Natural Pathways To Polyploidy in Plants and Cosequences For Genome Reorganization

Natural Pathways to Polyploidy and Consequences for Genome Organization and Genome Size
Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Published online: June 8, 2013
Natural Pathways to Polyploidy in Plants and Consequences for Genome Reorganization

A. Tayal C. Parisod
Laboratory of Evolutionary Botany, Institute of Biology, University of Neuchtel, Neuchtel, Switzerland
Key Words Chromosome pairing Dobzhansky-Muller incompatibility Hybrid dysregulation Genome evolution Genome merging Genome restructuring Speciation Transposable elements Unreduced gametes Whole genome doubling
incompatibilities through non-Mendelian mechanisms, fostering polyploid genome reorganization in association with the establishment of new lineages. See also sister article focusing on animals by Collares-Pereira et al., in this themed issue. Copyright 2013 S. Karger AG, Basel
2013 S. Karger AG, Basel 14248581/13/14040079$38.00/0 E-Mail karger@karger.com www.karger.com/cgr
Christian Parisod University of Neuchtel Rue Emile-Argand 11 CH2000 Neuchtel (Switzerland) E-Mail christian.parisod@unine.ch
Downloaded by: University of Alabama, Lister Hill Library 138.26.31.3 - 10/1/2013 5:24:10 PM
Abstract The last decade highlighted polyploidy as a rampant evolutionary 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 supporting polyploid speciation and stressing patterns of divergence between diploid progenitors as a suitable predictor of polyploid genome reorganization. The merging of genomes at the origin of a polyploid lineage may indeed reveal different kinds of incompatibilities (chromosomal, genic and transposable elements) that have accumulated in diverging progenitors and reduce the fitness of nascent polyploids. Accordingly, successful polyploids have to overcome these
Polyploidy (i.e. the merging of more or less divergent genomes associated with whole genome duplication) is an important factor in eukaryote evolution [Lynch, 2007; Otto, 2007]. For instance, it is now clear that all flowering plants have gone through at least one round of polyploidy [Jiao et al., 2011]. Polyploidy long remained a favored topic 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], although several animal taxa are known to contain polyploid forms [Otto and Whitton, 2000; Mable et al., 2011]. Cross-talk between these traditional fields as promoted by this issue is expected to foster advances in our understanding of the potential advantages and disadvantages of being polyploid.
Paleo- versus Neopolyploids and Auto- versus Allopolyploids
Fig. 1. Natural pathways to polyploidy. The origin of both autotetraploids and allotetraploids involve the merging of more or less divergent 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 chromosome doubling is assumed to be rare (dashed arrows). Recently formed neopolyploids go through a phase of intense genome reorganization (figured by changing colors) referred to as diploidization and leading to the evolution of paleopolyploids.
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The last decade has shown a renewed interest in examining and integrating the consequences of polyploidy in different organisms to shed light on this rampant evolutionary process. Here, we provide an overview of the current knowledge on the origins of polyploids and their consequences for genome organization in plants. We will first describe the different types of polyploids and the pathways leading to their formation. Then, we will expand on observed patterns of polyploidy-induced genome changes and explore their possible causes and consequences for the establishment of new polyploid lineages. As a whole, we highlight evidence supporting the emergence of a model stressing divergence between diploid progenitors as a suitable predictor of genome reorganization after polyploidization. The merging of genomes at the origin of polyploid lineages indeed reveals different kinds of incompatibilities that have accumulated during progenitor divergence and that reduce the fitness of nascent polyploids. Accordingly, successful polyploids have to overcome these incompatibilities through non-Mendelian mechanisms, fostering specific genome changes going along with their establishment.
Polyploidy may be a confusing term because of both changing terminologies and recent paradigm shifts. In particular, the last decade unraveled the considerable genetic redundancy presented by plant genomes and highlighted the highly dynamic nature of polyploid genomes [Soltis and Soltis, 2012]. Genome reorganization, involving drastic restructuring and functional alterations in association with polyploidy, is commonly referred to as diploidization and generally restores a secondary diploidlike behavior of polyploid genomes. Accordingly, a temporal distinction between paleopolyploids (i.e. ancient polyploids with diploidized genomes) and neopolyploids (i.e. young polyploids without diploidized genomes) seems useful [Blanc and Wolfe, 2004]. This review is mainly focused on neopolyploids, including both experimental (i.e. synthetic) and naturally formed (i.e. nascent or established) polyploids. Nascent, established and paleo-polyploids hardly represent clear-cut categories, but may highlight stages in the evolution of polyploid lineages likely driven by contrasting processes. The classification of neopolyploids into 2 main categories (fig. 1) based on their origin is still controversial [Clausen et al., 1945; Ramsey and Schemske, 1998]. Autopolyploids are generally considered to have arisen within or among populations of a single species by the doubling of structurally similar, homologous chromosome sets (AAAA), whereas allopolyploids typically involve interspecific hybridization associated with the doubling of non-homologous (i.e. homeologous) chromosome sets (AABB). To account for natural hybrid polyploids forming multivalents, Stebbins [1947] defined inter-racial autopolyploids or segmental allopolyploids to denote the doubling of partially differentiated genomes (AAAA). It is now widely accepted that polyploidy encompasses a continuum from the doubling of identical genomes to the doubling of highly differentiated genomes (fig. 1). Accordingly, all natural polyploids likely consist of more or less divergent genomes having been merged at their origin. The most obvious characteristic which may distinguish types of polyploids is the pairing behavior of the chromosomes in meiosis [Jackson, 1982]. Autopolyploids have multiple homologous chromosomes and thus mainly form multivalents, while allopolyploids form predominantly bivalents as homeologous chromosomes do not regularly pair [Ramsey and Schemske, 2002]. Chromosome pairing is, however, affected by sev-
eral factors and predominant bivalent pairing in autopolyploids or multivalent pairing in polyploids of hybrid origin is reported [Jenczewski and Alix, 2004; Otto, 2007]. Patterns of chromosome pairing may thus be a misleading criterion to classify polyploids. Accordingly, a classification of polyploid based on patterns of segregation should be preferred [Soltis et al., 2007; Parisod et al., 2010a]. Autopolyploids indeed present 4 homologous chromosomes that can randomly pair at meiosis, even if strictly forming bivalents, resulting in random segregation of chromosomes or chromatids and leading to polysomic inheritance with possible double reduction [Jackson and Jackson, 1996; Hauber et al., 1999; Landergott et al., 2006; Stift et al., 2008]. This results in the production of homozygotes and different types of partial heterozygotes (AAAa, AAaa, Aaaa for a tetraploid locus with 2 alleles [Bever and Felber, 1992; Ronfort et al., 1998; Butruille and Boiteux, 2000; Luo et al., 2006]). Polysomic inheritance occurs even if homologous chromosomes regularly pair as bivalents and thus is the key criterion distinguishing auto- from allopolyploid taxa [Soltis et al., 2007; Parisod et al., 2010a]. Noticeably, polysomic inheritance may represent a transient segregation pattern in neoautopolyploids and evolve toward disomic inheritance with ongoing diploidization. Accordingly, the distinction between auto- and allopolyploids would be blurred in paleopolyploids.
Natural Pathways at the Origins of Polyploids
Pathways to Polyploidy and Genome Reorganization
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Somatic Doubling versus Merging of Unreduced Gametes Several pathways involving the spontaneous doubling of chromosome sets in somatic cells and the reunion of unreduced gametes support the formation of new polyploid lineages in plants (fig.1). Such different pathways do not seem to be equally frequent in nature [reviewed in the meta-analysis of Ramsey and Schemske, 1998]. Mitotic nondisjunction supporting spontaneous doubling of chromosomes can occur throughout the life cycle of a plant and may result in mixoploid organisms potentially at the origin of polyploid meristematic cells that ultimately lead to a new polyploid organism (e.g. Primula kewensis [Grant, 1981]). Little is known about the frequency of spontaneous chromosome doubling, particularly after events such as interspecific hybridization or stress conditions [Lewis, 1980; Ramsey and Schemske, 1998]. Somatic doubling is commonly performed to produce synthetic polyploids supposed to mimic established
ones but is estimated to be a relatively minor pathway to polyploidy in natural populations. Unreduced gametes (i.e. diplogametes) are produced at a much higher rate than previously assumed and may be involved in the major pathways leading to polyploidy [Bretagnolle and Thompson, 1995; Otto and Whitton, 2000]. Several mechanisms resulting in the production of unreduced gametes have been identified in a variety of plant taxa [reviewed in Bretagnolle and Thompson, 1995; Brownfield and Khler, 2011]. The production of diplogametes is highly variable among and within species, and has been estimated at 0.56% in non-hybrid flowering plants [Ramsey and Schemske, 1998]. Diplogametes seem to be more frequent under environmental stresses, such as frost, wounding, herbivory, water or nutrient shortage [e.g. Mason et al., 2011]. Noticeably, hybrids between divergent genomes present up to a 50-fold increase in the production of unreduced gamete as compared to nonhybrid systems [e.g. Zhang et al., 2010]. In addition, the production of diplogametes appears to be heritable and governed by a few genes [dErfurth et al., 2008; Zhang et al., 2010]. However, the molecular basis underlying the formation of unreduced gamete begins to be unraveled, but much remains to be understood [Brownfield and Khler, 2011]. Given their high rate of production, the union of unreduced gametes likely supports the origin of both autoand allopolyploids under natural conditions (fig.1). Such events seem frequently enough to form polyploid at an estimated rate (105 for autotetraploids and 104 for allotetraploids) comparable with the one of genic mutations [Ramsey and Schemske, 1998]. Recent work having estimated the rate of polyploid formation in natural populations matched these expectations [Ramsey, 2007], but additional empirical studies assessing the frequency of the different pathways to polyploidy are needed. Unreduced Gametes: Unilateral versus Bilateral Polyploidization Given the low probability of uniting 2 unreduced gametes in a single step (i.e. bilateral polyploidization), the formation of tetraploids has early been anticipated as being mostly indirect, involving triploid intermediates (triploid bridge supporting unilateral polyploidization; fig. 1) [Harlan and DeWet, 1975]. Triploid individuals are indeed observed at low frequency in natural populations and easily obtained experimentally [Ramsey and Schemske, 1998]. The fusion of a reduced with an unreduced gamete is expected to produce triploids that can in turn generate tetraploids through selfing or crossing with
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other triploids or diploid progenitors. The establishment of tetraploids would thus critically depend on (i) the rate of triploid formation, (ii) the fitness of triploids and (iii) the ploidy level of the functional gametes produced by triploids [Husband, 2004]. Triploidy has long been considered detrimental as triploid seeds may early abort (i.e. triploid block) [Brink and Cooper, 1947]. The endosperm (i.e. the tissue, made of one paternal and 2 maternal genomes, surrounding and providing nutrients to the embryo) indeed seems sensitive to dosage of parental genes and may fail to properly develop in polyploids with misbalanced chromosome sets. Such emphasis on the endosperm is consistent with the reduced triploid block observed in species presenting a reduced endosperm [Ramsey and Schemske, 1998; Husband, 2004]. Successive models based on the relative ploidy of seed tissues have been developed to account for triploid seed production despite triploid block [Muntzing, 1930; Johnston et al., 1980; Lin, 1984]. Khler et al., [2010] recently pointed out that failure of endosperm development in both homoploid and interploid hybrids might be associated with differently imprinted genes of the Polycomb group. Accordingly, parental divergence and/or ratios of paternal versus maternal dosage would result in unbalanced interactions between global transcriptional repressors of the Polycomb group and their targets (i.e. homeotic genes and downstream genes as well as transposable elements), leading to a crash of the endosperm in triploids. Uncertainties about links between these mechanisms and expected incompatibilities reducing fitness remain. However, viable triploids present unexpected fertility. A mean pollen fertility of 31.9% has indeed been reported in triploid Angiosperms by Ramsey and Schemske [1998]. Triploids indeed produce a relatively large amount of viable, euploid gametes (n = x, 2x, 3x), regardless of their auto- or allopolyploid origin and may thus strongly impact on the formation of polyploids [Husband, 2004]. However, additional insights on the influence of triploid intermediates on the origin of polyploids in natural populations, particularly in primary contact zones between diploids and tetraploids, would be valuable. Tetraploids can be formed without triploid intermediates through either homoploid hybrids (i.e. homoploid bridge) or the direct union of 2 diplogametes (i.e. bilateral polyploidization; fig.1). Hybrids seem to present an increased production of diplogametes as shown by the average 27% reported in hybrid systems as compared to 5.6% in non-hybrid systems [Ramsey and Schemske, 1998]. Accordingly, homoploid hybrids could be ex-
pected to sustain polyploidization [Rieseberg and Willis, 2007]. Hybrids can also be directly polyploid when formed through bilateral polyploidization. This pathway has been reported at the origin of both auto- and allotetraploid taxa [Ramsey and Schemske, 1998; Husband, 2004]. Plants producing particularly high levels of diplogametes may indeed foster bilateral polyploidization, especially in the case of self-fertilizing individuals [Bretagnolle and Thompson, 1995; Bretagnolle, 2001]. Based on extensive data [analyzed in Ramsey and Schemske, 1998], bilateral polyploidization is estimated to produce polyploids at a rate almost similar to unilateral polyploidization. However, the frequency of spontaneous somatic doubling at the origin of natural auto- and allopolyploids should be further empirically estimated. Accordingly, the concluding remark of Ramsey and Schemske [1998] that comprehensive examination of the pathways, mechanisms and rate of polyploid formation in natural populations remains largely appropriate. Multiple Origins and Multiple Pathways Produce Variable Polyploids Polyploidy has long been considered exceptional with polyploid species typically being monophyletic and genetically depauperate [Ehrendorfer, 1980; Favarger, 1984]. Multiple origin of polyploid species is now considered 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; Soltis et al., 2004; Arrigo et al., 2010] and autopolyploids [Shore, 1991; Segraves et al., 1999; Soltis and Soltis, 1999; Parisod and Besnard, 2007], despite notable exceptions such as Arabidopsis suecica [Jakobsson et al., 2006] or Draba ladina [Widmer and Baltisberger, 1999]. Noticeably, multiple origins may occur over restricted geographical distributions and/or short evolutionary timescales as illustrated by the allopolyploid Tragopogon miscellus that formed at least 21 times independently during the last 5060 years [Soltis et al., 2012]. Multiple origins of polyploids may involve genetically and morphologically differentiated parents, and may result in considerable genetic and phenotypic variability as well as variable nuclear or nucleo-cytoplasmic interactions at the polyploid level [Soltis and Soltis, 1999; Wendel, 2000; Mable, 2003]. Adding to such complexity, independent polyploid lineages may have originated through varied pathways, multiplying interactions among genomes. Although likely, this hypothesis has apparently not been tested yet. Finally, independently formed polyploid lineages may further hybridize [e.g. Modliszewski
and Willis, 2012]. Accordingly, the evolutionary history of a given polyploid taxon may be much more complex than usually assumed and hardly disentangled. In particular, the multifarious origin of current lineages, together with genome reorganization (see below), certainly participates in the evolution of highly variable polyploid gene pools.
Patterns of Genome Changes after Polyploidization
The last decade revealed that polyploidization triggers genome changes highlighted as departure from the predicted additivity of parental genomes in polyploids. Thus, polyploidy has been compared to a genome shock inducing drastic genome reorganization [reviewed in Comai, 2005; Doyle et al., 2008; Leitch and Leitch, 2008]. Genome changes have early been categorized based on their genetic or epigenetic nature and their impact on either structural or functional genomic traits (fig. 2; table 1). The timing of such genome reorganization further distinguishes short-term revolutionary changes observed in the first few generations following polyploidization and the long-term evolutionary changes taking place during the lifespan of the polyploid lineage [Feldman et al., 2012]. Genome Restructuring following Polyploidization Genome restructuring events including DNA sequence loss, amplification or reduction of repetitive sequences, or large chromosome repatterning involving deletion, insertion, inversion, translocation of chromosomal segments has been reported following polyploidy in several systems (see table1 for references). Despite drastic restructuring reported in both the short- and the longterm in several polyploids (see Brassica, Nicotiana, Tragopogon or Triticum), a couple of counter examples revealed limited structural changes (see Gossypium or Spartina). Rapid loss of DNA sequences is common after polyploidy and genome downsizing seems to be a general response to 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 expansion [Leitch et al., 2008]. Large genome rearrangements such as inversion, translocation, deletion or aneuploidy have been reported in autopolyploids (see Arabidopsis or Goldbachia) and allopolyploids (see Brassica, Nicotiana or Tragopogon). Several studies highlighted a biased restructuring towards either the paternal (e.g. Nicotiana) or the maternal (e.g. Spartina) subgenomes.
Fig. 2. Commonly reported genome changes after polyploidization
(case studies reviewed in table1). Additive effects refer to changes in the dosage of genes and the level of heterozygosity in polyploids as compared to diploids. Polyploids usually show nonadditive changes (i.e. genome reorganization) including both restructuring events and functional modifications. Duplicated genes can go through either diversification via subfunctionalization and neofunctionalization or, in contrast, conversion via nonreciprocal homeologous exchanges. Genome restructuring can involve chromosomal rearrangements (e.g. translocations, inversions), loss of sequences and amplification of repetitive sequences such as transposable elements. Functional changes can occur without modifications of the nucleotide sequence through epigenetic changes, involving methylation repatterning and other types of chromatin remodeling. Transposable elements may play a pivotal role during genome reorganization, inducing both restructuring and epigenetic changes at a genome-wide scale. * = methylated site.
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Functional Changes following Polyploidization Numerous studies highlighted changes in epigenetic patterning and gene expression in both synthetic and established polyploids (see table1 for references). Reports from both synthetic and established polyploids indicate that functional changes occur quickly and are reproducible to a large extent (e.g. Brassica, Tragopogon or Triticum). Noticeably, methylation changes and expression of the alleles originating from one of the parental genome (i.e. expression bias) or changing expression towards the levels 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 in methylation patterns and gene expression have been reported in specific allopolyploids as well [e.g. Mestiri et al.,
Table 1. Examples of studies reporting genome reorganization in synthetic and/or established autopolyploid and allopolyploid systems
Auto/Allo Auto Auto S/L Chrom Accumulation of structural changes associated with increasing bivalent formation (085%) through 30 generations in synthetic accessions Translocation of the 45S rDNA from chromosome 4 to chromosome 3 in 2030 generations in synthetic accessions Gene Gene, Epi Gene NS Chrom Del Protein expression changes in synthetic autotetraploids (6.8%) No significant change in protein expression in synthetic accessions Paracentric inversions and rDNA restructuring differentiating putatively homolgous chromosomes Genome downsizing in synthetic (8.6%) and established (10%) accessions, indicating limited long-term changes in this cytologically diploidized polyploid Paracentric inversions and rDNA restructuring differentiating putatively homolgous chromosomes NS Chrom, Del NS Del Gene Del Gene Del Del Chrom, Del Del, Ampl No signifiant differences in gene expression among established accessions of various ploidy levels Asymmetrical relocation and loss of rDNA loci in established accessions Nonsignificant genome downsizing in multivalent forming (H. bulbosum) and cytologically diploidized (H. marinum) accessions Genome downsizing (23%) in cytologically diploidized accessions Changing expression of 4.2% of the genes in synthetic accessions Restructuring, mostly loss of AFLP bands, affecting 9.6% of the loci in synthetic accessions Changing expression of 1.3% of the genes in synthetic accessions Restructuring, mostly loss of AFLP bands, affecting 1523% of the loci in synthetic accessions Genome downsizing in synthetic autopolyploids (17% in F1, 25% in S3) associated with 3060% seed set increase Significant decrease in chromosome length, translocations and aneuploidy in established accessions S Gain/loss of fragments in autotetraploid regenerants of Solanum bulbocastanum (22%/48%), S. cardiophyllum (29%/32%) and S.tuberosum (18%/36%) Stable, nonstochastic alteration of the transcriptome, in association with DNA methylation changes; depends on the parental genome composition in synthetic accessions Expression changes in 5/34 genes in synthetic accessions Li et al., 2012 Yu et al., 2010 Santos et al., 2003 S NS No DNA loss in synthetic autopolyploids Ozkan et al., 2006 Timinga Structureb References Functionc Details
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Auto Auto Auto S S S/L Chrom Weiss and Maluszynska, 2001 Auto Auto Auto Auto S/L L S S Ng et al., 2012 Albertin et al., 2005 Mandkov and Lysak, 2008 Eilam et al., 2009 Auto Auto Auto Auto L S S S S S L L L L L Chrom Mandkov and Lysak, 2008 Church and Spaulding, 2009 Weiss-Schneeweiss et al., 2007 Eilam et al., 2009 Eilam et al., 2009 Lu et al., 2006 Martelotto et al., 2007 Martelotto et al., 2005 Martelotto et al., 2007 Raina et al., 1994 Rivero-Guerra, 2008 Aversano et al., 2011 Auto Auto Auto Auto Auto Auto Auto
Species
Arabidopsis thaliana
Brassica oleracea
Calepina irregularis
Elymus elongates
Goldbachia laevigata
Helianthus decapetalus
Hepatica nobilis
Hordeum bulbosum and H. marinum
Hordeum murinum L. subsp. murinum Auto
Isatis indigotica
Paspalum notatum
Tayal/Parisod
Paspalum notatum
Paspalum rufum
Phlox drummondii
Santolina pectina
Solanum spp.
Table 1 (continued)
Auto/Allo Auto Auto Allo S Del Reproducible loss of tandem repeats (7090%) in synthetic accessions (S2/S3) of Aegilops longissima Triticum urartu, Ae.sharonensis T. monococcum, T. aestivum Ae. speltoides Reproducible loss of low-copy sequences in synthetic polyploids of Aegilops sharonensis Ae. umbellulata and Ae. longissima Triticum urartu (6.7 and 16.6%, respectively; incl. 5.3 and 5.2% after hybridization), affecting mostly maternal genome Epi Del Epi Methylation changes (13%) in F1 hybrids and allopolyploids of Ae. sharonensis T. monococcum Loss of large portions of chromosomes in synthetic hybrids; methylation changes (25%, incl. nucleolar dominance) favoring the A.lyrata alleles Transcriptional activation of transposons in association with epigenetic remodeling in synthetic accessions; limited transposition Gene expression changes (up to 5.6%) in synthetic accessions, mostly (65%) differentially expressed genes in the parents Protein expression changes in F1F8 synthetic allotetraploids (8.2%) Loss of DNA and cDNA fragments and methylation changes in synthetic accessions (F2F5) Translocations and aneuploidy (24.171.4%) in synthetic accessions Genetic changes in 1.2% of the loci (fragment loss: 0.10.8%) in synthetic accessions after hybridization and/or genome doubling Epi Gene Chrom Del Del Epi Gene, Epi Alternative splicing in duplicated genes (2630%) in synthetic and established accessions Gene expression changes (38%) in synthetic and established accessions Sequence repeat and chromosomal rearrangements as well as activation of retrotransposon after hybridization Nonrandom fragment loss (3.5%, mostly in S5) and methylation changes (mostly in S0) in synthetic accessions Asymmetrical genetic changes (1.8%), DNA methylation (8.8%) and gene expression (5.1%) changes detected in synthetic F1 and/or allohexaploids. Sometimes reversed by genome doubling Han et al., 2005 S Gene No significant alteration in gene expression in synthetic autopolyploid series Riddle et al., 2010 S Gene Low expression changes in 10% of 9,000 genes surveyed in synthetic accessions Stupar et al., 2007 Timinga Structureb References Functionc Details
Species
Solanum phureja
Zea mays
Triticum Aegilops spp.

Allo S Del Shaked et al., 2001 Allo Allo S S Shaked et al., 2001 Beaulieu et al., 2009 Allo S Epi Madlung et al., 2005 Allo Allo Allo Allo Allo Allo Allo Allo Allo Allo S S S S/L S S Del S Chrom S Del Epi S Gene S Gene Wang et al., 2006 Ng et al., 2012 Song et al., 1995 Pires et al., 2004; Xiong et al., 2011 Lukens et al., 2006; Xu et al., 2012b Zhou et al., 2011 Pires et al., 2004; Albertin et al., 2007; Higgins et al., 2012 Zou et al., 2011 Gaeta et al., 2007 Xu et al., 2012a
Arabidopsis thaliana A. lyrata
Arabidopsis suecica
Arabidopsis suecica
Arabidopsis suecica
Brassica juncea, B. napus
Brassica napus
Brassica napus
Brassica napus
Brassica napus
Brassica napus
Brassica napus
Brassica rapa B. carinata
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Table 1 (continued)
Auto/Allo Allo Genome downsizing in natural accessions of B. napus (8%), B. juncea (8%) and B. carinata (3%) Gene Del Conserved colinearity, but high genome turnover due to smallscale deletions in the repetitive genome fraction as well as limited transposition Genome downsizing (18%) in established accessions Genome size changes in established accessions (reduction in N.tabacum, N. rustica, N. arentsii, N. nudicaulis about 1.914.3% and amplification in N. clevelandii, N. quadrivalis, N. repanda, N.nesophila, N. stocktonii about 2.528.6%) Complete genome turnover despite conserved karyotype in less than 5 million years; proliferation and deletion of transposable elements Up to 3 translocations in synthetic allopolyploids and intergenomic recombination in established accessions; similar translocation in all established and in 2/3 of synthetic accessions Loss of repeat sequences (18%) and retrotransposon fragments (2962.5%) mostly from the paternal genome as well as new insertions in synthetic (S4) and established accessions NS Chrom Gene Neither uniparental epigenetic silencing nor methylation changes in repeated sequences of established accessions Limited genetic changes in subtelomeric tandem repeats in established accessions Reorganization of gene expression networks in synthetic and established accessions; expression restored towards parental states after genome doubling Limited loss, but drastic methylation changes in random sequences and transposable elements (1222%) from the maternal genome in F1 hybrids; limited reorganization after genome doubling (0.19%) Gene expression changes at hybridization (6.4%) and genome doubling (4.6%), with important maternal dominance Aneuploidy (in 69% individuals) and translocations (in 76% individuals); only 3/68 plants exhibited the addition of the parental karyotypes Gene Gene Protein expression changes (14.3%) in synthetic and established accessions; impact of hybridization greater than polyploidization Loss of homeologous loci and changes in gene expression (mostly from T. dubius origin) in established accessions Gene silencing and subfunctionalization in synthetic and established accessions Adams et al., 2003 Grover et al., 2008; Hu et al., 2010 Eilam et al., 2009 Leitch et al., 2008 Johnston et al., 2005 Allo Allo L S/L L Del Timinga Structureb References Functionc Details
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Allo Allo L Del, Ampl L Del Allo S/L Del, Ampl Lim et al., 2007; Petit et al., 2010; Parisod et al., 2012 Lim et al., 2004; Skalick et al., 2005; Koukalova et al., 2010 Petit et al., 2007, 2010; Renny-Byfield et al., 2011 Fulneek et al., 2009 Lim et al., 2004 Hegarty et al., 2006 Allo S/L Chrom Allo S/L Del, Ampl Allo Allo Allo S/L L L Allo S/L Del Epi Parisod et al., 2009 Allo Allo S Chrom S/L Gene Chelaifa et al., 2010 Lim et al., 2008; Chester et al., 2012 Koh et al., 2012 Koh et al., 2010 Allo Allo L S/L
Species
Brassica spp.
Gossypium hirsutum
Gossypium hirsutum
Hordeum murinum subsp. leporinum
Nicotiana spp.
Nicotiana spp.
Nicotiana tabacum
Nicotiana tabacum
Nicotiana tabacum
Nicotiana. arentsii, N. rustica
Senecio cambrensis
Spartina anglica
Tayal/Parisod
Spartina anglica
Tragopogon miscellus, T. mirus
Tragopogon mirus
Tragopogon mirus
Table 1 (continued)
Auto/Allo Allo S/L Gene Loss (0.6%, mostly paternal) and gain (1%) of cDNA fragments in synthetic and established accessions; differential expression of the parental homeologs in 1/10 candidate genes Loss (20%, mostly paternal) of homeologous gene in established accessions No restructuring, but aneuploidy in the first generations (S1 and S2) of synthetic accessions Epi miRNAs increase (2144%) and siRNAs decrease (3412%) in synthetic accessions; siRNA repressing transposable elements downregulated in association with methylation changes at polyploidization but not hybridization Intergenomic translocations in 1520% of the synthetic accessions; restructuring (up to 0.5%) and methylation changes (28.5%) at loci adjacent to the retrotransposon Veju Deletion (50% in S0) and insertion (S1) of Veju retrotransposon associated with methylation changes (43% in S0) in synthetic accessions Parental dominance and nonadditive gene expression (up to 36.5%) in synthetic accessions (S4S5 generations) Gene loss at the Hardness locus due to large genomic deletion in established accessions Amplification/loss of subtelomeric repetitive sequences in synthetic accessions Nonrandom loss of low-copy and high-copy noncoding sequences (from 15.8% in F1 to 92% in S2) following both hybridization and genome doubling in synthetic accessions Genome downsizing in synthetic accessions similar to established accessions Fragment loss (6.658.8%) in synthetic accessions (F1 to S4) and genomic changes in EST (4064.7%) in both F1 hybrids and allopolyploids; elimination of retrotransposons, but no gross chromosomal rearrangements in Triticum aestivum, T. timopheevii T.monococcum, T. aestivum Secale cereale, T. monococcum Aegilops tauschii Gene Reproducible gene expression changes (2%) in established accessions due to gene silencing (75%) or gene loss; activated genes with known function were retrotransposons NS Gene Transcriptional activation of retrotransposon Wis 2-1A with impact on the expression of adjacent genes Buggs et al., 2009, 2012 Mestiri et al., 2010 Kenan-Eichler et al., 2011; Yaakov and Kashkush., 2011 Tate et al., 2006 Timinga Structureb References Functionc Details
Species
Tragopogon miscellus
Tragopogon miscellus
Allo Allo S S NS
Allo
Gene
Triticum aestivum

Allo S Chrom Epi Zhao et al., 2011 Allo S Del, Ampl Epi Kraitshtein et al., 2010 Allo Allo Allo Allo S Del S Del L Del Gene S Chrom Gene Qi et al., 2012 Chantret et al., 2005 Salina et al., 2004 Liu et al., 1998; Ozkan et al., 2001 Ozkan et al., 2003; Eilam et al., 2008, 2010 Han et al., 2003 Allo Allo S Del S/L Del Allo S Kashkush et al., 2002 Allo S Kashkush et al., 2003
Triticum aestivum
Triticum aestivum
Triticum aestivum
Triticum aestivum
Triticum aestivum
Triticum durum
Triticum turgidum
Allo = Allopolyploid; Ampl = sequence amplification; Auto = autopolyploid; Chrom = chromosomal rearrangement; Del = sequence deletion; Epi = epigenetic changes; Gene = change in gene expression; L = long term; NS = non-significant changes; S = short term; S/L = studies having examined both short- and long-term changes in synthetic and established accessions, respectively. a Short-term versus long-term genome reorganization. b Polyploidy-induced structural changes. c Polyploidy-induced functional changes.
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2010; Kovarik et al., 2012]. Few studies focused on autopolyploids (e.g. Arabidopsis, Brassica or Helianthus), but usually reported fewer changes than in allopolyploids [Parisod et al., 2010a]. Much remains to be understood about mechanisms such as new interactions between regulatory networks and small RNAs that may account for changing gene expression and methylation patterns in polyploids [Madlung and Wendel, this issue]. Activation of Transposable Elements following Polyploidization The parasitic biology of transposable elements inhabiting genomes makes them prone to play a pivotal role in the changes affecting polyploid genomes [Fedoroff, 2012]. Polyploidy indeed seems to immediately activate specific transposable elements [Parisod et al., 2010b]. Although such activation does not necessarily translate in (bursts of) transposition, these repetitive sequences are intimately associated with genome restructuring as well as epigenetic changes at a genome-wide scale (see table1 for references). Some studies reported amplification of specific transposable elements in natural polyploids (e.g. Nicotiana tabacum), whereas a majority of polyploid genomes seem to have specifically eliminated these repetitive sequences from either the maternal or parental genome (e.g. Spartina, Triticum). Immediate methylation changes were specifically reported in the vicinity of insertions of transposable elements and may thus interfere directly 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 elements on the long-term differentiation of polyploid genomes, but their intense dynamics in allopolyploids Nicotiana section Repandae associated with genome turnover within 5 million years suggest that repetitive elements may be central to the diploidization process [Lim et al., 2007; Parisod et al., 2012]. Genome Reorganization in Polyploids: A Common Theme? Studies that assessed both synthetic and established polyploids suggest rapid genome reorganization (i.e. restructuring and/or functional changes) after the polyploidy event, with further changes accumulating over evolutionary time [see e.g. Feldman et al., 2012]. General patterns hardly emerge yet, and additional work assessing the level and the timing of genome changes across the polyploidy continuum is required. In particular, few studies assessed synthetic autopolyploids mimicking established ones [Parisod et al., 2010a].
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Mechanisms of genome reorganization (fig.2) are possibly interconnected through cause-and-effect relationships, with restructuring events potentially having functional effects. Furthermore, activation of transposable elements likely impacts the structure and the functioning of polyploid genomes. As several studies in various species highlighted reproducible changes after independent polyploidization events, such particular modifications may be selected for, but this remains to be tested. Also, to what extent immediate genome changes support genome-wide diploidization in the longer term should be further assessed. A better understanding of the origins and consequences of genome reorganization may lead to heuristic categories of the polyploidy-induced molecular changes.
Origins and Consequences of Polyploidy-Induced Genome Reorganization
The formation of polyploid lineages involves the merging of more or less divergent genomes, potentially uniting incompatible loci that accumulated during the differentiation of the progenitors and resulting in hybrid sterility or inviability [Stebbins, 1958; Rieseberg, 2001b]. As incompatible chromosomal or genic combinations are unlikely to be purged through segregation in polyploids, non-Mendelian mechanisms involving genome doubling per se, genome restructuring and/or epigenetic changes may thus help restoring the fitness of the nascent polyploid [Rieseberg, 2001a]. Chromosomal Incompatibilities and Proper Meiotic Pairing The merging of structurally divergent genomes induces troubles at meiosis when homeologuous chromosomes do not pair properly in the F1 hybrids (i.e. chromosomal incompatibility [Rieseberg, 2001b; Grandant et al., this issue]). Accordingly, loosely paired chromosomes segregate randomly, resulting in increased frequencies of nonfunctional gametes and thus sterility (fig. 3A). In this context, whole genome duplication is restoring the fertility of hybrids between taxa with structurally divergent genomes, furnishing the exact complements to all chromosomes and allowing proper meiotic pairing. Unless chromosomal rearrangements further harbor genic incompatibilities [Noor and Feder, 2006; Maheshwari and Barbash, 2011], chromosomal divergence between diploid taxa thus likely promotes the origin of polyploid lineages as whole genome duplication provides pairing partTayal/Parisod
Fig. 3. Mechanisms of genetic incompatibilities in hybrids. A Structural incompati-
bilities (here, an inversion marked by arrows) leading to hybrid sterility. B, C Genic incompatibilities accumulated between divergent genomes leading to dysfunctional hybrids. D Mismatch between transposable elements and their repressors (siRNAs) leading to the activation of transposable elements in hybrids (i.e. hybrid dysgenesis).
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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 similar chromosomal regions resulting in improper pairing at meiosis and promoting intergenomic recombination and chromosomal rearrangements [Gaeta and Pires, 2010]. The processes governing meiotic pairing are not fully understood yet [Stewart and Dawson, 2008], but structural features as well as specific genetic factors, such as the Ph1 gene in wheat, are expected to promote homologous pair-
ing [Jenczewski and Alix, 2004; Griffiths et al., 2006]. Activation of DNA recombination/repair pathways is suggested to efficiently correct non-homologous recombination in synthetic auto- and allotetraploids [Wang et al., 2004]. Restructuring events in improperly paired regions of the chromosomes may thus sustain the differentiation of homeologous chromosomes and promote strict bivalent pairing (i.e. homologous recombination) during the first generations of the diploidization process [Ma and Gustafson, 2005]. This is consistent with the elimination
of sequences from homoeologous chromosome regions in both auto- and allopolyploids during cytological diploidization [Eilam et al., 2009, 2010; Feldman et al., 2012]. Nevertheless, the hypothesis that restructuring is adaptive, improving the fertility of neopolyploids, largely remains to be tested. Genic Incompatibilities and Their Purging Hybridization and genome doubling at the origin of polyploid lineages produces new combinations of interacting genes and, thereby, may reveal genic incompatibilities as well as new gene dosage configurations reducing the hybrid fitness [Maheshwari and Barbash, 2011]. The model of Dobzhansky-Muller interactions (fig.3B) offers the classical framework to understand genic incompatibilities reducing hybrid fitness due to dysfunctional interactions among neutrally or adaptively accumulated alleles at one or several loci [Coyne and Orr, 2004]. Alternative models, such as the mutation-rescue model, may also explain genic incompatibilities, including nucleo-cytoplasmic interactions [reviewed in Nei and Nozawa, 2011]. In the context of polyploid speciation, whole genome duplication will not alleviate the effect of genic incompatibilities revealed by genome merging. Accordingly, a nascent polyploid will suffer from reduced fitness, and its genome has to be rapidly purged from incompatible loci to establish a successful lineage. As loci affecting the viability of both the hybrid and its gametes (i.e. hybrid fertility) can hardly be eliminated through segregation in a polyploid, molecular events such as sequence loss or methylation changes may, therefore, be involved as major mechanisms eliminating or silencing genic incompatibilities [Rieseberg, 2001a]. Adaptive processes may thus partly account for the patterns of genome reorganization commonly observed in nascent polyploids and explain that specific polyploidy-induced genome changes are reproducible. Such a hypothesis, however, remains largely to be tested. Transposable Elements and Hybrid Dysgenesis Transposable elements represent the major and most dynamic fraction of plant genomes [Tenaillon et al., 2010]. Accordingly, diverging taxa likely accumulate differential arrangements of transposable elements, reducing recombination and likely resulting in chromosomal incompatibilities at hybridization [He and Dooner, 2009; Abbott et al., 2013]. Such differential dynamics of transposable elements can also lead to the accumulation of different amounts or differentiated copies in divergent ge90
nomes that may reveal conflicts after genome merging as the hybrid genome fails to regulate their activity (fig.3D). The activity of transposable elements is indeed controlled by repressive small interfering RNA (siRNA) targeting and silencing homologous inserted copies via DNA methylation and other epigenetic marks [Bourchis and Voinnet, 2010]. In somatic cells, siRNA and transposable elements match, ensuring proper repression and genome stability [Martienssen, 2010]. The soft reactivation of transposable elements during gametogenesis boost the production of siRNAs in accompanying cells and ensures the maintenance of repression across generations. However, cytoplasmic siRNA may fail to repress all copies after the merging of genomes presenting large divergence in their transposable elements content [reviewed in Parisod and Senerchia, 2013]. Such conflicts may even be stronger in the endosperm, where 2 maternal genomes are merged with the paternal one. The resulting activation of transposable elements during the merging of divergent genomes may lead to transposition burst and/or epigenetic repatterning, leading to developmental failure in the endosperm and deleterious mutations in the zygote (i.e. hybrid dysgenesis). In the context of polyploid speciation, genome doubling or the purging of localized loci is unexpected to mitigate the impact of the activation of interspersed transposable elements. Successful neopolyploids have to effectively repress active transposable elements at a genomewide scale through loss of sequences that would otherwise have proliferated and strong reorganization of epigenetic marks promoting their silencing. Accordingly, polyploidy seems to induce genome-wide restructuring and epigenetic re-patterning with genome changes specifically affecting transposable elements as soon as divergent genomes are merged [Parisod et al., 2010b]. Despite recent progresses [reviewed in Parisod and Senerchia, 2013; Bento et al., this issue], several aspects of the conflict among transposable elements and its resolution remain to be elucidated. Long-Term Diploidization Polyploidy is assumed to promote evolutionary novelties, and it is, therefore, essential to better understand the forces behind the maintenance of duplicated sequences [McGrath and Lynch, 2012]. Genome structural differentiation supports proper homologous paring (i.e. cytological diploidization) but is also suggested to facilitate functional diploidization by restricting intergenomic recombination and thus favoring the divergence of duplicated gene [Feldman et al., 2012]. Several models have been
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proposed to explain the fate of duplicated genes toward either nonfunctional pseudogenes or subfunctionalized genes having partitioned the ancestral function or neofunctionalized genes with new functions [Innan and Kondrashov, 2010]. In particular, the dosage balance hypothesis [Birchler and Veitia, 2012] seems to match observed patterns of long-term retention of dosage-sensitive genes better than the long-held hypothesis postulating relaxed purifying selection on redundant functions [Ohno, 1970; Force et al., 1999]. Whole genome duplication indeed creates whole sets of redundant functional genes that interact through proper stoichiometric relationships, representing a potentially strong constraint selecting for genome stability. Accordingly, it would be crucial to assess to what extent functional genes are differentially constrained in autoversus allopolyploids. Polyploidy is often considered as a mechanism of abrupt speciation [Coyne and Orr, 2004] and indeed appear as a major mechanism of speciation, accounting for at least 15% of speciation events in flowering plants [Wood et al., 2009]. However, post-zygotic barriers among ploidy levels are all but impermeable [e.g. Brochmann et al., 1992; Petit et al., 1999; Slotte et al., 2008; Chapman and Abbott, 2010], and the recurrent production of polyploid lineages may further contribute to indirect gene exchange between ploidy levels [Soltis and Soltis, 1999; Modliszewski and Willis, 2012]. In addition, recently formed polyploids must establish self-sustainable populations by colonizing new territories or persisting in sympatry with the parental populations [Levin, 2002]. Especially in the case of sympatry, neopolyploids must overcome the minority disadvantage and then have to adapt to new niches in order to avoid competition with the parental progenitors [Levin, 1975; Felber, 1991]. In other words, nascent polyploids have to achieve complete reproductive isolation, and this could be promoted by both restructuring and functional changes. Polyploidy-induced genome reorganization improving fertility in the short-term may thus further promote reproductive isolation of the neopolyploids. To what extent long-term diploidization fosters the diversification of established polyploids remains an open question. For instance, Okas model [Oka, 1957], which was later popularized as the duplication-degeneracycomplementation model [Force et al., 1999], suggests that pseudogenization or the transposition of alternative copies 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 unraveled in Arabidopsis and rice by showing that random seg-
regation of copies of a duplicated gene produced gametes and hybrids without functional copies, suffering from reduced fitness [Bikard et al., 2009; Mizuta et al., 2010]. In strike contrast, recent phylogenetic analyses suggest that recently formed polyploids show higher extinction rates and possibly lower net diversification rates than their diploid relatives [Mayrose et al., 2011; Arrigo and Barker, 2012]. Additional work on genome reorganization in auto- and allopolyploids as compared to diploids is needed to better understand the evolutionary consequences of polyploidy.
Perspectives
Impact of Hybridization and Pathways to Polyploidy on Genome Reorganization Additional studies addressing the patterns and the tempo of restructuring and functional changes in autoversus allopolyploid genomes are necessary to reach firm conclusions, but the limited evidence available in autopolyploids suggests lower levels of genome restructuring and epigenetic changes than in allopolyploids [Parisod et al., 2010a]. Correspondingly, the relative impact of hybridization and genome doubling on the genome/transcriptome shock deserves further attention. Hybridization more than genome doubling seems to trigger quick genome reorganization [Doyle et al., 2008; Hegarty and Hiscock, 2008; Feldman et al., 2012; Parisod and Senerchia, 2013]. For instance, hybridization induced at least 5 times more structural, epigenetic and gene expression changes across the genome than chromosome doubling in Spartina anglica [Parisod et al., 2009; Chelaifa et al., 2010]. Changes in gene expression were mostly attributed to genome merging in several systems [e.g. Albertin et al., 2005; Flagel et al., 2008], but changes induced by hybridization were, to a certain extent, reversed by genome doubling in others [e.g. Hegarty et al., 2006; Xu et al., 2012b]. A better understanding of the impact of merging increasingly divergent genomes in revealing hybrid incompatibilities and inducing genome reorganization seems crucial. In order to better understand genome reorganization in the short term, the early chain of events at the origin of a polyploid lineage may reveal crucial [Hegarty and Doyle, this issue]. Natural polyploids can indeed be formed through various pathways, potentially involving the merging of different dosage of parental genomes and different rounds of genome merging versus doubling. The exact pathway at the origin of a given polyploid may
thus play a fundamental role in triggering particular genome changes. Accordingly, allopolyploid lines of Brassica napus produced through somatic doubling of F1 homoploid hybrids versus pathways involving unreduced gametes showed different patterns of genome restructuring [Szadkowski et al., 2011]. In particular, patterns of genome reorganization in the polyploid formed through the fusion of unreduced gametes were similar to the changes observed in the established polyploid. Exceedingly few studies addressed the impact of the pathway to polyploidy on genome changes, but it may be fundamental. As the production of synthetic polyploids contrasts with the variety of possible pathways at the origin(s) of natural polyploids, a better understanding of the impacts of hybridization and whole genome duplication as well as the timing of these events on genome reorganization seems crucial to draw suitable conclusions from synthetic polyploids. Emergence of a Diverge, Merge and Diverge Model The realization that the origin of almost all polyploids involves the merging of more or less differentiated genomes emphasizes the need to focus on the nature of this divergence. In particular, genome divergence goes along with the accumulation of incompatible loci, which is consistent with the declining fertility of hybrids from closely related to more divergent taxa [Grant, 1981; Rieseberg and Willis, 2007]. Nevertheless, the potential for hybridization declines relatively slowly [Levin, 2012], and genomes harboring structural, genic and/or transposable element incompatibilities can merge to form new polyploid lineages [Buggs et al., 2011; Abbott et al., 2013]. Resulting interactions between genomes potentially affect the survival, establishment and persistence of nascent polyploids in the short-term [Parisod, 2012]. Polyploid lineages are seemingly formed more commonly than established, and only those having efficiently purged incompatible loci through genome reorganization may successfully establish lasting lineages. Accordingly, selection improving hybrid fitness could promote short-term reorganization of polyploid genomes. The divergence of diploid genomes at incompatible loci may thus be a suitable predictor of polyploid genome differentiation after genome merging and diverge, merge and diverge matches the observed genome dynamics during polyploid speciation. Successful polyploids formed from increasingly divergent genomes are expected to show increasing levels of restructuring and epigenetic repatterning to eliminate the gradually accumulated genic incompatibilities or con92
flicting copies of transposable elements [Abbott et al., 2013]. Genic incompatibilities should be purged through the reorganization of specific loci, whereas incompatibilities associated with transposable elements likely induce genome-wide changes [Parisod and Senerchia, 2013]. Structural incompatibilities are also expected to drive cytological diploidization, promoting an increased number of bivalents at the expense of multivalents [Feldman et al., 2012]. However, such diploidization may depend on the impact of multivalents on fitness, and patterns of restructuring may fundamentally differ in autoversus allopolyploids [Cifuentes et al., 2010; Parisod et al., 2010a; Soltis et al., 2010]. Cytological diploidization is still poorly understood, especially in autopolyploids, and both its genetic basis and adaptive value have to be firmly assessed [Le Comber et al., 2010]. Diverge, merge and diverge may be a useful metaphor, but several aspects of the relationship between divergence at the diploid level and genome reorganization at the polyploid level remain to be explored and tested. In particular, genome reorganization following the merging of diploids harboring various categories of incompatibilities may be hardly predictable [Abbott et al., 2013]. Moreover, the role of genetic drift versus selection in sorting genome changes occurring after polyploidy has to be firmly assessed. Genome reorganization may well improve the fitness of nascent polyploids, but to what extent revolutionary changes fostered by the purging of hybrid incompatibilities are reinforced to facilitate the establishment of polyploids remains an open question. Accordingly, the impact of short-term genome changes on the long-term maintenance of duplicated genes as well as the impact of long-term diploidization on the diversification of autoversus allopolyploids should be further examined. Polyploidy is more than the reshuffling of parental genomes and thus offers promising opportunities to integrate genome and phenotypic variation within a coherent evolutionary framework [Parisod, 2012].
Acknowledgements
We would like to thank Richard Buggs, Natacha Senerchia and 2 anonymous reviewers for constructive comments on the manuscript as well as the Swiss National Science Foundation (grant PZ00P3-131950) and the Velux Stiftung for funding.
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References
Abbott R, Lowe A: Origins, establishment and evolution of new polyploid species: Senecio cambrensis and S. eboracensis in the British Isles. Biol J Linn Soc Lond 82:467474 (2004). Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJ, et al: Hybridization and speciation. J Evol Biol 26:229246 (2013). Adams K, Cronn R, Percifield R, Wendel J: Genes duplicated by polyploidy show unequal contributions to the transcriptome and organspecific reciprocal silencing. Proc Natl Acad Sci USA 100:46494654 (2003). Albertin W, Brabant P, Catrice O, Eber F, Jenczewski E, et al: Autopolyploidy in cabbage (Brassica oleracea L.) does not alter significantly the proteomes of green tissues. Proteomics 5:21312139 (2005). Albertin W, Alix K, Balliau T, Brabant P, Davanture M, et al: Differential regulation of gene products in newly synthesized Brassica napus allotetraploids is not related to protein function nor subcellular localization. BMC Genomics 8:56 (2007). Arrigo N, Barker MS: Rarely successful polyploids and their legacy in plant genomes. Curr Op Pl Biol 15:140146 (2012). Arrigo N, Felber F, Parisod C, Buerki S, Alvarez N, et al: Origin and expansion of the allotetraploid Aegilops geniculata, a wild relative of wheat. New Phytol 187:11701180 (2010). Aversano R, Di Dato F, Di Matteo A, Frusciante L, Carputo D: AFLP analysis to assess genomic stability in Solanum regenerants derived from wild and cultivated species. Plant Biotech Rep 5:265271 (2011). Beaulieu J, Jean M, Belzile F: The allotetraploid Arabidopsis thalianaArabidopsis lyrata subsp. petraea as an alternative model system for the study of polyploidy in plants. Mol Genet Gen 281:421435 (2009). Bever JD, Felber F: The theoretical population genetics of polyploidy. Oxford Surv Evol Biol 8: 185217 (1992). Bikard D, Patel D, Le Mett C, Giorgi V, Camilleri C, et al: Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323:623626 (2009). Birchler JA, Veitia RA: Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Proc Natl Acad Sci USA 109:1474614753 (2012). Blanc G, Wolfe K: Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16: 16671678 (2004). Bourchis D, Voinnet O: A small-RNA perspective on gametogenesis, fertilization, and early zygotic development. Science 330: 617622 (2010). Bretagnolle F: Pollen production and spontaneous polyploidization in diploid populations of Anthoxanthum alpinum. Biol J Linn Soc 72: 241247 (2001). Bretagnolle F, Thompson J: Gametes with the stomatic chromosome number: mechanisms of their formation and role in the evolution of autopolypoid plants. New Phytol 129: 122 (1995). Brink RA, Cooper DC: The endosperm in seed development. Bot Rev 13:479541 (1947). Brochmann C, Soltis PS, Soltis DE: Multiple origins of the octoploid Scandinavian endemic Draba cacuminum: electrophoretic and morphological evidence. Nord J Bot 12: 257272 (1992). Brownfield L, Khler C: Unreduced gamete formation in plants: mechanisms and prospects. J Exp Bot 62:16591668 (2011). Buggs RJA, Doust A, Tate J, Koh J, Soltis K, et al: Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids. Heredity 103:7381 (2009). Buggs RJA, Soltis PS, Soltis DE: Biosystematic relationships and the formation of polyploids. Taxon 60:324332 (2011). Buggs RJA, Chamala S, Wu W, Tate JA, Schnable PS, et al: Rapid, repeated, and clustered loss of duplicate genes in allopolyploid plant populations of independent origin. Curr Biol 22: 248252 (2012). Butruille DV, Boiteux LS: Selection-mutation balance in polysomic tetraploids: impact of double reduction and gametophytic selection on the frequency and subchromosomal localization of deleterious mutations. Proc Natl Acad Sci USA 97:66086613 (2000). Chantret N, Salse J, Sabot F, Rahman S, Bellec A, et al: Molecular basis of evolutionary events that shaped the hardness locus in diploid and polyploid wheat species (Triticum and Aegilops). Plant Cell 17:10331045 (2005). Chapman MA, Abbott RJ: Introgression of fitness genes across a ploidy barrier. New Phytol 186: 6371 (2010). Chelaifa H, Monnier A, Ainouche M: Transcriptomic changes following recent natural hybridization and allopolyploidy in the salt marsh species Spartina townsendii and Spartina anglica (Poaceae). New Phytol 186: 161174 (2010). Chester M, Gallagher JP, Symonds VV, Cruz da Silva AV, Mavrodiev EV, et al: Extensive chromosomal variation in a recently formed natural allopolyploid species, Tragopogon miscellus (Asteraceae). Proc Natl Acad Sci USA 109:11761181 (2012). Church SA, Spaulding EJ: Gene expression in a wild autopolyploid sunflower series. J Hered 100:491495 (2009). Cifuentes M, Grandont L, Moore G, Chvre AM, Jenczewski E: Genetic regulation of meiosis in polyploid species: new insights into an old question. New Phytol 186:2936 (2010). Clausen J, Keck DD, Hiesey WM: Plant Evolution through Amphiploidy and Autoploidy, with Examples from the Madiinae (Carnegie Institution of Washington, Washington 1945). Comai L: The advantages and disadvantages of being polyploid. Nat Rev Genet 6: 836846 (2005). Coyne J, Orr H: Speciation (Sinauer Associates, Sunderland 2004). dErfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, et al: Mutations in AtPS1 (Arabidopsis thaliana Parallel Spindle 1) lead to the production of diploid pollen grains. PLoS Genet 4:e1000274 (2008). Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, et al: Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet 42:443461 (2008). Ehrendorfer F: Polyploidy and distribution, in Lewis WH (ed): Polyploidy. Biological Relevance, pp 4560 (Plenum Press, New York 1980). Eilam T, Anikster Y, Millet E, Manisterski J, Feldman M: Nuclear DNA amount and genome downsizing in natural and synthetic allopolyploids of the genera Aegilops and Triticum. Genome 51:616627 (2008). Eilam T, Anikster Y, Millet E, Manisterski J, Feldman M: Genome size in natural and synthetic autopolyploids and in a natural segmental allopolyploid of several Triticeae species. Genome 52:275285 (2009). Eilam T, Anikster Y, Millet E, Manisterski J, Feldman M: Genome size in diploids, allopolyploids, and autopolyploids of mediterranean Triticeae. J Bot 2010:ID341380 (2010). Favarger C: Cytogeography and biosystematics, in Grant WF (ed): Plant Biosystematics, pp 453476 (Academic Press, Vancouver 1984). Fedoroff NV: Transposable elements, epigenetics, and genome evolution. Science 338: 758767 (2012). Felber F: Establishment of a tetraploid cytotype in a diploid poplation: effect of relative fitness of the cytotypes. J Evol Biol 4:195207 (1991). Feldman M, Levy A, Chalhoub B, Kashkush K: Genomic plasticity in polyploid wheat, in Soltis PS, Soltis DE (eds): Polyploidy and Genome Evolution, pp 109135 (Springer, Berlin Heidelberg 2012). Flagel L, Udall J, Nettleton D, Wendel J: Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biol 6:16 (2008). Force A, Lynch M, Pickett F, Amores A, Yan Y, Postlethwait J: Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:15311545 (1999). Fulneek J, Matyek R, Kovak A: Faithful inheritance of cytosine methylation patterns in repeated sequences of the allotetraploid tobacco correlates with the expression of DNA methyltransferase gene families from both parental genomes. Mol Genet Genomics 281: 407420 (2009). Gaeta RT, Pires JC: Homeologous recombination in allopolyploids: the polyploid ratchet. New Phytol 186:1828 (2010).
93
94
Tayal/Parisod
Gaeta RT, Pires JC, Iniguez-Luy F, Leon E, Osborn TC: Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell 19: 3403 3417 (2007). Grant V: Plant Speciation (Columbia University Press, New York 1981). Griffiths S, Sharp R, Foote TN, Bertin I, Wanous M, et al: Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439:749752 (2006). Grover CE, Yu Y, Wing RA, Paterson AH, Wendel JF: A phylogenetic analysis of indel dynamics in the cotton genus. Mol Biol Evol 25: 14151428 (2008). Grover CE, Gallagher JP, Szadkowski EP, Yoo MJ, Flagel LE, Wendel JF: Homoeolog expression bias and expression level dominance in allopolyploids. New Phytol 196:966971 (2012). Han FP, Fedak G, Ouellet T, Liu B: Rapid genomic changes in interspecific and intergeneric hybrids and allopolyploids of Triticeae. Genome 46:716723 (2003). Han FP, Fedak G, Guo WL, Liu B: Rapid and repeatable elimination of a parental genomespecific DNA repeat (pGcIR-1a) in newly synthesized wheat allopolyploids. Genetics 170:12391245 (2005). Harlan J, DeWet J: On O. Winge and a prayer: the origins of polyploidy. Bot Rev 41: 361390 (1975). Hauber DP, Reeves A, Stack SM: Synapsis in a natural autotetraploid. Genome 42: 936949 (1999). He L, Dooner HK: Haplotype structure strongly affects recombination in a maize genetic interval polymorphic for Helitron and retrotransposon insertions. Proc Natl Acad Sci USA 106:84108416 (2009). Hegarty M, Hiscock S: Genomic clues to the evolutionary success of polyploid plants. Curr Biol 18:R435R444 (2008). Hegarty M, Barker G, Wilson I, Abbott R, Edwards K, Hiscock S: Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Curr Biol 16:16521659 (2006). Higgins J, Magusin A, Trick M, Fraser F, Bancroft I: Use of mRNA-seq to discriminate contributions to the transcriptome from the constituent genomes of the polyploid crop species Brassica napus. BMC Genomics 13:247 (2012). Hu G, Hawkins JS, Grover CE, Wendel JF: The history and disposition of transposable elements in polyploid Gossypium. Genome 53: 599607 (2010). Husband B: The role of triploid hybrids in the evolutionary dynamics of mixed-ploidy populations. Biol J Linn Soc 82:537546 (2004). Innan H, Kondrashov F: The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 11: 97108 (2010). Jackson RC: Polyploidy and diploidy: new perspectives on chromosome paring and its evolutionary implications. Am J Bot 69: 1512 1523 (1982).
Jackson RC, Jackson JW: Gene segregation in autotetraploids: prediction from meiotic configurations. Am J Bot 83:673678 (1996). Jakobsson M, Hagenblad J, Tavar S, Sll T, Halldn C, et al: A unique recent origin of the allotetraploid species Arabidopsis suecica: evidence from nuclear DNA markers. Mol Biol Evol 23:12171231 (2006). Jenczewski E, Alix K: From diploids to allopolyploids: the emergence of efficient pairing control genes in plants. Crit Rev Pl Sci 23: 2145 (2004). Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, et al: Ancestral polyploidy in seed plants and angiosperms. Nature 473:97100 (2011). Johnston JS, Pepper AE, Hall AE, Chen ZJ, Hodnett G, et al: Evolution of genome size in Brassicaceae. Ann Bot 95:229235 (2005). Johnston SA, Dennijs TPM, Peloquin SJ, Hanneman RE: The significance of genic balance to endosperm development in interspecific crosses. Theor Appl Genet 57:59 (1980). Kashkush K, Feldman M, Levy AA: Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160:16511659 (2002). Kashkush K, Feldman M, Levy AA: Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33:102106 (2003). Kenan-Eichler M, Leshkowitz D, Tal L, Noor E, Melamed-Bessudo C, et al: Wheat hybridization and polyploidization results in deregulation of small RNAs. Genetics 188: 263272 (2011). Koh J, Soltis PS, Soltis DE: Homeolog loss and expression changes in natural populations of the recently and repeatedly formed allotetraploid Tragopogon mirus (Asteraceae). BMC Genomics 11:97 (2010). Koh J, Chen S, Zhu N, Yu F, Soltis PS, Soltis DE: Comparative proteomics of the recently and recurrently formed natural allopolyploid Tragopogon mirus (Asteraceae) and its parents. New Phytol 196:292305 (2012). Khler C, Mittelsten Scheid O, Erilova A: The impact of the triploid block on the origin and evolution of polyploid plants. Trends Genet 26:142148 (2010). Koukalova B, Moraes AP, Renny-Byfield S, Matyasek R, Leitch AR, Kovarik A: Fall and rise of satellite repeats in allopolyploids of Nicotiana over c. 5 million years. New Phytol 186: 148160 (2010). Kovarik A, Renny-Byfield S, Grandbastien MA, Leitch AR: Evolutionary implications of genome and karyotype restructuring in Nicotiana tabacum L, in Soltis PS, Soltis DE (eds): Polyploidy and Genome Evolution, pp 209 224 (Springer, Berlin Heidelberg 2012). Kraitshtein Z, Yaakov B, Khasdan V, Kashkush K: Genetic and epigenetic dynamics of a retrotransposon after allopolyploidization of wheat. Genetics 186:801812 (2010).
Landergott U, Naciri Y, Schneller JJ, Holderegger R: Allelic configuration and polysomic inheritance of highly variable microsatellites in tetraploid gynodioecious Thymus praecox agg. Theor Appl Genet 113:453465 (2006). Le Comber SC, Ainouche ML, Kovarik A, Leitch AR: Making a functional diploid: from polysomic to disomic inheritance. New Phytol 186:113122 (2010). Leitch AR, Leitch IJ: Genomic plasticity and the diversity of polyploid plants. Science 320: 481483 (2008). Leitch IJ, Bennett MD: Genome downsizing in polyploid plants. Biol J Linn Soc 82: 651663 (2004). Leitch IJ, Hanson L, Lim KY, Kovarik A, Chase MW, et al: The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae). Ann Bot 101:805814 (2008). Levin D: Minority cytotype exclusion in local plant populations. Taxon 24:3543 (1975). Levin D: The Role of Chromosomal Change in Plant Evolution (Oxford University Press, New York 2002). Levin D: The long wait for hybrid sterility in flowering plants. New Phytol 196:666670 (2012). Lewis W: Polyploidy in species populations, in Lewis WH (ed): Polyploidy. Biological Relevance, pp 103144 (Plenum Press, New York 1980). Li X, Yu E, Fan C, Zhang C, Fu T, Zhou Y: Developmental, cytological and transcriptional analysis of autotetraploid Arabidopsis. Planta 236:579596 (2012). Lim KY, Matyasek R, Kovarik A, Leitch AR: Genome evolution in allotetraploid Nicotiana. Biol J Linn Soc 82:599606 (2004). Lim KY, Kovarik A, Matyasek R, Chase M, Clarkson J, et al: Sequence of events leading to nearcomplete genome turnover in allopolyploid Nicotiana within five million years. New Phytol 175:756 (2007). Lim KY, Soltis DE, Soltis PS, Tate J, Matyasek R, et al: Rapid chromosome evolution in recently formed polyploids in Tragopogon (Asteraceae). PLoS One 3:e3353 (2008). Lin BY: Ploidy barrier to endosperm development in maize. Genetics 107:103115 (1984). Liu B, Vega JM, Segal G, Abbo S, Rodova M, Feldman M: Rapid genomic changes in newly synthesized amphiploids of Triticum and Aegilops. I. Changes in low-copy noncoding DNA sequences. Genome 41:272277 (1998). Lu B, Pan X, Zhang L, Huang B, Sun L, et al: A genome-wide comparison of genes responsive to autopolyploidy in Isatis indigotica using Arabidopsis thaliana Affymetrix genechips. Plant Mol Biol Rep 24:197204 (2006). Lukens LN, Pires JC, Leon E, Vogelzang R, Oslach L, Osborn T: Patterns of sequence loss and cytosine methylation within a population of newly resynthesized Brassica napus allopolyploids. Plant Physiol 140:336348 (2006). Luo ZW, Zhang Z, Leach L, Zhang RM, Bradshaw JE, Kearsey MJ: Constructing genetic linkage maps under a tetrasomic model. Genetics 172: 26352645 (2006).
95
Lynch M: The Origins of Genome Architecture (Sinauer Associates Inc., Sunderland 2007). Ma XF, Gustafson J: Genome evolution of allopolyploids: a process of cytological and genetic diploidization. Cytogenet Genome Res 109: 236249 (2005). Mable BK: Breaking down taxonomic barriers in polyploidy research. Trends Plant Sci 8: 582 590 (2003). Mable BK: Why polyploidy is rarer in animals than in plants: myths and mechanisms. Biol J Linn Soc 82:453466 (2004). Mable BK, Alexandrou MA, Taylor MI: Genome duplication in amphibians and fish: an extended synthesis. J Zool 284:151182 (2011). Madlung A, Tyagi AP, Watson B, Jiang H, Kagochi T, et al: Genomic changes in synthetic Arabidopsis polyploids. Plant J 41: 221230 (2005). Maheshwari S, Barbash DA: The genetics of hybrid incompatibilities. Annu Rev Genet 45: 331355 (2011). Mandkov T, Lysak MA: Chromosomal phylogeny and karyotype evolution in x = 7 crucifer species (Brassicaceae). Plant Cell 20: 2559 2570 (2008). Martelotto LG, Ortiz JPA, Stein J, Espinoza F, Quarin CL, Pessino SC: A comprehensive analysis of gene expression alterations in a newly synthesized Paspalum notatum autotetraploid. Plant Sci 169:211220 (2005). Martelotto LG, Ortiz JPA, Stein J, Espinoza F, Quarin CL, Pessino SC: Genome rearrangements derived from autopolyploidization in Paspalum sp. Plant Sci 172:970977 (2007). Martienssen RA: Heterochromatin, small RNA and post-fertilization dysgenesis in allopolyploid and interploid hybrids of Arabidopsis. New Phytol 186:4653 (2010). Mason A, Nelson M, Yan G, Cowling W: Production of viable male unreduced gametes in Brassica interspecific hybrids is genotype specific and stimulated by cold temperatures. BMC Plant Biol 11:103 (2011). Mayrose I, Zhan SH, Rothfels CJ, MagnusonFord K, Barker MS, et al: Recently formed polyploid plants diversify at lower rates. Science 333:1257 (2011). McGrath CL, Lynch M: Evolutionary significance of whole-genome duplication, in Soltis PS, Soltis DE (eds): Polyploidy and Genome Evolution, pp 120 (Springer, Berlin Heidelberg 2012). Mestiri I, Chagu V, Tanguy AM, Huneau C, Huteau V, et al: Newly synthesized wheat allohexaploids display progenitor-dependent meiotic stability and aneuploidy but structural genomic additivity. New Phytol 186:86101 (2010). Mizuta Y, Harushima Y, Kurata N: Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes. Proc Natl Acad Sci USA 107:2041720422 (2010). Modliszewski JL, Willis JH: Allotetraploid Mimulus sookensis are highly interfertile despite independent origins. Mol Ecol 21: 52805298 (2012).
Muntzing A: Multiplication of chromosomes in galeopis crossbreeds and their phylogenetic significance. Hereditas 14:153172 (1930). Muntzing A: The evolutionary significance of autopolyploidy. Hereditas 21:363378 (1936). Nei M, Nozawa M: Roles of mutation and selection in speciation: from Hugo de Vries to the modern genomic era. Genome Biol Evol 3: 812829 (2011). Ng DWK, Zhang C, Miller M, Shen Z, Briggs SP, Chen ZJ: Proteomic divergence in Arabidopsis autopolyploids and allopolyploids and their progenitors. Heredity (Edinb) 108:419 430 (2012). Noor MAF, Feder JL: Speciation genetics: evolving approaches. Nat Rev Genet 7:851861 (2006). Ohno S: Evolution by Gene Duplication (Springer Verlag, Berlin 1970). Oka HI: Genetic analysis for the sterility of hybrids between distantly related varieties of cultivated rice. J Genet 55:397409 (1957). Otto S: The evolutionary consequences of polyploidy. Cell 131:452462 (2007). Otto S, Whitton J: Polyploid incidence and evolution. Annu Rev Genet 34:401437 (2000). Ozkan H, Levy AA, Feldman M: Allopolyploidyinduced rapid genome evolution in the wheat (Aegilops-Triticum) group. Plant Cell 13: 17351747 (2001). Ozkan H, Tuna M, Arumuganathan K: Nonadditive changes in genome size during allopolyploidization in the wheat (Aegilops-Triticum) group. J Hered 94:260264 (2003). Ozkan H, Tuna M, Galbraith DW: No DNA loss in autotetraploids of Arabidopsis thaliana. Plant Breed 125:288291 (2006). Parisod C: Polyploids integrate genomic changes and ecological shifts. New Phytol 193: 297 300 (2012). Parisod C, Besnard G: Glacial in situ survival in the Western Alps and polytopic autopolyploidy in Biscutella laevigata L. (Brassicaceae). Mol Ecol 16:27552767 (2007). Parisod C, Senerchia N: The response of transposable elements to polyploidy, in Grandbastien MA, Casacuberta JM (eds): Plant Transposable Elements, Topics in Current Genetics, pp 147168 (Springer, Berlin Heidelberg 2013). Parisod C, Holderegger R, Brochmann C: Evolutionary consequences of autopolyploidy. New Phytol 186:517 (2010a). Parisod C, Alix K, Just J, Petit M, Sarilar V, et al: Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytol 186:3745 (2010b). Parisod C, Salmon A, Zerjal T, Tenaillon M, Grandbastien MA, Ainouche M: Rapid structural and epigenetic reorganization near transposable elements in hybrid and allopolyploid genomes in Spartina. New Phytol 184: 10031015 (2009). Parisod C, Mhiri C, Lim KY, Clarkson JJ, Chase MW, et al: Differential dynamics of transposable elements during long-term diploidization of Nicotiana Section Repandae (Solanaceae) allopolyploid genomes. PLoS One 7: e50352 (2012).
Petit C, Bretagnolle F, Felber F: Evolutionary consequences of diploid-polyploid hybrid zones in wild species. Trends Ecol Evol 14:306311 (1999). Petit M, Lim KY, Julio E, Poncet C, Dorlhac de Borne F, et al: Differential impact of retrotransposon populations on the genome of allotetraploid tobacco (Nicotiana tabacum). Mol Genet Genomics 278:115 (2007). Petit M, Guidat C, Daniel J, Denis E, Montoriol E, et al: Mobilization of retrotransposons in synthetic allotetraploid tobacco. New Phytol 186: 135147 (2010). Pires JC, Zhao J, Schranz ME, Leon EJ, Quijada PA, et al: Flowering time divergence and genomic rearrangements in resynthesized Brassica polyploids (Brassicaceae). Biol J Linn Soc 82:675688 (2004). Qi B, Huang W, Zhu B, Zhong X, Guo J, et al: Global transgenerational gene expression dynamics in two newly synthesized allohexaploid wheat (Triticum aestivum) lines. BMC Biol 10:3 (2012). Raina SN, Parida A, Koul KK, Salimath SS, Bisht MS, et al: Associated chromosomal DNA changes in polyploids. Genome 37: 560564 (1994). Ramsey J: Unreduced gametes and neopolyploids in natural populations of Achillea borealis. Heredity 98:143150 (2007). Ramsey J, Schemske DW: Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst 29:467501 (1998). Ramsey J, Schemske DW: Neopolyploidy in flowering plants. Annu Rev Ecol Syst 33: 589639 (2002). Renny-Byfield S, Chester M, Kovak A, Le Comber SC, Grandbastien MA, et al: Next generation sequencing reveals genome downsizing in allotetraploid Nicotiana tabacum, predominantly through the elimination of paternally derived repetitive DNAs. Mol Biol Evol 28:28432854 (2011). Riddle N, Jiang H, An L, Doerge R, Birchler J: Gene expression analysis at the intersection of ploidy and hybridity in maize. Theor Appl Genet 120:341353 (2010). Rieseberg LH: Polyploid evolution: keeping the peace at genomic reunions. Curr Biol 11:R925R928 (2001a). Rieseberg LH: Chromosomal rearrangements and speciation. Trends Ecol Evol 16:351358 (2001b). Rieseberg LH, Willis JH: Plant speciation. Science 317:910914 (2007). Rivero-Guerra AO: Cytogenetics, geographical distribution, and pollen fertility of diploid and tetraploid cytotypes of Santolina pectinata Lag. (Asteraceae: Anthemideae). Bot J Linn Soc 156:657667 (2008). Ronfort J, Jenczewski E, Bataillon T, Rousset F: Analysis of population structure in autotetraploid species. Genetics 150:921930 (1998). Salina EA, Numerova OM, Ozkan H, Feldman M: Alterations in subtelomeric tandem repeats during early stages of allopolyploidy in wheat. Genome 47:860867 (2004).
Santos JL, Alfaro D, Sanchez-Moran E, Armstrong SJ, Franklin FCH, Jones GH: Partial diploidization of meiosis in autotetraploid Arabidopsis thaliana. Genetics 165: 1533 1540 (2003). Segraves KA, Thompson JN, Soltis PS, Soltis DE: Multiple origins of polyploidy and the geographic structure of Heuchera grossulariifolia. Mol Ecol 8:253262 (1999). Shaked H, Kashkush K, Ozkan H, Feldman M, Levy A: Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13: 17491759 (2001). Shore JS: Tetrasomic inheritance and isozyme variation in Turnera ulmifolia vars. elegans Urb. and intermedia Urb. (Turneraceae). Heredity 66:305312 (1991). Skalick K, Lim KY, Matyasek R, Matzke M, Leitch AR, Kovarik A: Preferential elimination of repeated DNA sequences from the paternal, Nicotiana tomentosiformis genome donor of a synthetic, allotetraploid tobacco. New Phytol 166:291303 (2005). Slotkin RK, Martienssen R: Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272285 (2007). Slotte T, Huang H, Lascoux M, Ceplitis A: Polyploid speciation did not confer instant reproductive isolation in Capsella (Brassicaceae). Mol Biol Evol 25:14721481 (2008). Soltis DE, Soltis PS: Polyploidy: recurrent formation and genome evolution. Trends Ecol Evol 14:348352 (1999). Soltis DE, Soltis PS: Polyploidy and Genome Evolution (Springer, Berlin Heidelberg 2012). Soltis DE, Soltis PS, Pires J, Kovarik A, Tate J, Mavrodiev E: Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytogentic, genomic and genetic comparisons. Biol J Linn Soc Lond 82:485501 (2004). Soltis DE, Soltis PS, Schemske DW, Hancock JF, Thompson JN, et al: Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon 56:1330 (2007). Soltis DE, Buggs RA, Doyle JJ, Soltis PS: What we still dont know about polyploidy. Taxon 59: 13871403 (2010). Soltis DE, Buggs RA, Barbazuk WB, Chamala S, Chester M, et al: The early stages of polyploidy: rapid and repeated evolution in Tragopogon, in Soltis PS, Soltis DE (eds): Polyploidy and Genome Evolution, pp 271292 (Springer, Berlin Heidelberg 2012). Song KM, Lu P, Tang KL, Osborn TC: Rapid genome change in synthetic polyploids of Brassica and its implication for polyploid evolution. Proc Natl Acad Sci USA 92: 77197723 (1995).
Stebbins G: The inviability, weakness, and sterility of interspecific hybrids. Adv Genet 9: 147 (1958). Stebbins GL: Types of polyploids: their classification and significance. Adv Genet 1: 403429 (1947). Stebbins GL: Chromosomal Evolution in Higher Plants (Edward Arnold, London 1971). Stewart MN, Dawson DS: Changing partners: moving from non-homologous to homologous centromere pairing in meiosis. Trends Genet 24:564573 (2008). Stift M, Berenos C, Kuperus P, van Tienderen PH: Segregation models for disomic, tetrasomic and intermediate inheritance in tetraploids: a general procedure applied to Rorippa (Yellow Cress) microsatellite data. Genetics 179: 21132123 (2008). Stupar RM, Bhaskar PB, Yandell BS, Rensink WA, Hart AL, et al: Phenotypic and transcriptomic changes associated with potato autopolyploidization. Genetics 176:20552067 (2007). Szadkowski E, Eber F, Huteau V, Lod M, Coriton O, et al: Polyploid formation pathways have an impact on genetic rearrangements in resynthesized Brassica napus. New Phytol 191: 884894 (2011). Tate JA, Ni Z, Scheen AC, Koh J, Gilbert CA, et al: Evolution and expression of homeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid. Genetics 173:15991611 (2006). Tenaillon MI, Hollister JD, Gaut BS: A triptych of the evolution of plant transposable elements. Trends Plant Sci 15:471478 (2010). Wang J, Tian L, Madlung A, Lee HS, Chen M, et al: Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. Genetics 167:19611973 (2004). Wang J, Tian L, Lee HS, Wei N, Jiang H, et al: Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172: 507517 (2006). Weiss H, Maluszynska J: Chromosomal rearrangement in autotetraploid plants of Arabidopsis thaliana. Hereditas 133: 255261 (2001). Weiss-Schneeweiss H, Schneeweiss GM, Stuessy TF, Mabuchi T, Park JM, et al: Chromosomal stasis in diploids contrasts with genome restructuring in auto- and allopolyploid taxa of Hepatica (Ranunculaceae). New Phytol 174: 669682 (2007). Wendel J, Flagel L, Adams K: Jeans, genes, and genomes: cotton as a model for studying polyploidy, in Soltis PS, Soltis DE (eds): Polyploidy and Genome Evolution, pp 181207 (Springer, Berlin Heidelberg 2012). Wendel JF: Genome evolution in polyploids. Plant Mol Biol 42:225249 (2000).
Wendel JF, Cronn RC: Polyploidy and the evolutionary history of cotton. Adv Agron 78:139 186 (2003). Widmer A, Baltisberger M: Molecular evidence for allopolyploid speciation and single origin of the narrow endemic Draba ladina (Brassicaceae). Am J Bot 86:12821289 (1999). Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH: The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci USA 106: 1387513879 (2009). Xiong Z, Gaeta RT, Pires JC: Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proc Natl Acad Sci USA 108:79087913 (2011). Xu Y, Zhao Q, Mei S, Wang J: Genomic and transcriptomic alterations following hybridisation and genome doubling in trigenomic allohexaploid Brassica carinata Brassica rapa. Plant Biol 14:734744 (2012a). Xu Y, Xu H, Wu X, Fang X, Wang J: Genetic changes following hybridization and genome doubling in synthetic Brassica napus. Biochem Genet 50:616624 (2012b). Yaakov B, Kashkush K: Massive alterations of the methylation patterns around DNA transposons in the first four generations of a newly formed wheat allohexaploid. Genome 54:42 49 (2011). Yang X, Ye CY, Cheng ZM, Tschaplinski T, Wullschleger S, et al: Genomic aspects of research involving polyploid plants. Plant Cell Tiss Org 104:387397 (2011). Yu Z, Haberer G, Matthes M, Rattei T, Mayer KFX, et al: Impact of natural genetic variation on the transcriptome of autotetraploid Arabidopsis thaliana. Proc Natl Acad Sci USA 107: 1780917814 (2010). Zhang LQ, Liu DC, Zheng YL, Yan ZH, Dai SF, et al: Frequent occurrence of unreduced gametes in Triticum turgidum-Aegilops tauschii hybrids. Euphytica 172:285294 (2010). Zhao N, Zhu B, Li M, Wang L, Xu L, et al: Extensive and heritable epigenetic remodeling and genetic stability accompany allohexaploidization of wheat. Genetics 188:499510 (2011). Zhou R, Moshgabadi N, Adams KL: Extensive changes to alternative splicing patterns following allopolyploidy in natural and resynthesized polyploids. Proc Natl Acad Sci USA 108:1612216127 (2011). Zou J, Fu D, Gong H, Qian W, Xia W, et al: De novo genetic variation associated with retrotransposon activation, genomic rearrangements and trait variation in a recombinant inbred line population of Brassica napus derived from interspecific hybridization with Brassica rapa. Plant J 68:212224 (2011).
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Natural Pathways To Polyploidy in Plants and Cosequences For Genome Reorganization

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Natural Pathways to Polyploidy and Consequences for Genome Organization and Genome Size

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Natural Pathways to Polyploidy in Plants and Consequences for Genome Reorganization

2013 S. Karger AG, Basel 14248581/13/14040079$38.00/0 E-Mail karger@karger.com www.karger.com/cgr

Paleo- versus Neopolyploids and Auto- versus Allopolyploids

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Natural Pathways at the Origins of Polyploids

Pathways to Polyploidy and Genome Reorganization

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Patterns of Genome Changes after Polyploidization

Fig. 2. Commonly reported genome changes after polyploidization

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Hordeum bulbosum and H. marinum

Hordeum murinum L. subsp. murinum Auto

Triticum Aegilops spp.

Pathways to Polyploidy and Genome Reorganization

Triticum Aegilops spp.

Triticum Aegilops spp.

Arabidopsis thaliana A. lyrata

Brassica juncea, B. napus

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Brassica rapa B. carinata

Hordeum murinum subsp. leporinum

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Nicotiana. arentsii, N. rustica

Tragopogon miscellus, T. mirus

Pathways to Polyploidy and Genome Reorganization

Triticum Aegilops spp.

Triticum Aegilops spp.

Triticum Aegilops spp.

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Triticum Aegilops spp.

Origins and Consequences of Polyploidy-Induced Genome Reorganization

Fig. 3. Mechanisms of genetic incompatibilities in hybrids. A Structural incompati-

Pathways to Polyploidy and Genome Reorganization

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Pathways to Polyploidy and Genome Reorganization

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Pathways to Polyploidy and Genome Reorganization

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Pathways to Polyploidy and Genome Reorganization

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

Cytogenet Genome Res 2013;140:7996 DOI: 10.1159/000351318

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