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First published online February 3, 2009; 10.1105/tpc.108.062273 The Plant Cell 21:373-385 (2009) © 2009 American Society of Plant Biologists Genetic Regulation of Meiotic Cross-Overs between Related Genomes in Brassica napus Haploids and Hybrids[C],[W]
a Institut National de la Recherche Agronomique, Unité Mixte de Recherche 118, Amélioration des Plantes et Biotechnologies Végétales, F-35653 Le Rheu, France 3 Address correspondence to ejenczewski{at}versailles.inra.fr.
Although the genetic regulation of recombination in allopolyploid species plays a pivotal role in evolution and plant breeding, it has received little recent attention, except in wheat (Triticum aestivum). PrBn is the main locus that determines the number of nonhomologous associations during meiosis of microspore cultured Brassica napus haploids (AC; 19 chromosomes). In this study, we examined the role played by PrBn in recombination. We generated two haploid x euploid populations using two B. napus haploids with differing PrBn (and interacting genes) activity. We analyzed molecular marker transmission in these two populations to compare genetic changes, which have arisen during meiosis. We found that cross-over number in these two genotypes was significantly different but that cross-overs between nonhomologous chromosomes showed roughly the same distribution pattern. We then examined genetic recombination along a pair of A chromosomes during meiosis of B. rapa x B. napus AAC and AACC hybrids that were produced with the same two B. napus genotypes. We observed significant genotypic variation in cross-over rates between the two AAC hybrids but no difference between the two AACC hybrids. Overall, our results show that PrBn changes the rate of recombination between nonhomologous chromosomes during meiosis of B. napus haploids and also affects homologous recombination with an effect that depends on plant karyotype.
Polyploidy has played a pervasive and prominent role in the evolution of plants (Otto, 2007  ). It is estimated that 30 to 80% of extant flowering plants are polyploid (Masterson, 1994; Ramsey and Schemske, 1998; Rieseberg and Willis, 2007) and that almost all angiosperms have experienced at least one round of whole-genome duplication during their evolution (De Bodt et al., 2005; Cui et al., 2006). Some of the world's most important crop plants, such as wheat (Triticum aestivum), cotton (Gossypium hirsutum), and oilseed rape (Brassica napus), are allopolyploids (i.e., they originated as hybrids [followed by chromosome doubling] and contain different sets of related but not completely homologous chromosomes, called homoeologs). Given its importance, polyploidy has attracted a great deal of interest, and rapid progress has been made in many fields (Comai, 2005; Udall and Wendel, 2006; Chen, 2007).
The genetic regulation of recombination in allopolyploid species is a pivotal issue in evolution and agronomy but has been largely underexplored in recent years, except in wheat. Cross-over (CO) suppression between homoeologous chromosomes is required to ensure proper chromosome segregation and fertility; therefore; this mechanism is a determining factor in polyploid speciation. Otherwise, complex meiotic configurations would lead to unbalanced gametes, aneuploid progenies, and, hence, impaired fertility (Ramsey and Schemske, 2002
Wheat is the only species in which a large number of continuing studies are devoted to characterizing loci that suppress COs between homoeologous chromosomes (Pairing homeologous loci). The main regulator, Ph1, was discovered 50 years ago (Riley and Chapman, 1958
Recently, evidence was obtained that a system regulating homoeologous associations might also exist in B. napus (Jenczewski et al., 2003
In the absence of homologous chromosomes, the associations observed at MI during meiosis in B. napus haploids could involve (1) homoeologous A and C chromosomes that have diverged for 4 million years (Inaba and Nishio, 2002
In this study, we aimed to further characterize the mode of action of PrBn (and the genes it interacts with), notably their effect on both the rate and distribution of meiotic COs between related genomes in B. napus haploids and hybrids. We first analyzed the transmission of molecular markers in two haploid x euploid F1 populations to compare the rate and distribution of chromosomal rearrangements generated by meiosis in two B. napus haploids showing different numbers of univalents at MI (and that therefore differ in PrBn and interacting genes activity). This survey was required to ascertain that the differences observed at MI between B. napus haploids were not simply due to genotypic variation for (1) achiasmatic associations that are commonplace in polyhaploids and interspecific hybrids (Orellana, 1985
The Number of Chromosomal Rearrangements Varies between the Progenies of Darmor-bzh and Yudal Haploids We assayed parental marker transmission within and between two haploid x euploid F1 populations. The first population was obtained by crossing five haploid Darmor-bzh plants (that display five univalents at MI on average) with one euploid Yudal plant. The second was generated from nine haploid Yudal plants (that display 12 univalents at MI on average) crossed with one Darmor-bzh euploid plant(Figure 1 , experiment 1). A total of 150 (population one) and 141 (population two) markers, including 86 codominant markers that allowed direct comparisons (see Supplemental Figure 1 online), were used to genotype these two F1 populations and compare the number of chromosomal rearrangements that were generated by meiosis of Darmor-bzh and Yudal haploids that differ in PrBn (and interacting genes) activity. We anticipated that meiotic COs would produce chromosomal rearrangements during the first meiotic division, which would then be subsequently transmitted to the progenies of each B. napus haploid by unreduced gametes generated by an equational division of the sister chromatids (see Nicolas et al., 2007 ).
Losses and duplications of parental markers were observed in the two F1 haploid x euploid populations, confirming that chromosomal rearrangements were generated during meiosis in Darmor-bzh and Yudal haploids. Very significant differences were observed between the two F1 populations regardless of the method used to score rearrangements (see Methods). For example, the average frequency of haploid parent allele loss was higher in the progeny of Darmor-bzh haploids than in the progeny of Yudal haploids (method 1 using codominant markers only: 5% versus 1.5%; P < 0.01%). Likewise, a total of 342 chromosomal rearrangements were detected in the 117 progeny of Darmor-bzh haploids compared with only 111 rearrangements in the 103 progeny of Yudal haploids (method 2 using codominant and dominant markers: P < 0.01%). We obtained the same results when comparisons were performed using only the codominant markers; this confirmed that variations in the number of rearrangements did not result from slight variations in genome coverage between the two genetic backgrounds (see Supplemental Figure 1 online). Analysis with codominant markers also showed that euploid parent alleles were missing at almost equal frequencies in both populations (0.17% in euploid Yudal versus 0.24% in euploid Darmor-bzh), but their numbers were too low for sound statistical comparisons.
Significant differences were also observed in the number of chromosomal rearrangements per individual offspring (Figure 2
). For example, rearrangements were absent in only six plants (out of 117) in the progeny of Darmor-bzh haploids compared with 34 plants (out of 103) in the progeny of Yudal haploids (
To confirm this, we compared the numbers of rearrangements observed in the two F1 populations with those expected from the cytological survey described by Jenczewski et al. (2003) . We first estimated that a total of 405 and 181 chromosomal rearrangements should be observed among the 117 and 103 plants surveyed in the progenies of Darmor-bzh and Yudal haploids, respectively, if (1) every chromosome association observed at MI was chiasmatic (i.e., triggered rearrangements that segregated to half the gametes; see Nicolas et al., 2007) and (2) there was no gametic/zygotic selection against rearranged chromosomes. In the two populations, these estimates were significantly higher than the total number of rearrangements detected with molecular markers spanning 75% of the genome (Darmor-bzh:  2 = 11; P < 0.001; and Yudal: 2 = 24; P < 0.001). Resampling procedures were used to extrapolate the total number of rearrangements that would have been detected if 100% of the genome was covered (see Supplemental Figure 2 online). These extrapolated numbers roughly matched expectations from the cytological survey; in fact, we estimated that  425 and 137 rearrangements should have been observed in the progenies of Darmor-bzh and Yudal haploids, respectively, if 100% of genome was covered. Given the substantial variability obtained across simulated data sets (see Supplemental Figure 2 online), these estimates are reasonably close to expectation. Thus, the higher number of bivalents/multivalents observed at MI in Darmor-bzh compared with Yudal haploids is closely paralleled by an increase in the number of chromosomal rearrangements, which could have arisen either from genome-wide or chromosome specific differences in recombination frequency. To determine which of the two possibilities occurred, we compared the distribution of rearrangements among linkage groups between the two F1 populations.
The Difference between Darmor-bzh and Yudal Haploids Is Not Due to Chromosome-Specific Differences in Recombination
We then observed that for six linkage groups in the progeny of Darmor-bzh haploids, the proportion of plants with rearrangements was not significantly different from that expected if the corresponding chromosome systematically formed a chiasmatic bivalent at meiosis (i.e., 25%; Figure 3). By contrast, this proportion was observed for none of the linkage groups tested in the progeny of Yudal haploids (Figure 3). It thus appears that at least six chromosomes could systematically form cross-overs during meiosis in Darmor-bzh haploids, while this was never the case for any chromosome during meiosis of Yudal haploids. Randomization tests then demonstrated that the highest frequencies of linkage group rearrangements observed in the progenies of Darmor-bzh and Yudal haploids would not be obtained if rearrangements occurred at random, with equal probabilities for all linkage groups. This means that some linkage groups were rearranged more often than expected by chance in these two populations.
Chromosomal Rearrangements Occur in Similar Patterns in the Progenies of Darmor-bzh and Yudal Haploids
We compared the proportion of rearrangements that entailed concurrent losses and duplications of homoeologous haploid parent alleles (i.e., for markers located in homoeologous regions) between the two populations to assess the relative frequency of homoeologous recombination (for methods, see Nicolas et al., 2007
MI chromosomes were labeled with the BoB014O06 probe, which specifically hybridizes to all C-genome chromosomes, to determine the relative proportion of autosyndetic (A-A or C-C) versus allosyndetic (A-C) bivalents. The average meiotic behavior of Yudal haploids at MI is shown in Table 2 . We observed that autosyndesis was as proportionally commonplace at MI in Yudal (Figure 4 ) as in Darmor-bzh haploids (Table 2; 2 = 0.99, P = 0.32) and represented 30% of the bivalents observed. We then compared the distribution of COs along chromosomes in the two F1 populations.
A wide variety of distal and interstitial rearrangements were observed in both progenies, which were classified according to the number of breakpoints they caused on linkage groups. The mean number of chromosomes per plant carrying single, double, and triple breakpoints was higher in the progeny of Darmor-bzh haploids than in the progeny of Yudal haploids (Figure 5A ). By contrast, the relative proportion of rearranged chromosomes in each class was strikingly similar in the two F1 populations ( 2 = 0.28, P = 0.85; Figure 5B). In other words, once a linkage group was rearranged in any of the two populations, there was the same chance, irrespective of the haploid genotype, that this rearrangement entailed one (70 to 75%), two (25%), or three (3%) breakpoints.
We compared the positions of COs along chromosomes between the two progenies, approximated by the positions of single breakpoints. We compared the genetic size of the missing distal regions between the two progenies. Linkage groups or regions with extensive coverage differences between the two progenies or that displayed only a few rearrangements were excluded from this comparison. The relative genetic size of the missing distal regions appeared to be slightly but significantly higher in the Darmor-bzh progeny than in Yudal, regardless of the way the breakpoints were located within the rearranged intervals (Table 3 ). The margin was small, however, suggesting that CO distribution along chromosomes was very similar during meiosis of Darmor-bzh and Yudal haploids.
Comparison of Homologous Recombination in Triploid and Tetraploid Hybrids Finally, genetic experiments were performed to compare the frequency of meiotic COs on a pair of homologous chromosomes (linkage group A7) between two tetraploid hybrids produced by crossing the same resynthesized B. napus to Darmor and Yudal, respectively (Figure 1, experiment 3). Using seven markers common to the two maps (Figure 6A ),we found that the total genetic size of the linkage group was slightly (1.25-fold) but not significantly higher (P = 0.002 >  ' =0.01 = 0.001) in the progeny of the tetraploid produced with Yudal compared with Darmor. Likewise, no significant difference was observed when we compared the number of cross-overs per interval (P = 0.2).
The frequency of homologous recombination between two triploid hybrids, produced by crossing the same B. rapa plant with Darmor and Yudal, respectively (Figure 1, experiment 2), was then compared on the same A7 linkage group. We observed a highly significant heterogeneity in genetic map distances between the progeny of the triploid hybrid produced with Darmor (ARADCD) versus Yudal (ARAYCY) (Morton test extended to multiple loci; P < 10–5; Figure 6B). The proportion of COs calculated for every interval between adjacent markers on A7 was higher in the ARADCD hybrid than the ARAYCY hybrid, although no significant differences were observed for COs in the vicinity of the centromere (close to marker E43M70.643; Pouilly et al., 2008 ) or at one end of the linkage group. Using 12 and 14 markers in the ARADCD and ARAYCY progenies, respectively, we observed that the mean number of exchange points per chromatid was 1.7 (ranging from 0 to 4) in the ARADCD hybrid and 1.0 (ranging from 0 to 3) in the ARAYCY hybrid. These results demonstrate that changing the genotype of the B. napus variety used to produce hybrids had a clear effect on the frequency of homologous recombination across A7 for the triploid hybrids but no effect for the tetraploid hybrids.
Natural euploid B. napus displays predominantly 19 bivalents at MI and an almost strict disomic inheritance; this shows that the vast majority of COs is formed between homologous chromosomes. Evidence for rare homoeologous exchanges have nonetheless been obtained in several B. napus cultivars (Parkin et al., 1995 ; Sharpe et al., 1995; Lombard and Delourme, 2001; Osborn et al., 2003; Piquemal et al., 2005; Udall et al., 2005), but their frequency remains very low. By contrast, the slightly irregular meiosis of resynthesized B. napus generates a higher proportion of homoeologous exchanges when compared with natural B. napus (Parkin et al., 1995; Sharpe et al., 1995; Udall et al., 2005; Lukens et al., 2006; Gaeta et al., 2007; A.M. Chèvre, unpublished results). These results collectively indicate that an element of meiotic correction has been selected during the evolution of B. napus. Evidence was recently obtained that a major locus, called PrBn, largely determines the number of bivalents and multivalents that form at meiosis in B. napus haploids (AC; n = 19) (Jenczewski et al., 2003; Liu et al., 2006). In this study, we showed that PrBn controls the frequency, but not the distribution, of COs between homoeologous chromosomes in haploid plants and between homologous chromosomes during meiosis of triploid ArAnC plants. We also showed that PrBn has no effect on the level of homologous recombination in tetraploid ArAnCC hybrids, suggesting that its effect on recombination depends on plant karyotype. Our study shows that the different meiotic behaviors observed between Darmor-bzh and Yudal haploids are caused by a threefold difference in the number of COs that are formed between nonhomologous chromosomes. Given that these two meiotic phenotypes are genetically determined by PrBn and the genes it interacts with, we conclude that these loci have an effect on recombination between nonhomologous chromosomes.
We first showed that the number of rearranged chromosomes in the progenies of Darmor-bzh and Yudal haploids matched the number of bound chromosomes at MI in each of the two haploid genotypes. These findings indicate that achiasmatic associations between nonhomologous chromosomes (Orellana, 1985 We then proved that the contrasted meiotic behaviors between Darmor-bzh and Yudal haploids were not caused by a difference in the number of chromosomes that are susceptible to recombine (because of preexisting chromosomal rearrangements, for example). Indeed, all chromosomes were able to recombine during meiosis in Yudal haploids (Figure 3) even if probably none of them systematically underwent a CO. We found that the chance, on average, of most chromosomes in Yudal haploids recombining was three times less than in Darmor-bzh haploids, indicating an overall reduction in recombination between nonhomologous chromosomes.
Finally, we found that the higher number of univalents observed in Yudal haploids cannot result from premature bivalent separation, a phenomenon that was previously observed for COs that were too close to telomeres (Lamb et al., 1996 This study thus highlights differences in the number of COs between Darmor-bzh and Yudal haploids but not their distribution among chromosomes. For example, the number of rearrangement breakpoints per linkage group detected in the progeny of Yudal haploids was highly and positively correlated with the number in the progeny of Darmor-bzh haploids. Likewise, the relative proportions of autosyndesis (i.e., bivalents between pairs of A or pairs of C chromosomes) versus allosyndesis (i.e., bivalents between A and C chromosomes) were found to be very similar in Darmor-bzh and Yudal haploids (Table 2). We also showed that COs were preferentially formed between homoeologous chromosomes in the two progenies (Table 1). These results demonstrate that CO distribution was not random (see randomization test) and followed roughly the same rules during meiosis in the two genotypes. It notably appears that in none of the genotypes were chromosomes randomly scattered in the meiotic nucleus and recombined by chance only when pairs of chromosomes happened to lie close to each other.
It is tempting to further interpret our data and infer that the stringency at which divergence is scrutinized by the meiotic machinery is the same in Darmor-bzh and Yudal haploids. However, for this assumption to be made, a clear and precise understanding of the level of divergence between all the regions that recombined during meiosis of Darmor-bzh and Yudal haploids is required. At present, this information is not available, notably because only two complete sets of paralogous regions were compared at the sequence level in either B. oleracea or B. rapa (Town et al., 2006
In this study, we showed that variations in COs between nonhomologous chromosomes among B. napus haploids are closely paralleled by a significant difference in recombination between homologous chromosomes in two triploid ArAnC hybrids produced using Darmor-bzh or Yudal genotypes (Figure 6B). Using the same plants, Leflon et al. (2006)
In a set of very similar experiments, Dubcovsky et al. (1995)
Does this mean that the overall capacity for forming CO is different between Darmor-bzh and Yudal? At least two observations do not support this hypothesis. One is that we did not observe a clear genotypic effect on the level of homologous recombination between the two tetraploid hybrids (Figure 6A). The second issue is that the relative proportion of rearrangements that entailed one, two, or three breakpoints was strikingly similar in the progenies of Darmor-bzh and Yudal haploids (Figure 5B), suggesting that only first cross-over formation between nonhomologous chromosomes differed between the two haploid genotypes. These two results are unexpected if the two genotypes only differ in the number of COs they are able to form and clearly demonstrate that CO variations depend on plant karyotype (for other relevant examples, see Nicolas et al., 2008
The underlying cause of this karyotypic effect on CO variation is unknown, but at least two hypotheses deserve further investigation. First, a dosage effect by genes on the B. napus C genome, notably PrBn, can be postulated; one copy of the gene(s) carried by the Yudal C genome would lead to fewer COs than one copy of the gene(s) carried by the Darmor-bzh C genome, but two copies of gene(s) carried by the C genomes would confer the same numbers of COs irrespective of the genotype (this may explain why there is no difference in the loss of markers from the euploid parent of each genotype). Dosage effects were shown to be commonplace among the genes regulating chromosome pairing and recombination in polyploid species (Naranjo and Palla, 1982
Meiosis impacts the evolution of polyploid species by (1) contributing to fertility, (2) enabling sexual propagation, and (3) generating, through meiotic errors, large-scale chromosomal variation upon which genetic drift and/or selection can act (Leitch and Leitch, 2008
Plant Material The production of haploid plants (AC; 19 chromosomes) from Brassica napus cv Darmor-bzh, a dwarf winter B. napus cultivar (ADCD), and B. napus cv Yudal, a spring korean line (AYCY), was described by Jenczewski et al. (2003) . The production and selection of haploid x euploid progenies were described by Nicolas et al. (2007). Briefly, haploid plants were used as female parents with the male euploids providing haploid pollen (Figure 1). A first F1 population was produced by crossing five Darmor-bzh haploid plants with one Yudal euploid plant; in this study, we refer to it as "the progeny of Darmor-bzh haploids." A second F1 population was obtained by crossing nine Yudal haploid plants with one Darmor-bzh euploid plant; in this study, we refer to it as "the progeny of Yudal haploids." Genetic variation was not expected among the different haploid plants that were used to produced each of the two progenies because these haploids were isolated from almost homozygous euploid lines that were recovered after more than six (Darmor-bzh) and 15 generations (Yudal) of single seed descent, respectively. A total of 117 and 103 plants carrying 38 chromosomes, which were derived from unreduced gametes produced by the haploid plants (see Nicolas et al., 2007), were sorted in the progenies of Darmor-bzh and Yudal haploids, respectively. These two progeny populations were used to compare the frequency and distributions of chromosomal rearrangements generated during meiosis of haploid B. napus (Figure 1). Two digenomic triploid hybrids (ARADCD and ARAYCY) were produced by crossing one single Brassica rapa cv Chicon, C1.3 (ARAR; 2n = 20) plant with Darmor (ADADCDCD; 2n = 38) and Yudal (AYAYCYCY; 2n = 38), respectively (Figure 1). One single ARADCD and one single ARAYCY hybrid were then backcrossed as female to Darmor and Yudal, respectively, and two progeny populations of 116 and 112 plants were generated. The same B. rapa plant, C1.3, was crossed, as male, with a Brassica oleracea doubled haploid line, RC (COCO; 2n = 18) (Figure 1). The resulting interspecific hybrid was colchicine doubled to produce one resynthesized B. napus (ARARCOCO). The resynthesized B. napus was then crossed as female to Darmor and Yudal; two digenomic tetraploid hybrids (ARADCDCO and ARAYCYCO) were obtained. One single ARADCDCO and one single ARAYCYCO hybrid were backcrossed as female to Darmor and Yudal, respectively, and two progenies of 116 plants were generated. The two progenies of digenomic triploid hybrids and the two progenies of digenomic tetraploid hybrids were used to compare the rate of homologous recombination on one pair of A chromosomes (linkage group A7).
FISH with a Genome-Specific BAC Clone
Molecular Analysis
Detection of Chromosomal Rearrangements in the Haploid Progenies with Molecular Markers
We used the chromosome/linkage group nomenclature that was recently proposed as a reference by the Multinational Brassica Genome Project Steering Committee where B. napus N1-N19 nomenclature is replaced by A1-A10 and C1-C9 designations (http://www.brassica.info/information/lg_assigments.htm; see Delourme et al. [2006]
All the markers used in this study were from published maps (Foisset et al., 1996
Analysis of Genetic Recombination in the Two Triploid and Two Tetraploid Hybrids
Statistical Analyses
Estimation of the Number of Rearrangements Expected Given the Number of Chromosomes Associated at MI
Comparison of the Observed Rearrangement Distributions among Linkage Groups with Those Expected if Rearrangements Occurred at Random
Comparison of Homologous Recombination Rates
The heterogeneity of cross-over rates among populations was also assessed separately for every interval.
Supplemental Data
We thank Jean-Claude Letanneur (Institut National de la Recherche Agronomique, Unité Mixte de Recherche 118, Amélioration des Plantes et de Biotechnologies Végétales, France) for his significant contribution to the production of plant material as well as Tomasz Ksiazczyk and Jolanta Maluszynska (University of Silesia, Poland) for providing a stab of BoB014O06. We also thank Harry Belcram, Karine Budin, and Boulos Chalhoub (Unité de Recherche en Génomique Végétale, Institut National de la Recherche Agronomique, Evry, France) for developing and screening Positional Functional Markers markers and Genoplante for funding their development. Mathilde Grelon, Christine Mézard, and Marta Cifuentes (Institut National de la Recherche Agronomique, Versailles, France) and Karine Alix (Unité Mixte de Recherche de Génétique Végétale du Moulon, France) are gratefully acknowledged for their critical reading and valuable comments on the manuscript, and Leigh Gebbie is acknowledged for English corrections. We also thank three anonymous reviewers for helpful comments on previous versions of the manuscript. Stéphane Nicolas was supported by a Centre Technique Interprofessionnel des Oléagineux Métropolitains and Institut National de Recherche Agronomique - Génétique et Amélioration des Plantes fellowship. This work was carried out with the financial support of the ANR- Agence Nationale de la Recherche–The French National Research Agency under the Programme Biodiversité project ANR-05-BDIV-015, Effet de la polyploïdie sur la biodiversité et l'évolution du génome des plantes.
1 Current address: Institut National de la Recherche Agronomique–Supagro, Unité Mixte de Recherche 1097 Diversité et Adaptation des Plantes Cultivées, Equipe Génétique de la Vigne, 2 place Viala, F-34060 Montpellier, France. 
2 Current address: Centre Technique Interprofessionnel des Oléagineux Métropolitains, Direction Scientifique, Avenue Lucien Brétignières, Campus de Grignon, F-78850 Thiverval Grignon, France. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: Eric Jenczewski (ejenczewski{at}versailles.inra.fr).
[C] Some figures in this article are displayed in color online but in black and white in the print edition.
[W] Online version contains Web-only data. www.plantcell.org/cgi/doi/10.1105/tpc.108.062273 Received July 23, 2008; Revision received December 18, 2008. accepted January 9, 2009.
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ABSTRACT
INTRODUCTION
(Nicolas et al., 2007
, where Li(
) and Lp(
