - maternal or paternal. Their segregation starts right after the nuclear envelope dissolution, the metaphase is omitted, and the paternal chromosomes enter a small daughter cell which, like the polar bodies, passes away during oogenesis. Thus, all spermatozoa receive only the maternal chromosomes, and males act only as intermediaries between purely female lineages. The construction of the spindle apparatus in this division is also unusual. It is not a bipolar spindle, but merely a half-spindle with only one pole. The maternal chromosomes move towards this pole, the paternal ones away from it.[6]
Some fungus gnats have, in addition to regular chromosomes, germline-limited or L-chromosomes (from limited), which are present only in cells of the germline and are eliminated from somatic cells. These segregate with the maternal regular chromosomes during spermatogenesis, thus enter the sperm unreduced.[56] This doubling of their number is compensated for at an early stage of embryonic development by eliminating excess L chromosomes from the nucleus, so that exactly two always remain.[57]
Cecidomyiidae
In Cecidomyiidae, spermatozoa also contain only the set of chromosomes of maternal origin, while paternal chromosomes are eliminated during meiosis I. Again, pairing of homologous chromosomes is omitted, cell division is inaequal, and only the maternal chromosomes move to a spindle pole, thereby entering the daughter cell from which two spermatozoa emerge after meiosis II, while the other daughter cell perishes. In addition, there are numerous germline-limited chromosomes, which, like those of fungus gnats, remain with the paternal regular chromosomes and are thus eliminated.[58][59]
Scale insects
In most
Plants
In the plant kingdom,
The
The South American sweetgrass Andropogon ternatus is also triploid, and during meiosis one set of chromosomes remains unpaired. In anaphase I, the univalents in both sexes remain between the segregating half-bivalents and form their own third nucleus, which is included in one of the two daughter cells. In female meiosis, this is the daughter cell facing the micropyle. Thus, in agreement with the two plant species discussed previously, the univalents are allocated directionally to the micropylar side. However, since here the embryo sac is formed at the other end of the tetrad facing the chalaza, this results in the elimination of the univalents from the inheritance. The compensation for this is done by the pollen, in that apparently only those pollen grains which arise from the dinucleate meiocytes and are therefore diploid, develop normally and become fertile.[62]
Significance
Fernando Pardo-Manuel de Villena and Carmen Sapienza discussed the significance of these non-randomnesses in a 2001 review limited to non-random segregation of single chromosomes or chromosome pairs. From the widespread occurrence of such phenomena (in plants, insects, and vertebrates) and the diversity of the respective sequence, they conclude that a functional asymmetry of spindle poles - one of the prerequisites of non-random segregation - is probably present in principle and not only exceptionally. This is also true for humans, where non-random segregation occurs when structurally abnormal chromosomes are present as a result of
Despite publications about non-random segregation in major journals and symposia the potential implications of a multitude of findings were ignored for several decades.[64]
Stem cells and non-random chromosome segregation
Non-random segregation of chromosomes is also found in
Pre-existing vs newly generated
Literature
- Bernard John: Meiosis. Cambridge University Press, Cambridge u. a. 1990. Kapitel Preferential segregation, page 238–247 [61]
- Fernando Pardo-Manuel de Villena, Carmen Sapienza: Nonrandom segregation during meiosis: the unfairness of females. In: Mammalian Genome 12, page 331–339 (2001).
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