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Uniparental Inheritance of Mitochondrial Genes in Yeast: Dependence on Input Bias of Mitochondrial Dna and Preliminary Investigations of the Mechanism

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Uniparental Inheritance of Mitochondrial Genes in Yeast: Dependence on Input Bias of Mitochondrial Dna and Preliminary Investigations of the Mechanism UNIPARENTAL INHERITANCE OF MITOCHONDRIAL GENES IN YEAST: DEPENDENCE ON INPUT BIAS OF MITOCHONDRIAL DNA AND PRELIMINARY INVESTIGATIONS OF THE MECHANISM C. WILLIAM BIRICY, JR.*t, CATHERINE A. DEMKO*, PHILIP S. PERLMAN*t, AND ROBERT STRAUSBERwt The Ohio Stale University, Columbus, Ohio 43210 Manuscript received September 26, 1977 Revised copy received March 17, 1978 ABSTRACT In Saccharomyces cerevisiae, previous studies on the inheritance of mito- chondrial genes controlling antibiotic resistance have shown that some crosses produce a substantial number of uniparental zygotes, which transmit to their diploid progeny mitochondrial alleles from only one parent. In this paper, we show that uniparental zygotes are formed especially when one parent (major- ity parent) contributes substantially more mitochondrial DNA molecules to the zygote than does the other (minority) parent. Cellular contents of mito- chondrial DNA (mtDNA) are increased in these experiments by treatment with cycloheximide, alpha-factor, or the uvsp5 nuclear mutation. In such a biased cross, some zygotes are uniparental for mitochondrial alleles from the majority parent, and the frequency of such zygotes increases with increasing bias. In two- and three-factor crosses, the cupl, ery1, and oli1 loci behave coordinately, rather than independently; minority markers tend to be trans- mitted or lost as a unit, suggesting that the uniparental mechanism acts on entire mtDNA molecules rather than on individual loci. This rules out the possibility that uniparental inheritance can be explained by the conversion of minority markers to the majority alleles during recombination. Exceptions to the coordinate behavior of different loci can be explained by marker rescue via recombination. Uniparental inheritance is largely independent of the posi- tion of buds on the zygote. We conclude that it is due to the failure of minority markers to replicate in some zygotes, possibly involving the rapid enzymatic destruction of such markers. We have considered two general classes of mech- anisms: (1) random selection of molecules for replication, as for example by competition for replicating sites on a membrane; and (2) differential marking of mtDNA molecules in the two parents, possibly by modification enzymes, followed by a mechanism that “counts” molecules and replicates only the majority type. These classes of models are distinguished genetically by the fact that the first predicts that the output frequency of a given allele among the progeny of a large number of zygotes will approximately equal the aver- age input frequency of that allele, while the second class predicts that any * Department of Genetics. t Developmental Biology Program. $ Present address: Department of Biochemistry, University of Texas, Health Sciences Center at Dallas, Dallas, Texas 75235. Genetics 89: 015-651 August, 1078 616 c. WILLIAM BIRKY, JR. et al. input bias will be aniplified in the output. The data suggest that bias amplifi- cation does occur. We hypothesize that maternal inheritance of mitochondrial or chloroplast genes in many organisms may depend upon a biased input of organelle DNA molecules, which usually favors the maternal parent, followed by failure of the minority (paternal) molecules to replicate in many or all zygotes. ITOCHONDRIAL and chloroplast genes are transmitted to progeny pre- Mdominantly or entirely by only one parent in a number of different organ- isms. This uniparental inheritance is generally through the maternal parent in organisms with oogamy, and in such cases may be attributable to the male gamete containing many fewer organelles than the egg, or to failure of the organelles from the male gamete to enter the egg (see BIRKY1976 for references). But in the geranium (Pelargonium), many crosses involving chloroplast mutants produce three classes of zygotes: those transmitting only maternal markers, those transmitting only paternal markers, and those transmitting both to vary- ing extents (TILNEY-BASSETT1975). In the algae Chlamydomonas reinhardtii (SAGER1975; GILLHAM1974) and C. eugametos (MCBRIDEand McBRIDE 1975), chloroplast markers are transmitted principally from one parent, but in both of these isogamous species the zygote receives the entire chloroplast of both parent gamctes. In these cases, it is clear that the failure of uniparental zygotes to transmit organelle markers from one parent must be due to the failure of those markers to replicate in the zygote and to their loss by dilution or enzymatic degradation, or to the conversion of the markers to the corresponding alleles from the other parent. At first sight, it may appear that mitochondrial genes in baker’s yeast (Sac- charomyces cereuisiae) are always inherited biparentally, since an examination of the mixed progeny of a large number of zygotes (random diploid analysis) always shows that mitochondrial genes from both parents can be recovered among the progeny (LINNANEet al. 1968; THOMASand WILKIE1968; COEN et al. 1970). When the progeny of individual zygotes were analyzed separately (zygote clone analysis), some zygotes were found that transmitted to their progeny mitochondrial genes from only one parent (COENet al. 1970; RANK and BECH-HANSEN1972; WILKIE1972; WILKIEarid THOMAS1973; WAXMAN, EATONand WILKIE1973; CALLEN1974; LINNANE,HOWELL and LUKINS1974). The number of such zygotes, however, was usually small, and they might have resulted from matings between spontaneous petite mutant cells that had lost the mitochondrial genes in question and a wild-type cell that retained them. BIRKY (1974, 1975a,b,c) first called attention to these zygotes and argued that they indicated uniparental inheritance analogous to that seen in other organisms, after finding that some yeast matings produced uniparental zygotes in substantial proportions: too many to be accounted for by petites, by sampling or scoring errors, or by zygotes that produce a single bud pure for one genotype and then die. Neither is it possible to explain uniparental zygotes by the transmission of only a very small number of identical genomes from the zygote to its buds; INHERITANCE OF YEAST MITOCHONDRIAL GENES 61 7 genetic and physical evidence argue against this (CALLEN1974; BIRKY1975c; DUJONand SLONIMSKI1976; BIRKYet al. 1977; SENA,WELCH and FOGEL1976). We now report further studies investigating the circumstances in which uni- parental inheritance occurs and examining possible mechanisms. These studies show, for several different crosses, that uniparental zygotes are consistently pro- duced when the two parents contribute different numbers of mtDNA molecules to the zygote (biased input) ; most uniparental zygotes transmit only mitochon- drial alleles from the majority parent. Increasing input bias in a cross results in increasing frequencies of uniparental zygotes, whether the input bias is induced by treatment with cycloheximide or the mating hormone alpha-factor or by a nuclear gene. In a two-factor or three-factor cross, a given zygote may show uniparental inheritance of mitochondrial genes at only one locus, or at two or three loci. The most common class of uniparental zygotes are those uniparental at all loci studied. A possible explanation for uniparental zygotes is random loss and fixa- tion of alleles due to multiple rounds of random mating and gene conversion. We have ruled this out as a sufficient explanation by showing that the capl, eryl, and olil loci tend to become uniparental as a unit, although they are probably rarely or never included in the same gene conversion event, and that uniparental inheritance is not found in higher frequency among zygotes having a greater opportunity for recombination. Mitochondrial DNA (mtDNA) molecules are singled out for transmission or loss soon after the formation of the zygote; never- theless, markers may apparently be rescued by recombination from genomes destined to be lost. The effect of input bias may be explained by two different types of models: those invoking random selection of a small sample of mtDNA molecules for replication, and those in which the zygote differentially marks and “counts” mtDNA molecules from the two parents and replicates the majority type. Preliminary data relating input and output ratios of mitochondrial alleles favor the latter kind of model. Some of our data and conclusions were summarized earlier by PERLMANet al. (1976). MATERIALS AND METHODS Stocks The stocks, their sources, and their genotypes are listed in Table I.For the sake of brevity we have used the symbols CR and Cs, ER and ES, OR and Os, PR and PS as abbreviations for the mitochondrial allele pairs caplr and capla, erylr and eryls, 0127 and OMs, par17 and par18 All crosses were homopolar (U+ x U+ or U- x U-), so that the phenomenon of polarity (DUJON, SLONIMSKIand WEILL1974) is not involved in any of our experiments or interpretations. Media YEPD, YEPG, and YEPGal contained 1% Difco yeast extract plus 2% Difco proteose pep- tone, and 2% dextrose (glucose), 4% glycerol, or 2% galactose, respectively. (All concentrations are w/v.) Comparable results were obtained with the semisynthetic media RD and RG, which contain 0.5% yeast extract, 0.1% (NH,)$O,, 0.1% KH,PO,, 0.05% MgSO,, and 0.05% NaCl at pH 6.5, plus carbon sources as above. These media were sometimes supplemented with amino TABLE 1 Strains used Genotype Strain Nuclear w C EO P Abbreviation Source ~___~ NI23 a his ss NIB E. MOUSTACCHI NI23 UVSrho5 a his UVSp5 - ss P5 E. MOUSTACCHI D6 a arg met + ss D6 D. Y. THOMAS 2-3b a irp-I + RS 2-36 R. KLEESE 4810 a lys-I + ss 4810 R. KLEESE 48 10 diploid a/a lys-l/lys-I + ss 4810 diploid Diploidization of 4810 induced by cycloheximide n IL458-1A a: his + R32 1 R221 S S IL458 P. P. SLONIMSKI DPI-1 B/517 a his trp + R517 ss S DPI P. P. SLONIMSKI IL126-1 B a his R32l R221 S S IL126 P. P. SLONIMSKI 41-1 a: ade R321 R514 R4 R 41-1 C. A. DEMKO(spore from 4810 x ID4/1) ID4/1 a a& trp R32l R514 R4 S ID4/1 R. YOUNG(spore from (32)l-2/3 x DPl-lB/514) D243-4A-OR a ade lys + S S R4 S D243 R.
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