Frequency distributions for chloroplast genes in Chlamydomonas zygote clones: Evidence for random drift

Mitochondria and chloroplasts of eucaryotic cells contain populations of DNA molecules. In certain cases, e.g., the chloroplasts of Chlamydomonas reinhardtii and the mitochondria of Saccharomyces cerevisiae, organelles contributed by the two parents are known to fuse in the zygote, creating a single population of DNA molecules. In a cross, this population will include molecules of both parental genotypes. There is reason to suspect that organelle DNA molecules in this population are selected randomly for replication and recombination. This would result in random changes in the frequency of a particular allele or genotype within the organelle gene pool of a single zygote and also within its clone of progeny cells. A given gene frequency would increase in some zygote clones and decrease in others, analogous to random drift of gene frequencies in small Mendelian populations. To test this, we have examined the distribution of chloroplast gene frequencies among the zygote clones produced in each of a number of crosses of Chlamydomonas. These distributions are typically U or L shaped as predicted by the random drift hypothesis. They include uniparental zygote clones, in which a chloroplast allele from one parent has been fixed (frequency 100%) and the alternative allele from the other parent has been lost (frequency 0%). Among the remaining (biparental) zygote clones, there is a linear distribution of allele frequencies, showing a great increase in variance over the input frequencies. In these experiments both biparental and uniparental zygotes show a bias favoring chloroplast alleles from the mt⁺ (maternal) parent, and there is no statistically significant mode at the allele frequency of 0.5 corresponding to the equal input of alleles from the maternal and paternal (mt^-) parents. The observed distributions support the hypothesis that both uniparental inheritance and the high variance of allele frequencies among zygote clones are due to random drift of allele frequencies, coupled with a directional force which favors fixation of the maternal allele. In addition, statistical analysis of the data shows a strong but incomplete tendency for linked chloroplast markers to be fixed or lost together in uniparental zygotes. Possible cellular and molecular mechanisms for these observations are discussed.