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Syngamy in the Yeast Saccharomyces Cerevisiae Proc. Natl. Acad. Sci. USA Vol. 93, pp. 908-912, January 1996 Genetics Significant competitive advantage conferred by meiosis and syngamy in the yeast Saccharomyces cerevisiae JOHN BIRDSELL* AND CHRISTOPHER WILLS*t *Department of Biology and tCenter for Molecular Genetics, University of California, San Diego, La Jolla, CA 92093-0116 Communicated by Dan L. Lindsley, Department of Biology, University of California, San Diego, La Jolla, CA, October 2, 1995 ABSTRACT The presumed advantages of genetic recom- Eight of the nine competitions were between MATa/a and bination are difficult to demonstrate directly. To investigate MATa/a strains, and the ninth was between a MATa/a and an the effects of recombination and background heterozygosity isogenic MA Ta/a strain. There were five controls, in which no on competitive ability, we have performed serial-transfer meiotic recombination was permitted, and four treatments, in competition experiments between isogenic sexual and asexual which the sexual strain was allowed to undergo one round of strains of the yeast Saccharomyces cerevisiae. The members of meiosis prior to the beginning of the competition. This was, these diploid pairs of strains differed only in being heterozy- strictly speaking, automixis, since after meiosis diploidy was gous (sexual) or homozygous (asexual) at the mating type or restored by allowing the haploid spores to mate within the MAT locus. Competing pairs had either a completely homozy- ascus. gous or a heterozygous genetic background, the latter being This experimental design eliminates Williams' (4) 2-fold cost heterozygous at many different loci throughout the genome. A of sex, since syngamy occurs within the ascus and involves no round of meiotic recombination (automixis) conferred a large "genome dilution." No males are produced, eliminating May- and statistically significant enhancement of competitive abil- nard Smith's (5) 2-fold cost. The cellular and mechanical costs ity on sexual strains with a heterozygous genetic background. (6, 7) associated with meiosis, syngamy, and karyogamy are By contrast, in homozygous background competitions, meiosis also eliminated by allowing the sexual strains that have un- decreased the sexual strains' initial relative competitive abil- dergone meiosis to enter competition only after the diploid ity. In all cases, however, the sexual strains outcompeted their phase has been reestablished. There are none of the traditional isogenic asexual counterparts, whether meiotic recombination costs of sex [with the possible exception of recombinational had occurred or not. In some genetic backgrounds, this was and segregational costs (6, 8)], allowing a more accurate due in part to an overdominance effect on competitive advan- assessment of the role of recombination in different genetic tage of heterozygosity at the MAT locus. The advantage of the backgrounds. sexual strains also increased significantly during the course of the homozygous background competitions, particularly MATERIALS AND METHODS when meiosis had occurred. This latter effect either did not occur or was very weak in heterozygous background compe- We designate sexual strains as "S" and asexual strains as "A", titions. Overall, sexual strains with heterozygous genetic homozygous background by "HOM" and heterozygous back- backgrounds had a significantly higher initial relative com- ground by "HET." Two different isogenic diploid pairs of petitive ability than those with homozygous backgrounds. The strains, each pair with the same heterozygous background (S advantage of mating type heterozygosity in this organism HET 1 and A HET 1; S HET 2 and A HET 2), were constructed extends far beyond the ability to recombine to search for effects of heterozygosity and for any effects that meiotically. might be confined to a particular strain. These strains were constructed by a series of steps. First, two haploid strains Saccharomyces cerevisiae is an excellent model for examining having substantial genetic differences were mated, yielding an the selective pressures that might have led to the evolution of a/a diploid which was transformed with the nonintegrating sex (1-3). Strains of this yeast with genotype MA Ta/a are pGAL-HO plasmid (9) carrying an inducible HO (or ho- sexual and are capable of undergoing meiosis, while MA Ta/a mothallism) gene for mating type interconversion. Mating type and MAT a/a strains are asexual and are incapable of switching occurs through cassette transposition from one of undergoing meiosis. To avoid confusion between MAT het- two silent loci to the expressed MAT locus (10). After MAT erozygotes and strains with a heterozygous genetic back- switching was induced, halo assay strains (strains supersensi- ground, we will use the terms "sexual" and "asexual" as a tive to the mating pheromone of the opposite mating type) (11, shorthand to denote MAT heterozygotes and MAT homozy- 12) were used to screen for either MATa/a or MA Ta/a gotes respectively, even though under most conditions both colonies. After being cured of the plasmid, the asexual strain sexual and asexual strains reproduce mitotically. MA Ta/a cells of each pair was-with the exception of the MAT locus- can be induced to undergo meiosis (sporulation) by nitrogen heterozygous at the same loci as the sexual strain. starvation, while MATa/a or MA Ta/a cells cannot. To inves- A MA Ta/a strain was also isolated from a MAT-switched S tigate the effects of both meiotic and mitotic recombination on HET 2 and designated A HET 2 (a/a), to test whether competitive ability in Saccharomyces, we employed a 2 x 2 competitive ability was due to heterozygosity at MAT per se or experimental design, with four types of competition (Table 1). was simply due to the presence of an a allele in the hetero- Sexual strains with either a homozygous or a heterozygous zygote. genetic background were competed against asexual strains that Two genetically different, isogenic pairs of homozygous had the identical background and differed only at the MAT background strains were also constructed (S HOM 1 and A (mating type) locus. These are referred to as homozygous or HOM 1; S HOM 2 and A HOM 2). A haploid strain was heterozygous competitions, respectively. transformed with pGAL-HO and MAT switching was induced. The MAT-switched haploid was then mated to the original The publication costs of this article were defrayed in part by page charge (unswitched) haploid. MAT switching was induced again, and payment. This article must therefore be hereby marked "advertisement" in MA Ta/a colonies were isolated as before. Isogenic sexual and accordance with 18 U.S.C. §1734 solely to indicate this fact. asexual strains were allowed to compete in a complete liquid 908 Downloaded by guest on September 30, 2021 Genetics: Birdsell and Wills Proc. Natl. Acad. Sci. USA 93 (1996) 909 Table 1. Design of competition experiments Genetic background No meiotic recombination Meiotic recombination Homozygous 1. Baseline control 2. Measures effect of meiotic recombination on a homozygous genetic background Heterozygous 3. Measures effect of degree 4. Measures effect of meiotic recombination of heterozygosity on preexisting variation medium, through serial transfers of 25 ,tl of the mixed culture each set of replicates, while values in Table 2 were calculated (-5 x 106 cells) to 5 ml of fresh medium after the culture had by fitting the equation separately to the data from each reached the plateau phase. Each transfer represented approx- replicate and then determining average values and statistics on imately 7 or 8 cell generations. In the competitions between S the basis of these individual estimations. To obtain the statis- HOM 1 and A HOM 1 and between S HET 1 and A HET 1, tics, the proportions were transformed to the arcsine of the there were two controls (six replicates each) without meiotic square root, to correct for the fact that the variance of recombination, and two treatments (seven replicates each) in proportions is a function of the mean (13). The interval scale which both the sexual and asexual strains were placed on of the ordinate axis reflects this angular transformation, but all nitrogen-limited medium, inducing meiosis only in the sexual values are displayed as proportions. In the figure, error bars strain. These treatments induced 34% of the S HOM 1 cells represent standard errors of these transformed means, which and 30% of the S HET 1 cells to undergo meiosis. In the in many cases are too small to be visible on the graphs. competitions between S HET 2 and A HET 2 and between S HOM 2 and A HOM 2, both controls and treatments consisted of eight replicates each. Nitrogen limitation induced 38% of RESULTS the S HOM 2 cells and 31% of the S HET 2 cells to undergo In each of the nine competitions, the sexual strain outcom- meiosis. peted its isogenic asexual counterpart (Fig. 1). Four compo- Following meiosis, and prior to the competition, the sexual nents of this competitive advantage could be detected. and asexual strains were grown to plateau on complete me- (i) Meiosis-dependent alterations in advantage. There were dium, permitting the haploid spores produced by the sexual four cases in which a control competition was compared with strain to mate within the same ascus (automixis). All compe- a treatment competition after the sexual strain titions were initiated by mixing equal numbers of sexual and had undergone asexual cells. one round of meiosis. In the two heterozygous-background The proportion of sexual cells was determined by comparisons, meiotic recombination resulted an plating samples from each of the replicated competitions to in immediate, yield -25 colonies per plate. Ten plates from each replicate substantial, and highly significant increase in relative fitness of were incubated for 48 h at 30°C and then sprayed with an the sexual strains. In contrast, in the two homozygous-back- aerosol of an assay strain that is hypersensitive to the phero- ground comparisons, meiosis actually decreased the sexual mone produced by the asexual colonies.
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