Proc. Natl. Acad. Sci. USA Vol. 92, pp. 11331-11338, December 1995 Review Uniparental inheritance of mitochondrial and chloroplast genes: Mechanisms and evolution (organelles/non-Mendelian inheritance/maternal inheritance) C. William Birky, Jr. Department of Molecular Genetics, Ohio State University, 484 West Twelfth Avenue, Columbus, OH 43210 ABSTRACT In nearly all eukaryotes, Left with the example of maize, for which that die before the colony is examined. at least some individuals inherit mito- more progeny have been analyzed (com- This inheritance pattern is similar to that chondrial and chloroplast genes from piled in ref. 4). Crosses of green females by ofPelargonium if one looks at single mark- only one parent. There is no single mech- mutant males (variegated plants with mu- ers in zygote clones, except that the ho- anism of uniparental inheritance: or- tant white germ-line cells supported by moplasmic cells in a clone are individuals ganelle gene inheritance is blocked by a sectors of green tissue) produce only rather than differentiated cells within an variety of mechanisms and at different green progeny; the reciprocal cross pro- individual. stages of reproduction in different spe- duces only mutant embryos. Baur found a Another way of looking at the variation cies. Frequent changes in the pattern of different pattern in the geranium (Pelar- in patterns of uniparental vs. biparental organelle gene inheritance during evolu- gonium zonale; Fig. 1 Center): some off- inheritance is to plot frequency distribu- tion suggest that it is subject to varying spring inherited chloroplast genes from tions of the frequencies of alleles from the selective pressures. Organelle genes often the female parent only; others, from both two parents in the progeny of different fail to recombine even when inherited parents; and still others, from the male zygotes. Many different frequency distri- biparentally; consequently, their inheri- parent only. The reciprocal cross also gives butions have been observed in different tance is asexual. Sexual reproduction is a mixture of the three different kinds of species and often in different crosses of apparently less important for genes in progeny but in different proportions. The the same species (e.g., refs. 5 and 6). The organelles than for nuclear genes, prob- plants that inherit chloroplasts from both different patterns can be classified accord- ably becadse there are fewer of them. As a parents are variegated with green and ing to whether they contain uniparental or result organelle sex can be lost because of white clonal sectors. Although the fertil- biparental zygotes, or both, as in Fig. 2. selection for special reproductive features ized eggs (zygotes) are heteroplasmic, Pattern I (Um) is the same as Fig. 1 Left. such as oogamy or because uniparental containing plastids of both genotypes, Pattern II (UmB) is seen in Oenothera inheritance reduces the spread of cyto- these segregate rapidly during vegetative crosses in which most progeny inherit plasmic parasites and selfish organelle cell divisions. Consequently, the mature chloroplast genes from the female parent DNA. plant consists of clonal sectors of ho- only, while a few inherit them from both moplasmic mutant and wild-type cells. parents. Pattern III (UBU) can be subdi- Genes in chloroplasts were first detected The Mirabilis and Pelargonium inheri- vided according to the relative numbers of by Baur (1) and Correns (2) in 1909 tance patterns are often called maternal genomes contributed by the two parents. because their inheritance departed from and biparental, respectively, but this ter- Different crosses involving chloroplast the Mendelian rules. Much later, mito- minology is not generally applicable. genes in Pelargonium or mitochondrial chondrial genes were identified in the Looking at individual progeny, one sees genes in yeast show patterns Illa-IlIc, same way. The non-Mendelian inheri- that Pelargonium crosses produce a mix- depending on the nuclear and organelle tance of organelle genes became manifest ture of maternal, biparental, and paternal genotypes of the parents. Illd (UU) is in two ways: the rapid segregation of zygotes. Additional terminological prob- seen in the blue mussel (Mytilus edulis), in alleles during vegetative (mitotic) repro- lems appear in microorganisms that do which there are two separate uniparental duction and inheritance from one parent not have differentiated male and female lineages, one transmitted via females and only. Vegetative segregation of chloro- sexes (i.e., are isogamous). Fig. 1 Right the other via males (7, 8). Patterns IV plast genes is a consequence of random- diagrams the inheritance of mitochondrial (BUp) and V (Up) are seen in gymno- ness of replication and partitioning of genes in yeast (3). Haploid cells of mating sperms. organelles and organelle DNA molecules types a and a carry different alleles of a In many cases sample sizes are insuffi- at cell division (3). Uniparental inheri- mitochondrial gene (e.g., conferring resis- cient to distinguish between patterns (e.g., tance proved to be even more complex; tance and sensitivity to an antibiotic). between I and II or III). Moreover, the the variety of molecular and cellular Haploid cells fuse to form zygotes that are stochastic processes that can cause unipa- mechanisms found in different organisms heterozygous a/a and heteroplasmic antrl rental inheritance are probably always op- is matched only by the variety of hypoth- ants. During subsequent mitotic divisions, erating. Consequently, strictly uniparental eses devised to explain the evolution of the the mitochondrial alleles segregate so that inheritance is probably not as common as phenomenon. virtually all daughter cells are homoplas- is generally believed. The inheritance of mic after about 10 cell divisions. In addi- mtDNA in interspecific crosses of mice Genetics tion, some clones produced by individual was believed to be strictly uniparental (9) zygotes contain only antr or only ants cells. until a more sensitive technique (PCR There Are Many Different Patterns of This is also a consequence of relaxed amplification) was used to detect low lev- Uniparental Inheritance. Correns found replication and partitioning of mtDNA: in els of paternal mtDNA (10). These pat- that chloroplasts are inherited only from some zygotes, only mitochondrial ge- the female parent in the four-o'clock nomes from one parent are replicated and Abbreviations: UPI, uniparental inheritance; (Mirabilis jalapa). Strictly maternal inher- partitioned into buds, while those from BPI, biparental inheritance; mtDNA, mito- itance is shown diagrammatically in Fig. 1 the other parent remain in mother cells chondrial DNA. 11331 Downloaded by guest on September 25, 2021 11332 Review: Birky Proc. Natl. Acad. Sci. USA 92 (1995) fixed by stochastic processes in a fraction -4AP~ ~~ p/(m + p) of cells in the progeny, where p and m are the numbers of organelle genomes in the male and female gametes, 0 0 a erys a eryr respectively. The remaining cells will have (iB) no copies of the paternal allele. In the \ls/ mouse, p/m is estimated to be 1-4 x 10-5 (10). In extreme cases, organelles may be ± @ NS completely excluded from the gametes of one sex by unequal cytokinesis (Table 1, mechanism b); an example is the sperm of the crayfish (23). Organelles can be de- stroyed in the gametes (Table 1, mecha- nism c), as they are in the isogametes of FIG. 1. Examples of uniparental inheritance in maize (Left), Pelargonium (Middle), and the filamentous green alga Temnogyra. In Saccharomyces cerevisiae (Right). another green alga, Bryopsis, organelle terns are for single markers; if recombi- each biparental zygote whenever possible DNA disappears during the differentia- nation occurs, some zygotes classified as and publish the observed frequency dis- tion of male gametes (Table 1, mechanism uniparental for an allele from one parent tribution(s). d). may contain alleles of another locus from There Are Many Different Mechanisms Other mechanisms eliminate organelles is fre- during fertilization. In some organisms the other parent. Recombination of Uniparental Inheritance. The underly- (e.g., the tunicate Ascidia), sperm or- quent in the chloroplasts of Chlamydomo- ing mechanisms of uniparental inheri- ganelles fail to enter the egg (Table 1, nas (11) and the mitochondria of the fungi tance are as diverse as the patterns (Table mechanism e). Only nuclei are exchanged Saccharomyces (12, 13), Schizosaccharo- 1). The transmission of organelle genes to during sexual reproduction of other or- myces (14), and Aspergillus (15). Recom- offspring can be blocked at any step in the ganisms (Table 1, mechanism f), as during binant restriction fragment-length poly- reproductive process. conjugation of ciliated protozoa. Mecha- morphism (RFLP) patterns have been Prezygotic mechanisms eliminate or- nisms b-f in Table 1 are called monoga- found in some matings of the slime mold ganelles or organelle genomes during ga- metic transmission (13). Physarum, but it is not clear whether these metogenesis. In some organisms, the mei- Some zygotic mechanisms eliminate or- are due to recombination between the two otic divisions produce gametes that are ganelles from the embryo by unvarying parental mitochondrial genomes, in- morphologically identical (isogamy). In (deterministic) processes. A striking ex- tragenolbic rearrangements, or plasmid others, unequal cell divisions or differen- ample is the degradation of the chloro- integration (16). In contrast,