8.4 Polyploidy Is the Presence of More Than Two Sets of Chromosomes

As discussed in the introduction to this chapter, some organisms (such as bananas) possess more than two sets of chromosomes and are polyploid. Polyploids include triploids (3n), tetraploids (4n), pentaploids (5n), and even higher numbers of chromosome sets.

Polyploidy is common in plants and is a major mechanism by which new plant species have evolved. Approximately 40% of all flowering-plant species and 70% to 80% of grasses are polyploids. They include a number of agriculturally important plants, such as wheat, oats, cotton, potatoes, and sugar cane. Polyploidy is less common in animals but is found in some invertebrates, fishes, salamanders, frogs, and lizards. No naturally occurring, viable polyploids are known in birds, but at least one polyploid mammal—a rat in Argentina—has been reported.

We will consider two major types of polyploidy: autopolyploidy, in which all chromosome sets are from a single species and allopolyploidy, in which chromosome sets are from two or more species.

Autopolyploidy

Autopolyploidy is caused by accidents of mitosis or meiosis that produce extra sets of chromosomes, all derived from a single species. Nondisjunction of all chromosomes in mitosis in an early 2n embryo, for example, doubles the chromosome number and produces an autotetraploid (4n), as depicted in Figure 8.26a. An autotriploid (3n) may arise when nondisjunction in meiosis produces a diploid gamete that then fuses with a normal haploid gamete to produce a triploid zygote (Figure 8.26b). Alternatively, triploids may arise from a cross between an autotetraploid that produces 2n gametes and a diploid that produces 1n gametes. Nondisjunction can be artificially induced by colchicine, a chemical that disrupts spindle formation. Colchicine is often used to induce polyploidy in agriculturally and ornamentally important plants.

Figure 8.26: Autopolyploidy can arise through nondisjunction in mitosis or meiosis.

Because all the chromosome sets in autopolyploids are from the same species, they are homologous and attempt to align in prophase I of meiosis, which usually results in sterility. Consider meiosis in an autotriploid (Figure 8.27). In meiosis in a diploid cell, two chromosome homologs pair and align, but, in autotriploids, three homologs are present. One of the three homologs may fail to align with the other two, and this unaligned chromosome will segregate randomly (see Figure 8.27a). Which gamete gets the extra chromosome will be determined by chance and will differ for each homologous group of chromosomes. The resulting gametes will have two copies of some chromosomes and one copy of others. Even if all three chromosomes align, two chromosomes must segregate to one gamete and one chromosome to the other (see Figure 8.27b). Occasionally, the presence of a third chromosome interferes with normal alignment, and all three chromosomes move to the same gamete (see Figure 8.27c).

Figure 8.27: In meiosis of an autotriploid, homologous chromosomes can pair or not pair in three ways. This example illustrates the pairing and segregation of a single homologous set of chromosomes.

No matter how the three homologous chromosomes align, their random segregation will create unbalanced gametes, with various numbers of chromosomes. A gamete produced by meiosis in such an autotriploid might receive, say, two copies of chromosome 1, one copy of chromosome 2, three copies of chromosome 3, and no copies of chromosome 4. When the unbalanced gamete fuses with a normal gamete (or with another unbalanced gamete), the resulting zygote has different numbers of the four types of chromosomes. This difference in number creates unbalanced gene dosage in the zygote, which is often lethal. For this reason, triploids do not usually produce viable offspring.

In even-numbered autopolyploids, such as autotetraploids, the homologous chromosomes can theoretically form pairs and divide equally. However, this event rarely takes place, so these types of autotetraploids also produce unbalanced gametes.

The sterility that usually accompanies autopolyploidy has been exploited in agriculture. As discussed in the introduction to this chapter, triploid bananas (3n = 33) are sterile and seedless. Similarly, seedless triploid watermelons have been created and are now widely sold.

Allopolyploidy

Allopolyploidy arises from hybridization between two species; the resulting polyploid carries chromosome sets derived from two or more species. Figure 8.28 shows how allopolyploidy can arise from two species that are sufficiently related so that hybridization takes place between them. Species 1 (AABBCC, 2n = 6) produces haploid gametes with chromosomes ABC, and species 2 (GGHHII, 2n = 6) produces gametes with chromosomes GHI. If gametes from species 1 and 2 fuse, a hybrid with six chromosomes (ABCGHI) is created. The hybrid has the same chromosome number as that of both diploid species, so the hybrid is considered diploid. However, because the hybrid chromosomes are not homologous, they will not pair and segregate properly in meiosis; this hybrid is functionally haploid and sterile.

Figure 8.28: Most allopolyploids arise from hybridization between two species followed by chromosome doubling.

The sterile hybrid is unable to produce viable gametes through meiosis, but it may be able to perpetuate itself through mitosis (asexual reproduction). On rare occasions, nondisjunction takes place in a mitotic division, which leads to a doubling of chromosome number and an allotetraploid with chromosomes AABBCCGGHHII. This type of allopolyploid, consisting of two combined diploid genomes, is sometimes called an amphidiploid. Although the chromosome number has doubled compared with what was present in each of the parental species, the amphidiploid is functionally diploid: every chromosome has one and only one homologous partner, which is exactly what meiosis requires for proper segregation. The amphidiploid can now undergo normal meiosis to produce balanced gametes having six chromosomes.

George Karpechenko created polyploids experimentally in the 1920s. Cabbage (Brassica oleracea, 2n = 18) and radishes (Raphanus sativa, 2n = 18) are agriculturally important plants, but only the leaves of the cabbage and the roots of the radish are normally consumed. Karpechenko wanted to produce a plant that had cabbage leaves and radish roots so that no part of the plant would go to waste. Because both cabbage and radish possess 18 chromosomes, Karpechenko was able to successfully cross them, producing a hybrid with 2n = 18, but, unfortunately, the hybrid was sterile. After several crosses, Karpechenko noticed that one of his hybrid plants produced a few seeds. When planted, these seeds grew into plants that were viable and fertile. Analysis of their chromosomes revealed that the plants were allotetraploids, with 2n = 36 chromosomes. To Karpechencko’s great disappointment, however, the new plants possessed the roots of a cabbage and the leaves of a radish.

The Significance of Polyploidy

In many organisms, cell volume is correlated with nuclear volume, which, in turn, is determined by genome size. Thus, the increase in chromosome number in polyploidy is often associated with an increase in cell size, and many polyploids are physically larger than diploids. Breeders have used this effect to produce plants with larger leaves, flowers, fruits, and seeds. The hexaploid (6n = 42) genome of wheat probably contains chromosomes derived from three different wild species (Figure 8.29). As a result, the seeds of modern wheat are larger than those of its ancestors. Many other cultivated plants also are polyploid (Table 8.2).

Figure 8.29: Modern bread wheat, Triticum aestivum, is a hexaploid with genes derived from three different species. Two diploid species, T. uratu (n = 14) and probably Aegilops speltoides or a related species (n = 14), originally crossed to produce a diploid hybrid (2n = 14) that underwent chromosome doubling to create T. turgidum (4n = 28). A cross between T. turgidum and A. tauschii (2n = 14) produced a triploid hybrid (3n = 21) that then underwent chromosome doubling to eventually produce T. aestivum, which is a hexaploid (6n = 42).

Polyploidy is less common in animals than in plants for several reasons. As discussed, allopolyploids require hybridization between different species, which happens less frequently in animals than in plants. Animal behavior often prevents interbreeding among species, and the complexity of animal development causes most interspecific hybrids to be non-viable. Many of the polyploid animals that do arise are in groups that reproduce through parthenogenesis (a type of reproduction in which the animal develops from an unfertilized egg). Thus, asexual reproduction may facilitate the development of polyploids, perhaps because the perpetuation of hybrids through asexual reproduction provides greater opportunities for nondisjunction than does sexual reproduction. Only a few human polyploid babies have been reported, and most died within a few days of birth. Polyploidy—usually triploidy—is seen in about 10% of all spontaneously aborted human fetuses.

Importance of Polyploidy in Evolution

Polyploidy, particularly allopolyploidy, often gives rise to new species and has been particularly important in the evolution of flowering plants. Occasional genome doubling through polyploidy has been a major contributor to evolutionary success in several groups. For example, Saccharomyces cerevisiae (yeast) is a tetraploid, having undergone whole-genome duplication about 100 million years ago. The vertebrate genome has duplicated twice, once in the common ancestor of jawed vertebrates and again in the ancestor of fishes. Certain groups of vertebrates, such as some frogs and some fishes, have undergone additional polyploidy. Cereal plants have undergone several genome-duplication events. Different types of chromosome mutations are summarized in Table 8.3.