natural pathways to polyploidy in plants and cosequences for genome reorganization

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Natural Pathways to Polyploidy and Consequences forGenome Organization and Genome Size

Cytogenet Genome Res 2013;140:7996

DOI: 10.1159/000351318

Natural Pathways to Polyploidy inPlants and Consequences for GenomeReorganization

A. Tayal C. Parisod

Laboratory of Evolutionary Botany, Institute of Biology, University of Neuchtel, Neuchtel, Switzerland

incompatibilities through non-Mendelian mechanisms, fos-

tering polyploid genome reorganization in association with

the establishment of new lineages. See also sister article fo-

cusing on animals by Collares-Pereira et al., in this themed

issue. Copyright 2013 S. Karger AG, Basel

Polyploidy (i.e. the merging of more or less divergentgenomes associated with whole genome duplication) isan important factor in eukaryote evolution [Lynch, 2007;Otto, 2007]. For instance, it is now clear that all floweringplants have gone through at least one round of polyploidy[Jiao et al., 2011]. Polyploidy long remained a favoredtopic of evolutionary studies in plants [Muntzing, 1936;Clausen et al., 1945; Stebbins, 1971; Grant, 1981; Levin,

2002; Comai, 2005; Doyle et al., 2008; Leitch and Leitch,2008; Parisod et al., 2010a; Soltis and Soltis, 2012], al-though several animal taxa are known to contain poly-ploid forms [Otto and Whitton, 2000; Mable et al., 2011].Cross-talk between these traditional fields as promotedby this issue is expected to foster advances in our under-standing of the potential advantages and disadvantages ofbeing polyploid.

Key Words

Chromosome pairing Dobzhansky-Muller incompatibility

Hybrid dysregulation Genome evolution Genome

merging Genome restructuring Speciation Transposable

elements Unreduced gametes Whole genome doubling

Abstract

The last decade highlighted polyploidy as a rampant evolu-

tionary process that triggers drastic genome reorganization,

but much remains to be understood about their causes and

consequences in both autopolyploids and allopolyploids.

Here, we provide an overview of the current knowledge on

the pathways leading to different types of polyploids and

patterns of polyploidy-induced genome restructuring and

functional changes in plants. Available evidence leads to a

tentative diverge, merge and diverge model supportingpolyploid speciation and stressing patterns of divergence

between diploid progenitors as a suitable predictor of poly-

ploid genome reorganization. The merging of genomes at

the origin of a polyploid lineage may indeed reveal different

kinds of incompatibilities (chromosomal, genic and trans-

posable elements) that have accumulated in diverging pro-

genitors and reduce the fitness of nascent polyploids. Ac-

cordingly, successful polyploids have to overcome these

Published online: June 8, 2013

Christian ParisodUniversity of NeuchtelRue Emile-Argand 11CH2000 Neuchtel (Switzerland)E-Mail christian.parisod @ unine.ch

2013 S. Karger AG, Basel14248581/13/14040079$38.00/0

www.karger.com/cgr
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The last decade has shown a renewed interest in exam-ining and integrating the consequences of polyploidy indifferent organisms to shed light on this rampant evolu-tionary process. Here, we provide an overview of the cur-rent knowledge on the origins of polyploids and theirconsequences for genome organization in plants. We willfirst describe the different types of polyploids and thepathways leading to their formation. Then, we will ex-pand on observed patterns of polyploidy-induced ge-nome changes and explore their possible causes and con-sequences for the establishment of new polyploid line-ages. As a whole, we highlight evidence supporting theemergence of a model stressing divergence between dip-

loid progenitors as a suitable predictor of genome reorga-nization after polyploidization. The merging of genomesat the origin of polyploid lineages indeed reveals differentkinds of incompatibilities that have accumulated duringprogenitor divergence and that reduce the fitness of na-scent polyploids. Accordingly, successful polyploids haveto overcome these incompatibilities through non-Men-delian mechanisms, fostering specific genome changesgoing along with their establishment.

Paleo- versus Neopolyploids and Auto- versus

Allopolyploids

Polyploidy may be a confusing term because of bothchanging terminologies and recent paradigm shifts. Inparticular, the last decade unraveled the considerable ge-

netic redundancy presented by plant genomes and high-lighted the highly dynamic nature of polyploid genomes[Soltis and Soltis, 2012]. Genome reorganization, involv-ing drastic restructuring and functional alterations in as-sociation with polyploidy, is commonly referred to asdiploidization and generally restores a secondary diploid-like behavior of polyploid genomes. Accordingly, a tem-poral distinction between paleopolyploids (i.e. ancientpolyploids with diploidized genomes) and neopolyploids(i.e. young polyploids without diploidized genomes)seems useful [Blanc and Wolfe, 2004]. This review ismainly focused on neopolyploids, including both experi-

mental (i.e. synthetic) and naturally formed (i.e. nascentor established) polyploids. Nascent, established and pa-leo-polyploids hardly represent clear-cut categories, butmay highlight stages in the evolution of polyploid lineag-es likely driven by contrasting processes.

The classification of neopolyploids into 2 main categ-ories (fig. 1) based on their origin is still controversial[Clausen et al., 1945; Ramsey and Schemske, 1998]. Au-topolyploids are generally considered to have arisen with-in or among populations of a single species by the dou-bling of structurally similar, homologous chromosomesets (AAAA), whereas allopolyploids typically involve in-terspecific hybridization associated with the doubling ofnon-homologous (i.e. homeologous) chromosome sets(AABB). To account for natural hybrid polyploids form-ing multivalents, Stebbins [1947] defined inter-racial au-topolyploids or segmental allopolyploids to denote thedoubling of partially differentiated genomes (AAAA). Itis now widely accepted that polyploidy encompasses acontinuum from the doubling of identical genomes to thedoubling of highly differentiated genomes (fig. 1). Ac-cordingly, all natural polyploids likely consist of more orless divergent genomes having been merged at their ori-

gin.The most obvious characteristic which may distin-guish types of polyploids is the pairing behavior of thechromosomes in meiosis [Jackson, 1982]. Autopoly-ploids have multiple homologous chromosomes andthus mainly form multivalents, while allopolyploidsform predominantly bivalents as homeologous chromo-somes do not regularly pair [Ramsey and Schemske,2002]. Chromosome pairing is, however, affected by sev-

Fig. 1.Natural pathways to polyploidy. The origin of both autotet-raploids and allotetraploids involve the merging of more or lessdivergent diploid genomes through the formation of diploid (i.e.homoploid bridge), triploid (i.e. unilateral pathway) or tetraploid(i.e. bilateral pathway) hybrids. Spontaneous somatic chromo-some doubling is assumed to be rare (dashed arrows). Recentlyformed neopolyploids go through a phase of intense genome reor-ganization (figured by changing colors) referred to as diploidiza-tion and leading to the evolution of paleopolyploids.


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eral factors and predominant bivalent pairing in auto-polyploids or multivalent pairing in polyploids of hybridorigin is reported [Jenczewski and Alix, 2004; Otto,2007]. Patterns of chromosome pairing may thus be amisleading criterion to classify polyploids. Accordingly,a classification of polyploid based on patterns of segrega-

tion should be preferred [Soltis et al., 2007; Parisod et al.,2010a]. Autopolyploids indeed present 4 homologouschromosomes that can randomly pair at meiosis, even ifstrictly forming bivalents, resulting in random segrega-tion of chromosomes or chromatids and leading to poly-somic inheritance with possible double reduction [Jack-son and Jackson, 1996; Hauber et al., 1999; Landergott etal., 2006; Stift et al., 2008]. This results in the productionof homozygotes and different types of partial heterozy-gotes (AAAa, AAaa, Aaaa for a tetraploid locus with 2alleles [Bever and Felber, 1992; Ronfort et al., 1998;Butruille and Boiteux, 2000; Luo et al., 2006]). Polysomic

inheritance occurs even if homologous chromosomesregularly pair as bivalents and thus is the key criteriondistinguishing auto- from allopolyploid taxa [Soltis et al.,2007; Parisod et al., 2010a]. Noticeably, polysomic in-heritance may represent a transient segregation patternin neoautopolyploids and evolve toward disomic inheri-tance with ongoing diploidization. Accordingly, the dis-tinction between auto- and allopolyploids would beblurred in paleopolyploids.

Natural Pathways at the Origins of Polyploids

Somatic Doubling versus Merging of UnreducedGametesSeveral pathways involving the spontaneous doubling

of chromosome sets in somatic cells and the reunion ofunreduced gametes support the formation of new poly-ploid lineages in plants (fig. 1). Such different pathwaysdo not seem to be equally frequent in nature [reviewed inthe meta-analysis of Ramsey and Schemske, 1998].

Mitotic nondisjunction supporting spontaneous dou-bling of chromosomes can occur throughout the life cycle

of a plant and may result in mixoploid organisms poten-tially at the origin of polyploid meristematic cells that ul-timately lead to a new polyploid organism (e.g. Primulakewensis [Grant, 1981]). Little is known about the fre-quency of spontaneous chromosome doubling, particu-larly after events such as interspecific hybridization orstress conditions [Lewis, 1980; Ramsey and Schemske,1998]. Somatic doubling is commonly performed to pro-duce synthetic polyploids supposed to mimic established

ones but is estimated to be a relatively minor pathway topolyploidy in natural populations.

Unreduced gametes (i.e. diplogametes) are producedat a much higher rate than previously assumed and maybe involved in the major pathways leading to polyploidy[Bretagnolle and Thompson, 1995; Otto and Whitton,

2000]. Several mechanisms resulting in the production ofunreduced gametes have been identified in a variety ofplant taxa [reviewed in Bretagnolle and Thompson, 1995;Brownfield and Khler, 2011]. The production of diplo-gametes is highly variable among and within species, andhas been estimated at 0.56% in non-hybrid floweringplants [Ramsey and Schemske, 1998]. Diplogametes seemto be more frequent under environmental stresses, suchas frost, wounding, herbivory, water or nutrient shortage[e.g. Mason et al., 2011]. Noticeably, hybrids between di-vergent genomes present up to a 50-fold increase in theproduction of unreduced gamete as compared to non-

hybrid systems [e.g. Zhang et al., 2010]. In addition, theproduction of diplogametes appears to be heritable andgoverned by a few genes [dErfurth et al., 2008; Zhang etal., 2010]. However, the molecular basis underlying theformation of unreduced gamete begins to be unraveled,but much remains to be understood [Brownfield andKhler, 2011].

Given their high rate of production, the union of un-reduced gametes likely supports the origin of both auto-and allopolyploids under natural conditions (fig. 1). Suchevents seem frequently enough to form polyploid at anestimated rate (105for autotetraploids and 104for allo-tetraploids) comparable with the one of genic mutations[Ramsey and Schemske, 1998]. Recent work having esti-mated the rate of polyploid formation in natural popula-tions matched these expectations [Ramsey, 2007], but ad-ditional empirical studies assessing the frequency of thedifferent pathways to polyploidy are needed.

Unreduced Gametes: Unilateral versus BilateralPolyploidizationGiven the low probability of uniting 2 unreduced gam-

etes in a single step (i.e. bilateral polyploidization), the

formation of tetraploids has early been anticipated asbeing mostly indirect, involving triploid intermediates(triploid bridge supporting unilateral polyploidization;fig. 1) [Harlan and DeWet, 1975]. Triploid individualsare indeed observed at low frequency in natural popula-tions and easily obtained experimentally [Ramsey andSchemske, 1998]. The fusion of a reduced with an unre-duced gamete is expected to produce triploids that can inturn generate tetraploids through selfing or crossing with


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other triploids or diploid progenitors. The establishmentof tetraploids would thus critically depend on (i) the rateof triploid formation, (ii) the fitness of triploids and (iii)the ploidy level of the functional gametes produced bytriploids [Husband, 2004].

Triploidy has long been considered detrimental as

triploid seeds may early abort (i.e. triploid block) [Brinkand Cooper, 1947]. The endosperm (i.e. the tissue, madeof one paternal and 2 maternal genomes, surroundingand providing nutrients to the embryo) indeed seemssensitive to dosage of parental genes and may fail to prop-erly develop in polyploids with misbalanced chromo-some sets. Such emphasis on the endosperm is consistentwith the reduced triploid block observed in species pre-senting a reduced endosperm [Ramsey and Schemske,1998; Husband, 2004]. Successive models based on therelative ploidy of seed tissues have been developed to ac-count for triploid seed production despite triploid block

[Muntzing, 1930; Johnston et al., 1980; Lin, 1984]. Khleret al., [2010] recently pointed out that failure of endo-sperm development in both homoploid and interploidhybrids might be associated with differently imprintedgenes of the Polycomb group. Accordingly, parental di-vergence and/or ratios of paternal versus maternal dosagewould result in unbalanced interactions between globaltranscriptional repressors of the Polycomb group andtheir targets (i.e. homeotic genes and downstream genesas well as transposable elements), leading to a crash of theendosperm in triploids. Uncertainties about links be-tween these mechanisms and expected incompatibilitiesreducing fitness remain. However, viable triploids pre-sent unexpected fertility. A mean pollen fertility of 31.9%has indeed been reported in triploid Angiosperms byRamsey and Schemske [1998]. Triploids indeed producea relatively large amount of viable, euploid gametes (n =x, 2x, 3x), regardless of their auto- or allopolyploid originand may thus strongly impact on the formation of poly-ploids [Husband, 2004]. However, additional insights onthe influence of triploid intermediates on the origin ofpolyploids in natural populations, particularly in primarycontact zones between diploids and tetraploids, would be

valuable.Tetraploids can be formed without triploid intermedi-ates through either homoploid hybrids (i.e. homoploidbridge) or the direct union of 2 diplogametes (i.e. bilat-eral polyploidization; fig. 1). Hybrids seem to present anincreased production of diplogametes as shown by theaverage 27% reported in hybrid systems as compared to5.6% in non-hybrid systems [Ramsey and Schemske,1998]. Accordingly, homoploid hybrids could be ex-

pected to sustain polyploidization [Rieseberg and Wil-lis, 2007]. Hybrids can also be directly polyploid whenformed through bilateral polyploidization. This pathwayhas been reported at the origin of both auto- and allotet-raploid taxa [Ramsey and Schemske, 1998; Husband,2004]. Plants producing particularly high levels of diplo-

gametes may indeed foster bilateral polyploidization, es-pecially in the case of self-fertilizing individuals [Breta-gnolle and Thompson, 1995; Bretagnolle, 2001].

Based on extensive data [analyzed in Ramsey andSchemske, 1998], bilateral polyploidization is estimatedto produce polyploids at a rate almost similar to unilat-eral polyploidization. However, the frequency of sponta-neous somatic doubling at the origin of natural auto- andallopolyploids should be further empirically estimated.Accordingly, the concluding remark of Ramsey andSchemske [1998] that comprehensive examination of thepathways, mechanisms and rate of polyploid formation

in natural populations remains largely appropriate.

Multiple Origins and Multiple Pathways ProduceVariable PolyploidsPolyploidy has long been considered exceptional with

polyploid species typically being monophyletic andgenetically depauperate [Ehrendorfer, 1980; Favarger,1984]. Multiple origin of polyploid species is now consid-ered the rule rather than the exception [Soltis and Soltis,1999]. It has been demonstrated for several allopolyploids[Wendel and Cronn, 2003; Abbott and Lowe, 2004; Soltiset al., 2004; Arrigo et al., 2010] and autopolyploids [Shore,1991; Segraves et al., 1999; Soltis and Soltis, 1999; Parisodand Besnard, 2007], despite notable exceptions such asArabidopsis suecica[Jakobsson et al., 2006] or Draba ladi-na [Widmer and Baltisberger, 1999]. Noticeably, multipleorigins may occur over restricted geographical distribu-tions and/or short evolutionary timescales as illustratedby the allopolyploid Tragopogon miscellusthat formed atleast 21 times independently during the last 5060 years[Soltis et al., 2012].

Multiple origins of polyploids may involve geneticallyand morphologically differentiated parents, and may re-

sult in considerable genetic and phenotypic variability aswell as variable nuclear or nucleo-cytoplasmic interac-tions at the polyploid level [Soltis and Soltis, 1999; Wen-del, 2000; Mable, 2003]. Adding to such complexity,independent polyploid lineages may have originatedthrough varied pathways, multiplying interactions amonggenomes. Although likely, this hypothesis has apparentlynot been tested yet. Finally, independently formed poly-ploid lineages may further hybridize [e.g. Modliszewski


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and Willis, 2012]. Accordingly, the evolutionary historyof a given polyploid taxon may be much more complexthan usually assumed and hardly disentangled. In par-ticular, the multifarious origin of current lineages, to-gether with genome reorganization (see below), certainlyparticipates in the evolution of highly variable polyploid

gene pools.

Patterns of Genome Changes after Polyploidization

The last decade revealed that polyploidization triggersgenome changes highlighted as departure from the pre-dicted additivity of parental genomes in polyploids. Thus,polyploidy has been compared to a genome shock induc-ing drastic genome reorganization [reviewed in Comai,2005; Doyle et al., 2008; Leitch and Leitch, 2008]. Genomechanges have early been categorized based on their ge-

netic or epigenetic nature and their impact on eitherstructural or functional genomic traits (fig. 2; table 1).The timing of such genome reorganization further distin-guishes short-term revolutionary changes observed in thefirst few generations following polyploidization and thelong-term evolutionary changes taking place during thelifespan of the polyploid lineage [Feldman et al., 2012].

Genome Restructuring following PolyploidizationGenome restructuring events including DNA se-

quence loss, amplification or reduction of repetitive se-quences, or large chromosome repatterning involving de-letion, insertion, inversion, translocation of chromosom-al segments has been reported following polyploidy inseveral systems (see table 1 for references). Despite drasticrestructuring reported in both the short- and the long-term in several polyploids (see Brassica,Nicotiana, Trago-pogonor Triticum), a couple of counter examples revealedlimited structural changes (see Gossypiumor Spartina).Rapid loss of DNA sequences is common after polyploidyand genome downsizing seems to be a general responseto both auto- and allopolyploidy [Leitch and Bennett,2004; Eilam et al., 2010; Yang et al., 2011]. Nevertheless,

some studies reported no DNA loss [Ozkan et al., 2006;Mestiri et al., 2010; Zhao et al., 2011] or genome expan-sion [Leitch et al., 2008]. Large genome rearrangementssuch as inversion, translocation, deletion or aneuploidyhave been reported in autopolyploids (seeArabidopsisorGoldbachia) and allopolyploids (see Brassica,Nicotianaor Tragopogon). Several studies highlighted a biased re-structuring towards either the paternal (e.g. Nicotiana) orthe maternal (e.g. Spartina) subgenomes.

Functional Changes following PolyploidizationNumerous studies highlighted changes in epigenetic

patterning and gene expression in both synthetic and es-tablished polyploids (see table 1 for references). Reportsfrom both synthetic and established polyploids indicatethat functional changes occur quickly and are reproduc-

ible to a large extent (e.g. Brassica,Tragopogonor Triti-cum). Noticeably, methylation changes and expression ofthe alleles originating from one of the parental genome(i.e. expression bias) or changing expression towards thelevels of one of the parental (i.e. expression dominance)is commonly reported [Grover et al., 2012; Soltis et al.,2012; Wendel et al., 2012]. However, limited changes inmethylation patterns and gene expression have been re-ported in specific allopolyploids as well [e.g. Mestiri et al.,

Fig. 2.Commonly reported genome changes after polyploidization(case studies reviewed in table 1). Additive effects refer to changesin the dosage of genes and the level of heterozygosity in polyploidsas compared to diploids. Polyploids usually show nonadditivechanges (i.e. genome reorganization) including both restructuringevents and functional modifications. Duplicated genes can gothrough either diversification via subfunctionalization and neo-functionalization or, in contrast, conversion via nonreciprocal ho-meologous exchanges. Genome restructuring can involve chro-mosomal rearrangements (e.g. translocations, inversions), loss ofsequences and amplification of repetitive sequences such as trans-posable elements. Functional changes can occur without modifica-tions of the nucleotide sequence through epigenetic changes, in-

volving methylation repatterning and other types of chromatin

remodeling. Transposable elements may play a pivotal role duringgenome reorganization, inducing both restructuring and epige-netic changes at a genome-wide scale. *= methylated site.


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2010; Kovarik et al., 2012]. Few studies focused on auto-polyploids (e.g.Arabidopsis,Brassicaor Helianthus), butusually reported fewer changes than in allopolyploids[Parisod et al., 2010a]. Much remains to be understoodabout mechanisms such as new interactions between reg-ulatory networks and small RNAs that may account for

changing gene expression and methylation patterns inpolyploids [Madlung and Wendel, this issue].

Activation of Transposable Elements followingPolyploidizationThe parasitic biology of transposable elements inhab-

iting genomes makes them prone to play a pivotal role inthe changes affecting polyploid genomes [Fedoroff,2012]. Polyploidy indeed seems to immediately activatespecific transposable elements [Parisod et al., 2010b]. Al-though such activation does not necessarily translate in(bursts of) transposition, these repetitive sequences are

intimately associated with genome restructuring as wellas epigenetic changes at a genome-wide scale (see table 1for references). Some studies reported amplification ofspecific transposable elements in natural polyploids (e.g.Nicotiana tabacum), whereas a majority of polyploid ge-nomes seem to have specifically eliminated these repeti-tive sequences from either the maternal or parental ge-nome (e.g. Spartina,Triticum). Immediate methylationchanges were specifically reported in the vicinity of inser-tions of transposable elements and may thus interfere di-rectly or indirectly with gene expression [Kashkush et al.,2003; Slotkin and Martienssen, 2007; Parisod et al., 2009].Not much is known about the role of transposable ele-ments on the long-term differentiation of polyploid ge-nomes, but their intense dynamics in allopolyploids Ni-cotiana section Repandaeassociated with genome turn-over within 5 million years suggest that repetitive elementsmay be central to the diploidization process [Lim et al.,2007; Parisod et al., 2012].

Genome Reorganization in Polyploids: A CommonTheme?Studies that assessed both synthetic and established

polyploids suggest rapid genome reorganization (i.e. re-structuring and/or functional changes) after the polyploi-dy event, with further changes accumulating over evolu-tionary time [see e.g. Feldman et al., 2012]. General pat-terns hardly emerge yet, and additional work assessingthe level and the timing of genome changes across thepolyploidy continuum is required. In particular, fewstudies assessed synthetic autopolyploids mimicking es-tablished ones [Parisod et al., 2010a].

Mechanisms of genome reorganization (fig. 2) are pos-sibly interconnected through cause-and-effect relation-ships, with restructuring events potentially having func-tional effects. Furthermore, activation of transposable el-ements likely impacts the structure and the functioningof polyploid genomes. As several studies in various spe-

cies highlighted reproducible changes after independentpolyploidization events, such particular modificationsmay be selected for, but this remains to be tested. Also, towhat extent immediate genome changes support ge-nome-wide diploidization in the longer term should befurther assessed. A better understanding of the originsand consequences of genome reorganization may lead toheuristic categories of the polyploidy-induced molecularchanges.

Origins and Consequences of Polyploidy-Induced

Genome Reorganization

The formation of polyploid lineages involves the merg-ing of more or less divergent genomes, potentially unitingincompatible loci that accumulated during the differen-tiation of the progenitors and resulting in hybrid sterilityor inviability [Stebbins, 1958; Rieseberg, 2001b]. As in-compatible chromosomal or genic combinations are un-likely to be purged through segregation in polyploids,non-Mendelian mechanisms involving genome doublingper se, genome restructuring and/or epigenetic changesmay thus help restoring the fitness of the nascent poly-ploid [Rieseberg, 2001a].

Chromosomal Incompatibilities and Proper MeioticPairingThe merging of structurally divergent genomes induc-

es troubles at meiosis when homeologuous chromosomesdo not pair properly in the F1 hybrids (i.e. chromosomalincompatibility [Rieseberg, 2001b; Grandant et al., thisissue]). Accordingly, loosely paired chromosomes segre-gate randomly, resulting in increased frequencies of non-functional gametes and thus sterility (fig. 3A). In this

context, whole genome duplication is restoring the fertil-ity of hybrids between taxa with structurally divergent ge-nomes, furnishing the exact complements to all chromo-somes and allowing proper meiotic pairing. Unless chro-mosomal rearrangements further harbor genic incom-patibilities [Noor and Feder, 2006; Maheshwari andBarbash, 2011], chromosomal divergence between dip-loid taxa thus likely promotes the origin of polyploid lin-eages as whole genome duplication provides pairing part-


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ners to all chromosomes in hybrids and may restore their

fertility [Rieseberg and Willis, 2007; Buggs et al., 2011].Homeologous chromosomes likely display similarchromosomal regions resulting in improper pairing atmeiosis and promoting intergenomic recombination andchromosomal rearrangements [Gaeta and Pires, 2010].The processes governing meiotic pairing are not fully un-derstood yet [Stewart and Dawson, 2008], but structuralfeatures as well as specific genetic factors, such as the Ph1gene in wheat, are expected to promote homologous pair-

ing [Jenczewski and Alix, 2004; Griffiths et al., 2006]. Ac-

tivation of DNA recombination/repair pathways is sug-gested to efficiently correct non-homologous recombina-tion in synthetic auto- and allotetraploids [Wang et al.,2004]. Restructuring events in improperly paired regionsof the chromosomes may thus sustain the differentiationof homeologous chromosomes and promote strict biva-lent pairing (i.e. homologous recombination) during thefirst generations of the diploidization process [Ma andGustafson, 2005]. This is consistent with the elimination

Fig. 3. Mechanisms of genetic incompati-

bilities in hybrids. AStructural incompati-bilities (here, an inversion marked by ar-rows) leading to hybrid sterility. B, CGenicincompatibilities accumulated between di-

vergent genomes leading to dysfunctionalhybrids. DMismatch between transposableelements and their repressors (siRNAs)leading to the activation of transposable el-ements in hybrids (i.e. hybrid dysgenesis).


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of sequences from homoeologous chromosome regionsin both auto- and allopolyploids during cytological dip-loidization [Eilam et al., 2009, 2010; Feldman et al., 2012].Nevertheless, the hypothesis that restructuring is adap-tive, improving the fertility of neopolyploids, largely re-mains to be tested.

Genic Incompatibilities and Their PurgingHybridization and genome doubling at the origin of

polyploid lineages produces new combinations of inter-acting genes and, thereby, may reveal genic incompatibil-ities as well as new gene dosage configurations reducingthe hybrid fitness [Maheshwari and Barbash, 2011]. Themodel of Dobzhansky-Muller interactions (fig. 3B) offersthe classical framework to understand genic incompati-bilities reducing hybrid fitness due to dysfunctional inter-actions among neutrally or adaptively accumulated al-leles at one or several loci [Coyne and Orr, 2004]. Alter-

native models, such as the mutation-rescue model, mayalso explain genic incompatibilities, including nucleo-cy-toplasmic interactions [reviewed in Nei and Nozawa,2011].

In the context of polyploid speciation, whole genomeduplication will not alleviate the effect of genic incompat-ibilities revealed by genome merging. Accordingly, a na-scent polyploid will suffer from reduced fitness, and itsgenome has to be rapidly purged from incompatible locito establish a successful lineage. As loci affecting the via-bility of both the hybrid and its gametes (i.e. hybrid fer-tility) can hardly be eliminated through segregation ina polyploid, molecular events such as sequence loss ormethylation changes may, therefore, be involved as majormechanisms eliminating or silencing genic incompatibil-ities [Rieseberg, 2001a]. Adaptive processes may thuspartly account for the patterns of genome reorganizationcommonly observed in nascent polyploids and explainthat specific polyploidy-induced genome changes are re-producible. Such a hypothesis, however, remains largelyto be tested.

Transposable Elements and Hybrid Dysgenesis

Transposable elements represent the major and mostdynamic fraction of plant genomes [Tenaillon et al.,2010]. Accordingly, diverging taxa likely accumulate dif-ferential arrangements of transposable elements, reduc-ing recombination and likely resulting in chromosomalincompatibilities at hybridization [He and Dooner, 2009;Abbott et al., 2013]. Such differential dynamics of trans-posable elements can also lead to the accumulation of dif-ferent amounts or differentiated copies in divergent ge-

nomes that may reveal conflicts after genome merging asthe hybrid genome fails to regulate their activity (fig. 3D).The activity of transposable elements is indeed controlledby repressive small interfering RNA (siRNA) targetingand silencing homologous inserted copies via DNA meth-ylation and other epigenetic marks [Bourchis and Voin-

net, 2010]. In somatic cells, siRNA and transposable ele-ments match, ensuring proper repression and genomestability [Martienssen, 2010]. The soft reactivation oftransposable elements during gametogenesis boost theproduction of siRNAs in accompanying cells and ensuresthe maintenance of repression across generations. How-ever, cytoplasmic siRNA may fail to repress all copies af-ter the merging of genomes presenting large divergencein their transposable elements content [reviewed in Pari-sod and Senerchia, 2013]. Such conflicts may even bestronger in the endosperm, where 2 maternal genomesare merged with the paternal one. The resulting activa-

tion of transposable elements during the merging of di-vergent genomes may lead to transposition burst and/orepigenetic repatterning, leading to developmental failurein the endosperm and deleterious mutations in the zygote(i.e. hybrid dysgenesis).

In the context of polyploid speciation, genome dou-bling or the purging of localized loci is unexpected to mit-igate the impact of the activation of interspersed trans-posable elements. Successful neopolyploids have to effec-tively repress active transposable elements at a genome-wide scale through loss of sequences that would otherwisehave proliferated and strong reorganization of epigeneticmarks promoting their silencing. Accordingly, polyploi-dy seems to induce genome-wide restructuring and epi-genetic re-patterning with genome changes specificallyaffecting transposable elements as soon as divergent ge-nomes are merged [Parisod et al., 2010b]. Despite recentprogresses [reviewed in Parisod and Senerchia, 2013;Bento et al., this issue], several aspects of the conflictamong transposable elements and its resolution remainto be elucidated.

Long-Term Diploidization

Polyploidy is assumed to promote evolutionary novel-ties, and it is, therefore, essential to better understand theforces behind the maintenance of duplicated sequences[McGrath and Lynch, 2012]. Genome structural differen-tiation supports proper homologous paring (i.e. cytolog-ical diploidization) but is also suggested to facilitate func-tional diploidization by restricting intergenomic recom-bination and thus favoring the divergence of duplicatedgene [Feldman et al., 2012]. Several models have been


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proposed to explain the fate of duplicated genes towardeither nonfunctional pseudogenes or subfunctionalizedgenes having partitioned the ancestral function or neo-functionalized genes with new functions [Innan andKondrashov, 2010]. In particular, the dosage balance hy-pothesis [Birchler and Veitia, 2012] seems to match ob-

served patterns of long-term retention of dosage-sensi-tive genes better than the long-held hypothesis postulat-ing relaxed purifying selection on redundant functions[Ohno, 1970; Force et al., 1999]. Whole genome duplica-tion indeed creates whole sets of redundant functionalgenes that interact through proper stoichiometric rela-tionships, representing a potentially strong constraint se-lecting for genome stability. Accordingly, it would be cru-cial to assess to what extent functional genes are differen-tially constrained in auto- versus allopolyploids.

Polyploidy is often considered as a mechanism ofabrupt speciation [Coyne and Orr, 2004] and indeed ap-

pear as a major mechanism of speciation, accounting forat least 15% of speciation events in flowering plants[Wood et al., 2009]. However, post-zygotic barriersamong ploidy levels are all but impermeable [e.g. Broch-mann et al., 1992; Petit et al., 1999; Slotte et al., 2008;Chapman and Abbott, 2010], and the recurrent produc-tion of polyploid lineages may further contribute to indi-rect gene exchange between ploidy levels [Soltis and Sol-tis, 1999; Modliszewski and Willis, 2012]. In addition, re-cently formed polyploids must establish self-sustainablepopulations by colonizing new territories or persisting insympatry with the parental populations [Levin, 2002]. Es-pecially in the case of sympatry, neopolyploids must over-come the minority disadvantage and then have to adaptto new niches in order to avoid competition with the pa-rental progenitors [Levin, 1975; Felber, 1991]. In otherwords, nascent polyploids have to achieve complete re-productive isolation, and this could be promoted by bothrestructuring and functional changes. Polyploidy-in-duced genome reorganization improving fertility in theshort-term may thus further promote reproductive isola-tion of the neopolyploids.

To what extent long-term diploidization fosters the di-

versification of established polyploids remains an openquestion. For instance, Okas model [Oka, 1957], whichwas later popularized as the duplication-degeneracy-complementation model [Force et al., 1999], suggeststhat pseudogenization or the transposition of alternativecopies of duplicated genes may lead to hybrid inviability(fig. 3C) and thus foster speciation at the polyploid level.Experimental proofs of Okas model were recently unrav-eled inArabidopsisand rice by showing that random seg-

regation of copies of a duplicated gene produced gametesand hybrids without functional copies, suffering fromreduced fitness [Bikard et al., 2009; Mizuta et al., 2010].In strike contrast, recent phylogenetic analyses suggestthat recently formed polyploids show higher extinctionrates and possibly lower net diversification rates than

their diploid relatives [Mayrose et al., 2011; Arrigo andBarker, 2012]. Additional work on genome reorganiza-tion in auto- and allopolyploids as compared to diploidsis needed to better understand the evolutionary conse-quences of polyploidy.

Perspectives

Impact of Hybridization and Pathways to Polyploidyon Genome ReorganizationAdditional studies addressing the patterns and the

tempo of restructuring and functional changes in auto-versus allopolyploid genomes are necessary to reach firmconclusions, but the limited evidence available in auto-polyploids suggests lower levels of genome restructuringand epigenetic changes than in allopolyploids [Parisod etal., 2010a]. Correspondingly, the relative impact of hy-bridization and genome doubling on the genome/tran-scriptome shock deserves further attention. Hybridiza-tion more than genome doubling seems to trigger quickgenome reorganization [Doyle et al., 2008; Hegarty andHiscock, 2008; Feldman et al., 2012; Parisod and Sener-chia, 2013]. For instance, hybridization induced at least 5times more structural, epigenetic and gene expressionchanges across the genome than chromosome doublingin Spartina anglica[Parisod et al., 2009; Chelaifa et al.,2010]. Changes in gene expression were mostly attributedto genome merging in several systems [e.g. Albertin et al.,2005; Flagel et al., 2008], but changes induced by hybrid-ization were, to a certain extent, reversed by genome dou-bling in others [e.g. Hegarty et al., 2006; Xu et al., 2012b].A better understanding of the impact of merging increas-ingly divergent genomes in revealing hybrid incompati-bilities and inducing genome reorganization seems cru-

cial.In order to better understand genome reorganizationin the short term, the early chain of events at the origin ofa polyploid lineage may reveal crucial [Hegarty andDoyle, this issue]. Natural polyploids can indeed beformed through various pathways, potentially involvingthe merging of different dosage of parental genomes anddifferent rounds of genome merging versus doubling.The exact pathway at the origin of a given polyploid may


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thus play a fundamental role in triggering particular ge-nome changes. Accordingly, allopolyploid lines of Bras-sica napusproduced through somatic doubling of F1 ho-moploid hybrids versus pathways involving unreducedgametes showed different patterns of genome restructur-ing [Szadkowski et al., 2011]. In particular, patterns of

genome reorganization in the polyploid formed throughthe fusion of unreduced gametes were similar to thechanges observed in the established polyploid. Exceed-ingly few studies addressed the impact of the pathway topolyploidy on genome changes, but it may be fundamen-tal. As the production of synthetic polyploids contrastswith the variety of possible pathways at the origin(s) ofnatural polyploids, a better understanding of the impactsof hybridization and whole genome duplication as well asthe timing of these events on genome reorganizationseems crucial to draw suitable conclusions from synthet-ic polyploids.

Emergence of a Diverge, Merge and Diverge ModelThe realization that the origin of almost all polyploids

involves the merging of more or less differentiated ge-nomes emphasizes the need to focus on the nature of thisdivergence. In particular, genome divergence goes alongwith the accumulation of incompatible loci, which is con-sistent with the declining fertility of hybrids from closelyrelated to more divergent taxa [Grant, 1981; Riesebergand Willis, 2007]. Nevertheless, the potential for hybrid-ization declines relatively slowly [Levin, 2012], and ge-nomes harboring structural, genic and/or transposableelement incompatibilities can merge to form new poly-ploid lineages [Buggs et al., 2011; Abbott et al., 2013]. Re-sulting interactions between genomes potentially affectthe survival, establishment and persistence of nascentpolyploids in the short-term [Parisod, 2012]. Polyploidlineages are seemingly formed more commonly than es-tablished, and only those having efficiently purged in-compatible loci through genome reorganization may suc-cessfully establish lasting lineages. Accordingly, selectionimproving hybrid fitness could promote short-term reor-ganization of polyploid genomes. The divergence of dip-

loid genomes at incompatible loci may thus be a suitablepredictor of polyploid genome differentiation after ge-nome merging and diverge, merge and diverge matchesthe observed genome dynamics during polyploid specia-tion.

Successful polyploids formed from increasingly diver-gent genomes are expected to show increasing levels ofrestructuring and epigenetic repatterning to eliminate thegradually accumulated genic incompatibilities or con-

flicting copies of transposable elements [Abbott et al.,2013]. Genic incompatibilities should be purged throughthe reorganization of specific loci, whereas incompatibil-ities associated with transposable elements likely inducegenome-wide changes [Parisod and Senerchia, 2013].Structural incompatibilities are also expected to drive cy-

tological diploidization, promoting an increased numberof bivalents at the expense of multivalents [Feldman et al.,2012]. However, such diploidization may depend on theimpact of multivalents on fitness, and patterns of restruc-turing may fundamentally differ in auto- versus allopoly-ploids [Cifuentes et al., 2010; Parisod et al., 2010a; Soltiset al., 2010]. Cytological diploidization is still poorly un-derstood, especially in autopolyploids, and both its ge-netic basis and adaptive value have to be firmly assessed[Le Comber et al., 2010].

Diverge, merge and diverge may be a useful meta-phor, but several aspects of the relationship between di-

vergence at the diploid level and genome reorganizationat the polyploid level remain to be explored and tested. Inparticular, genome reorganization following the mergingof diploids harboring various categories of incompatibil-ities may be hardly predictable [Abbott et al., 2013].Moreover, the role of genetic drift versus selection in sort-ing genome changes occurring after polyploidy has to befirmly assessed. Genome reorganization may well im-prove the fitness of nascent polyploids, but to what extentrevolutionary changes fostered by the purging of hybridincompatibilities are reinforced to facilitate the establish-ment of polyploids remains an open question. Accord-ingly, the impact of short-term genome changes on thelong-term maintenance of duplicated genes as well as theimpact of long-term diploidization on the diversificationof auto- versus allopolyploids should be further exam-ined. Polyploidy is more than the reshuffling of parentalgenomes and thus offers promising opportunities to in-tegrate genome and phenotypic variation within a coher-ent evolutionary framework [Parisod, 2012].

Acknowledgements

We would like to thank Richard Buggs, Natacha Senerchia and2 anonymous reviewers for constructive comments on the man-uscript as well as the Swiss National Science Foundation (grantPZ00P3-131950) and the Velux Stiftung for funding.


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natural pathways to polyploidy in plants and cosequences for genome reorganization

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