Genetic regulation of meiosis in polyploid species - Wiley Online Library

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Research review Genetic regulation of meiosis in polyploid species: new insights into an old question Author for correspondence: Eric Jenczewski Tel: +33 130 833308 Email: [email protected] Received: 21 July 2009 Accepted: 21 September 2009

Marta Cifuentes1,*, Laurie Grandont1,*, Graham Moore2, Anne Marie Che`vre3 and Eric Jenczewski1 1

INRA – Institut Jean Pierre Bourgin, Station de Ge´ne´tique et Ame´lioration des Plantes, Route de

Saint-Cyr, 78026 Versailles Cedex, France; 2John Innes Centre, Colney, Norwich NR4 7UH, UK; 3

INRA, UMR 118, Ame´lioration des Plantes et Biotechnologies Ve´ge´tales, BP 35327, F-35653 Le

Rheu, France

Summary New Phytologist (2010) 186: 29–36 doi: 10.1111/j.1469-8137.2009.03084.x

Key words: chiasmata, cytological diploidization, evolution, genetic regulation, meiosis, Pairing homeologous genes, polyploidy.

Precise chromosome segregation is vital for polyploid speciation. Here, we highlight recent findings that revitalize the old question of the genetic control of diploid-like meiosis behaviour in polyploid species. We first review new information on the genetic control of autopolyploid and allopolyploid cytological diploidization, notably in wheat and Brassica. These major advances provide new opportunities for speculating about the adaptation of meiosis during polyploid evolution. Some of these advances are discussed, and it is suggested that research on polyploidy and on meiosis should no longer be unlinked.

Introduction Meiosis is a fundamental process for all sexual species with direct relevance to natural selection; meiosis leads to the formation of gametes, contributes to genome stability and generates genetic diversity. All these outcomes result from one round of DNA replication followed by two rounds of chromosome segregation, during which chromosome number is halved and genetic recombination occurs. Meiosis relies on the interrelated events of homologous chromosomes recognition, intimate association, synapsis and recombination (Hamant et al., 2006; de Muyt et al., 2009; Fig. 1). Correct segregation of chromosomes requires the formation of stable bivalents at metaphase I (MI) which result from physical connections between homologues (chiasmata) resulting from sister chromatid cohesion and meiotic crossover (Fig. 1; Tease, 1978). Mei*These authors contributed equally to this work.

The Authors (2009) Journal compilation New Phytologist Trust (2009)

otic crossovers are one of the products of meiotic recombination (de Muyt et al., 2009; Gaeta & Pires, 2010) and result in reciprocal exchanges of DNA between homologous chromosomes that are essential for their proper disjunction at the first meiotic division. At least one crossover per chromosome is thus required and it must take place between homologous chromosomes pairs only. Noncrossovers are a second product of meiotic recombination which do not yield reciprocal exchanges and which may occur between nonhomologous chromosomes (e.g. Salmon et al., 2010). Correct segregation of chromosomes is especially demanding in polyploid species which contain more than two sets of chromosomes which need to be sorted out during meiosis to produce balanced gametes; otherwise multiple or illegitimate chiasmatic associations would result in aneuploidy and partial fertility because of homologous chromosome missegregation. Despite intense activity in the research fields of polyploidy and meiosis in

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Review

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Research review Prophase I

Diploid

(a) DNA replication

Leptotene

Zygotene

Pachytene

Diplotene

Diakinesis

Sister chromatids Homologous chromosomes

Autotetraploid

(b)

(c)

Pairs of homologous chromosomes

Allotetraploid

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Pairs of homologous chromosomes

Cohesins

Partner switch

Synaptonemal complex

Chiasma

Bouquet

Fig. 1 Pre-meiotic and early meiotic events in diploid, autotetraploid and allotetraploid species. The figure illustrates the regular meiotic behaviour during prophase I in a diploid (a), an autotetraploid (b) and an allotetraploid (c) species. Meiosis is preceded by one round of DNA replication during which sister chromatids are generated and physically associated by cohesins. For clarity, cohesins (and sister-chromatids) are not represented at every stage of prophase I, although cohesins are present until the end of metaphase I (centromeric cohesion persists until anaphase II). Genetic recombination is initiated during leptotene at the same time as meiotic chromosomes start to condense and search for their homologue. Homologue recognition is thought to be facilitated by the clustering of telomeres forming the bouquet (D) and is followed by synchronized chromatin remodelling of homologues (Prieto et al., 2004; Colas et al., 2008). In allopolyploids, unsynchronized chromatin conformational changes between homeologues (in red and blue) make them less likely to pair. During zygotene, chromosomes start to synapse via the formation of a protein structure known as the synaptonemal complex (SC). The SC forms between pairs of homologous chromosomes in diploids (a) but it can form between more than two homologues in autotetraploids (b, arrow) and between homeologous chromosomes in allotetraploids (c, arrow), resulting in synaptic partner switches at pachytene (w). The formation of SCs and the progression of recombination are intimately related so that, in some species, multiple ⁄ homeologous associations are corrected before crossovers are formed (White et al., 1988; Jenkins & White, 1990). By contrast, in other species, specific localization of crossovers between pairs of homologous chromosomes is responsible for the resolution of multiple ⁄ homeologous associations at diplotene, when the SC is disassembled (Jenkins, 1985). Irrespective of when the corrections occur, only bivalents are visualized at diakinesis when chromosomes recondense.

the last decade (e.g. Doyle et al., 2008; Mercier & Grelon, 2008), research in these two areas has tended to be unlinked. This review aims to provide an updated summary of recent findings showing how correct chromosome segregation is ensured in both autopolyploid and allopolyploid species (notably how it is genetically regulated) and to raise several questions that should be addressed to integrate knowledge of meiosis and the evolution of polyploid species.

New insights into the cytological diploidization of autopolyploid and allopolyploid species Cytological diploidization, the process by which meiosis in polyploids leads to chromosomally and genetically balanced

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gametes, has long been viewed as a critical step for polyploid speciation. This process is fundamentally different in autopolyploid and allopolyploid species, because of their chromosome composition (Fig. 1). Meiosis in autopolyploids Autopolyploids have more than two copies of each chromosome, which have the same chance of recombining at meiosis; crossovers can thus be formed between more than two homologues, resulting in multivalents at MI and chromosome missegregation at anaphase I. The cytological diploidization of autopolyploids is thus viewed as an increased number of bivalents at MI to the detriment of multivalents, but without any consequence for the assortment of chromo-


New Phytologist somes into pairs, which can still be random (Fig. 1b shows only one of the equally probable products of prophase I). Cytological diploidization of autopolyploids has mostly been investigated by comparison to theoretical models and ⁄ or by surveying the evolution of meiosis in newly formed autopolyploids. Theoretical models predicted that two-thirds of the possible number of quadrivalents would be expected if there is no pairing preference, synapsis initiation at both ends of chromosomes and pronounced distal chiasmata location (reviewed in Gillies, 1989). This expectation was experimentally verified in some newly produced and natural autotetraploids, while other species showed fewer quadrivalents than expected (Gillies, 1989; Sybenga, 1996 and references therein). Deviations from expectation may be explained by various factors (see Gillies, 1989 and Santos et al., 2003), including the establishment of a genetic control. For example, Avivi (1976) showed that the frequency of quadrivalents varied depending on the genetic background of Aegilops longissima induced autotetraploid lines. It is also noteworthy that the meiotic behaviour of newly formed autopolyploids can evolve over generations with no obvious reliance on pre-existing genetic variability. In a recent example, Santos et al. (2003) observed that established autotetraploid lines of Arabidopsis thaliana ecotype Columbia showed fewer multivalents than newly synthesized ones, suggesting that partial cytological diploidization occurred over 13 generations. This effect was shown to be line and chromosome dependent and with no clear connection with the number of crossovers per chromosome (Santos et al., 2003). Thus, the cytological diploidization of autopolyploids, and the mechanism(s) involved, vary among lineages and are poorly understood. The genetic basis for reduced multivalent formation, which has been demonstrated in several species (Gillies, 1989), has never been characterized. More investigations are thus required to decipher how this process is achieved and ⁄ or genetically controlled. Meiosis in allopolyploids Allopolyploid species, which have a hybrid origin, combine different sets of related but distinct chromosomes (homeologues). In contrast to the situation in autopolyploids, the cytological diploidization of allopolyploids requires a nonrandom assortment of chromosomes into pairs, with crossovers being exclusively formed between homologues despite possible early promiscuity between homeologues (Fig. 1c). The diploid-like meiotic behaviour of allopolyploids is thought to result from the divergence between homeologous chromosomes, which may already exist and ⁄ or be accentuated at the onset of polyploid formation (Le Comber et al., 2010) and involve the rearrangement of large chromosome fragments, or from the activity of Pairing homeologous (Ph) genes (reviewed in Jenczewski & Alix, 2004). Little is known about the prevalence of these


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two factors, although it is noteworthy that homeologues have usually been found to retain sufficient similarity to be able to recombine with one another under certain circumstances; for example, when chromosome 5B is lacking in wheat (Triticum aestivum and Triticum turgidum), in tall fescue (Festuca arundinacea) and oat (Avena sativa) aneuploids or in oilseed rape (Brassica napus) haploids (Jenczewski & Alix, 2004). In all these species, genetic determination of exclusive crossover formation between homologues is thus predominant and has been shown to rely on a polygenic control, with one locus more influential than the others and frequent gene-dosage effects (Moore, 2002 and references therein). Similarly, reduced chiasma frequency is genetically based in some Lolium interspecific hybrids and corresponding amphidiploids (Taylor & Evans, 1977; Aung & Evans, 1985; Evans & Davies, 1985), demonstrating that genes suppressing crossover formation between nonhomologues can be segregating within a genus that contains no natural polyploid species. Although the systems in oat, fescues and Lolium have not been characterized beyond the demonstration that they exist, new insights have recently been obtained in wheat and Brassica. New advances in wheat Wheat is the only allopolyploid species in which a substantial amount of work has been carried out to study cytological diploidization and identify genes involved in the genetic control of recombination (Boden et al., 2007, 2009; de Bustos et al., 2007), notably between homeologous chromosomes (Sutton et al., 2003; Griffiths et al., 2006; AlKaff et al., 2008). Common bread wheat, T. aestivum, is an allohexaploid species (AABBDD; 2n = 6x = 42) resulting from hybridization between tetraploid wheat, T. turgidum (AABB; 2n = 4x = 28), and Aegilops tauschii (DD; 2n = 14) (Caldwell et al., 2004). Both tetraploid and hexaploid wheats behave as diploids at meiosis. They are strictly bivalent forming and display a disomic inheritance; this demonstrates that bivalents are exclusively formed between homologous chromosomes despite the genetic similarity of homeologues (Sears, 1976). The diploid-like meiotic behaviour of wheat is ensured by a multigenic system (for a review, see Sears, 1976) which includes a locus with a major dominant effect, named Ph1, localized to the long arm of chromosome 5B (Riley & Chapman, 1958). This locus was discovered 50 yr ago but has only recently been characterized at the molecular level; Ph1 was defined as a region containing a cluster of CDK (Cyclin-Dependent Kinase)-related genes interrupted by a heterochromatin segment which made it distinct from its homeologous loci (Griffiths et al., 2006; Al-Kaff et al., 2008). These loci also differ in the number of CDK-like genes (seven for 5B compared with five on 5A and two on 5D), which suggests that these clusters arose by different


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tandem duplication events. Protein alignments showed that these CDK-like genes were closely related to human Cdk2 (Al-Kaff et al., 2008), a functional homologue of the budding yeast meiosis-specific Cdk-like kinase Inducer of meiosis Ime2 (Szwarcwort-Cohen et al., 2009). Recent evidence suggests that Ph1 may behave like a master co-ordinator, as this locus has an effect on premeiotic chromosome arrangement, chromatin organization, chromosome synapsis and recombination (Holm & Wang, 1988; Feldman, 1993; Luo et al., 1996; Mikhailova et al., 1998; Prieto et al., 2004; Colas et al., 2008). Most CDKlike genes from 5A and 5D homeologous regions are not transcribed when Ph1 is present, whereas some of them are expressed when Ph1 is absent (Al-Kaff et al., 2008). This suggests that Ph1 regulates the overall activity of these CDK-like genes. TaASY1 (T. aestivum ASYnapsis) is one of the earliest expressed meiotic genes which encodes a protein associated with the synaptonemal complex (Boden et al., 2007). It was recently shown that absence of Ph1 causes 20-fold increased transcription of TaASY1, implying that Ph1 is activated before TaASY1 expression (Boden et al., 2009). This result may also suggest that Ph1 could also control the transcription of meiotic genes that contribute to the fidelity of synapsis or crossover formation. This ‘causal relationship’ needs to be further investigated to elucidate how Ph1 ensures cytological diploidization in wheat. In addition, different doses of Ph1 were shown to induce different meiotic behaviour (Moore, 2002 for review). Future work should thus be devoted to elucidating how the molecular data are related to all the phenotypic effects associated with the Ph1 locus. A second locus that has been shown to suppress crossovers between homeologous chromosomes is Ph2, located on 3DS (Mello-Sampayo, 1968). The contribution of Ph2 to the diploid-like meiotic behaviour of wheat has been debated because very few homeologous bivalents were observed at MI in a ph2 mutant (Sears, 1982); however, this mutant had an active Ph1 locus that could mask the effect of the Ph2 deletion. When combined with the ph1b mutation, the ph2b mutation was shown to induce a slight increase in crossovers between homeologues (Ceoloni & Donini, 1993), which has kept the debate open. The molecular characterization of Ph2 is still in progress (Sutton et al., 2003) and nothing suggests that the task will be easier than for Ph1. Ph2 was shown to have a different effect from Ph1 and to be involved in the progression of synapsis (Martinez et al., 2001; Prieto et al., 2005). However, the link established between Ph1 and synapsis through TaASY1 (Boden et al., 2009) may lead to the consideration of new relationships between Ph1 and Ph2. Additional, less effective suppressors of crossovers between homeologous chromosomes were discovered on several other chromosomes (Sears, 1976) but they have not been studied to date. Also, high levels of recombination between homeo-


logous chromosomes were observed in some Aegilops speltoides · T. aestivum and Aegilops mutica · T. aestivum hybrids, revealing the presence of Ph1 suppressors in some genotypes of these diploid species (Dvorak et al., 2006). The genes responsible for these phenotypes and their phylogenetic and ⁄ or functional relationships with Ph1 remain to be characterized. New advances in Brassica napus Brassica napus (AACC, 2n = 38) is a recent allotetraploid originating from multiple hybridizations between ancestors of Brassica rapa (AA, 2n = 20) and Brassica oleracea (CC, 2n = 18). B. napus shows a complete diploid-like meiotic behaviour, with only bivalents at MI and a disomic inheritance; thus, in all euploid genotypes, crossovers mostly occur between homologous chromosomes, even if the A and C homeologues are prone to recombine (Nicolas et al., 2007). By contrast, haploids (AC, 19 chromosomes) produced from different varieties of B. napus show different meiotic behaviours at MI, with two main phenotypes being clearly distinguished; some haploids show 8.1–13.8 univalents at MI while others show only 2.35–5.75 univalents at MI depending on the varieties they were isolated from (M. Cifuentes et al., unpublished). Using one segregating population of haploids, these two meiotic phenotypes were shown to be inherited in a seemingly Mendelian fashion, compatible with the segregation of a major gene, called Pairing regulator in B. napus (PrBn), in a background of polygenic variation (Jenczewski et al., 2003). The PrBn locus was localized on C genome linkage group C9 within a 10–20 cM interval. Mapping of PrBn also demonstrated that this locus displayed an incomplete penetrance and that four to six additive and two epistatic quantitative trait loci (QTLs) contributed to determining the meiotic behaviour (at MI) of B. napus haploids (Liu et al., 2006). More recently, by surveying chromosomal rearrangements in two progenies of B. napus haploids with differing PrBn activities, Nicolas et al. (2009) have demonstrated that the two meiotic behaviours observed at MI reflect differences in recombination between homeologous chromosomes; PrBn was shown to have an effect on the frequency but not the distribution of crossovers between homeologous chromosomes during meiosis in B. napus haploids. All chromosomes were found to be rearranged at least once in each population, demonstrating that they were all able to recombine in both genotypes, but with an overall threefold rate difference. Moreover, the same chromosomes were found to be rearranged at a proportionally high, intermediate, or low frequency in the two populations, which indicated that crossover distribution was not random but followed roughly the same rules during meiosis in the B. napus haploids showing different PrBn activi-


New Phytologist ties. Finally, differences in the frequency of homologous recombination were observed in AAC (2n = 29) but not AACC (2n = 38) hybrids produced using the same two B. napus genotypes with different PrBn activities. This may suggest that the PrBn effect on recombination could be dosage sensitive (Nicolas et al., 2009). This hypothesis is currently being tested. The Ph1 story indicates that detailed understanding of the PrBn mode of action requires both an accurate, comparative description of the phenotypes and molecular characterization of this locus. Work is currently underway with the aim of achieving these goals, although they will certainly be as challenging as for Ph1.

New perspectives into the evolution of polyploid meiosis regulation What occurs at the onset of polyploid formation? Meiotic aberrations are commonplace in most newly formed autopolyploid and allopolyploid plants, with direct negative consequences for their fertility, and presumably their early demographic success (Ramsey & Schemske, 2002; Gaeta & Pires, 2010). However, bivalents represent the main meiotic configuration observed at MI in most synthetic polyploids and the reduction of fertility can be modest in some of these plants (Ramsey & Schemske, 2002). Also, natural populations of recently formed allotetraploid Tragopogon mirus and Tragopogon miscellus were shown to contain a high number of plants with unbalanced genomic composition, some of them being highly fertile (Lim et al., 2008). Although the long-term fate of these populations is uncertain, they demonstrate that newly formed polyploids can persist for c. 40 generations, sometimes despite early bottlenecks of reduced fertility. May this period of time, whose duration is difficult to predict, provide a ‘window of opportunity’ for natural selection to promote increased cytological diploidization, by favouring the most fertile individuals among which those with the most regular meiosis are likely to be overrepresented? And is there a general molecular basis for increased cytological diploidization (Le Comber et al., 2010)? As fertility selection on neopolyploid populations usually results in increased bivalent formation (Ramsey & Schemske, 2002 and references therein), the genesis or selection of Ph-like genes is a logical process to consider.

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they developed subsequent to the origin of the polyploid species. Because of its very idiosyncratic structure, the Ph1 locus of wheat is very likely to be the result of a chromosomal rearrangement that occurred at the onset of tetraploid wheat formation (Griffiths et al., 2006). However, the molecular and cell biological characterization of Ph1 suggests its involvement in a fundamental mechanism which could be conserved across kingdoms. Indeed, the genes that are most closely related to Ph1 in yeast and mammals were shown to be required for proper chromosome pairing and recombination in vertebrates (Viera et al., 2009) and notably to control the expression of Homolog pairing Hop1 (Szwarcwort-Cohen et al., 2009), which may perform a role similar to that of Asy1 (Armstrong et al., 2002). It is thus possible that the apparent downstream effect of Ph1 on synapsis (Boden et al., 2009) is a conserved mechanism that has just been slightly adapted to deal with polyploidy. More work is needed to examine this possibility and it remains to be demonstrated that the CDK-like genes at the Ph1 locus are functional homologues of Cdk2 ⁄ Ime2 genes in mammals and yeast. More broadly speaking, is suppression of crossovers between homeologous chromosomes just a matter of a fine regulation of the basic meiotic machinery? Deregulation of TaASY1 in wheat is consistent with this assertion, as both decreased (TaASY1 RNAi lines) and increased (ph1b mutant) expression of TaASY1 resulted in crossover formation between homeologous chromosomes (Boden et al., 2009). In that respect, it would also be worthwhile to investigate how and why accessory B-chromosomes, which are usually mostly heterochromatic, drastically reduce crossover formation between nonhomologues in some interspecific hybrids (Evans & Macefield, 1973; Jenkins & Jimenez, 1995 and references therein) and even compensate for the absence of the Ph1 locus in some wheat · Aegilops hybrids (Dover & Riley, 1972). Do the diploid genotypes that suppress crossovers in interspecific hybrids (Taylor & Evans, 1977; Evans & Davies, 1985) display changes in meiotic gene expression and are some of these changes triggered by the presence of accessory B-chromosomes? Is homologue recognition achieved in a graded, rheostat-like manner, in which the control stringency is variable, adaptable and coupled directly to the level of divergence between the chromosomes that must be sorted out? Could the potential for increased variation in expression of dosage-regulated genes in polyploids contribute to adaptation of the specificity of homologue pairing and recombination in these species?

Where do Ph-like genes come from? The origin and evolution of Ph-like regulators in allopolyploid species have been subjects of debate for many years (reviewed in Jenczewski & Alix, 2004); some authors suggested that these loci may already have been present in some diploid progenitor genotypes, while others proposed that


Recurrent polyploidy formation and prospective diversity of Ph genes Recurrent polyploidy is known to be the rule, not the exception, and there are only a few examples of well-studied polyploidy taxa for which only a single origin appears likely.


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Recurrent polyploidy has profound genetic implications as distinct polyploid populations can be created from genetically different diploids and gene flow may produce novel polyploid genotypes through recombination. Little is known about the consequences of this broadened diversity for the establishment of polyploid species, especially for processes that have a direct effect on fertility. In particular we have few insights into the effect of multiple origins on the regulation of meiotic processes in polyploidy species. Wheat is the only model in which some data are available. The evolution of bread wheat occurred from diploid to tetraploid, and then from tetraploid to hexaploid, but the polyphyletic origin is still unclear; at least two genetically distinct progenitors are thought to have contributed to the D genome gene pool of hexaploid wheat, whereas introgression from parental species is likely to have had a role in its diversification (Caldwell et al., 2004). All polyploid wheat species, including Triticum timopheevi and Triticum araraticum (AAGG), show Ph1 activity and they display a conserved structure at the Ph1 locus (PCR assays anchored into the heterochromatin block and a CDK-like pseudogene; Griffiths et al., 2006). This conserved structure is in contrast with the phenotypic diversity found in polyploid wheat species. Martinez et al. (2005) analysed meiotic prophase and MI in haploids from different bread wheat cultivars and found slight but significant differences in synapsis and recombination between homeologues. Similarly, Ozkan & Feldman (2001) demonstrated genotypic variation in tetraploid wild wheat species affecting homoeologous recombination in interspecific hybrids. How can these different observations be explained? Are there allelic variants at the Ph1 locus that have not yet been identified, for instance, in the number of CDK-like genes forming the 5B cluster? Or is there variation at other loci involved in recombination between homeologous chromosomes? In this respect, is there variation at the Ph2 locus that may originate from the multiple origin of the bread wheat D genome? A better understanding is required of meiotic phenotype variation with respect to genotypic variation in wheat and its relatives. In addition, other species must be studied to broaden our understanding of the consequences of multiple origins in the evolution of Ph genes. What becomes of Ph genes when polyploids revert to diploids? Although almost all angiosperms have experienced at least one round of polyploidy during their evolution, much of the original genetic redundancy was erased by a massive removal of some but not all duplicated gene copies (Doyle et al., 2008). This process of ‘genetic diploidization’ is not random, and duplicated gene copies of some functional categories have been shown to be preferentially retained or lost (Doyle et al., 2008 for review). How do the Ph-like genes


evolve in such a context? Are they retained or are they lost? And if they are retained, do they contribute to homologue recognition in paleopolyploid species in which related regions need still to be sorted out at meiosis? In this respect, it is interesting to note that recombination between nonhomologous chromosomes is observed in meiotic mutants of maize (Zea mays) (e.g. mutants for Radiation sensitive Rad51, which encodes a protein required for the early steps of DNA repair; Li et al., 2007) and Arabidopsis thaliana (e.g. mutants for ZYP1 homolog of the budding yeast Zipper Zip1, which encodes a protein associated with the synaptonemal complex; Higgins et al., 2005), which both display extensive duplicated regions within their genomes. Finally, do these genes contribute to the spontaneous occurrence of a high number of homologous bivalents from the very first meiosis of newly formed or synthetic polyploids (see Ramsey & Schemske, 2002)? This question is linked to the first one we raised, demonstrating that all these questions are connected. Thus, all of them should be addressed to obtain a broader understanding of the evolution of meiosis in polyploids. Conclusion Meiosis in polyploids has long been studied from a cytological perspective but this work has been poorly integrated with modern understanding of the mechanisms involved obtained from studies of model species. More information is available on the cytological diploidization of allopolyploids compared with that available for autopolyloids. Diploid-like meiotic behaviour is genetically controlled in (at least) some allopolyploid species. Although this behaviour can be subject to a polygenic control, only one locus has been characterized at the molecular level (Ph1 from wheat), and more work is needed to obtain a complete picture of its mode of action. Different models are certainly required to understand how and when the mechanisms leading to proper chromosome segregation are established in polyploid species. This question is important because meiosis is an essential process for understanding polyploid speciation, and, reciprocally, polyploidy could provide valuable data for understanding how chromosome recognition is achieved in these species. Thus, as proposed by Hamant et al. (2006), ‘polyploid species could be used more often in the future as model organisms for meiosis’.

Acknowledgements We thank Mathilde Grelon and Wayne Crismani (INRA, Versailles, France) for their critical reading of the manuscript. We appreciate the comments of three anonymous reviewers which improved the manuscript. LG is supported by a PhD fellowship from the French Ministe`re de l’Ens-


New Phytologist eignement Supe´rieur et de la Recherche. MC is supported by a Marie Curie postdoctoral fellowship (PIEF-GA-2008219661). This work was carried out with the financial support of the French Agence Nationale de la Recherche, project ANR-05-BDIV-015.

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