Aneuploidy is the second major category of chromosome mutations in which chromosome number is abnormal. An aneuploid is an individual organism whose chromosome number differs from the wild type by part of a chromosome set. Generally, the aneuploid chromosome set differs from wild type by only one or a small number of chromosomes. Aneuploids can have a chromosome number either greater or smaller than that of the wild type. Aneuploid nomenclature is based on the number of copies of the specific chromosome in the aneuploid state. For example, the aneuploid condition 2n − 1 is called monosomic (meaning “one chromosome”) because only one copy of some specific chromosome is present instead of the usual two found in its diploid progenitor. The aneuploid 2n + 1 is called trisomic,2n − 2 is nullisomic, and n + 1 is disomic.
Nullisomics (2n − 2)
Although nullisomy is a lethal condition in diploids, an organism such as bread wheat, which behaves meiotically like a diploid although it is a hexaploid, can tolerate nullisomy. The four homoeologous chromosomes apparently compensate for a missing pair of homologs. In fact, all the possible 21 bread wheat nullisomics have been produced; they are illustrated in Figure 18-15. Their appearances differ from the normal hexaploids; furthermore, most of the nullisomics grow less vigorously.
Ears of the nullisomics of wheat. The number and letter under each ear designates the absent chromosome. Although nullisomics are usually lethal in regular diploids, organisms such as wheat, which “pretends” to be diploid but is hexaploid, (more...)
Monosomics (2n − 1)
Monosomic chromosome complements are generally deleterious for two main reasons. First, the missing chromosome perturbs the overall gene balance in the chromosome set. (We encountered this effect earlier). Second, having a chromosome missing allows any deleterious recessive allele on the single chromosome to be hemizygous and thus to be directly expressed phenotypically. Notice that these are the same effects produced by deletions.
Nondisjunction in mitosis or meiosis is the cause of most aneuploids. Disjunction is the normal separation of homologous chromosomes or chromatids to opposite poles at nuclear division. Nondisjunction is a failure of this disjoining process, and two chromosomes (or chromatids) go to one pole and none to the other. Nondisjunction occurs spontaneously; it is another example of a chance failure of a basic cellular process.
In meiotic nondisjunction, the chromosomes may fail to disjoin at either the first or second division (Figure 18-16). Either way, n + 1 and n − 1 gametes are produced. If an n − 1 gamete is fertilized by an n gamete, a monosomic(2 n − 1) zygote is produced. The fusion of an n + 1 and an n gamete yields a trisomic 2n + 1
The origin of aneuploid gametes by nondisjunction at the first or second meiotic division.
The precise molecular processes that fail in nondisjunction are not known, but, in experimental systems, the frequency of nondisjunction can be increased by interference with microtubule action. It appears that disjunction is more likely to go awry in meiosis I. This likelihood may not be surprising, because normal anaphase I disjunction requires that proper homologous associations be maintained during prophase I and metaphase I. In contrast, proper disjunction at anaphase II or at mitosis requires that the centromere splits properly but does not require nearly as elaborate a process during prophase and metaphase.
Meiosis I nondisjunction can be viewed as the failure to form or maintain a tetrad (a group of four chromatids) until anaphase I. Crossovers are implicit in this process normally. In most organisms, the amount of crossing-over is sufficient to ensure that all tetrads will have at least one exchange per meiosis. In Drosophila, many of the nondisjunctional chromosomes in newly arising disomic gametes are nonrecombinant, with one nondisjunctional homolog carrying the markers of one input chromosome and the other homolog carry- ing the markers of the other chromosome. Similar observations have been made in human trisomies. In addition, in several different experimental organisms, mutations that interfere with recombination have the effect of massively increasing the frequency of meiosis I nondisjunction. This effect points to an important role of crossing-over in maintaining chromosomal associations in the tetrad; in the absence of these associations, chromosomes are vulnerable to anaphase I nondisjunction.
In humans, a sex-chromosomemonosomic complement of 44 autosomes + 1 X produces a phenotype known as Turner syndrome. Affected people have a characteristic, easily recognizable phenotype: they are sterile females, are short in stature, and often have a web of skin extending between the neck and shoulders (Figure 18-17). Although their intelligence is near normal, some of their specific cognitive functions are defective. About 1 in 5000 female births have this monosomic chromosomal complement. Monosomics for all human autosomes die in utero.
Characteristics of Turner syndrome, which results from having a single X chromosome (XO). (After F. Vogel and A. G. Motulsky, Human Genetics. Springer-Verlag, 1982.)
Geneticists have used viable plant nullisomics and monosomics to identify the chromosomes that carry the loci of newly found recessive mutant alleles. For example, a geneticist may obtain different monosomic lines, each of which lacks a different chromosome. Homozygotes for the new mutant allele are crossed with each monosomic line, and the progeny of each cross are inspected for expression of the recessive phenotype. The phenotype appears in some of the progeny of the parent that is monosomic for the locus-bearing chromosome and thus identifies it. Figure 18-18 shows that this test works because meiosis in the monosomic parent produces some gametes that lack the chromosome bearing the locus. When one of these gametes forms a zygote, the single chromosome contributed by the other homozygous recessive parent determines the phenotype.
Meiosis in which the chromosome of interest is monosomic. Two of the resulting gametes are haploid (n); the other two gametes contain a set lacking a chromosome (n − 1).
Genetic analysis of humans occasionally reveals a similar unmasking of a recessive phenotype by an n − 1gamete. For example, two people whose vision is normal may produce a daughter who has Turner syndrome and who is also red-green colorblind. This coincidence is interpreted as follows. First, because the father is not colorblind, the mother must be heterozygous for the recessive allele and must have passed this allele on to the Turner daughter. Nondisjunction must have occurred in the father, resulting in an n − 1 sperm, which combined with an egg bearing the colorblind allele from the mother.
Monosomics show the deleterious effects of genome inbalance, as well as unexpected expression of recessive alleles carried on the monosomicchromosome.
Trisomics (2n + 1)
The trisomic condition also is one of chromosomal imbalance and can result in abnormality or death. However, there are many examples of viable trisomics. You might remember that we studied the trisomics of the Jimson weed Datura stramonium in Chapter 3 (see Figure 3-7). Furthermore, trisomics can be fertile. When cells from some trisomic organisms are observed under the microscope at the time of meiotic chromosome pairing, the trisomic chromosomes are seen to form a trivalent, an associated group of three, whereas the other chromosomes form regular bivalents. What genetic ratios might we expect for genes on the trisomic chromosome? Let us consider a gene, A, that is close to the centromere on that chromosome, and let us assume that the genotype is A/a/a. Furthermore, if we postulate that two of the centromeres disjoin to opposite poles as in a normal bivalent and that the other chromosome passes randomly to either pole, then we can predict the three equally frequent segregations shown in Figure 18-19. These segregations result in an overall gametic ratio of 1A:2A/a:2a:1a/a. This ratio and the one corresponding to a trisomic of genotype A/A/a are observed in practice. If a trisomic tester set is available (much like the nullisomic tester set described earlier), then a new mutation can be located to a chromosome by determining which of the testers gives the special ratio.
Genotypes of the meiotic products of an A/a/a trisomic. Three segregations are equally likely.
There are several examples of viable trisomics in humans. The combination XXY (1 in 1000 male births) results in Klinefelter syndrome, males with lanky builds who are mentally retarded and sterile (Figure 18-20). Another combination, XYY, also occurs in about 1 in 1000 male births. Attempts have been made to link the XYY condition with a predisposition toward violence. This linkage is still hotly debated, although it is now clear that an XYY condition in no way guarantees such behavior. Nevertheless, several enterprising lawyers have attempted to use the XYY genotype as grounds for acquittal or compassion in crimes of violence. The XYY males are usually fertile. Their meioses are of the XY type; the extra Y is not transmitted, and their gametes contain either X or Y, never YY or XY.
Characteristics of Klinefelter syndrome (XXY). (After F. Vogel and A. G. Motulsky, Human Genetics. Springer-Verlag, 1982.)
The most common type of viable human aneuploid is Down syndrome (Figure 18-21), occurring at a frequency of about 0.15 percent of all live births. We have already encountered the translocation form of Down syndrome in Chapter 17. However, by far the most common type of Down syndrome is trisomy 21, caused by nondisjunction of chromosome 21 in a parent who is chromosomally normal. Like any mechanism, chromosome disjunction is error prone and sometimes produces aneuploid gametes. In this type of Down syndrome, there is no family history of aneuploidy, unlike the translocation type described earlier.
Characteristics of Down syndrome (trisomy 21). (a) Diagrammatic representation of the syndrome in an infant. (b) Athletes with Down syndrome. (Part a after F. Vogel and A. G. Motulsky, Human Genetics. Springer-Verlag, 1982; part b from Bob Daemmrich/The (more...)
Down syndrome is related to maternal age; older mothers run a greatly elevated risk of having Down-syndrome children (Figure 18-22). For this reason, fetal chromosome analysis (by amniocentesis or by chorionic villus sampling) is now recommended for older mothers. A less pronounced paternal-age effect also has been demonstrated.
Maternal age and the production of Down-syndrome offspring. (From L. S. Penrose and G. F. Smith, Down’s Anomaly. Little, Brown and Company, 1966.)
Even though the maternal-age effect has been known for many years, its cause is still not known. Nonetheless, there are some interesting biological correlations. It is possible that one aspect of the strong maternal-age effect on nondisjunction is an age-dependent decrease in the probability of keeping the chromosomal tetrad together during prophase I of meiosis. Meiotic arrest of oocytes (female meiocytes) in late prophase I is a common phenomenon in many animals. In female humans, all oocytes are arrested at diplotene before birth. Meiosis continues only at menstruation, which means that proper chromosome associations in the tetrad must be maintained for decades. If we speculate that, by accident through time, these associations have an increasing probability of breaking down, we can envision a mechanism contributing to increased maternal nondisjunction with age. Consistent with this speculation, most nondisjunction related to the maternal-age effect is due to nondisjunction at anaphase I, not anaphase II.
The multiple phenotypes that make up Down syndrome include mental retardation, with an IQ in the 20 to 50 range; broad, flat face; eyes with an epicanthic fold; short stature; short hands with a crease across the middle; and a large, wrinkled tongue. Females may be fertile and may produce normal or trisomic progeny, but males have never reproduced. Mean life expectancy is about 17 years, and only 8 percent survive past age 40.
The only other human autosomal trisomics to survive to birth are afflicted with either trisomy 13 (Patau syndrome) or trisomy 18 (Edwards syndrome). Both show severe physical and mental abnormalities. The generalized phenotype of trisomy 13 includes a harelip; a small, malformed head; “rockerbottom” feet; and a mean life expectancy of 130 days. That of trisomy 18 includes “faunlike” ears, a small jaw, a narrow pelvis, and rockerbottom feet; almost all babies with trisomy 18 die within the first few weeks after birth.
Chromosome mutation in general plays a prominent role in determining genetic ill health in humans. Figure 18-23 summarizes the surprisingly high levels of various chromosome abnormalities at different human developmental stages. In fact, the incidence of chromosome mutations ranks close to that of gene mutations in human live births (Table 18-1). This fact is particularly surprising when we realize that virtually all the chromosome mutations listed in Table 18-1 arise anew with each generation. In contrast, gene mutations (as we shall see in Chapter 24) owe their level of incidence to a complex interplay of mutation rates and environmental selection that spans many human generations.
The fate of a million implanted human zygotes. (Robertsonian translocations are due to fusion or dissociation of centromeres.) (From K. Sankaranarayanan, Mutation Research 61, 1979.)
Relative Incidence of Human Ill Health Due to Gene Mutation and to Chromosome Mutation.
When the frequencies of various chromosome mutations in live births are compared with the corresponding frequencies found in spontaneous abortions (Table 18-2), it becomes clear that the chromosome mutations that we know about as clinical abnormalities are just the tip of an iceberg of chromosome mutations. First, we see that many more types of abnormalities are produced than survive to birth; for example, trisomies of chromosome 2, 16, and 22 are relatively common in abortuses but never survive to birth. Second, the specific aberrations that survive are part of a much larger number that do not survive; for example, Down syndrome (trisomy 21) is produced at almost 20 times the frequency in live births. The comparison is even more striking for Turner syndrome (XO). An estimated minimum of 10 percent of conceptions have a major chromosome abnormality; our reproductive success depends on the natural weeding-out process that eliminates most of these abnormalities before birth. Incidentally, no evidence suggests that these aberrations are produced by environmental insult to our reproductive systems or that the frequency of the aberrations is increasing.
Number and Type of Chromosomal Abnormalities Among Spontaneous Abortions and Live Births in 100,000 Pregnancies.
Trisomics show the deleterious effects of genome inbalance and produce chromosome-specific modified phenotypic ratios.
Disomics (n + 1)
A disomic is an aberration of a haploid organism. In fungi, they can result from meiotic nondisjunction. In the fungus Neurospora (a haploid), an n − 1 meiotic product aborts and does not darken like a normal ascospore; so we may detect MI and MII nondisjunctions by observing asci with 4:4 and 6:2 ratios of normal to aborted spores, respectively, as shown here.
These diagrams correspond exactly to the outcomes of the chromosomal events shown in Figure 18-16. In these organisms, the disomic (n + 1) meiotic product becomes a disomic strain directly. The abortion patterns themselves are diagnostic for the presence of disomics in the asci. Another way of detecting disomics in fungi is to cross two strains with homologous chromosomes bearing multiple auxotrophic mutations; for example:
From such a cross, large populations of ascospores are plated onto minimal medium. Only ascospores of genotype + + + + + + can grow and form colonies. Most of these colonies are found to be disomics and not multiple crossover types.
Disomics in fungi can be selected from asci showing special spore abortion patterns or as meiotic progeny that must contain homologous chromosomes from both parents.
Aneuploid cells can arise spontaneously in somatic tissue or in cell culture. In such cases, the initial result is a genetic mosaic of cell types.
Human sexual mosaics—individuals whose bodies are a mixture of male and female tissue—are good examples. One type of sexual mosaic, (XO)(XYY), can be explained by postulating an XY zygote in which the Y chromatids fail to disjoin at an early mitotic division, so both go to one pole:
The phenotypic sex of such individuals depends on where the male and female sectors end up in the body. In the type of nondisjunction being considered, nondisjunction at a later mitotic division would produce a three-way mosaic (XY)(XO)(XYY), which contains a clone of normal male cells. Other sexual mosaics have different explanations; as examples, XO/XY is probably due to early X-chromosome loss in a male zygote (Figure 18-24), and (XX)(XY) is probably the result of a double fertilization (fused twins). In general, sexual mosaics are called gynandromorphs.
Origin of a human sexual mosaic (XY)(XO) by Y chromosome loss at the first mitotic division of the zygote. (a) Fertilization. (b) Chromosome loss. (c) Resulting male and female cells. (d) Mosaic blastocyst. (After C. Stern, Principles of Human Genetics,(more...)
Geneticists working with many species of experimental animals occasionally find gynandromorphs among their stocks. A classic example is the Drosophilagynandromorph shown in Figure 18-25. In this case, the zygote started out as a female heterozygous for two X-linked genes, white eye and miniature wing (w+ m+/w m). Loss of the wild-type allele–bearing X chromosome at the first mitotic division resulted in the two cell lines and ultimately in a fly differing from one side to the other in sex, eye color, and size of wing. A similar gynandromorph in the Io moth is shown in Figure 18-26.
A bilateral gynandromorph of Drosophila. The zygote was w+ m+/w m, but loss of the w+ m+ chromosome in the first mitotic division produced a fly that was 1/2 O/w m and male (left) and 1/2w+ m+/w m and female (more...)
A bilateral gynandromorph in the Io moth, Automeris io io. One half of the body is female and happens to carry the sex chromosome mutation “broken eye”; the other half of the body is male and carries the normal allele of the broken-eye (more...)
Mitotic nondisjunction and other types of aberrant mitotic chromosome behavior can give rise to mosaics consisting of two or more chromosomally distinct cell types, including aneuploids.
Somatic aneuploidy and its resulting mosaics are often observed in association with cancer. People suffering from chronic myeloid leukemia (CML), a cancer of the white blood cells, frequently harbor cells containing the so-called Philadelphia chromosome. This chromosome was once thought to represent an aneuploid condition, but it is now known to be a translocation product in which part of the long arm of chromosome 22 attaches to the long arm of chromosome 9. However, CML patients often show aneuploidy in addition to the Philadelphia chromosome. In one study of 67 people with CML, 33 proved to have an extra Philadelphia chromosome and the remainder had various aneuploidies; the most common aneuploidy was trisomy for the long arm of chromosome 17, which was detected in 28 people. Of 58 people with acute myeloid leukemia, 21 were shown to have aneuploidy for chromosome 8; 16 for chromosome 9; and 10 for chromosome 21. In another study of 15 patients with intestinal tumors, 12 had cells with abnormal chromosomes, at least some with trisomy for chromosome 8, 13, 15, 17, or 21. Such studies merely established correlations, and it is not clear whether the abnormalities are best thought of as a cause or as an effect of cancer.
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