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Polyploidy

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Not to be confused with "polypoid", resembling apolyp.
This image shows haploid (single), diploid (double), triploid (triple), and tetraploid (quadruple) sets of chromosomes. Triploid and tetraploid chromosomes are examples of polyploidy.

Polyploidyis a condition in which thecellsof anorganismhave more than one pair of (homologous)chromosomes.Most species whose cells havenuclei(eukaryotes) arediploid,meaning they have two complete sets of chromosomes, one from each of two parents; each set contains the same number of chromosomes, and the chromosomes are joined in pairs of homologous chromosomes. However, some organisms arepolyploid.Polyploidy is especially common in plants. Most eukaryotes have diploidsomatic cells,but producehaploidgametes(eggs and sperm) bymeiosis.Amonoploidhas only one set of chromosomes, and the term is usually only applied to cells or organisms that are normally diploid. Males ofbeesand otherHymenoptera,for example, are monoploid. Unlike animals,plantsand multicellularalgaehavelife cycleswith twoalternating multicellular generations.Thegametophytegeneration is haploid, and produces gametes bymitosis;thesporophytegeneration is diploid and producessporesbymeiosis.

Polyploidy is the result of whole-genome duplication during the evolution of species. It may occur due to abnormalcell division,either during mitosis, or more commonly from the failure of chromosomes to separate during meiosis or from the fertilization of an egg by more than one sperm.[1]In addition, it can be induced in plants andcell culturesby some chemicals: the best known iscolchicine,which can result in chromosome doubling, though its use may have other less obvious consequences as well.Oryzalinwill also double the existing chromosome content.

Amongmammals,a high frequency of polyploid cells is found in organs such as the brain, liver, heart, and bone marrow.[2]It also occurs in the somatic cells of otheranimals,such asgoldfish,[3]salmon,andsalamanders.It is common amongfernsand floweringplants(seeHibiscus rosa-sinensis), including both wild and cultivatedspecies.Wheat,for example, after millennia ofhybridizationand modification by humans, has strains that arediploid(two sets of chromosomes),tetraploid(four sets of chromosomes) with the common name ofdurumor macaroni wheat, andhexaploid(six sets of chromosomes) with the common name of bread wheat. Many agriculturally important plants of the genusBrassicaare also tetraploids.Sugarcanecan have ploidy levels higher thanoctaploid.[4]

Polyploidization can be a mechanism ofsympatric speciationbecause polyploids are usually unable to interbreed with their diploid ancestors. An example is the plantErythranthe peregrina.Sequencing confirmed that this species originated fromE. × robertsii,a sterile triploid hybrid betweenE. guttataandE. lutea,both of which have been introduced and naturalised in the United Kingdom. New populations ofE. peregrinaarose onthe Scottish mainlandand theOrkney Islandsvia genome duplication from local populations ofE. × robertsii.[5]Because of a rare genetic mutation,E. peregrinais not sterile.[6]

On the other hand, polyploidization can also be a mechanism for a kind of 'reverse speciation',[7]whereby gene flow is enabled following the polyploidy event, even between lineages that previously experienced no gene flow as diploids. This has been detailed at the genomic level inArabidopsis arenosaandArabidopsis lyrata.[8]Each of these species experienced independent autopolyploidy events (within-species polyploidy, described below), which then enabled subsequent interspecies gene flow of adaptive alleles, in this case stabilising each young polyploid lineage.[9]Such polyploidy-enabled adaptive introgression may allow polyploids at act as 'allelic sponges', whereby they accumulate cryptic genomic variation that may be recruited upon encountering later environmental challenges.[10]

Terminology

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Types

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"Triploid" redirects here. For the human chromosomal disorder (69 XXX, etc.), seeTriploid syndrome.

Organ-specific patterns of endopolyploidy (from 2xto 64x) in the giant antDinoponera australis

Polyploidtypes are labeled according to the number of chromosome sets in thenucleus.The letterxis used to represent the number of chromosomes in a single set:

Classification

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Autopolyploidy

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Autopolyploidsare polyploids with multiple chromosome sets derived from a singletaxon.

Two examples of natural autopolyploids are the piggyback plant,Tolmiea menzisii[18]and the white sturgeon,Acipenser transmontanum.[19]Most instances of autopolyploidy result from the fusion of unreduced (2n) gametes, which results in either triploid (n+ 2n= 3n) or tetraploid (2n+ 2n= 4n) offspring.[20]Triploid offspring are typically sterile (as in the phenomenon oftriploid block), but in some cases they may produce high proportions of unreduced gametes and thus aid the formation of tetraploids. This pathway to tetraploidy is referred to as thetriploid bridge.[20]Triploids may also persist throughasexual reproduction.In fact, stable autotriploidy in plants is often associated withapomicticmating systems.[21]In agricultural systems, autotriploidy can result in seedlessness, as inwatermelonsandbananas.[22]Triploidy is also utilized in salmon and trout farming to induce sterility.[23][24]

Rarely, autopolyploids arise from spontaneous, somatic genome doubling, which has been observed in apple (Malus domesticus)bud sports.[25]This is also the most common pathway of artificially induced polyploidy, where methods such asprotoplast fusionor treatment withcolchicine,oryzalinormitotic inhibitorsare used to disrupt normalmitoticdivision, which results in the production of polyploid cells. This process can be useful in plant breeding, especially when attempting to introgress germplasm across ploidal levels.[26]

Autopolyploids possess at least threehomologous chromosomesets, which can lead to high rates of multivalent pairing duringmeiosis(particularly in recently formed autopolyploids, also known as neopolyploids) and an associated decrease in fertility due to the production ofaneuploidgametes.[27]Natural or artificial selection for fertility can quickly stabilize meiosis in autopolyploids by restoring bivalent pairing during meiosis. Rapid adaptive evolution of the meiotic machinery, resulting in reduced levels of multivalents (and therefore stable autopolyploid meiosis) has been documented inArabidopsis arenosa[28]andArabidopsis lyrata,[29]with specific adaptive alleles of these species shared between only the evolved polyploids.[30][31]

The high degree ofhomologyamong duplicated chromosomes causes autopolyploids to displaypolysomic inheritance.[32]This trait is often used as a diagnostic criterion to distinguish autopolyploids from allopolyploids, which commonly display disomic inheritance after they progress past the neopolyploid stage.[33]While most polyploid species are unambiguously characterized as either autopolyploid or allopolyploid, these categories represent the ends of a spectrum of divergence between parental subgenomes. Polyploids that fall between these two extremes, which are often referred to as segmental allopolyploids, may display intermediate levels of polysomic inheritance that vary by locus.[34][35]

About half of all polyploids are thought to be the result of autopolyploidy,[36][37]although many factors make this proportion hard to estimate.[38]

Allopolyploidy

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Allopolyploidsoramphipolyploidsorheteropolyploidsare polyploids with chromosomes derived from two or more diverged taxa.

As in autopolyploidy, this primarily occurs through the fusion of unreduced (2n) gametes, which can take place before or afterhybridization.In the former case, unreduced gametes from each diploid taxon – or reduced gametes from two autotetraploid taxa – combine to form allopolyploid offspring. In the latter case, one or more diploidF1hybridsproduce unreduced gametes that fuse to form allopolyploid progeny.[39]Hybridization followed by genome duplication may be a more common path to allopolyploidy because F1hybrids between taxa often have relatively high rates of unreduced gamete formation – divergence between the genomes of the two taxa result in abnormal pairing betweenhomoeologouschromosomes ornondisjunctionduring meiosis.[39]In this case, allopolyploidy can actually restore normal,bivalentmeiotic pairing by providing each homoeologous chromosome with its own homologue. If divergence between homoeologous chromosomes is even across the two subgenomes, this can theoretically result in rapid restoration of bivalent pairing and disomic inheritance following allopolyploidization. However multivalent pairing is common in many recently formed allopolyploids, so it is likely that the majority of meiotic stabilization occurs gradually through selection.[27][33]

Because pairing between homoeologous chromosomes is rare in established allopolyploids, they may benefit from fixedheterozygosityof homoeologous alleles.[40]In certain cases, such heterozygosity can have beneficialheteroticeffects, either in terms of fitness in natural contexts or desirable traits in agricultural contexts. This could partially explain the prevalence of allopolyploidy among crop species. Both breadwheatandtriticaleare examples of an allopolyploids with six chromosome sets.Cotton,peanut,orquinoaare allotetraploids with multiple origins. InBrassicaceouscrops, theTriangle of Udescribes the relationships between the three common diploid Brassicas (B. oleracea,B. rapa,andB. nigra) and three allotetraploids (B. napus,B. juncea,andB. carinata) derived from hybridization among the diploid species. A similar relationship exists between three diploid species ofTragopogon(T. dubius,T. pratensis,andT. porrifolius) and two allotetraploid species (T. mirusandT. miscellus).[41]Complex patterns of allopolyploid evolution have also been observed in animals, as in the frog genusXenopus.[42]

Aneuploid

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Main article:Aneuploidy

Organisms in which a particular chromosome, or chromosome segment, is under- or over-represented are said to beaneuploid(from the Greek words meaning "not", "good", and "fold" ). Aneuploidy refers to a numerical change in part of the chromosome set, whereas polyploidy refers to a numerical change in the whole set of chromosomes.[43]

Endopolyploidy

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Polyploidy occurs in some tissues of animals that are otherwise diploid, such as humanmuscletissues.[44]This is known asendopolyploidy.Species whose cells do not have nuclei, that is,prokaryotes,may be polyploid, as seen in the largebacteriumEpulopiscium fishelsoni.[45]Henceploidyis defined with respect to a cell.

Monoploid

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Main article:Monoploidy

A monoploid has only one set of chromosomes and the term is usually only applied to cells or organisms that are normally diploid. The more general term for such organisms ishaploid.

Temporal terms

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Neopolyploidy

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A polyploid that is newly formed.

Mesopolyploidy

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That has become polyploid in more recent history; it is not as new as a neopolyploid and not as old as a paleopolyploid. It is a middle aged polyploid. Often this refers to whole genome duplication followed by intermediate levels of diploidization.

Paleopolyploidy

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Thisphylogenetic treeshows the relationship between the best-documented instances ofpaleopolyploidyin eukaryotes.
Main article:Paleopolyploidy

Ancient genome duplications probably occurred in the evolutionary history of all life. Duplication events that occurred long ago in the history of variousevolutionary lineagescan be difficult to detect because of subsequentdiploidization(such that a polyploid starts to behave cytogenetically as a diploid over time) asmutationsand gene translations gradually make one copy of each chromosome unlike the other copy. Over time, it is also common for duplicated copies of genes to accumulate mutations and become inactive pseudogenes.[46]

In many cases, these events can be inferred only through comparingsequenced genomes.Examples of unexpected but recently confirmed ancient genome duplications includebaker's yeast(Saccharomyces cerevisiae), mustard weed/thale cress (Arabidopsis thaliana),rice(Oryza sativa), and two rounds of whole genome duplication (the2R hypothesis) in an earlyevolutionaryancestorof thevertebrates(which includes thehumanlineage) and another near the origin of theteleostfishes.[47]Angiosperms(flowering plants) have paleopolyploidy in their ancestry. Alleukaryotesprobably have experienced a polyploidy event at some point in their evolutionary history.

Other similar terms

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Karyotype

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Main article:Karyotype

A karyotype is the characteristic chromosome complement of aeukaryotespecies.[48][49]The preparation and study of karyotypes is part ofcytologyand, more specifically,cytogenetics.

Although the replication and transcription of DNA is highly standardized ineukaryotes,the same cannot be said for their karyotypes, which are highly variable between species in chromosome number and in detailed organization despite being constructed out of the same macromolecules. In some cases, there is even significant variation within species. This variation provides the basis for a range of studies in what might be called evolutionary cytology.

Homoeologous chromosomes

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Main article:Homoeology

Homoeologous chromosomesare those brought together followinginter-species hybridizationandallopolyploidization,and whose relationship was completely homologous in an ancestral species. For example,durum wheatis the result of the inter-species hybridization of two diploid grass speciesTriticum urartuandAegilops speltoides.Both diploid ancestors had two sets of 7 chromosomes, which were similar in terms of size and genes contained on them. Durum wheat contains ahybrid genomewith two sets of chromosomes derived fromTriticum urartuand two sets of chromosomes derived fromAegilops speltoides.Each chromosome pair derived from theTriticum urartuparent ishomoeologousto the opposite chromosome pair derived from theAegilops speltoidesparent, though each chromosome pair unto itself ishomologous.

Examples

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Animals

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Examples in animals are more common in non-vertebrates[50]such asflatworms,leeches,andbrine shrimp.Within vertebrates, examples of stable polyploidy include thesalmonidsand manycyprinids(i.e.carp).[51]Some fish have as many as 400 chromosomes.[51]Polyploidy also occurs commonly in amphibians; for example the biomedically important genusXenopuscontains many different species with as many as 12 sets of chromosomes (dodecaploid).[52]Polyploid lizards are also quite common. Most are sterile and reproduce byparthenogenesis;[citation needed]others, likeLiolaemus chiliensis,maintain sexual reproduction. Polyploidmole salamanders(mostly triploids) are all female and reproduce bykleptogenesis,[53]"stealing"spermatophoresfrom diploid males of related species to trigger egg development but not incorporating the males' DNA into the offspring.

While some tissues of mammals, such asparenchymalliver cells, are polyploid,[54][55]rare instances of polyploidmammalsare known, but most often result inprenataldeath. AnoctodontidrodentofArgentina's harshdesertregions, known as theplains viscacha rat(Tympanoctomys barrerae) has been reported as an exception to this 'rule'.[56]However, careful analysis using chromosome paints shows that there are only two copies of each chromosome inT. barrerae,not the four expected if it were truly a tetraploid.[57]This rodent is not arat,but kin toguinea pigsandchinchillas.Its "new" diploid (2n) number is 102 and so its cells are roughly twice normal size. Its closest living relation isOctomys mimax,theAndeanViscacha-Rat of the same family, whose 2n= 56. It was therefore surmised that anOctomys-like ancestor produced tetraploid (i.e., 2n= 4x= 112) offspring that were, by virtue of their doubled chromosomes, reproductively isolated from their parents.

Polyploidy was induced in fish byHar Swarup(1956) using a cold-shock treatment of the eggs close to the time of fertilization, which produced triploid embryos that successfully matured.[58][59]Cold or heat shock has also been shown to result in unreduced amphibian gametes, though this occurs more commonly in eggs than in sperm.[60]John Gurdon(1958) transplanted intact nuclei from somatic cells to produce diploid eggs in the frog,Xenopus(an extension of the work of Briggs and King in 1952) that were able to develop to the tadpole stage.[61]The British scientistJ. B. S. Haldanehailed the work for its potential medical applications and, in describing the results, became one of the first to use the word "clone"in reference to animals. Later work byShinya Yamanakashowed how mature cells can be reprogrammed to become pluripotent, extending the possibilities to non-stem cells. Gurdon and Yamanaka were jointly awarded the Nobel Prize in 2012 for this work.[61]

Humans

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Schematickaryogramof a human, showing the normaldiploid(that is, non-polyploid)karyotype.It shows 22homologous chromosomes,both the female (XX) and male (XY) versions of thesex chromosome(bottom right), as well as themitochondrial genome(to scale at bottom left).
Further information:Karyotype
Further information:Triploid syndrome

True polyploidy rarely occurs in humans, although polyploid cells occur in highlydifferentiatedtissue, such as liverparenchyma,heart muscle, placenta and in bone marrow.[62][63]Aneuploidyis more common.

Polyploidy occurs in humans in the form oftriploidy,with 69 chromosomes (sometimes called 69, XXX), and tetraploidy with 92 chromosomes (sometimes called 92, XXXX). Triploidy, usually due topolyspermy,occurs in about 2–3% of all human pregnancies and ~15% of miscarriages.[citation needed]The vast majority of triploid conceptions end as amiscarriage;those that do survive to term typically die shortly after birth. In some cases, survival past birth may be extended if there ismixoploidywith both adiploidand a triploid cell population present. There has been one report of a child surviving to the age of seven months with complete triploidy syndrome. He failed to exhibit normal mental or physical neonatal development, and died from aPneumocystis cariniiinfection, which indicates a weak immune system.[64]

Triploidy may be the result of eitherdigyny(the extra haploid set is from the mother) ordiandry(the extra haploid set is from the father). Diandry is mostly caused by reduplication of the paternal haploid set from a single sperm, but may also be the consequence of dispermic (two sperm)fertilizationof the egg.[65]Digyny is most commonly caused by either failure of one meiotic division during oogenesis leading to a diploidoocyteor failure to extrude onepolar bodyfrom theoocyte.Diandry appears to predominate among earlymiscarriages,while digyny predominates among triploid zygotes that survive into the fetal period.[66]However, among early miscarriages, digyny is also more common in those cases less than8+1⁄2weeks gestational age or those in which an embryo is present. There are also two distinctphenotypesin triploidplacentasandfetusesthat are dependent on the origin of the extrahaploidset. In digyny, there is typically an asymmetric poorly grownfetus,with markedadrenalhypoplasiaand a very smallplacenta.[67]In diandry, a partialhydatidiform moledevelops.[65]These parent-of-origin effects reflect the effects ofgenomic imprinting.[citation needed]

Complete tetraploidy is more rarely diagnosed than triploidy, but is observed in 1–2% of early miscarriages. However, some tetraploid cells are commonly found in chromosome analysis atprenatal diagnosisand these are generally considered 'harmless'. It is not clear whether these tetraploid cells simply tend to arise duringin vitrocell culture or whether they are also present in placental cellsin vivo.There are, at any rate, very few clinical reports of fetuses/infants diagnosed with tetraploidy mosaicism.

Mixoploidyis quite commonly observed in human preimplantation embryos and includes haploid/diploid as well as diploid/tetraploid mixed cell populations. It is unknown whether these embryos fail to implant and are therefore rarely detected in ongoing pregnancies or if there is simply a selective process favoring the diploid cells.

Fish

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A polyploidy event occurred within the stem lineage of theteleostfish.[47]

Plants

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Speciationvia polyploidy: Adiploidcell undergoes failedmeiosis,producing diploidgametes,which self-fertilize to produce a tetraploidzygote.

Polyploidy is frequent in plants, some estimates suggesting that 30–80% of living plant species are polyploid, and many lineages show evidence of ancient polyploidy (paleopolyploidy) in their genomes.[68][69][70][71]Huge explosions inangiospermspecies diversity appear to have coincided with the timing of ancient genome duplications shared by many species.[72]It has been established that 15% of angiosperm and 31% of fernspeciationevents are accompanied by ploidy increase.[73]

Polyploid plants can arise spontaneously in nature by several mechanisms, including meiotic or mitotic failures, and fusion of unreduced (2n) gametes.[40]Both autopolyploids (e.g. potato[74]) and allopolyploids (such as canola, wheat and cotton) can be found among both wild and domesticated plant species.

Most polyploids display novel variation or morphologies relative to their parental species, that may contribute to the processes ofspeciationand eco-niche exploitation.[69][40]The mechanisms leading to novel variation in newly formed allopolyploids may include gene dosage effects (resulting from more numerous copies of genome content), the reunion of divergent gene regulatory hierarchies, chromosomal rearrangements, andepigeneticremodeling, all of which affect gene content and/or expression levels.[75][76][77][78]Many of these rapid changes may contribute to reproductive isolation and speciation. However, seed generated frominterploidy crosses,such as between polyploids and their parent species, usually have aberrant endosperm development which impairs their viability,[79][80]thus contributing topolyploid speciation.Polyploids may also interbreed with diploids and produce polyploid seeds, as observed in the agamic complexes ofCrepis.[81]

Some plants are triploid. Asmeiosisis disturbed, these plants are sterile, with all plants having the same genetic constitution: Among them, the exclusively vegetatively propagatedsaffron crocus(Crocus sativus). Also, the extremely rare Tasmanian shrubLomatia tasmanicais a triploid sterile species.

There are few naturally occurring polyploidconifers.[82]One example is the Coast RedwoodSequoia sempervirens,which is a hexaploid (6x) with 66 chromosomes (2n= 6x= 66), although the origin is unclear.[83]

Aquatic plants, especially theMonocotyledons,include a large number of polyploids.[84]

Crops

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The induction of polyploidy is a common technique to overcome the sterility of a hybrid species during plant breeding. For example,triticaleis the hybrid ofwheat(Triticum turgidum) andrye(Secale cereale). It combines sought-after characteristics of the parents, but the initial hybrids are sterile. After polyploidization, the hybrid becomes fertile and can thus be further propagated to become triticale.

In some situations, polyploid crops are preferred because they are sterile. For example, many seedless fruit varieties are seedless as a result of polyploidy. Such crops are propagated using asexual techniques, such asgrafting.

Polyploidy in crop plants is most commonly induced by treating seeds with the chemicalcolchicine.

Examples
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Some crops are found in a variety of ploidies:tulipsandliliesare commonly found as both diploid and triploid;daylilies(Hemerocalliscultivars) are available as either diploid or tetraploid; apples andkinnow mandarinscan be diploid, triploid, or tetraploid.

Fungi

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Besides plants and animals, the evolutionary history of variousfungal speciesis dotted by past and recent whole-genome duplication events (see Albertin and Marullo 2012[88]for review). Several examples of polyploids are known:

In addition, polyploidy is frequently associated withhybridizationand reticulate evolution that appear to be highly prevalent in several fungal taxa. Indeed,homoploid speciation(hybrid speciation without a change inchromosomenumber) has been evidenced for some fungal species (such as thebasidiomycotaMicrobotryum violaceum[96]).

Schematic phylogeny of the Chromalveolata. Red circles indicate polyploidy, blue squares indicate hybridization. From Albertin and Marullo, 2012[88]

As for plants and animals, fungal hybrids and polyploids display structural and functional modifications compared to their progenitors and diploid counterparts. In particular, the structural and functional outcomes of polyploidSaccharomycesgenomes strikingly reflect the evolutionary fate of plant polyploid ones. Large chromosomal rearrangements[97]leading tochimericchromosomes[98]have been described, as well as more punctual genetic modifications such as gene loss.[99]The homoealleles of the allotetraploid yeastS. pastorianusshow unequal contribution to thetranscriptome.[100]Phenotypicdiversification is also observed following polyploidization and/or hybridization in fungi,[101]producing the fuel fornatural selectionand subsequentadaptationand speciation.

Chromalveolata

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Other eukaryotictaxahave experienced one or more polyploidization events during their evolutionary history (see Albertin and Marullo, 2012[88]for review). Theoomycetes,which are non-true fungi members, contain several examples of paleopolyploid and polyploid species, such as within the genusPhytophthora.[102]Some species of brownalgae(Fucales,Laminariales[103]anddiatoms[104]) contain apparent polyploid genomes. In theAlveolatagroup, the remarkable speciesParameciumtetraureliaunderwent three successive rounds of whole-genome duplication[105]and established itself as a major model for paleopolyploid studies.

Bacteria

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EachDeinococcus radioduransbacteriumcontains 4-8 copies of itschromosome.[106]Exposure ofD. radioduranstoX-rayirradiation ordesiccationcan shatter itsgenomesinto hundred of short random fragments. Nevertheless,D. radioduransis highly resistant to such exposures. The mechanism by which the genome is accurately restored involves RecA-mediatedhomologous recombinationand a process referred to as extendedsynthesis-dependent strand annealing (SDSA).[107]

Azotobacter vinelandiican contain up to 80 chromosome copies per cell.[108]However this is only observed in fast growing cultures, whereas cultures grown in synthetic minimal media are not polyploid.[109]

Archaea

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ThearchaeonHalobacterium salinariumis polyploid[110]and, likeDeinococcus radiodurans,is highly resistant to X-ray irradiation and desiccation, conditions that induceDNAdouble-strand breaks.[111]Although chromosomes are shattered into many fragments, complete chromosomes can be regenerated by making use of overlapping fragments. The mechanism employs single-strandedDNA binding proteinand is likelyhomologous recombinationalrepair.[112]

See also

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References

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Further reading

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Look upmesopolyploidin Wiktionary, the free dictionary.
Look upneopolyploidin Wiktionary, the free dictionary.
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