Polyploidy

The analysis of plant and animal cells shows that chromosomes are present in homologous pairs, with each member of the pair carrying very similar or identical genes. In humans, for example, there are forty-six chromosomes, but these can be grouped into twenty-three pairs. This set of twenty-three unique chromosomes is known as the haploid number for humans, while the full complement of forty-six chromosomes (two sets of twenty-three) is known as the diploid number. Virtually every somatic (non-sex) cell in the body contains the diploid number, while gametes (egg and sperm) contain the haploid number. Arabidopsis thaliana (a well-studied model plant) has ten chromosomes in a somatic nucleus, two each of five different types. Like humans, Arabidopsis is diploid, with a diploid number of ten and a haploid number of five.

While some plants show this diploid pattern of chromosome number, many others show a different pattern, called polyploidy. In this pattern, near-identical chromosomes occur in numbers greater than two, and the number of chromosomes in somatic cells therefore is greater than the diploid number. For instance, the potato has forty-eight chromosomes, but analysis shows that these can be grouped into four sets of twelve, with foursomes (instead of pairs) carrying very similar genes. The potato is said to be tetraploid, which is one form of polyploidy.

Polyploidy does not have to lead to large number of chromosomes, but it often does. For instance, cultivated polyploid plants such as sugarcane are known to have as many as 150 or more chromosomes, while wild plants may have even higher numbers. Most angiosperm (flowering plant) genomes are thought to have incurred one or more polyploidization events. Many of the world's leading crops are polyploid.

Chromosome Numbers

A simple nomenclature is widely used to provide geneticists with information about chromosome numbers in different organisms. The number of unique chromosomes making up one set is referred to as "x." For example, for humans x 23, for Arabidopsis thaliana x 5, and for potato x12. The number of chromosomes in the gametes of an organism is referred to as "n." For humans n 23, and for Arabidopsis thaliana n 5. In potato, n 24, half the total number of chromosomes. Note that for diploid organisms, n x, meaning the chromosome number of the gamete will be equal to the number of unique chromosome types. By contrast, for polyploids, n will be some multiple of x, and the simple formula n/x reflects the number of different sets of chromosomes in the nucleus. For the potato, n/x 2, indicating that the tetraploid potato carries twice the diploid number of chromosomes. Prefixes for other numbers of chromosomes are tri-(3), tetra-(4), penta-(5), hepta-(7), octo-(8), and so on.

During gamete formation, near-identical chromosomes (homologs) must pair up and undergo recombination (crossing over) before they are segregated into separate gametes. In diploid organisms, this pairing brings together the members of each homologous pair, so that (in Arabidopsis, for example), the five chromosomes from one set pair up with the five nearly identical chromosomes from the other set. In polyploid organisms, however, the number of possible pairings is larger. Scientists in fact recognize two different types of polyploidy (autopolyploidy and allopolyploidy, discussed next), based on the tendency of chromosomes from different sets to pair with one another.

Autopolyploidy

In autopolyploid (self-polyploid) organisms, such as the potato, the multiple sets of chromosomes are very similar to one another, and a member of one set can pair with the corresponding member of any of the other sets. For the potato, this means that a single chromosome from the first set can pair with up to three other chromosomes. This can lead to multivalent pairing at meiosis, with one chromosome pairing with different partners along different parts of its length.

Further, because any one chromosome can have several different partners, it is impossible to establish allelic relationships. Because of the possible presence of four, six, eight, even ten or more copies of a particular chromosome, genetic analysis of autopolyploids is complex.

Examples of autopolyploids in addition to potato include alfalfa (4x), sugarcane (8-18x), sugar beet (3x), ryegrass (4x), bermuda grass (3-4x), cassava (4x), red clover (4x), Gros Michel banana (3x), apple cultivars (3x), and many ornamentals (3x). Note that many autopolyploids are biomass crops, grown for vegetative parts other than seeds. The multivalent pairing associated with autopolyploidy is often not conducive to seed fertility. Many autopolyploids are difficult to obtain seed from and are propagated by vegetative clones, such as cuttings.

Allopolyploidy

Bread wheat (Triticum aestivum) is an example of allopolyploidy, in which the multiple sets of chromosomes are not composed of nearly identical chromosomes. In bread wheat, there are 42 chromosomes, divided into six sets of seven chromosomes each. These sets are denoted A, A, B, B, D, and D. While a particular member of A can pair with its homolog in the other A set, it cannot pair with any members of B or D. In effect, bread wheat has three different genomes, which are believed to have arisen from three different diploid ancestors, one each contributing the A, B, and D chromo-some sets. These different ancestors are thought to have come together to form the allohexaploid genome of bread wheat. While each ancestor carried many similar genes, they were not arranged in precisely the same way on each chromosome set. Since members of A are not homologous to members of B or D, pairing between the different sets during meiosis is normally not possible.

Therefore, at meiosis in normal bread wheat, there are twenty-one pairs of chromosomes formed, but A chromosomes are paired only with A, B only with B, and D only with D. Thus, despite the presence of six chromosome sets in the same nucleus, each has only one possible pairing partner, and all chromosomes pair as bivalents (one-to-one). Because of strict bivalent pairing, genetic analysis of allopolyploids is similar to that of diploids.

Examples of allopolyploids include cotton (6x), wheat (4x, 6x), oat (6x), soybean (4x), peanut (4x), canola (4x), tobacco (4x), and coffee (4x). Note that many allopolyploids are seed crops. The strict bivalent pairing associated with allopolyploidy is conducive to a high level of seed fertility.

Finally, it is significant that autopolyploidy and allopolyploidy are not mutually exclusive alternatives. Plants can contain multiple copies of some chromosomes and divergent copies of others, a state known as auto-allopolyploidy.

Formation of Polyploids

Every plant has the potential to form an autopolyploid at every meiotic cycle, since (as in all sexually reproducing cells) the chromosome number is doubled prior to the first meiotic cycle. Normally, the chromosome number is then reduced by two rounds of chromosome separation during ga-mete formation. Autopolyploids may be formed when this chromosome separation fails to occur.

Allopolyploids are thought to form from rare hybridization events between diploids that contain different genomes (such as AA and DD diploid wheats). Initially, the hybrid of such a cross, with a genetic constitution AD, would be unbalanced, since A and D chromosomes would not pair. As a result, such a hybrid would be sterile and would not be genetically stable over time. In rare cases, the AD hybrid may produce a gamete that fails to go through the normal reduction in chromosome number during meiosis, thereby doubling its chromosome number. Such an unreduced gamete may be of genetic constitution AADD, and both A and D chromosomes would have pairing partners, creating a genetically stable polyploid genotype:

Unreduced gametes can be artificially induced by various compounds, most notably colchicine, which interferes with the action of the meiotic spindle normally responsible for separating chromosomes. Colchicine has been widely used by geneticists to create synthetic polyploid plants, both for experimental purposes and to introduce valuable genes from wild diploids into major crops. Synthetic polyploids developed by humans from wild plants have contributed to improvement of cotton, wheat, peanut, and other crops. One artifically induced polyploid, triticale (which combines the genomes of wheat and rye), shows promise as a major crop itself.

Finally, many crops that are grown for vegetative parts are bred based on crosses between genotypes of different ploidy, which produce sterile progeny. For example, many cultivated types of banana (Musa spp.) and Bermuda grass (Cynodon spp.) are triploid, made from crosses between a diploid and a tetraploid. In each of these crops, seed production is undesirable for human purposes, and the unbalanced genetic constitution of the triploids usually results in seed abortion. Each of these crops is propagated clonally by cuttings. This is a good example of how humans have applied basic research knowledge to improved quality and productivity of agricultural products.

Occurrence in Plants, Including Economically Important Crops.

Many additional plant genomes may have once been polyploid. For example, maize has twenty chromosomes in its somatic nucleus and exhibits strict bivalent pairing—however at the deoxyribonucleic acid (DNA) level, large chromosome segments are found to be duplicated (i.e., contain largely common sets of genes in similar arrangements). In most cases, the duplicated regions no longer comprise entire chromosomes, although they may once have. Other examples of such ancient polyploids include broccoli and turnips. Hints of ancient chromosomal duplications are found in many plants and are particularly well characterized in sorghum and rice. Recent data from DNA sequencing has supported earlier suggestions from genetic mapping that even the simple genome of Arabidopsis may contain duplicated chromosomal segments. As large quantitites of DNA sequence information provide geneticists with new and powerful data, it is likely we will discover that many organisms that we think of as diploid are actually ancient polyploids.

Importance in Evolution.

Because of the abundance of polyploid plants, it can be argued that the joining of two divergent genomes into a common polyploid nucleus is the single most important genetic mechanism in plant evolution. Geneticists have long debated whether the abundance of polyploid plants simply reflects plant promiscuity or if a selective advantage is conferred by polyploid formation. Plants appear to enjoy greater freedom than animals to interbreed between diverse genotypes, even between geno-types that would normally be considered to be different species. However, one could also envision that the presence of multiple copies of a gene in a plant nucleus offers flexibility to evolve. While mutation (changes in the genetic code) is necessary for evolution, most mutations disrupt the genetic information rather than improve it. In polyploids, if one copy of a gene is disrupted, other copies can still provide the required function—therefore there may be more flexibility to experiment—and allow rare favorable changes to occur.

Autopolyploids may have a different type of genetic buffering. Most autopolyploids are highly heterozygous, with two, three, or more alleles represented at any one genetic locus. This may provide the organism with different avenues of response to the demands of different sets of environmental conditions.

SEE ALSO CHROMOSOMES; COTTON; SPECIATION; WHEAT.

Andrew H. Paterson

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