328. Heslop-Harrison JS. 2017. Polyploidy. In: Reference Module in Life Sciences, Elsevier, ISBN: 978-0-12- 809633-8, http://dx.doi.org/10.1016/B978-0-12-809633-8.06934-X (££$$€€) (see https://www.elsevier.com/solutions/sciencedirect/content/reference-modules for information about the series.)

Abstract
Polyploid organisms are eukaryotes that have more than two complete sets of chromosomes (one from each parent or ancestor) in somatic and germline cells of animals, fungi, and plants. Polyploidy of individual cells or cell types (endopolyploidy), arising from chromosome replication without cell division, is involved in the normal (eg, secretory cells) or abnormal (eg, many cancers) development of organisms. Polyploidy or “whole-genome duplication” is an important feature of genome evolution and speciation, and most lineages of plants and animals include rounds of such duplications in their evolutionary history. Many plant species, in particular, have both ancient whole-genome duplications and more recent polyploidy events in their ancestry. Polyploid individuals are found occasionally in all groups of eukaryotic organisms as a result of incorrect meiosis, fertilization, or cell division, although most spontaneously occurring animal polyploids are inviable. Polyploids can be generated experimentally by treatment with chemicals such as colchicine or by fusion of diploid nuclei. Many polyploids, particularly among plants, develop normally, and depending on the nature of the polyploidy may be sterile, or undergo meiosis that is indistinguishable from a normal diploid giving viable gametes.

Keywords
Amphidiploid; Autopolyploid; Eukaryotes; Tetraploid

FULL AUTHOR TEXT SUMMARY:

POLYPLOIDY

Amphipolyploid A species or hybrid having more than two sets of chromosomes that originate from more than one parental or ancestral species.

Autopolyploid A species or hybrid having more than two sets of chromosomes originating from the same parental or ancestral species.

Polyploid A species, individual organism, or cell having more than two sets of chromosomes (more than two genomes) in each cell nucleus.

Tetraploid A species or individual organism having four sets of chromosomes (four genomes or typically 4 times the basic haploid chromosome number of x) in each cell. A single cell may also be tetraploid.

Types of polyploidy and nomenclature

Polyploidy may occur by the number of chromosomes in a cell doubling because of a failure of chromosome sets to divide at mitosis, by fusion of nuclei from diploid cells, or by a failure of meiosis giving a 2n gamete, so the resulting embryo has at least one extra chromosome set. In presenting chromosome numbers or karyotype constitutions, the letter x is used to refer to the basic chromosome number of the ancestor of a polyploid. The diploid chromosome number, 2n, refers to the number of chromosomes in a cell of the individual normally producing the germ cells (the sporophyte): a non-polyploid, diploid organism as represented by most higher plants and animals would be described as 2n=2x with the number of chromosomes given. Polyploids still have 2n chromosomes, but more than two genomes, so a triploid with three genomes would be 3x; a tetraploid, 4x; a pentaploid, 5x; a hexaploid, 6x; an octaploid, 8x; or a dodecaploid, 12x. Many plant species are polyploid, and they can include multiple chromosome sets from one (autopolyploids) or more than one (allopolyploids) ancestral species. The group of species including wheat, rye, and barley (the grass tribe Triticeae) is a good example where many polyploid forms are known. The base chromosome number is x=7, found in the diploid species barley (Hordeum vulgare, 2n=2x=14), for example. The crop bread wheat, Triticum aestivum, is a hexaploid species with six sets each of seven chromosomes, and is designated as 2n=6x=42. A pentaploid with an additional chromosome (made perhaps by crossing a tetraploid with hexaploid wheat) would have a chromosome constitution of 2n=5x=35. Autotetraploids contain four sets of chromosomes from the same species of origin, and so they have double the chromosome number of their diploid ancestor. Sometimes, autopolyploids are classified in the same species as the diploid, and they may be fertile; there are morphologically similar diploid, 2n=2x=14, and tetraploid, 2n=4x=28, forms of the wall barley, Hordeum murinum. Allotetraploids contain four sets of chromosomes, but in contrast to autotetraploids, the four chromosome sets are derived from two distinct parental species (eg, in an intergeneric hybrid). Where the parental species are known, the allotetraploid species or individual can be described as amphidiploid or amphipolyploid. Allotetraploids include oilseed rape, Brassica napus, 2n=4x=38.

Detection of polyploidy

Examination and counting of chromosome number by light microscopy is used to detect straightforward cases of polyploidy in cells or species: a multiple or sum of the number of chromosomes in related (diploid) species will be counted. Measurement of the DNA content of nuclei, finding a stepped series with increase in size equivalent to the size of the x, haploid, genome, is also used to measure ploidy. Other methods to test for polyploidy include construction of haploids that reach meiosis and show bivalent formation between the ancestral chromosome sets, or crossing of the polyploid to a suspected diploid ancestor; bivalents will pair between the ancestor and one genome in the polyploid (although chromosomes of an autopolyploid could pair with themselves leaving the suspected ancestral chromosomes as univalents). Molecular cytogenetic methods including in situ hybridization using species-specific repetitive DNA sequences or genomic DNA are proving valuable to analyze the constitution of allopolyploids. Duplications in the genome may involve ancestral polyploidy, but chromosomal aberration, aneuploidy, and sequence duplication can also occur; indeed, polyploids often tolerate aneuploidy well, and the occurrence of monosomic lines, where one chromosome is missing from a plant’s karyotype, is good evidence for polyploidy. With the wide application of DNA markers and sequencing methods, many whole-genome duplication and polyploid events that were not expected by scientists are being detected: dense molecular marker maps show the duplication of whole chromosome sets in species that were not previously considered as polyploids – the diploid Brassica mustards are of hexaploid origin (and thus, the cultivated B. napus (oilseed rape, canola) is a dodecaploid with originally 12 chromosome sets). Nevertheless, detection of polyploidy is often difficult because diploid relatives or ancestors no longer exist, and genetic mechanisms restore pseudodiploid behavior, involving strictly homologous chromosome pairing, so even amphidiploids may be fully fertile. Without such mechanisms, chromosomes will produce an assortment of pairing configurations, including trivalents and quadrivalents, which will not assort regularly to give balanced gametes. Where there is clear evidence of polyploidy in the ancestry, but it is both ancient and accompanied by diploid-like behavior, species may be referred to as having a palaeopolyploid origin.

Palaeopolyploidy in evolution

Polyploidy, involving the presence of multiple copies of identical or similar chromosome sets in one species, is an important feature of species evolution in the plant, animal, and fungal kingdoms. Polyploidy is widely considered as an enabling force in evolution. Because chromosome sets are duplicated in polyploids, heterozygosity may be fixed, and random mutation or factors modulating gene expression may be buffered (unlike a diploid), so new genes and gene functions may evolve, leaving the original function in the other chromosome set. More than 50% of plants are obvious polyploids, while detailed studies are showing that many other species are palaeopolyploids with repeated rounds of whole-genome duplication during evolution. Polyploidy, though, does not feature in the evolution of the other major plant group, gymnosperms, and very few recent polyploid gymnosperms have been discovered. In animals, polyploid species are well known among leeches, brine shrimp, and lizards, although many of these reproduce asexually as meiotic chromosome pairing is irregular. Detailed comparison of the gene content of chromosomes of animals combined with comparative analysis of chromosomes and genes in distantly related species is giving evidence of whole-genome duplication or palaeopolyploidy: in the evolutionary split of vertebrates from invertebrates, there are two rounds of polyploidy detected (one occurring after the split of the lampreys), with more recent whole-genome duplications in the Xenopus and fish lineages. In the fungi, there are examples of both autopolyploids (including asexually reproducing lines of the baker’s yeast Saccharomyces cerevisiae), allopolyploids and palaeopolyploids.

Origin of polyploidy

Polyploidy may occur spontaneously in cells, either because of abnormal divisions or as part of differentiation. Fertilization involving unreduced (2n) gametes is a frequent source of triploid and tetraploid organisms: a meiotic division fails or a polar body is not expelled, giving a 2n gamete. Fertilization by two male gametes may give triploids. In humans, triploid (2n=3x=69) and tetraploid conceptuses (2n=4x=92) (arising from both mechanisms) are found in as many as 20 and 6%, respectively, of spontaneous abortions. Polyploid cells and organisms can be made by treatment of cells with mitotic inhibitors (such as colchicine) which enable chromosome replication to occur without cell division.

Polyploidy in crop plants

The world’s four most important crops provide examples of the range of ploidy levels found in plants. Bread wheat is a hexaploid (2n=6x=42), derived as little as 30,000 years ago from a diploid species (2n=2x=14), Triticum tauschii, and a tetraploid, durum wheat (2n=4x=28), Triticum turgidum, itself derived from two diploid species Triticum monococcum and a species similar to Aegilops speltoides. The second most important crop, rice, is considered diploid, while molecular mapping data, the fertility of monosomic chromosome lines, cytogenetic comparisons with wild species, and some chromosome pairing data show that maize, the third most important crop, is a palaeotetraploid. Banana, another important crop, is cultivated as a triploid (2n=3x=33) to give sterile fruit with parthenocarpic development. A few “new” crops have been generated as synthetic hybrids: the wheat rye amphidiploid Triticale is widely grown in dry and colder areas of Canada and Poland. In horticulture, polyploids, whether species, natural, or artificial hybrids, are widely selected by breeders, not least because the fruit tends to be larger than that found in the diploid ancestor, as is found in strawberry and blueberry.

Polyploid cell types

Many normal individual plants and animals include polyploid cells with specialized functions, in particular those with secretory or nutritional functions. The reason why this endoreduplication of the genome (up to 1000 times or more, where the chromosomes replicate but there is no cell division) is needed for these functions is unclear. Examples include the mammalian placenta, salivary glands in some insects, or the tapetum surrounding the haploid pollen grains in plants. In many mammalian cancers, where cell division becomes unregulated, polyploid cells are also found, presumably as a consequence of decoupling of DNA replication and the cell cycle.

Relevant reading

Frawley LE, Orr-Weaver TL. 2015. Polyploidy. Current Biology 25 (9), R353–R358.

Heslop-Harrison JS. 2012. Genome evolution: Extinction, continuation or explosion? Current Opinion in Plant Biology 15 (2), 115–121.

Jiao Y, Wickett NJ, Ayyampalayam S. et al. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473 (7345), 97–100.

Renny-Byfield S, Wendel JF. 2014. Doubling down on genomes: Polyploidy and crop plants. American Journal of Botany 101 (10), 1711–1725.

FROM: Heslop-Harrison JS. 2017. Polyploidy. In: Reference Module in Life Sciences, Elsevier, ISBN: 978-0-12- 809633-8, http://dx.doi.org/10.1016/B978-0-12-809633-8.06934-X (££$$€€) (see https://www.elsevier.com/solutions/sciencedirect/content/reference-modules for information about the series.)