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Originally published as Genetics Published Articles Ahead of Print on March 31, 2005.

Genetics, Vol. 170, 807-812, June 2005, Copyright © 2005
doi:10.1534/genetics.104.040055

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Crossover Interference on Nucleolus Organizing Region-Bearing Chromosomes in Arabidopsis

Sandy Y. Lam*, Sarah R. Horn*, Sarah J. Radford{dagger}, Elizabeth A. Housworth{ddagger}, Franklin W. Stahl§ and Gregory P. Copenhaver*,1

* Department of Biology and The Carolina Center for Genome Sciences, University of North Carolina, Chapel Hill, North Carolina 27599
{dagger} Curriculum in Genetics and Molecular Biology, University of North Carolina, Chapel Hill, North Carolina 27599
{ddagger} Department of Mathematics and Department of Biology, Indiana University, Bloomington, Indiana 47405
§ Institute of Molecular Biology, University of Oregon, Eugene, Oregon 97403-1229

1 Corresponding author: Department of Biology and The Carolina Center for Genome Sciences, Campus Box 3280, Coker Hall 305, University of North Carolina, Chapel Hill, NC 27499.
E-mail: gcopenhaver{at}bio.unc.edu

Manuscript received December 17, 2004. Accepted for publication February 15, 2005.


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
In most eukaryotes, crossovers are not independently distributed along the length of a chromosome. Instead, they appear to avoid close proximity to one another—a phenomenon known as crossover interference. Previously, for three of the five Arabidopsis chromosomes, we measured the strength of interference and suggested a model wherein some crossovers experience interference while others do not. Here we show, using the same model, that the fraction of interference-insensitive crossovers is significantly smaller on the remaining two chromosomes. Since these two chromosomes bear the Arabidopsis NOR domains, the possibility that these chromosomal regions influence interference is discussed.

CROSSOVER interference, first observed by STURTEVANT (1915), governs the genome-wide distribution of recombination events during meiosis. It can be characterized as a quasi-uniform, rather than exponential, distribution of intercrossover map distances. To better understand these processes, we are exploring the regulation of recombination events in Arabidopsis thaliana by taking advantage of the quartet mutation, which enables the use of tetrad analysis (PREUSS et al. 1994). Previously we reported that crossovers on chromosomes 1, 3, and 5 of Arabidopsis display intercrossover length distributions consistent with a mixture of both interference-sensitive and interference-insensitive recombination events (COPENHAVER et al. 2002). The observed data best fit a model in which 20% of the crossovers in Arabidopsis are insensitive to interference. That analysis was not powerful enough to draw conclusions for chromosomes 2 and 4. Chromosomes 2 and 4 are short acrocentric chromosomes that harbor large arrays of ribosomal RNA (rRNA) genes on the distal end of their short arms (COPENHAVER et al. 1995; COPENHAVER and PIKAARD 1996). DNA encoding rRNA (rDNA) is commonly referred to as a nucleolus organizing region (NOR) because of the distinct suborganellar structure that forms around rRNA genes during interphase (MCCLINTOCK 1934). Interestingly, NORs have been proposed to function as cis-acting chromosome pairing centers in several species. To examine the influence of both chromosome length and structure on interference, we expanded our previous analysis of Arabidopsis tetrads. Our results indicate that the observed distribution of intercrossover lengths on chromosomes 2 and 4 is also consistent with a mixture of both interference-sensitive and interference-insensitive crossovers. However, the fraction of interference-insensitive crossovers on the short, NOR-bearing chromosomes appears to be about sevenfold smaller than that on the long chromosomes.


   MATERIALS AND METHODS
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 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Plant material:
A. thaliana qrt1-1 in the Landsberg background (CS8050) was crossed to qrt1-2 in the Columbia background (CS8846) to create F1 plants. Individual pollen tetrads from F1 plants were manually crossed onto Landsberg male-sterile1 plants (CS75). Crosses that generated three or four meiotically related seeds were selected for analysis. Seeds were sown on Pro-mix (Professional Horticulture) and stratified for 3–4 days at 4°. Plants were germinated and grown under long-day conditions (18 hr light). All parental strains are available from the Arabidopsis Biological Resource Center at Ohio State University (http://www.biosci.ohio-state.edu/~plantbio/Facilities/abrc/abrchome.htm).

DNA preparation and marker analysis:
DNA was extracted from meiotically related progeny plants by grinding single cauline leaves (~0.5–1 cm) in 200 µl of 50 mM Tris·HCl (pH 8.0), 200 mM NaCl, 0.2 mM EDTA, 0.5% SDS, and 100 µg/ml Pronase E (Sigma, St. Louis). After incubation at 37° for 30 min samples were extracted with phenol and then chloroform. DNA was precipitated by the addition of 0.1 volume of sodium acetate and 2 volumes of 100% ethanol. After centrifugation, DNA pellets were washed twice in 70% ethanol, resuspended in 100 µl TE (10 mM Tris·HCl, pH 8.0, 1 mM EDTA), and stored at 4°. The PCR-based markers used in this analysis are described at the Arabidopsis Information Resource (http://www.arabidopsis.org/) and include for chromosome 2, RGA, nga1145, m246, mi310, T10J7-t7, THY1B, PLS2, PLS4, PLS8, nga1126, nga361, m323, nga168, BIO2, ML, GBF3, and SGCSNP1098 and for chromosome 4, Tel4N, JV30/31, CIW5, GA1, T5L23.3, nga8, nga1111, DET1, SGCSNP385, CIW6, COP9B, SC5, g4539, AG, CIW7, RPS2, nga1139, JM411, nga1107, DHS1, and SGCSNP53. PCR primers were purchased from Research Genetics (Huntsville, AL), Invitrogen Life Technologies (Carlsbad, CA), or MWG (Highpoint, NC). Markers were amplified by PCR using the following parameters: hotstart at 95°, 30 sec; denaturing at 94°, 15 sec (40 cycles); annealing optimized for each marker between 52° and 57° (10 cycles) followed by 54°–61° (30 cycles); and extension at 72° (40 cycles) in an MJ Research (Cambridge, MA) DYAD. Markers were visualized with UV light following electrophoresis of PCR products using either 1% agarose gels or 14% native polyacrylamide gels and staining with ethidium bromide. If necessary, polymorphisms were detected by digesting PCR reactions with restriction enzymes prior to electrophoresis (KONIECZNY and AUSUBEL 1993).

Data analysis:
Marker scores for 143 tetrads were recorded and then verified by two individuals to avoid clerical errors. The tetrad data were analyzed using the methods described in the Appendix of HOUSWORTH and STAHL (2003). The details of the analysis differ from those given in COPENHAVER et al. (2002), but the results of the two methods for the two chromosomes studied in this article are statistically equivalent. The methods of HOUSWORTH and STAHL (2003) are appropriate here because the chromosomes in this article are so well marked that the position of a crossover on a chromosome is known within an error never exceeding 4 cM. The methods of HOUSWORTH and STAHL (2003) are also computationally faster and facilitate simulations required for assessing significance and providing confidence intervals for the data studied in this article.


   RESULTS
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Fundamental recombination parameters:
We examined the frequency and distribution of crossover events in 143 Arabidopsis tetrads by scoring 17 molecular markers on chromosome 2 and 21 markers on chromosome 4. These markers span 98 and 97% of chromosomes 2 and 4, respectively. This coverage represents a 19% improvement for chromosome 2 and 9% improvement for chromosome 4 over tetrad analysis data reported for Arabidopsis previously (COPENHAVER et al. 1998). Adjacent markers on both chromosomes are separated by <10 cM. Pollination with single-pollen tetrads sometimes results in fewer than four progeny plants. Both four- and three-member tetrads are useful for tetrad analysis since for most purposes the fourth member can be inferred from the genotype of the remaining three members. In this study, 32 of the 143 tetrads examined contained only three members. In addition, due to limited DNA stocks, in 7 cases for chromosome 2 and 14 cases for chromosome 4 scores were not recorded for at least one marker in one member of an otherwise four-member tetrad.

A summary of the observed crossover events for each chromosome is presented in Table 1. The average number of crossovers per chromosome tetrad (bivalent) was similar, with chromosome 2 experiencing 1.7 per meiosis and chromosome 4 experiencing 1.5. Importantly, these bivalents experienced multiple crossovers in sufficient meioses to enable an examination of interference parameters (Figure 1). On both chromosomes the majority of crossovers occurred on the longer arm of these short, acrocentric chromosomes. In only one case, on chromosome 2, did we observe a meiosis that apparently lacked a crossover. This could be due to the occurrence of two closely spaced 2-chromatid crossovers not separated by an intervening marker. However, the observed ratio of 2:3:4-chromatid double crossovers argues that our marker density is sufficient to detect nearly all double crossovers. Alternatively, the single meiosis apparently lacking a crossover on chromosome 2 could be explained by an undetected crossover on one or the other extreme terminus of the chromosomes. Such events have been observed in Arabidopsis using cytological analysis (SANCHEZ-MORAN et al. 2001, 2002). It is also possible that this bivalent did not experience a crossover: the model we used to simulate expected distributions of intercrossover distances in Arabidopsis predicts ~1% nonexchange bivalents for chromosome 2.


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  		TABLE 1 Crossover distribution and frequency parameters for Arabidopsis NOR-bearing chromosomes

 


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  		FIGURE 1.— Distribution of crossover events on NOR-bearing Arabidopsis chromosomes. Crossover events (solid boxes) in 16 intervals on chromosome 2 and 20 intervals on chromosome 4 (open boxes) were detected by scoring PCR-based molecular markers in 143 Arabidopsis tetrads (vertical axis). Intervals are not drawn to scale but are represented as equal-sized boxes (horizontal axis). Chromosome arms are defined by the centromere positions (shaded circle) described in COPENHAVER et al. (1999).

 
Interference-sensitive and insensitive crossovers occur on the NOR-bearing chromosomes in Arabidopsis:
Our previous analyses suggest that the distribution of intercrossover distances on Arabidopsis chromosomes 1, 3, and 5 is consistent with the presence of a fraction of crossovers that are insensitive to interference. The paucity of crossover events on chromosomes 2 and 4 prevented our drawing any statistically relevant conclusion for these short, acrocentric NOR-bearing chromosomes. To remedy this, we scored a denser set of molecular markers that covers a greater proportion of chromosomes 2 and 4 in approximately 3 times as many tetrads. Using a likelihood-ratio test, we examined this expanded data set and asked whether a model wherein each crossover is subject to interference (p = 0) was more or less likely than a model wherein some fraction of crossovers is resistant to interference (p > 0). The results of this analysis are presented in Table 2. Like the results previously shown for chromosomes 1, 3, and 5, the data fit the two-pathway model substantially better than the interference-only model. Although the likelihood-ratio testing we have presented provides a powerful method of comparing models and gives strong evidence that the addition of interference-insensitive crossovers improves the original counting model, goodness-of-fit assessment would require on the order of 10 times the number of tetrads and is beyond the scope of this study. That is, while the two-pathway model is significantly more likely, due to lack of power in goodness-of-fit testing procedures, we have no statistical evidence that either model fails to fit the data.


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  		TABLE 2 Estimates of interference parameters

 
Interference-insensitive crossovers occur less frequently on the NOR-bearing chromosomes:
Our previous analysis of crossover interference on chromosomes 1, 3, and 5 in Arabidopsis yielded an estimate of the fraction of crossovers insensitive to interference, p, of 0.2 for each chromosome (COPENHAVER et al. 2002). The current analysis reveals that chromosome 2 and 4 have much smaller values of p, ~0.03 and 0.05, respectively, with 95% confidence intervals of (0.003, 0.059) and (0.023, 0.097), respectively. Thus, the distributions of crossovers on small, acrocentric, NOR-bearing chromosomes of Arabidopsis conform more closely to the simple counting model (FOSS et al. 1993) than do those on the remaining chromosomes, which are longer, metacentric, and lack NOR regions.


   DISCUSSION
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 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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 LITERATURE CITED
 
Pairing centers and interference:
Pairing is an essential step in organizing and properly distributing homologous chromosomes during meiosis (MCKEE 2004). Genetic and cytological analyses indicate that pairing is not dependent on the formation of double-strand breaks (DSBs) but that DSB repair by crossing over likely plays a role in stabilizing pairing (ZICKLER and KLECKNER 1999; CHA et al. 2000). Conversely, homologous meiotic recombination is operationally dependent on some juxtaposition of homologous chromosomes. Homologous chromosome pairing can also be stabilized via specialized pairing centers. In Caenorhabditis elegans each chromosome has a pairing site (MCKIM et al. 1988), and pairing centers have been observed in plants as well (MAGUIRE 1986). In Drosophila the NOR is a well-characterized pairing site (MCKEE and KARPEN 1990). Indeed, it has been determined that only a few copies of the intergenic spacer regions of the Drosophila rDNA are necessary to mediate chromosome pairing (MCKEE et al. 1992). Similar NOR-driven chromosome pairing has been observed in mammals (STITOU et al. 1997). Given the necessity of homolog pairing, the relationship between pairing and recombination, the ability of NORs to serve as pairing centers, and the interference data presented in this article, it is pertinent to ask if there is a relationship between the presence of an NOR on a chromosome and the frequency of noninterfering crossovers.

In Arabidopsis, homologous chromosome association appears to involve telomeres. FISH analysis of Arabidopsis chromosomes shows that telomeres associate with the NOR during premeiotic interphase. That association presumably assists in pairing and is later lost during leptotene and replaced with a loose bouquet formation in zygotene (ARMSTRONG et al. 2001). Whether loose zygotene telomere association is comparable to the strong "classical bouquet" seen in other organisms remains unclear. In asy1, an Arabidopsis mutant that abolishes synapsis, the premeiotic NOR-associated telomere clustering is maintained. However, because asy1 mutants fail to synapse the chromosome pairs eventually disjoin, yielding univalents, including the NOR-bearing chromosomes (ARMSTRONG et al. 2001). Thus, the NOR regions may be implicated in assisting chromosome organization during meiosis, but more analysis needs to be done to determine any specific role in pairing.

The shortage of noninterfering crossovers on the NOR-bearing chromosomes of Arabidopsis can be rationalized in the framework presented in COPENHAVER et al. (2002) and expanded in STAHL et al. (2004). By several criteria, Arabidopsis is a "group II" organism, whose chromosome synapsis depends on recombination functions (GRELON et al. 2001). We postulate that the crossovers resulting from these presynaptic events are interference free. Events initiated postsynaptically, on the other hand, give rise to crossovers that are subject to interference (among each other), presumably according to the counting rules of FOSS et al. (1993). Within this framework, the presence of NORs acting as pairing centers on the two short chromosomes reduces the need for the noninterfering crossovers. It is possible that the differentiation from noninterfering to interfering crossovers is controlled by the establishment of synapsis.

In Drosophila melanogaster and C. elegans, both of which are group I organisms lacking synapsis-promoting recombination events (STAHL et al. 2004), deletion of pairing centers, such as NORs, decreases crossing over and deters synapsis (HAWLEY 1980; VILLENEUVE 1994). Examination of pairing partner switches in autotetraploid lines suggests that Arabidopsis chromosomes also harbor multiple autonomous pairing sites (SANTOS et al. 2003). Low frequencies of chromosome 2 and 4 multivalent formation in autotetraploid lines may indicate the existence of a particularly strong pairing site, perhaps the NOR, that dominates the pairing choice for the length of these chromosomes (SANTOS et al. 2003). It is interesting to note that in these studies chromosome 2 exhibits the lowest multivalent frequencies (and therefore the most persistent bivalent pairing), and in our experiments chromosome 2 exhibits the fewest noninterfering crossovers. These observations suggest that the presence of NOR domains (putative pairing centers) influences the relative frequencies of two distinct classes of crossovers in Arabidopsis. We find this hypothesis particularly interesting since it implies that interference is regulated at a chromosomal level in a manner that reflects chromosome architecture.

Distribution of interference-sensitive and insensitive crossovers:
The mathematical model that we used to simulate the distribution of intercrossover distances on the chromosomes of Arabidopsis has two variables: p, which is the portion of interference-insensitive crossovers out of the total crossover population, and m, which is the obligate number of "failures" between any two interfering crossovers. As an aside, it should be noted that many other intriguing models of interference have been proposed (e.g., KING and MORTIMER 1990; FUJITANI et al. 2002; BORNER et al. 2004). The interference parameters for chromosomes 1, 3, and 5 in our previous study varied from 10 to 17, and all estimates in that range were statistically indistinguishable due to the lack of statistical power of the analysis. The level of interference for chromosomes 2 and 4 estimated in this study is ~m = 9 (±2). Thus, interference-sensitive crossovers may be subject to the same intensity of interference (m) on all the Arabidopsis chromosomes. This is striking given the large difference in the frequencies (p) of the interference-insensitive crossovers. We propose that this reflects a fundamental difference in the way that interference-insensitive and -sensitive crossovers are apportioned on chromosomes, while the strength of interference (m) is consistent for all crossovers subject to interference, regardless of chromosome.

HIGGINS et al. (2004) recently provided genetic support for the two-pathway model of recombination in Arabidopsis by examining mutants in the MSH4 gene. In Saccharomyces cerevisiae msh4 mutants have reduced crossover frequency and the residual crossovers are free of interference (NOVAK et al. 2001) Chiasmata in Atmsh4 mutants are reduced by ~85% and the remaining chiasmata are distributed randomly among cells and chromosomes, suggesting that they are free of interference. However, the initial analysis of Atmsh4 lacked the resolution to measure interference on individual chromosomes. Nonetheless, it is intriguing to note that the observed 85% reduction in chiasmata is consistent with the modeling prediction that ~80% of all crossovers on chromosomes 1, 3, and 5 are insensitive to interference (COPENHAVER et al. 2002). It should be noted that HIGGINS et al. (2004) did not report any differences in the level of noninterfering crossovers among the five Arabidopsis chromosomes.

This study examines interference on chromosomes 2 and 4 of Arabidopsis. In addition to harboring large NOR domains these chromosomes are also shorter than the other three Arabidopsis chromosomes. In yeast, short chromosomes have been shown to have a higher crossover density and exhibit weaker interference when compared to longer chromosomes (KABACK et al. 1999). Consistent with these observations, DE LOS SANTOS et al. (2003) report that interference-insensitive crossovers occur more frequently on smaller chromosomes in yeast. Taken together these findings suggest that one would expect that chromosomes 2 and 4 should have a relatively higher fraction of interference-insensitive crossovers—precisely the opposite of what we observe. This discrepancy highlights the need for analysis that disentangles the effects of chromosome stature and chromosome architecture (NOR presence) on crossover interference.

The counting model of FOSS et al. (1993) proposes that m represents noncrossover gene conversion events. We have calculated the predicted number of gene conversions expected on chromosomes 2 and 4, using the assumptions and formulas described in COPENHAVER et al. (2002) for similar calculations on chromosomes 1, 3, and 5. These calculations predict 0.74 and 0.83 gene conversions for chromosomes 2 and 4, respectively, in the 143 tetrads assayed. This is consistent with our observed data described here, which did not detect any gene conversions.


   ACKNOWLEDGEMENTS
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
LITERATURE CITED
 
We thank two anonymous reviewers for helpful suggestions. G.P.C. was supported by the University of North Carolina Biology Department and the Carolina Center for Genome Sciences. The computational portion of this research was supported in part by the Indiana Genomics Initiative, which is supported in part by Lilly Endowment. Additional support to E.A.H. comes from the National Science Foundation (DMS-0306243). F.W.S.'s lab is supported by the National Science Foundation (MCB-0109809). F.W.S. is an American Cancer Society Research Professor.


   LITERATURE CITED
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 

ARMSTRONG, S. J., F. C. H. FRANKLIN and G. JONES, 2001 Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J. Cell Sci. 114: 4207–4217.[Abstract/Free Full Text]

BORNER, G. V., N. KLECKNER and N. HUNTER, 2004 Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29–45.[CrossRef][Medline]

CHA, R. S., B. M. WEINER, S. KEENEY, J. DEKKER and N. KLECKNER, 2000 Progression of meiotic DNA replication is modulated by interchromosomal interaction proteins, negatively by Spo11p and positively by Rec8p. Genes Dev. 14: 493–503.[Abstract/Free Full Text]

COPENHAVER, G. P., and C. S. PIKAARD, 1996 RFLP and physical mapping with an rDNA-specific endonuclease reveals that nucleolus organizer regions of Arabidopsis thaliana adjoin the telomeres on chromosomes 2 and 4. Plant J. 9: 259–272.[CrossRef][Medline]

COPENHAVER, G. P., J. D. DOELLING, J. S. GENS and C. S. PIKAARD, 1995 Use of RFLPs larger than 100 kbp to map the position and internal organization of the nucleolus organizer region on chromosome 2 in Arabidopsis thaliana. Plant J. 7: 273–286.[CrossRef]

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]

COPENHAVER, G. P., K. NICKEL, T. KUROMORI, M. I. BENITO, S. KAUL et al., 1999 Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286: 2468–2474.[Abstract/Free Full Text]

COPENHAVER, G. P., E. A. HOUSWORTH and F. W. STAHL, 2002 Crossover interference in Arabidopsis. Genetics 160: 1631–1639.[Abstract/Free Full Text]

DE LOS SANTOS, T., N. HUNTER, C. LEE, B. LARKIN, J. LOIDL et al., 2003 The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics 164: 81–94.[Abstract/Free Full Text]

FOSS, E., R. LANDE, F. W. STAHL and C. M. STEINBERG, 1993 Chiasma interference as a function of genetic distance. Genetics 133: 681–691.[Abstract]

FUJITANI, Y., S. MORI and I. KOBAYASHI, 2002 A reaction-diffusion model for interference in meiotic crossing over. Genetics 161: 365–372.[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.[CrossRef][Medline]

HAWLEY, R. S., 1980 Chromosomal sites necessary for normal levels of meiotic recombination in Drosophila melanogaster. I. Evidence for and mapping of the sites. Genetics 94: 625–646.[Abstract/Free Full Text]

HIGGINS, J. D., S. J. ARMSTRONG, F. C. H. FRANKLIN and G. JONES, 2004 The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev. 18: 2557–2570.[Abstract/Free Full Text]

HOUSWORTH, E. A., and F. W. STAHL, 2003 Crossover interference in humans. Am. J. Hum. Genet. 73: 188–197.[CrossRef][Medline]

KABACK, D. B., D. BARBER, J. MAHON, J. LAMB and J. YOU, 1999 Chromosome size-dependent control of meiotic reciprocal recombination in Saccharomyces cerevisiae: the role of crossover interference. Genetics 152: 1475–1486.[Abstract/Free Full Text]

KING, J. S., and R. K. MORTIMER, 1990 A polymerization model of chiasma interference and corresponding computer simulation. Genetics 126: 1127–1138.[Abstract]

KONIECZNY, A., and F. M. AUSUBEL, 1993 A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 4: 403–410.[CrossRef][Medline]

MAGUIRE, M. P., 1986 The pattern of pairing that is effective for crossing over in complex B-A chromosome rearrangements in maize. III. Possible evidence for pairing centers. Chromosoma 94: 71–85.[CrossRef][Medline]

MCCLINTOCK, B., 1934 The relationship of a particular chromosomal element to the development of the nucleoli in Zea mays. Zeit. Zellforsch. Mik. Anat. 21: 294–328.[CrossRef]

MCKEE, B. D., 2004 Homologous pairing and chromosome dynamics in meiosis and mitosis. Biochim. Biophys. Acta 1677: 165–180.[Medline]

MCKEE, B. D., and G. H. KARPEN, 1990 Drosophila ribosomal RNA genes function as an X-Y pairing site during male meiosis. Cell 61: 61–72.[CrossRef][Medline]

MCKEE, B. D., L. HABERA and J. A. VRANA, 1992 Evidence that intergenic spacer repeats of Drosophila melanogaster rRNA genes function as X-Y pairing sites in male meiosis, and a general model for achiasmatic pairing. Genetics 132: 529–544.[Abstract]

MCKIM, K. S., A. M. HOWELL and A. M. ROSE, 1988 The effects of translocations on recombination frequency in Caenorhabditis elegans. Genetics 120: 987–1001.[Abstract/Free Full Text]

NOVAK, J. E., P. B. ROSS-MACDONALD and G. S. ROEDER, 2001 The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158: 1013–1025.[Abstract/Free Full Text]

PREUSS, D., S. Y. RHEE and R. W. DAVIS, 1994 Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264: 1458–1460.[Abstract/Free Full Text]

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

SANCHEZ-MORAN, E., S. J. ARMSTRONG, J. L. SANTOS, F. C. FRANKLIN and G. H. JONES, 2002 Variation in chiasma frequency among eight accessions of Arabidopsis thaliana. Genetics 162: 1415–1422.[Abstract/Free Full Text]

SANTOS, J. L., D. ALFARO, E. SANCHEZ-MORAN, S. J. ARMSTRONG, F. C. FRANKLIN et al., 2003 Partial diploidization of meiosis in autotetraploid Arabidopsis thaliana. Genetics 165: 1533–1540.[Abstract/Free Full Text]

STAHL, F. W., H. M. FOSS, L. S. YOUNG, R. H. BORTS, M. F. ABDULLAH et al., 2004 Does crossover interference count in Saccharomyces cerevisiae? Genetics 168: 35–48.[Abstract/Free Full Text]

STITOU, S., M. BURGOS, F. ZURITA, R. JIMENEZ, A. SANCHEZ et al., 1997 Recent evolution of NOR-bearing and sex chromosomes of the North African rodent Lemniscomys barbarus. Chromosome Res. 5: 481–485.[CrossRef][Medline]

STURTEVANT, A. H., 1915 The behavior of chromosomes as studied through linkage. Z. Indukt. Abstammungs-Vererbungsl. 13: 234–287.

VILLENEUVE, A. M., 1994 A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics 136: 887–902.[Abstract]

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

Communicating editor: R. S. HAWLEY




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