Variation in Chiasma Frequency Among Eight Accessions of Arabidopsis thaliana

Corresponding author: G. H. Jones, The University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom., g.h.jones{at}bham.ac.uk (E-mail)

Communicating editor: C. S. GASSER

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Natural variation in meiotic recombination frequency in Arabidopsis thaliana has been assessed by analyzing chiasma frequency variation among a range of geographically and ecologically diverse accessions. Fifty pollen mother cells at metaphase I of meiosis were analyzed from each of eight accessions and fluorescence in situ hybridization was applied to enable identification of all 10 chromosome arms. There was no significant variation in mean chiasma frequency between plants within accessions, but there was significant variation between accessions. Further analysis confirmed this finding and identified two particular accessions, Cvi and Ler, as having chiasma frequencies significantly lower than those of the other accessions. The analysis also revealed that the pattern of chiasma distribution between arms and among chromosomes is not consistent over accessions. Further detailed analyses were conducted on each individual chromosome (1–5) in turn, revealing that chromosome 4, one of the acrocentric chromosomes, is the least variable while the other acrocentric chromosome (2) is the most variable. These findings indicate the existence of recombination regulatory elements in Arabidopsis and we conclude that it may be possible in the future to identify these elements and determine their mode of action. The practical implications of such developments are considerable.

MEIOTIC recombination has a long history of investigation by cytological and genetical methods and, more recently, by molecular approaches. The cytological method, which depends on recording the numbers and locations of chiasmata in bivalents at late prophase I or metaphase I of meiosis, has been validated by BrdU labeling experiments that demonstrate that chiasmata correspond to the points of physical exchange between homologous nonsister chromatids (TEASE and JONES 1978 ; ALLEN 1979 ; LATOS-BIELENSKA and VOGEL 1990 ). Because chiasmata can be scored rapidly from large samples of meiocytes, this represents an efficient approach to assaying genome-wide levels of recombination as well as the distribution of recombination events among and within chromosomes. Chiasma/recombination frequency, like other features of meiosis, is subject to stringent genetic control (REES 1961 ; BAKER et al. 1976 ). Several genes that are essential for normal meiotic levels of recombination have been identified and characterized. These are mainly genes that encode proteins required for the pairing and synapsis of chromosomes or that are involved in catalyzing key steps in DNA breakage, repair, and recombination (ROEDER 1997 ; ZICKLER and KLECKNER 1999 ). Disrupting these genes usually results in extreme phenotypes that have very depressed levels of recombination (e.g., ALANI et al. 1989 ; BAKER et al. 1996 ; GRELON et al. 2001 ). In addition, there is evidence for less extreme, more quantitative, genetically determined variation in chiasma frequency or recombination frequency. Significant differences, of a quantitative nature, have been demonstrated between isogenic or near-isogenic lines of rye (REES 1961 ), maize (WILLIAMS et al. 1995 ), and barley (SALL 1990 ; NILSSON and PELGER 1991 ) and these have been interpreted as indicating the existence of genetic elements that have minor or modifying effects on recombination. The mode of action of these elements is unknown, but they are potentially of great interest since they may provide the means to regulate and adjust the expression of recombination. Other indications of quantitative genetic variation in recombination come from selection experiments (e.g., CHARLESWORTH and CHARLESWORTH 1985 ) and from studies of chiasma frequency variation between populations (HEWITT 1964 ; PRICE 1974 ; WHITEHOUSE et al. 1981 ) or between closely related, karyotypically identical or very similar, species (HEWITT 1964 ; ZARCHI et al. 1972 ).

Information on meiotic genetic recombination in Arabidopsis derives from a number of sources, including conventional genetic mapping (http://nasc.nott.ac.uk, ALONSO-BLANCO et al. 1998 ), tetrad analysis exploiting the quartet mutation (COPENHAVER et al. 1998 ), and selective antibiotic marker-based systems (BARTH et al. 2000 ). Although Arabidopsis thaliana has a small genome and correspondingly small chromosomes, we have shown that it is feasible to score chiasmata from pollen mother cells at metaphase I. Despite suggestions of nonconcurrence between mean chiasma frequencies and genetic recombination frequencies in some plant species (reviewed by SYBENGA 1996 ), the available evidence indicates good agreement of these parameters in Arabidopsis (SANCHEZ-MORAN et al. 2001 ). Furthermore, by applying appropriate fluorescence in situ hybridization (FISH) probes we were able to identify and separately record the chiasma frequencies of each chromosome and chromosome arm.

Although several meiotic mutants of Arabidopsis have been shown to have severely depressed chiasma frequencies (COUTEAU et al. 1999 ; CARYL et al. 2000 ; CAI and MAKAROFF 2001 ), relatively little is known concerning natural variation in chiasma/recombination frequency in this species or the genetic basis of any such variation. Two studies have identified a significant effect of sex on recombination frequency (VIZIR and KOROL 1990 ; BARTH et al. 2000 ), but otherwise there is little information on the extent of variation for this character in wild-type Arabidopsis material. Although some natural populations of Arabidopsis have been shown to have significant levels of outcrossing, most natural accessions are almost exclusively self-pollinating and are therefore near isogenic in their genetic structure. Nevertheless different accessions show much variation at the DNA sequence level and therefore represent a valuable resource for investigating genetic variation affecting any characters of interest (ALONSO-BLANCO and KOORNNEEF 2000 ). In this study we extend the analysis of chiasmata to include eight different accessions of Arabidopsis, with the aim of identifying accessions that show significant differences in chiasma frequency.

	MATERIALS AND METHODS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Plant material:
The eight accessions of A. thaliana used in this study include some familiar accessions that have a long history of experimental use and exploitation (e.g., Col and Ler) while others are of more recent extraction from the wild and represent a wide geographical diversity. Table 1 summarizes the origins and sources of these accessions. All accessions were sown simultaneously onto soilless compost and grown to flowering in a constant environment chamber at a temperature of 18° and a day length of 16 hr.

Fixation:
Immature flower buds were detached from the plants and fixed in Carnoy's fixative (6 ethanol:3 chloroform:1 acetic acid). Fixed flower buds were stored in fixative at -20° until required.

Slide preparation:
Air-dried spreads of pollen mother cells were prepared according to the method of FRANSZ et al. 1998 and ARMSTRONG et al. 1998 , with minor modifications as described by SANCHEZ-MORAN et al. (2001). Fixed buds were washed in fixative (3 ethanol:1 glacial acetic acid) followed by citrate buffer (pH 4.5) and then incubated in enzyme mixture, 0.3% w/v pectolyase, 0.3% w/v cytohelicase, and 0.3% w/v cellulase (all Sigma, St. Louis) in citrate buffer, for 1.5 hr at 37°. Replacing the mixture with ice-cold buffer stopped the reaction. Single buds were transferred to clean slides, together with a small volume of buffer, and macerated with a needle. Ten microliters of 60% acetic acid was added to the slide before placement on a hot plate at 45° for 1 min while being stirred with a needle. A further 10 µl of 60% acetic acid was added to the slide off the hot plate before addition of 200 µl of cold 3:1 fixative. The fixative was drained away, and the slide was dried with a hair dryer.

Fluorescence in situ hybridization:
The FISH technique used was that previously described by ARMSTRONG et al. 1998 and FRANSZ et al. 1998 . Slides were counterstained with 4',6-diamidino-2-phenylindole (DAPI; 4 µg/ml) in Vectashield antifade mounting medium (Vector, Burlingame, CA).

The following DNA probes were used:

• Clone pTa71 (GERLACH and BEDBROOK 1979 ) containing a 9-kb EcoRI fragment of Triticum aestivum consisting of the 18S-5.8S-25S rRNA genes and the spacer regions. This probe was directly labeled with Spectrum green (Amersham, Arlington Heights, IL) by nick translation following the manufacturer's instructions (Boehringer Mannheim, Mannheim, Germany).

• Plasmid pCT4.2 containing the 5S rDNA gene from A. thaliana as a 500-bp insert cloned in pBlu. This probe was generated by PCR using M13 primers (Pharmacia, Piscataway, NJ). Biotin dUTP was incorporated in a secondary PCR reaction.

The FISH preparations were viewed with an epifluorescence microscope (Nikon E600) having filters for DAPI, TRITC, and FITC and equipped with a Quips image capture and analysis system (Applied Imaging International Ltd).

Statistical analyses:
Chiasma data were analyzed statistically using Minitab software. In appropriate cases of two-way and three-way analyses of variance, the main effects (accessions, chromosomes, and arms) were treated as being fixed effects (model 1). This is obvious in the case of chromosomes and arms, while in the case of accessions it was determined on the basis that they were not drawn randomly from a population of possible accessions.

	RESULTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Chromosome identification:
It has been shown previously (FRANSZ et al. 1998 ; SANCHEZ-MORAN et al. 2001 ) that 45S and 5S rDNA FISH probes, combined with chromosome morphology, uniquely identify each of the Arabidopsis chromosomes and chromosome arms (Fig 1). The short acrocentric chromosomes 2 and 4 both carry 45S sequences on their short arms in all accessions that have been examined, coinciding with the locations of the nucleolus organizing regions (NORs). In addition, all accessions examined also have a 5S rDNA site located proximally on the short arm of chromosome 4, which serves to distinguish the two acrocentric chromosomes. A further invariant large 5S site occurs proximally on the shorter arm of the submetacentric chromosome 5, which serves to distinguish this chromosome from chromosome 1. Chromosome 3 is the smallest of the submetacentric/metacentric group of chromosomes (1, 3, and 5) and is variable with respect to possession, location, and size of a third 5S site. Among the eight accessions included in this study, four (Ws, Ri-0, Fei0, and Cvi) lack a 5S site on chromosome 3. Col, C24, and Hey-0 have a 5S site located proximally on the short arm of chromosome 3; this site is smaller in Hey-0 compared to the other two accessions, but this difference is barely detectable in meiotic metaphase I bivalents. The remaining accession Ler has a 5S site located interstitially in the long arm of chromosome 3. These results are broadly in agreement with those reported by FRANSZ et al. 1998 , except for some minor discrepancies involving the 5S sites on chromosome 3. They described a 5S site on the short arm of chromosome 3 in Cvi, which was not found in the this study, and they did not observe a 5S signal on chromosome 3 in C24, indicating the possibility of some intra-accession polymorphisms for 5S rDNA sites.

View larger version (45K): In this window In a new window Download PPT slide   Figure 1. Schematic haploid karyotypes of Arabidopsis showing the numbers and locations of 45S and 5S rDNA sequences in different accessions.

Chiasma analysis:
Chiasmata were recorded according to the criteria established previously (SANCHEZ-MORAN et al. 2001 ). Bivalent configurations at metaphase I in Arabidopsis fall into two categories, rods and rings. Rods are bound by chiasmata in one arm only, whereas rings have both arms bound by chiasmata. These configurations were taken as having a single chiasma per bound arm unless there was clear evidence of a second chiasma in an arm. Bivalent morphology also depends on centromere location (metacentric vs. acrocentric) and on chiasma location within the bivalent arms (proximal, interstitial, or distal; see Fig 2 in SANCHEZ-MORAN et al. 2001 ). Some rod bivalents had apparently terminal (near-terminal) attenuated interhomolog connections. We regarded these as chiasmate associations resulting from extremely subterminal crossover events. This was independently verified by applying a telomere DNA probe to metaphase I cells (not shown). In the case of the acrocentric chromosomes 2 and 4, rod bivalents could be subdivided into those having bound long arms and those having bound short arms.

View larger version (20K): In this window In a new window Download PPT slide   Figure 2. Three representative examples of metaphase I of meiosis in accessions Col (a), Ws (c), and Cvi (e) following FISH to identify the sites of 45S and 5S rDNA sequences. Individual bivalents are indicated (1–5). The accompanying line drawings show our interpretation of the DAPI plus FISH images. (a and c) Three rings and two rod bivalents are present in both these cells; in both cases the rods (bivalents 2 and 4) have long arm chiasmata. (e) This cell has two ring bivalents and three rods; the chromosome 4 rod has a single short arm chiasma (arrow).

All bound arms of metaphase I bivalents were considered to be associated by chiasmate bonds, including the short arms of chromosomes 2 and 4 that contain NORs and associated heterochromatin, usually considered to be free of crossovers. In most cases these short arms appeared to be associated via their distal NORs (45S signals). However, closer examination revealed that in a proportion of cases the short arm bonds had a continuous strip of unlabeled (no 45S signal) chromatin running continuously between the homologs, flanked by 45S signals (see Figure 3 in SANCHEZ-MORAN et al. 2001 ). These images show that the chiasmata are located in the euchromatic parts of the short arms. In those cases in which the 45S signal formed a solid continuous block, it was reasoned that these are also chiasmatic bonds but the diagnostic unlabeled strip is invisible due to the plane of viewing.

The five chromosome pairs invariably formed five bivalents at metaphase I in all accessions (Fig 2). No univalents were observed in the sample of 50 cells per accession (400 cells in total) analyzed by FISH. Ring bivalents predominated in the metacentric/submetacentric chromosomes (1, 3, and 5), with only a minority forming rod bivalents. In contrast, the acrocentric chromosomes 2 and 4 generally showed much higher frequencies of rod bivalents and of these the majority were bound via their long arms.

The first step in analyzing the chiasma frequency data, before considering bivalent and bivalent arms, was to analyze mean cell chiasma frequencies of accessions and individual plants within accessions, by means of a hierarchical or "nested" analysis of variance. To obtain data from 50 cells per accession, observations were taken from two or three plants per accession (Table 2), and it was therefore necessary first to investigate "between accessions" and "between plants within accession" variation, on the basis of plant means. This analysis shows a highly significant difference between accessions, but no significant differences between plants within accession (Table 3).

The mean chiasma frequencies recorded for the five bivalents in all eight accessions are summarized in Table 4. Bivalent 1, consisting of the longest chromosome pair, consistently had the highest mean chiasma frequency (range 1.88–2.14, overall mean 2.00), predominantly in the form of rings. Chromosomes 3 and 5 had overall mean chiasma frequencies of 1.93 and 1.84, respectively, with a broadly similar pattern of chiasma distribution to chromosome 1. The shorter acrocentric chromosomes 2 and 4 had lower overall mean chiasma frequencies at 1.58 and 1.60, respectively. Evidently the mean chiasma frequencies of the different bivalents are proportional to chromosome size, in the general sense that bivalents show the same ranking according to chiasma frequency as they do according to size; this does not of course imply direct proportionality of chiasma frequency and chromosome size. Similarly there appears to be proportionality between chromosome arm length and chiasma frequency; this is particularly evident in the cases of chromosomes 2 and 4, although again direct proportionality is not implied.

We are especially interested in detecting chiasma frequency variation between accessions of Arabidopsis. Some evidence of such variation has already emerged from the hierarchical analysis of variance above and also from a consideration of individual bivalent chiasma frequencies. Mean cell chiasma frequencies of accessions range from 9.36 in Fei-0 to 7.90 in Cvi. To determine whether this variation is statistically significant we conducted a three-way analysis of variance (Table 5). This analysis confirmed that the accessions included in this study differ significantly for chiasma frequency. As expected, the other main effects, chromosomes and arms, are also highly significant. It should also be noted that the three first-order interaction items (accessions x chromosomes, accessions x arms, chromosomes x arms) and the second-order interaction (accessions x chromosomes x arms) are also all highly significant. This indicates that the pattern of chiasma distribution between arms and among chromosomes is not consistent over accessions. In other words, the accessions differ not only in overall mean chiasma frequency but also in their particular patterns of chiasma formation in certain bivalents and bivalent arms. Some of these effects are apparent from an inspection of Table 4. For example, it can be seen that Cvi and Ler, the two accessions having the lowest overall mean cell chiasma frequencies, have particularly low values for bivalent 2 and especially the short arm of this bivalent. Cvi also has a very low chiasma frequency for bivalent 5, again mainly attributable to the short arm.

Accession Cvi stands out as having a particularly low chiasma frequency, reflected in the individual chiasma frequencies of all the bivalents. This raises the obvious question whether this accession is wholly, or mainly, responsible for the significant "accessions" item in the ANOVA. To examine this, the analysis was repeated omitting accession Cvi. The remaining seven accessions still differed significantly for chiasma frequency, indicating that the significant difference between accessions in the previous analysis was not wholly attributable to Cvi. Furthermore, the three first-order interactions and the second-order interaction also remained significant. Accession Ler, with a mean chiasma frequency of 8.70 has the next lowest value after Cvi. When the analysis of variance was repeated again, this time omitting both Cvi and Ler, the remaining accessions did not differ significantly for chiasma frequency. We conclude that both Cvi and Ler have chiasma frequencies significantly lower than those of the other six accessions included in this study, which constitute a homogeneous group with very similar chiasma frequencies. In addition, the first-order interaction, "accessions x chromosomes," and the second-order interaction, "accessions x chromosomes x arms," were both nonsignificant in the absence of Cvi and Ler, indicating that among this group of six accessions chiasma distribution among chromosomes and arms is, in general, consistent across accessions, although it will be seen (below) that this is not entirely so for chromosome arms when individual bivalents are analyzed.

The three-way ANOVAs above included all five bivalents, six, seven, or eight accessions, and long vs. short arms. To gain a more detailed understanding of the main sources of chiasma frequency variation, two-way ANOVAs were conducted for each individual bivalent, and separate analyses were performed for all eight accessions, seven accessions (excluding Cvi), and six accessions (excluding Cvi and Ler). The results of these analyses are summarized in Table 6 and reveal some interesting trends. When all eight accessions are included, all chromosomes except chromosome 4 show significant differences between accessions. Chromosome 4 also shows the lowest levels of significance for the accessions x arms interaction item (<0.05 in all three analyses, irrespective of whether Cvi and Ler are included or excluded). Thus it appears that chromosome 4, one of two acrocentric chromosomes in the genome, is the least variable of the chromosomes, has relatively constant chiasma frequencies, and also has the least variable between-arm distributions, across the accessions studied. On the other hand, chromosome 2, the other acrocentric chromosome, is the only chromosome that maintains significant chiasma frequency variation between accessions when Cvi is excluded, and this chromosome also shows the highest levels of significance for the accessions x arms interaction item. It thus appears that chromosome 2, which is structurally very similar to chromosome 4, shows the greatest amount of chiasma frequency variation and also the most between-arm variation. Chromosomes 1, 3, and 5 show intermediate effects in that they are all significantly different when all eight accessions are included, but none of them are significant when Cvi is excluded. The accessions x arms interactions for these three chromosomes also display intermediate levels of significance.

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

The results of this study confirm and extend our earlier findings that reported chiasma frequency in accession Ws and in two meiotic mutants (SANCHEZ-MORAN et al. 2001 ). Five of the new accessions analyzed form a fairly uniform grouping with Ws, whereas two accessions (Cvi and Ler) have significantly lower chiasma frequencies. It was reasoned previously that the mean chiasma frequency of Ws was in reasonable agreement with genetic map length, based on recombinant inbred lines, and also with genome-wide recombination frequency derived from the analysis of meiotic tetrads. It has previously been shown that sex differences in recombination frequency are present in Arabidopsis (VIZIR and KOROL 1990 ; BARTH et al. 2000 ; ARMSTRONG and JONES 2001 ) and need to be taken into account when estimating recombination frequencies and making comparisons between different sources of information. We now show that different accessions of Arabidopsis may differ significantly for chiasma frequency and that this could be an important source of error in comparisons between genetical and cytological measures of recombination frequency, if based on different accessions.

The inclusion of FISH in this study, to identify individual bivalents, has revealed some subtle chromosome- and chromosome arm-specific contributions to the interaccession differences in chiasma frequency. Chromosomes 2 and 4 are structurally similar acrocentric chromosomes, both having NORs located distally on their short arms. Nevertheless they differ markedly in their contributions to the interaccession chiasma frequency variation. Chromosome 4 is the least variable while chromosome 2 and especially the NOR-bearing short arm are the most variable. This situation shows some parallels with the differential behavior of these two chromosomes with regard to residual bivalent and chiasma formation in asynaptic and desynaptic mutants (SANCHEZ-MORAN et al. 2001 ). These mutants are characterized by frequent univalents at metaphase I, but retain a low number of mainly very subterminal chiasmatic bivalent associations. In this earlier study it was found that the chromosome 2 short arm had the highest residual bivalent and chiasma frequency, despite its short length and large proportion of heterochromatin, whereas chromosome 4 showed no such effect and had a much lower residual bivalent and chiasma frequency. These observations suggest that the short arm of chromosome 4 possesses some unusual properties, perhaps related to differential recombination effects through different chromatin states associated with varying rDNA transcriptional levels or varying rDNA copy number. Another interesting observation regarding these chromosomes is that whereas in most accessions the two NORs form a single common nucleolus in meiotic prophase I cells, in one accession included in this study (Fei-0) they regularly formed two separate and independent nucleoli. The meaning and possible effects of this difference can only be guessed at, but it is interesting to note that Fei-0 has the highest mean chiasma frequencies for the short arms of chromosomes 2 and 4 of all the accessions examined.

The existence of significant interaccession variation for chiasma frequency implies that the accessions concerned differ for genetic factors or elements with effects on chiasma frequency. Either these could be genes that have modifying or regulatory effects on chiasma frequency or, alternatively, they could reflect chromosome structural elements that differ between accessions. These preliminary findings therefore indicate that it may be possible, eventually, to identify these elements and thereby gain a better understanding of how recombination frequencies are regulated. There is also an obvious interest in the possibility of manipulating this variation to experimentally modify recombination frequencies. The potential practical implications of such developments for plant breeding are very considerable.

	FOOTNOTES

¹ Present address: School of Biosciences, The University of Birmingham, Birmingham B15 2TT, United Kingdom.

Manuscript received April 30, 2002; Accepted for publication August 5, 2002.

	LITERATURE CITED

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

ALANI, E., S. SUBBIAH, and N. KLECKNER, 1989  The yeast RAD50 gene encodes a predicted 153-kD protein containing a purine nucleotide-binding domain and two large heptad-repeat regions. Genetics 122:47-57.[Abstract/Free Full Text]

ALLEN, J. W., 1979  BrdU-dye characterization of late replication and meiotic recombination in Armenian hamster germ cells. Chromosoma 74:189-207.[Medline]

ALONSO-BLANCO, C. and M. KOORNNEEF, 2000  Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. Trends Plant Sci. 5:22-29.[Medline]

ALONSO-BLANCO, C., A. J. M. PEETERS, M. KOORNNEEF, C. LISTER, and C. DEAN et al., 1998  Development of an Aflp based linkage map of Ler, Col and Cvi Arabidopsis thaliana ecotypes and construction of a Ler/Cvi recombinant inbred line population. Plant J. 14:259-271.[Medline]

ARMSTRONG, S. J. and G. H. JONES, 2001  Female meiosis in wild-type Arabidopsis thaliana and in two meiotic mutants. Sex. Plant Reprod. 13:177-183.

ARMSTRONG, S. J., P. FRANSZ, D. F. MARSHALL, and G. H. JONES, 1998  Physical mapping of DNA repetitive sequences to mitotic and meiotic chromosomes of Brassica oleracea var. alboglabra by fluorescence in situ hybridization. Heredity 81:666-673.

BAKER, B. S., A. T. C. CARPENTER, M. S. ESPOSITO, R. E. ESPOSITO, and L. SANDLER, 1976  The genetic control of meiosis. Annu. Rev. Genet. 10:53-134.[Medline]

BAKER, S. M., A. W. PLUG, T. A. PROLLA, C. E. BRONNER, and A. C. HARRIS et al., 1996  Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat. Genet. 13:336-342.[Medline]

BARTH, S., A. E. MELCHINGER, B. DEVEZI-SAVULA, and T. LUBBERSTEDT, 2000  A high-throughput system for genome-wide measurement of genetic recombination in Arabidopsis thaliana based on transgenic markers. Funct. Integr. Genomics 1:200-206.[Medline]

CAI, X. and C. A. MAKAROFF, 2001  The dsy10 mutation of Arabidopsis results in desynapsis and a general breakdown in meiosis. Sex. Plant Reprod. 14:63-67.

CARYL, A. P., S. J. ARMSTRONG, G. H. JONES, and F. C. H. FRANKLIN, 2000  A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1.. Chromosoma 109:62-71.[Medline]

CHARLESWORTH, B. and D. CHARLESWORTH, 1985  Genetic variation in recombination in Drosophila. I. Responses to selection and preliminary genetic analysis. Heredity 54:71-83.

COPENHAVER, G. P., W. E. BROWNE, and D. PREUSS, 1998  Assaying genome-wide recombination and centromere functions with Arabidopsis tetrads. Proc. Natl. Acad. Sci. USA 95:247-252.[Abstract/Free Full Text]

COUTEAU, F., F. BELZILE, C. HORLOW, O. GRANDJEAN, and D. VEZON et al., 1999  Random chromosome segregation without meiotic arrest in both male and female meiocytes of dmc1 mutant of Arabidopsis. Plant Cell 11:1623-1634.[Abstract/Free Full Text]

FRANSZ, P., S. ARMSTRONG, C. ALONSO-BLANCO, T. C. FISCHER, and R. A. TORRES-RUIZ et al., 1998  Cytogenetics for the model system Arabidopsis thaliana. Plant J. 13:867-876.[Medline]

GERLACH, W. L. and J. R. BEDBROOK, 1979  Cloning and characterisation of ribosomal RNA genes from wheat and barley. Nucleic Acids Res. 7:1869-1885.[Abstract/Free Full Text]

GRELON, M., D. VEZON, G. GENDROT, and G. PELLETIER, 2001  AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J. 20:589-600.[Medline]

HEWITT, G. M., 1964  Population cytology of British grasshoppers. I. Chiasma variation in Chorthippus brunneus, Chorthippus parallelus and Omocestus viridulus. Chromosoma 15:212-230.[Medline]

LATOS-BIELENSKA, A. and W. VOGEL, 1990  Frequency and distribution of chiasmata in Syrian hamster spermatocytes studied by the BrdU antibody technique. Chromosoma 99:267-272.[Medline]

NILSSON, N. O. and S. PELGER, 1991  The relationship between natural variation in chiasma frequencies and recombination frequencies in barley. Hereditas 115:121-126.

PRICE, D. J., 1974  Variation in chiasma formation in Cepea nemoralis.. Heredity 32:211-217.[Medline]

REES, H., 1961  Genotypic control of chromosome form and behaviour. Bot. Rev. 27:288-318.

ROEDER, G. S., 1997  Meiotic chromosomes: it takes two to tango. Genes Dev. 11:2600-2621.[Free Full Text]

SALL, T., 1990  Genetic control of recombination in barley. II. Variation in linkage between marker genes. Hereditas 112:171-178.

SANCHEZ-MORAN, E., S. J. ARMSTRONG, J. L. SANTOS, F. C. H. FRANKLIN, and G. H. JONES, 2001  Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosome Res. 9:121-128.[Medline]

SYBENGA, J., 1996  Recombination and chiasmata: few but intriguing discrepancies. Genome 39:473-484.

TEASE, C. and G. H. JONES, 1978  Analysis of exchanges in differentially stained meiotic chromosomes of Locusta migratoria after BrdU-substitution and FPG staining. I. Crossover exchanges in mono-chiasmate bivalents. Chromosoma 69:163-178.

VIZIR, I. Y. and A. B. KOROL, 1990  Sex difference in recombination frequency in Arabidopsis. Heredity 65:379-383.

WHITEHOUSE, C., L. A. EDGAR, G. H. JONES, and J. S. PARKER, 1981  The population cytogenetics of Crepis capillaris. I. Chiasma variation. Heredity 47:95-103.

WILLIAMS, C. G., M. M. GOODMAN, and C. W. STUBER, 1995  Comparative recombination distances among Zea mays L. inbreds, wide crosses and interspecific hybrids. Genetics 141:1573-1581.[Abstract]

ZARCHI, Y., G. SIMCHEN, J. HILLEL, and T. SCHAAP, 1972  Chiasmata and the breeding system in wild populations of diploid wheats. Chromosoma 38:77-94.

ZICKLER, D. and N. KLECKNER, 1999  Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33:603-754.[Medline]

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				J. Drouaud, C. Camilleri, P.-Y. Bourguignon, A. Canaguier, A. Berard, D. Vezon, S. Giancola, D. Brunel, V. Colot, B. Prum, et al. Variation in crossing-over rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination "hot spots" Genome Res., January 1, 2006; 16(1): 106 - 114. [Abstract] [Full Text] [PDF]

				J. D. Higgins, E. Sanchez-Moran, S. J. Armstrong, G. H. Jones, and F. Chris. H. Franklin The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over Genes & Dev., October 15, 2005; 19(20): 2488 - 2500. [Abstract] [Full Text] [PDF]

				S. Y. Lam, S. R. Horn, S. J. Radford, E. A. Housworth, F. W. Stahl, and G. P. Copenhaver Crossover Interference on Nucleolus Organizing Region-Bearing Chromosomes in Arabidopsis Genetics, June 1, 2005; 170(2): 807 - 812. [Abstract] [Full Text] [PDF]

				V. V. Symonds, A. V. Godoy, T. Alconada, J. F. Botto, T. E. Juenger, J. J. Casal, and A. M. Lloyd Mapping Quantitative Trait Loci in Multiple Populations of Arabidopsis thaliana Identifies Natural Allelic Variation for Trichome Density Genetics, March 1, 2005; 169(3): 1649 - 1658. [Abstract] [Full Text] [PDF]

				E. Sanchez-Moran, G. H. Jones, F. C. H. Franklin, and J. L. Santos A Puromycin-Sensitive Aminopeptidase Is Essential for Meiosis in Arabidopsis thaliana PLANT CELL, November 1, 2004; 16(11): 2895 - 2909. [Abstract] [Full Text] [PDF]

				J. L. Santos, D. Alfaro, E. Sanchez-Moran, S. J. Armstrong, F. C. H. Franklin, and G. H. Jones Partial Diploidization of Meiosis in Autotetraploid Arabidopsis thaliana Genetics, November 1, 2003; 165(3): 1533 - 1540. [Abstract] [Full Text] [PDF]