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Segregation in Yeast LYLE 0 Proc. Natl. Acad. Sci. USA Vol. 93, pp. 4979-4983, May 1996 Genetics Exchanges are not equally able to enhance meiotic chromosome segregation in yeast LYLE 0. Ross*, REBECCA MAXFIELD, AND DEAN DAWSONt Department of Molecular Biology and Microbiology, Tufts University, 136 Harrison Avenue, Boston, MA 02111 Communicated by Nancy Kleckner, Harvard University, Cambridge, MA, January 18, 1996 (received for review July 1, 1995) ABSTRACT Homologous chromosomes pair, and then Crossovers do not guarantee disjunction, rather they en- migrate to opposite poles of the spindle at meiosis I. In most hance the chances that it will occur. The observation of eukaryotic organisms, reciprocal recombinations (cross- nondisjoined homologs that have experienced crossovers raises overs) between the homologs are critical to the success of this the possibility that some crossovers may have properties that process. Individuals with defects in meiotic recombination cause them to form less effective chiasmata than other cross- typically produce high levels of aneuploid gametes and exhibit overs. The experiments described here were designed to test low fertility or are sterile. The experiments described here systematically whether different crossovers were equally able were designed to test whether different crossovers are equally to enhance the fidelity of meiotic chromosome segregation. To able to contribute to the fidelity of meiotic chromosome test the ability of a chromosomal exchange to influence segregation in yeast. These experiments were performed with disjunction, it is necessary that the exchange be the only one model chromosomes with which it was possible to control and between the homologs whose segregation is being monitored. measure the distributions of meiotic crossovers in wild-type This situation is rare in yeast, because even the smallest cells. Physical and genetic approaches were used to map chromosomes typically experience two or more exchanges in crossover positions on model chromosomes and to correlate most meioses. Yeast artificial chromosomes and derivatives of crossover position with meiotic segregation behavior. The yeast natural chromosomes offer the advantage that they can results show that crossovers at different chromosomal posi- be constructed such that they experience one (El) or zero (Eo) tions have different abilities to enhance the fidelity of meiotic exchanges in most meioses (6-8). The experiments presented segregation. here show that exchanges in different genetic intervals of these model chromosomes have different abilities to enhance dis- Reciprocal recombination is critical for successful sexual re- junction. production in most eukaryotes. Haploid gametes are gener- ated by meiosis in which a single round of DNA replication is followed by two successive rounds of chromosome segregation. MATERIALS AND METHODS In meiosis I, homologous chromosomes pair and recombine, Strains, Media, and Genetic Methods. Media was prepared and then segregate to opposite poles of the cell (disjoin) at as described (9). Saccharomyces cerevisiae strains are described anaphase (Fig. la) (for review see ref. 1). Crossovers between in Table 1. Mini chromosomes and artificial chromosomes can homologs are critical for the formation of chiasmata, the vary in copy number. Sporulation and tetrad analysis was linkages between homologous chromosomes that can be ob- performed as described (8). Only four spore viable tetrads with served in cytologically tractable organisms, which keep ho- two copies of each chromosome of interest were informative mologs joined until anaphase I. In the absence of chiasmata, for these experiments. A tabulation of all of the classes of four homologous chromosomes have a greatly elevated chance of spore viable tetrads observed in each experiment is found in segregating independently of each other, often migrating to the corresponding figure legend. Statistical analyses were the same pole at anaphase I (nondisjunction) (Fig. lb) (for a performed using the G test (10) or comparisons of the 95% discussion of exceptions see ref. 1). Organisms with mutations confidence limits of Poisson sampling variability (11). that abolish meiotic recombination experience randomized Construction ofArtificial Chromosomes and Mini III Chro- partitioning of chromosomes at meiosis I, leading to aneuploid mosomes. The construction and features of the yeast linear gametes and reduced fertility or sterility. In humans, the failure plasmids (YLps) and the mini III chromosomes have been of chromosomes to experience exchange in meiosis is corre- described (6, 8, 12). Chromosomal alterations were accom- lated with the generation of gametes aneuploid for certain plished using one- and two-step gene replacement techniques chromosomes (2). (13, 14). The mini III chromosomes diagrammed in Fig. 4 are Exchange alone is not sufficient for securing paired homol- the same as those described in ref. 8. The artificial chromo- ogous chromosomes until anaphase I. A second uncharacter- somes diagrammed in Fig. 3 are derived from those described ized activity, termed chiasma binder, is needed to stabilize the in ref. 8 with the following modifications. The left arm XbaI linkage between homologs (3, 4). The requirement for chiasma site on YLp201 has been removed so that crossover positions binder is illustrated in Fig. 2a, which shows that a resolved on the left arm can be determined with respect to the location crossover, by itself, would not be expected to hold a pair of of the XbaI site (Fig. 3). pA252p6 (6), which carries sequences homologous chromosomes together. There are two basic mod- corresponding to part of the left arm of the YLp including a els for the way in which chiasma binder function is achieved (4). telomere LEU2 and a fragment of A phage DNA with the XbaI In the first model, chiasma binder maintains the association of site, was cut with XbaI, with flush ends created using T4 sister chromatids distal to the chiasma (Fig. 2b). In the second polymerase and recircularized to create pL29. A strain carry- model, chiasma binder acts at the chiasma (Fig. 2c). These ing a leu2, trpl, URA3, ARG4, his3 YLp was transformed with models are not mutually exclusive, and evidence consistent a BamHI fragment of pL29. This fragment includes the with both of them has been described (for review see ref. 5). *Present address: Institute for Molecular Genetics, Baylor College of The publication costs of this article were defrayed in part by page charge Medicine, Houston, TX 77030. payment. This article must therefore be hereby marked "advertisement" in fTo whom reprint requests should be addressed. e-mail: ddawson@ accordance with 18 U.S.C. §1734 solely to indicate this fact. opal.tufts.edu. 4979 Downloaded by guest on September 23, 2021 4980 Genetics: Ross et al. Proc. Natl. Acad. Sci. USA 93 (1996) a b a b C _0 meiosis _0 I W N4* --meiosis ~~II FIG. 2. Models for chiasma binder activity. (a) A pair of homologs i0 joined by a chiasma. (b) Chiasma binder is represented as cohesion between sister chromatids. (c) Chiasma binder acting at the site of the FIG. 1. Meiosis I disjunction (a). Meiosis I nondisjunction (b). exchange to fix the chiasma in place. telomere, LEU2, and the A DNA with the modified restriction with yeast genes and an XbaI restriction site dimorphism site. After transformation, Leu+ transformants were screened making it possible to assign exchanges to one of five intervals by Southern blot analysis for loss of the XbaI site. YLp200 is (Fig. 3a). Genetic analysis of a strain containing these YLps leu2, TRPI, ura3, arg4, HIS3, but has had the NheI site removed (DL363) was used to determine the segregation fidelity of and replaced with three HO endonuclease recognition sites. YLps that had experienced exchanges in each of the genetic The strains used in these experiments are ho/ho, and in this intervals. The analysis was performed in three steps. (i) strain background the presence of the HO sites results in no Tetrads were dissected on rich medium and spore colonies detectable change in the levels of crossing-over in the left arm were replica-plated to media lacking leucine, tryptophan, of the YLps (data not shown). The effect of double-strand uracil, arginine, histidine, or adenine. Artificial chromosomes breaks at these sites in meiosis will be described elsewhere. A that disjoined, either with or without an exchange, were 502-bp SspI to BamHI fragment of A bacteriophage DNA (A identified by the growth of spores containing them on these map position 34,499 to 35,001) that carries the NheI site was plates. Additionally, this step identified tetrads in which the cloned into SspI, BamHI digested YIp5. The NheI site was sister chromatids of one of the YLps had precociously segre- cleaved and filled in with T4 polymerase. Three copies of a gated at meiosis I (PSSC), and tetrads in which one of the YLps 24-bp oligomer with an HO endonuclease cut site and a KpnI had been lost from the cell or was carried in two copies prior restriction site was ligated into the blunted site to create to meiosis. (ii) We attempted to determine the genetic maps plasmid pD148 (a URA3 vector). A strain carrying an leu2, of chromosomes in spores containing more than one YLp as TRP1, ura3, arg4, HIS3 version of the artificial chromosome a result of nondisjunction or PSSC. Because of the mitotic was transformed with pD148 digested with BstXI, and a instability of the artificial chromosomes, it was possible to two-step selection was used to construct YLps that had been isolate two derivatives of each spore carrying nondisjoined modified by the NheI/HO site sequences on pD148 (14). artificial chromosomes; cells that had lost one of the nondis- Candidates were then screened by Southern blot analysis for joined artificial chromosomes and cells that had lost the other. loss of the plasmid but maintenance of the KpnI carrying The growth characteristics of these two derivatives were tested, inserts. using the media described above, to determine whether the Extrapolation of Crossover Positions in the Left Arm.
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