Organelles have DNA

KEY TERMS:

• Maternal inheritance describes the preferential survival in the progeny of genetic markers provided by one parent.
• Extranuclear genes reside outside the nucleus in organelles such as mitochondria and chloroplasts.
• Cytoplasmic inheritance is a property of genes located in mitochondria or chloroplasts.

KEY CONCEPTS:

• Mitochondria and chloroplasts have genomes that show nonMendelian inheritance. Typically they are maternally inherited.
• Organelle genomes may undergo somatic segregation in plants.
• Comparisons of mitochondrial DNA suggest that humans are descended from a single female who lived 200,000 years ago in Africa. 

The first evidence for the presence of genes outside the nucleus was provided by nonMendelian inheritance in plants (observed in the early years of this century, just after the rediscovery of Mendelian inheritance). NonMendelian inheritance is sometimes associated with the phenomenon of somatic segregation. They have a similar cause:

• NonMendelian inheritance is defined by the failure of the progeny of a mating to display Mendelian segregation for parental characters. It reflects lack of association between the segregating character and the meiotic spindle.
• Somatic segregation describes a phenomenon in which parental characters segregate in somatic cells, and therefore display heterogeneity in the organism. This is a notable feature of plant development. It reflects lack of association between the segregating character and the mitotic spindle.

NonMendelian inheritance and somatic segregation are therefore taken to indicate the presence of genes that reside outside the nucleus and do not utilize segregation on the meiotic and mitotic spindles to distribute replicas to gametes or to daughter cells, respectively.Figure 3.36 shows that this happens when the mitochondria inherited from the male and female parents have different alleles, and by chance a daughter cell receives an unbalanced distribution of mitochondria that represents only one parent (see 13.24 How do mitochondria replicate and segregate?).

The extreme form of nonMendelian inheritance is uniparental inheritance, when the genotype of only one parent is inherited and that of the other parent is permanently lost. In less extreme examples, the progeny of one parental genotype exceed those of the other genotype. Usually it is the mother whose genotype is preferentially (or solely) inherited. This effect is sometimes described as maternal inheritance. The important point is that the genotype contributed by the parent of one particular sex predominates, as seen in abnormal segregation ratios when a cross is made between mutant and wild type. This contrasts with the behavior of Mendelian genetics when reciprocal crosses show the contributions of both parents to be equally inherited.

The bias in parental genotypes is established at or soon after the formation of a zygote. There are various possible causes. The contribution of maternal or paternal information to the organelles of the zygote may be unequal; in the most extreme case, only one parent contributes. In other cases, the contributions are equal, but the information provided by one parent does not survive. Combinations of both effects are possible. Whatever the cause, the unequal representation of the information from the two parents contrasts with nuclear genetic information, which derives equally from each parent.

NonMendelian inheritance results from the presence in mitochondria and chloroplasts of DNA genomes that are inherited independently of nuclear genes. In effect, the organelle genome comprises a length of DNA that has been physically sequestered in a defined part of the cell, and is subject to its own form of expression and regulation. An organelle genome can code for some or all of the RNAs, but codes for only some of the proteins needed to perpetuate the organelle. The other proteins are coded in the nucleus, expressed via the cytoplasmic protein synthetic apparatus, and imported into the organelle.

Genes not residing within the nucleus are generally described as extranuclear genes; they are transcribed and translated in the same organelle compartment (mitochondrion or chloroplast) in which they reside. By contrast, nuclear genes are expressed by means of cytoplasmic protein synthesis. (The term cytoplasmic inheritance is sometimes used to describe the behavior of genes in organelles. However, we shall not use this description, since it is important to be able to distinguish between events in the general cytosol and those in specific organelles.)

Higher animals show maternal inheritance, which can be explained if the mitochondria are contributed entirely by the ovum and not at all by the sperm. Figure 3.37 shows that the sperm contributes only a copy of the nuclear DNA. So the mitochondrial genes are derived exclusively from the mother; and in males they are discarded each generation.

Conditions in the organelle are different from those in the nucleus, and organelle DNA therefore evolves at its own distinct rate. If inheritance is uniparental, there can be no recombination between parental genomes; and usually recombination does not occur in those cases where organelle genomes are inherited from both parents. Since organelle DNA has a different replication system from that of the nucleus, the error rate during replication may be different. Mitochondrial DNA accumulates mutations more rapidly than nuclear DNA in mammals, but in plants the accumulation in the mitochondrion is slower than in the nucleus (the chloroplast is intermediate).

One consequence of maternal inheritance is that the sequence of mitochondrial DNA is more sensitive than nuclear DNA to reductions in the size of the breeding population. Comparisons of mitochondrial DNA sequences in a range of human populations allow an evolutionary tree to be constructed. The divergence among human mitochondrial DNAs spans 0.57%. A tree can be constructed in which the mitochondrial variants diverged from a common (African) ancestor. The rate at which mammalian mitochondrial DNA accumulates mutations is 2-4% per million years, >10× faster than the rate for globin. Such a rate would generate the observed divergence over an evolutionary period of 140,000-280,000 years. This implies that the human race is descended from a single female, who lived in Africa ~200,000 years ago (Cann, Stoneking, and Wilson, 1987).