Each species of multicellular organisms has a set number of chromosomes that carry all genes required for development and living processes. However, some species in both the plant and animal kingdoms have extra chromosomes, called B chromosomes, which are dispensable. They only exist in some individuals of a species and often are variable in number. Variation in number of the normal chromosomes is highly detrimental, but B chromosomes seldom have any detrimental effects unless many copies are present. Thus, they are considered to be mostly inert, being neither required nor detrimental. They exist in populations because they have properties that foster their accumulation; normal chromosomes do not possess these properties. In some plant species, particularly corn, they have been used to make translocations with the normal chromosomes, which have proven to be useful for mutation mapping, chromosomal dosage studies, and recently production of engineered minichromosomes.
Origin and nature of accumulation
The origin of B chromosomes remains a mystery, although it is assumed that they are derived from a normal A chromosome at some point. Because B chromosomes have few if any active genes, inactivation processes must occur to generate these chromosomes. Distinct properties must evolve for the B chromosome to accumulate and be maintained. Thus, it is likely that the mechanisms that initially produce B chromosomes are more common than the observed occurrence of these chromosomes. Nearly 2000 species of plants have been observed to harbor B chromosomes. B chromosomes are almost exclusively reported in diploid rather than polyploid species and in those with an outcrossing mating system as opposed to species with inbreeding.
The nature of accumulation mechanisms of various B chromosomes varies, but this usually involves the process of nondisjunction in which one daughter cell receives two copies of the chromosome and the other daughter cell receives none from a dividing mother cell with one B chromosome. This nondisjunction occurs at a time in the life cycle that will place more copies of the B chromosome into the next generation than were present in the previous generation. Thus, nondisjunction occurs in the developmental lineage leading to formation of gametes.
The B chromosome of corn is the most thoroughly studied (Fig. 1). There are 10 pairs of normal chromosomes in corn. The B chromosome is about two-thirds the length of the smallest normal chromosome and is highly heterochromatic; that is, it stains heavily with chromatin dyes, which is an indication of inactivity. The centromere of the corn B chromosome is near one end, which is different from all of the normal chromosomes. The basis of its accumulation mechanisms is that it nondisjoins at a high frequency during the second pollen mitosis that produces the two corn sperm (Fig. 2). The sperm that contains the two B chromosomes then preferentially fertilizes the egg cell rather than the polar nuclei during the process of double fertilization. Because the fertilized egg cell develops into the new generation and the fertilized polar nuclei develop into the dead-end storage tissue called the endosperm, this combination of traits increases the number of B chromosomes. The corn B chromosome divides normally in most other cell divisions in the life cycle. In most genetic backgrounds, 10–15 copies of the B chromosome are tolerated without any effect on the plant. The highest documented number of B chromosomes in corn was 34, which was associated with stunted growth and sterility.
The nature of the nondisjunction property has been studied in corn. The centromeric region is the site of nondisjunction, but other parts of the B chromosome must be present. One of these regions resides at the tip of the other end of the chromosome. When this site is removed, the centromere will behave in a normal manner without nondisjunction at the second pollen mitosis. If this part of the B chromosome is returned to the genotype via genetic crosses, the centromere will again exhibit nondisjunction. In other words, the terminal site is required to be in the same nucleus during the second pollen mitosis, but it need not be present on the same chromosome as the B centromeres that it affects.
The corn B chromosome centromere contains all normal DNA repeats that are typical of a centromere in corn. However, it also has a B-specific repeat that is interspersed throughout the centromeric region and a few other minor sites on the chromosome. There are at least two other repetitive DNA sequences that are found exclusively on the B chromosome. Other sequences on the B chromosome are shared with the normal chromosomes. The normal chromosomes contain many copies of mobile elements. Different families of these mobile elements have had previous periods of major transpositions dating back about 4–5 million years. All of these elements are also represented on the B chromosome, indicating that the B chromosome has been present in the evolutionary history of corn during these periods of transposition.
The B chromosome of corn has been capitalized upon by corn geneticists to develop many research tools. By irradiating corn materials with B chromosomes, translocations have been induced that place a part of a normal chromosome onto the B centromere. This confers the property of nondisjunction to the translocated chromosomal region. Thus, sperm are produced that are missing the chromosomal segment or that have it in duplicate. Upon fertilization, a dosage series for that portion of the chromosome is generated; thus, among the progeny, there are individuals with only one copy, some with two copies (in those rare cases in which the B centromere disjoined), and some with three copies of the translocated segment. Recessive mutations in the maternal parent of such crosses are exposed in the progeny that do not inherit the translocated segment. In this way, recessive mutations can be located to the chromosome arm by crossing these materials by a collection of B-A translocations covering the whole genome.
The B chromosome of rye has also been studied extensively. In this case, the unusual behavior occurs at the first pollen mitosis with a high frequency of directed nondisjunction of the B chromosomes to the generative nucleus, which divides again to produce the two sperm. This behavior generates sperm with a greater number of B chromosomes than the parent plant. There is also directed nondisjunction in the female gametophyte such that the egg cell receives a greater number of B chromosomes. Nondisjunction appears to be mediated by sequences surrounding the centromere, but also requires presence of a heterochromatic region at the tip of the rye B chromosome long arm. This region can act on the centromeric regions of other rye B chromosomes and need not be present on the same chromosome to function in this capacity.
B chromosomes in different species often affect the rate of recombination in the normal chromosomes during meiosis. This effect in different species can be positive or negative, but it usually increases in magnitude in relation to copy number of B chromosomes in the cell.
A recent application of B chromosomes is to convert them into artificial chromosome platforms. By introducing the cloned natural ends of chromosomes called telomeres, truncations are produced that remove the terminal end of the chromosome that conditions nondisjunction. At the same time, the truncating sequences are accompanied by recombination sites that will permit further additions to the chromosome. These constructs would permit further additions to the chromosome in a sequential manner so that many new genes could be added to a plant as a newly designed chromosome.