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Polyploidy

Polyploidy

In eukaryotic organisms, chromosomes come in sets. The somatic cells, called soma, usually have a diploid chromosome number, which in scientific notation is abbreviated as 2N. The diploid state contains two sets of chromosomes, one set of which has been contributed by each parent. A single set of chromosomes composes the haploid chromosome number, which is abbreviated as N. The haploid set is found in reproductive cells or gametes (also called the germplasm). In humans the diploid number is 46, and is represented as 2N = 46. Human sperm or eggs, however, have a haploid number of 23, which is represented as N = 23. In some circumstances, however, an organism can have more than two chromosomal sets. This occurrence is called polyploidy.

One cause of polyploidy is polyspermy. If two sperm fertilize an egg, the resulting zygote or fertilized egg will have three sets of chromosomes, and thus have a triploid number (3N). When this occurs in humans, 3N = 96. Triploidy in humans and most other animals is incompatible with life. Triploid individuals abort or fail to survive the first days of life after birth. Polyploidy is more common in plants, and polyploid forms often survive to produce much larger cells and plant organs. Ferns, which may have up to 1,500 chromosomes, are frequently polyploid, as are varieties of domesticated cereal plants. Most often, polyploids run in sets of three to eight (triploid to octoploid).

Polyploidy in Animals

Geneticist Hermann Muller argued that polyploidy is more rare in animals than plants because animals have a more complex development, with more organ systems that are fine-tuned to dosages of genes. Any given gene is represented three times in a triploid. If the amount (dosage) of gene product causes a heart, brain, or other vital organ not to form, the embryo will abort. When these developmental genes produce too much or too little of the products that induce organ formation, as they might if there are too many or too few copies of the genes, events occur too soon or too late to be coordinated. Muller raised the possibility that the sex chromosomes serve as a barrier to polyploidy in most animals. Plants, by contrast, do not usually have sex chromosomes, and thus this sexual reproductive barrier is not a problem for them.

Muller noted that most animals use a sex-chromosome mechanism for sex determination. In fruit flies and humans, diploid males have the sex chromosomes XY, whereas diploid females have XX. A triploid fly or human would have three chromosomes along with three sets of autosomes . In such a triploid, XXX will result in a female. However, a zygote having XXY XYY may not produce a male. Rather, it may result in an intersex organism, with abnormal mixed male and female reproductive organs.

While human triploids do not survive, this is not the case for fruit flies. The XXY or XYY is an intersex, sterile form, but the triploid female is fertile. If the 3N female is mated to a 2N XY male, however, only a relatively few offspring will emerge, because many of the eggs will have an incorrect number of chromosomes. This state of excesses or deficits of chromosomes in an otherwise diploid or triploid cell is called aneuploidy. Aneuploid embryos rarely survive in humans or other animals, although there are exceptions (such as infants born with Down syndrome).

Human triploid embryos are a major reason for first-trimester spontaneous abortions (popularly called miscarriages). Polyploid amphibians, on the other hand, have evolved an alternate means of sex determination that allows them to have fertile triploid or tetraploid (4N) forms. As with polyploid plants, these forms are generally larger in size than their diploid relatives. It is not yet known why stillborn or short-lived human triploids do not display this enlarged size.

Polyploidy in Plants

Polyploidy can be induced with chemicals such as colchicine, as O. J. Eigsti first demonstrated in 1935. His work extended that done by F. A. Blakeslee, and the technique he used has been adopted commercially to produce products such as seedless watermelon. The seeds are missing because the embryos abort from aneuploidy before they can form seeds.

In nature there are different kinds of polyploids. An autopolyploid plant has all its chromosomes derived from one haploid set. An allopolyploid plant has its sets derived from two different plant species. In general, allopolyploids are fertile and survive, whereas autopolyploids are sterile and must be propagated as clones (identical twins), by cuttings.

The difference between autopolyploidy and allopolyploidy can be appreciated by an example. No one knows the reasons for mitotic failure leading to spontaneous tetraploids, but artificial ones are induced by mitotic poisons, like colchicine, that prevent spindle fiber formation. If one species has chromosomes ABCD in a (haploid) gamete , and a related species has chromosomes FGHI, the resulting (diploid) zygote will have a chromosome set consisting of ABCDFGHI. If that collection of chromosomes undergoes a spontaneous doubling, the resulting plant is AABBCCDDFFGGHHII. Such a plant will produce ABCDFGHI gametes and by self-pollination, which is common in many flowering plants, the new allopolyploid will be fertile.

In the case of autopolyploids, by contrast, the chromosomes ABCD become triplicated (3N: AAABBBCCCDDD) or quadruplicated (4N: AAAABBBBCCCCDDDD). This may lead to nondisjunctional separations during meiosis, wherein the chromosomes will divide improperly or incompletely. In the 3N plant many of the gametes may be AABCDD or ABCCD or other variations of aneuploidy that will disturb embryonic development.

Among familiar plant polyploids are strains of wheat with chromosome numbers of 14 (2N), 28 (4N), and 42(6N), all of which are based on an ancestral form whose haploid number was 7. Chrysanthemums have a series of varieties with a range of chromosome numbers: 18, 36, 54, 72, and 90. The ancestral haploid is assumed to be 9. About half of all flowering plant species are believed to have polyploid varieties. If an accidental doubling of the zygote chromosome number is the major mechanism involved, most of these forms are tetraploid.

Genetic Analysis

The transmission of genetic traits in polyploids is more difficult to calculate than in diploids because a gene for a recessive trait in a triploid, for example, would have to appear in the same location on all three of its homologous chromosomes in order for it to be phenotypically apparent. Such calculations, when done for diploids, rely upon binomial equations and generate a familiar ratio of 9AB:3aB:3Ab:1ab, whereas the calculations for polyploid plants require the use of trinomial equations for triploids and quadrinomial equations for tetraploids, instead of the traditional binomial (A + B)2 that generates the familiar 9AB:3aB:3Ab:1ab ratio for diploids. Thus for a trinomial (three gene) the equation will be the expansion of (A + B + C)3.

The use of polyploids in laboratory research has allowed research into the function of specific genes. For instance, triploid female fruit flies crossed to diploid males were used to create a diploid offspring with a chromosome of a sibling species. In this experiment, the tiny fourth chromosome of Drosophila simulans was inserted into an otherwise diploid D. melanogaster offspring. This permitted analysis of the genes shared in common (most of them) as well as gene differences that led to visible malformations in the hybrid fly. Triploid flies have also been crossed to irradiated diploid males to prove that X rays induce breaks in chromosomes, causing apoptosis and embryonic abortion.

see also Chromosomal Aberrations; Meiosis; Muller, Hermann; Sex Determination; X Chromosome, Y Chromosome.

Elof Carlson

Bibliography

Muller, H. J. "Why Polyploidy is Rarer in Animals than in Plants." The American Naturalist LIX (1925): 346-353.

Dobzhansky, Theodosius. "Patterns of Evolution." In Genetics and the Origin of Species, Theodosius Dobzhansky, ed. New York: Columbia University Press, 1951.

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Arabidopsis thaliana

Arabidopsis thaliana

Arabidopsis thaliana, or thale cress, is a small flowering plant in the mustard family. Arabidopsis has no inherent agricultural value and is even considered a weed, but it is one of the favored model organisms of plant geneticists and molecular biologists, and it is the most thoroughly studied plant species at the molecular level. Model organisms have traits that make them attractive and convenient for biologists, who anticipate being able to extend their findings to other, less easily studied species. Arabidopsis is small and easy to grow, allowing researchers to cultivate it with minimal investments in effort and laboratory space. It has a short generation time, taking about six weeks for a seed to grow into a mature plant that produces more seeds. This rapid maturation enables biologists to conduct genetic cross experiments in a relatively short period of time. A single mature plant can produce over 5,000 seeds, another property that makes Arabidopsis convenient for use in genetic analysis.

A Small and Simple Genome

Beyond these basic traits, other attributes of Arabidopsis make it particularly well-suited for analysis by modern molecular genetic methods. Its genome (the amount of DNA in each set of chromosomes) is only about 125 million base pairs. This is small compared to many other plants, and makes searching for particular genes easier in Arabidopsis than in plants with larger genomes. For comparison, the genome sizes for rice (Oryza sativa ), wheat (Triticum aestivum ), and corn (Zea mays ) are 420 million, 16 billion, and 2.5 billion base pairs, respectively. Furthermore, the Arabidopsis genome is contained on just five pairs of chromosomes, making it easier for geneticists to locate specific genes.

Geneticists can carry out crosses (interbreeding two different plant strains) with Arabidopsis by introducing the pollen from one plant to the stigma on another. This mode of reproduction, called outcrossing, is useful for combining mutations from different plants. Alternatively, Arabidopsis can reproduce by a process called selfing, in which an individual plant uses its own pollen to fertilize its ovules .

Selfing, which is not possible in many plants, is very useful for geneticists who wish to study mutations. Most mutations are recessive, which means that they physically manifest themselves (display a phenotype ) only when they are present on the chromosomes contributed by both the ovule and the fertilizing pollen. In selfing, heterozygous mutations (which are present on only one of the two sets of chromosomes) will become homozygous (present on both) in one quarter of the progeny produced in this manner.

Arabidopsis and Transformation

Another property that endears Arabidopsis to plant molecular biologists is that it is easily transformed. Transformation is a method for introducing foreign DNA into an organism. This technique is invaluable for studying how genes function and interact with other genes. Biologists usually transform plants by infecting them with genetically engineered varieties of a bacterium, Agrobacterium tumefaciens. In nature, when Agrobacterium infects plants, it inserts certain genes directly into the plant cells, causing a disease called crown gall. The genetically engineered Agrobacterium strains have had their disease-causing genes removed. They can still infect a plant and insert their DNA, but do not cause a disease. To transform plants, the molecular biologist inserts the foreign gene to be studied into Agrobacterium, which will then transfer the gene to a plant that it infects. This transformation technique does not work well on many other plant species, limiting the utility of those plants for molecular genetic analysis.

Arabidopsis researchers also use a variation on the Agrobacterium -mediated transformation technique to introduce mutations in the plant. Studying the effect of a mutation in a particular gene often yields critical information about the normal function of that gene. Because Agrobacterium inserts its transforming DNA randomly in the genome, in many cases the DNA gets inserted directly within a gene sequence. This usually destroys the function of the disrupted gene, resulting in a "knockout mutant." Furthermore, the piece of transformed DNA (T-DNA) that is inserted in the disrupted plant gene can serve as a flag for tracking down the gene by molecular biology methods. Large-scale projects using this T-DNA insertion technique are underway to mutate, identify, and characterize every gene in the Arabidopsis genome.

The First Completely Sequenced Plant Genome

At the end of 2000, an international team of researchers announced that Arabidopsis was the first plant to have its complete genome sequencethe exact order of essentially all 125 million DNA base pairsdetermined. The project revealed that Arabidopsis contains over 25,500 genes. By identifying and studying these genes, biologists are learning lessons about plant biology that could provide important advances in agriculture, such as improved crop resistance to pathogens, salt, light stress, and drought, and to the production of more healthful edible oils, pharmaceuticals, and biodegradable plastics.

Arabidopsis research has also produced important discoveries in fundamental plant science, such as the identification of a plant hormone receptor, a clearer understanding of how plants sense and respond to light, and more about the processes that induce plants to form flowers. Arabidopsis research may even have direct relevance to human biology. For example, a photoreceptor protein that regulates circadian rhythms in Arabidopsis was found to share sequence similarity to a retinal photoreceptor, which may perform a similar role in mammals.

see also Inheritance Patterns; Model Organisms; Transformation; Transgenic Plants.

Paul J. Muhlrad

Bibliography

Meinke, David W., et al. "Arabidopsis thaliana: A Model Plant for Genome Analysis." Science 283, no. 5389 (1998): 662-681.

Internet Resources

The Arabidopsis Information Resource. <http://www.arabidopsis.org/>.

Nature, Vol. 408, December 2000. (Issue devoted to Arabidopsis thaliana; <http://www.nature.com/genomics/papers/a_thaliana.html>).

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Polyploidy

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 pairinghowever 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 functiontherefore there may be more flexibility to experimentand 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

Bibliography

Irvine, J. E. "Saccharum Species as Horticultural Classes." Theoretical and Applied Genetics 98 (1999): 186-94.

Jiang, C., R. Wright, K. El-Zik, and A. H. Paterson. "Polyploid Formation Created Unique Avenues for Response to Selection in Gossypium (Cotton)." Proceedings of the National Academy of Sciences of the USA 95 (1998): 4419-24.

Leitch, I., and M. Bennett. "Polyploidy in Angiosperms." Trends in Plant Science 2(1997): 470-76.

Masterson, J. "Stomatal Size in Fossil Plants: Evidence for Polyploidy in the Majority of Angiosperms." Science 264 (1994): 421-24.

Ming, R., et al. "Alignment of the Sorghum and Saccharum Chromosomes: Comparative Genome Organization and Evolution of a Polysomic Polyploid Genus and Its Diploid Cousin." Genetics 150 (1998): 1663-82.

Simmonds, N. W. Principles of Crop Improvement. London: Longman Group, 1998.

Stebbins, G. L. "Chromosomal Variation and Evolution; Polyploidy and Chromo-some Size and Number Shed Light on Evolutionary Processes in Higher Plants." Science 152 (1966): 1463-69.

Wendel, J. F., M. M. Goodman, and C. W. Stuber. "Mapping Data for 34 Isozyme Loci Currently Being Studied." Maize Genetics Cooperative News Letter 59 (1985): 90.

Wu, K. K., et al. "The Detection and Estimation of Linkage in Polyploids Using Single-Dose Restriction Fragments." Theoretical and Applied Genetics 83 (1992): 294-300.

Zeven, A. C. "Polyploidy and Domestication: The Origin and Survival of Polyploids in Cytotype Mixtures." In Polyploidy, Biological Relevance, ed. W. H. Lewis. New York: Plenum Press, 1979.

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polyploidy

polyploidy The condition in which an individual possesses one or more sets of homologous chromosomes in excess of the normal two sets found in diploid organisms. It is caused by the replication within a nucleus of complete chromosome sets without subsequent nuclear division. Examples are triploidy (3n), tetraploidy (4n), hexaploidy (6n), and octoploidy (8n). Polyploids are not always allopolyploids.

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polyploidy

polyploidy The condition in which an individual possesses one or more sets of homologous chromosomes in excess of the normal two sets found in diploid organisms. It is caused by the replication within a nucleus of complete chromosome sets without subsequent nuclear division. Examples are triploidy (3n), tetraploidy (4n), hexaploidy (6n), and octoploidy (8n).

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polyploidy

polyploidy The condition in which an individual possesses 1 or more sets of homologous chromosomes in excess of the normal 2 sets found in diploid organisms. It is caused by the replication within a nucleus of complete chromosome sets without subsequent nuclear division. Examples are triploidy (3n), tetraploidy (4n), hexaploidy (6n), and octoploidy (8n).

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