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Meiotic Recombination and Segregation of Human-Derived Proc. Natl. Acad. Sci. USA Vol. 89, pp. 5296-5300, June 1992 Genetics Meiotic recombination and segregation of human-derived artificial chromosomes in Saccharomyces cerevisiae (meiosis/yeast artificial chromosomes/recombination/chromosome segregation) DOROTHY D. SEARSt, JOHANNES H. HEGEMANNt, AND PHILIP HIETERt§ tMolecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore, MD 21205; and tInstitut fuer Mikrobiologie und Molekularbiologie, Justus Liebig Universitaet, 6300 Giessen, Federal Republic of Germany Communicated by John W. Littlefield, February 12, 1992 ABSTRACT We have developed a system that utilizes between meiotic recombination and meiosis I disjunction human DNA-derived yeast artificial chromosomes (YACs) as comes from cytological observation or genetic analysis of marker chromosomes to study factors that contribute to the recombination-deficient mutants in several organisms (for fidelity of meiotic chromosome transmission. Since aneuploidy review, see ref. 2). Recombination mutants exhibit increased for the YACs does not affect spore viability, different classes of levels of meiosis I nondisjunction and/or high levels of meiotic missegregation can be scored accurately in four-viable- gamete inviability that are presumably caused by missegre- spore tetrads including precocious sister separation, meiosis I gation events that give rise to aneuploid meiotic products. nondisjunction, meiotic chromatid loss, and meiosis II nondis- Although these observations support the view that recombi- junction. Segregation of the homologous pair of 360-kilobase nation directly affects the fidelity ofchromosome segregation marker YACs was shown to occur with high fidelity in the first during meiosis I, no systematic analysis of this relationship meiotic division and was associated with a high frequency of has been undertaken in the context of a wild-type genetic recombination within the human DNA segment. By using this background. experimental system, a series of YAC deletion derivatives Because missegregation of chromosomes can give rise to ranging in size from 50 to 225 kilobases was analyzed to directly inviable meiotic products that do not contain the full com- assess the relationship between meiotic recombination and plement of a haploid genome, chromosome loss/gain in dead meiosis I disjunction in a genotypically wild-type background. gametes must be inferred from the chromosome content of The relationship between physical distance and recombination the viable gametes that remain. Therefore, the type or frequency within the human DNA segment was measured to be frequency of meiotic missegregation events cannot be accu- comparable to that of endogenous yeast chromosomal DNA- rately scored. We have developed a system that allows ranging from <2.0 to 7.7 kilobases/centimorgan. Physical thorough examination of chromosome transmission during analysis of recombinant chromosomes detected no unequal meiosis in S. cerevisiae. Meiotic chromosome recombination crossing-over at dispersed repetitive elements distributed along are human DNA-derived the YACs. Recombination between YACs containing unrelated and segregation analyzed using DNA segments was not observed. Furthermore, the segrega- yeast artificial chromosome (YAC) pairs. Unlike endogenous tional data indicated that meioses in which YAC pairs failed to chromosome missegregation, aberrant segregation of these recombine exhibited dramatically increased levels of meiosis I nonessential YACs can be scored easily because all four missegregation, including both precocious sister chromatid meiotic products are viable regardless of YAC copy number. separation and nondisjunction. Furthermore, the YACs and yeast host strain are suitably marked so that specific types ofaberrant transmission can be distinguished and further analysis of each spore is possible. Meiotic chromosome segregation consists of two distinct We find that homologous YACs disjoin from one another types ofchromosome disjunction and results in a reduction of with high fidelity during meiosis I and that the frequency of genome content from a diploid to a haploid state. During meiotic recombination between human DNA-derived YAC meiosis I, homologous sister chromatid pairs are segregated homolog pairs is comparable to that of yeast endogenous to opposite poles; during meiosis II, sister chromatids are chromosomes. By altering the structure ofone member ofthe separated (in a manner analogous to mitotic chromosome YAC homolog pair, we demonstrate directly that failure to segregation). New combinations of genetic information are recombine has a deleterious effect on meiosis I segregation generated by independent assortment of chromosomes and levels of precocious sister separation by recombination. The product of a meiosis event in Sac- fidelity causing high charomyces cerevisiae is a tetrad that is made up of four (PSS) and nondisjunction (NDI). haploid spores enclosed in an ascus. Segregation of chromo- somes through meiosis occurs with high fidelity to ensure the MATERIALS AND METHODS formation of four euploid spore products. The measured Replacement of CEN6 with ACEN6::LEU2-CEN11. Two frequency of spontaneous chromosome V missegregation genomic HindIII-Taq I fragments, fragment A, 0.5 kilobase during meiosis I is less than one event in 104 viable spores (1). (kb) and fragment B, 0.6 kb (Fig. 1), which flank a 392-base- Meiosis I errors involving chromosomes III and VII occur in I -1 in 103 and 1 in 104 meioses, respectively (M. Goldway, T. pair Taq CEN6 fragment were subcloned into pRS25 (R. Arbel, and G. Simchen, personal communication). Sikorski and P.H., unpublished data), a LEU2-containing High fidelity of chromosome segregation during meiosis I derivative of pBluescript 1 (Stratagene), to give pJHH56. A is thought to be enhanced by recombination between non- 0.65-kb CENI I fragment (D. Jager and J.H.H., unpublished sister chromatids and the subsequent formation of chiasmata data) was ligated into pJHH56 to make pJHH57 (Fig. 1). between homologs. Evidence for a positive relationship Abbreviations: YAC, yeast artificial chromosome; PSS, precocious sister separation; NDI and NDII, nondisjunction in meiosis I and I1, The publication costs of this article were defrayed in part by page charge respectively; PD, parental ditype; NPD, nonparental ditype; T, payment. This article must therefore be hereby marked "advertisement" tetratype; CL, meiotic chromatid loss; cM, centimorgan(s). in accordance with 18 U.S.C. §1734 solely to indicate this fact. §To whom reprint requests should be addressed. 5296 Downloaded by guest on September 29, 2021 Genetics: Sears et al. Proc. Natl. Acad. Sci. USA 89 (1992) 5297 URA3 SUPIl TRPI a. 0 TEL CEN4 HUMAN INSERT LYS2 TEL CEN4 HUMAN INSERT A B b CHR VI PD URA<T A CEN6 B CHR VI CEN1I NPD A B FIG. 1. Structure of the ACEN6::LEU2-CEN1I deletion/ insertion vector pJHH57 and replacement of CEN6 with LEU2- CENII on chromosome VI (CHR VI). H, HindIII; T, Taq I; A and B, fragments A and B, respectively. T LYS2 pJHH57 was cleaved with HindIII and transformed into yeast strain YPH250 by the lithium acetate method (3) to select Leu+ transformants (Fig. 1). Replacement of the genomic FIG. 2. (a) YAC pair A. Each YAC is 360 kb long and has a 392-base-pair CEN6 fragment by the LEU2-CENJJ cassette centromere-linked marker (URA3-SUP) I or L YS2), a distal marker on chromosome VI yielded YPH424 (MATa ura3-52 ade2-101 (TRPJ or HIS3), a centromere sequence derived from chromosome trpl-A1 lys2-801 his3A200 leu2-AJ ACEN6::LEU2-CEN11), IV (CEN4), a human DNA insert, and two telomeres (TEL). (b) which was verified by Southern blot analysis (data not Possible tetrad configurations resulting from sporulation of a diploid strain containing YAC pair A. PD, parental ditype (distal markers were shown). All derivatives ofYPH424 made using standard associate with the same centromere markers as in the parent diploid; genetic methods (4). i.e., every spore is nonrecombinant for YAC markers); NPD, Yeast Strains. All S. cerevisiae diploid strains used in this nonparental ditype (all four spores are recombinant for YAC mark- study are of the following genotype: MATa/MATa ura3-52/ ers, for example, as a result of a four-strand double recombination ura3-52 ade2-101/ade2-101 trpJAJ/trpJAJ lys2-801/lys2-801 between distal markers; note that a two-strand double crossover his3A200/his3A200 leu2-J/Ileu2-AJ CEN6/ACEN6:: between two nonsister chromatids results in a PD tetrad); T, tetra- LEU2-CENJ1. Most YACs used in this study are derived type (two spores are recombinant and two spores are nonrecombi- nant for YAC markers; e.g., as a result of a single crossover). from a characterized YAC (5) that is 360 kb long and contains a human genomic fragment. Prototrophic markers at the The patterns for proper segregation of a YAC homolog pair centromere-proximal and -distal ends of the YACs were with respect to a LEU2 sister spore marker are shown in Fig. modified by gene replacement with a set of marker change 3a. In our diploid strains, CEN6 is replaced by a LEU2- A plasmids (6). YPH607 contains YAC pair (Fig. 2a). CENJJ casette on one copy of chromosome VI (Fig. 1). YPH787, YPH788, and YPH789 carry YAC pairs B, C, and Exchange between this region and the wild-type CEN6 D, respectively (see Fig. 4). YPH785 and YPH880 contain sequence by homologous recombination cannot occur. YAC pairs E (which includes a 390-kb mouse DNA-derived Therefore, the presence of LEU2 will always denote a sister YAC, ref. 7) and F (which includes a 300-kb human chro- spore pair as it is perfectly CEN-linked. If the YACs segre- mosome 21-derived YAC, ref. 7), respectively (see Fig. 4). gate correctly, centromere-linked markers will segregate to Sporulation and Tetrad Analysis. Yeast strains were sporu- sister spore pairs (Fig. 3a). Ifthe YACs segregate incorrectly, lated on plates containing 1% potassium acetate, 0.05% Bacto the different types of aberrant segregation can be determined yeast extract, 0.05% dextrose, and a full complement of by scoring the centromere-linked markers with respect to the nutritional supplements (4). Sporulating cultures were incu- LEU2 sister spore marker (described in Fig.
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