How did a situation evolve in which an organelle contains genetic information for some of its functions, while others are coded in the nucleus? Figure 3.41 shows the endosymbiosis model for mitochondrial evolution, in which primitive cells captured bacteria that provided the functions that evolved into mitochondria and chloroplasts. At this point, the proto-organelle must have contained all of the genes needed to specify its functions.
Sequence homologies suggest that mitochondria and chloroplasts evolved separately, from lineages that are common with eubacteria, with mitochondria sharing an origin with α-purple bacteria, and chloroplasts sharing an origin with cyanobacteria. The closest known relative of mitochondria among the bacteria is Rickettsia (the causative agent of typhus), which is an obligate intracellular parasite that is probably descended from free-living bacteria. This reinforces the idea that mitochondria originated in an endosymbiotic event involving an ancestor that is also common to Rickettsia (for review see Lang, Gray, and Burger, 1999).
Two changes must have occurred as the bacterium became integrated into the recipient cell and evolved into the mitochondrion (or chloroplast). The organelles have far fewer genes than an independent bacterium, and have lost many of the gene functions that are necessary for independent life (such as metabolic pathways). And since the majority of genes coding for organelle functions are in fact now located in the nucleus, these genes must have been transferred there from the organelle.
Transfer of DNA between organelle and nucleus has occurred over evolutionary time periods, and still continues. The rate of transfer can be measured directly by introducing into an organelle a gene that can function only in the nucleus, for example, because it contains a nuclear intron, or because the protein must function in the cytosol. In terms of providing the material for evolution, the transfer rates from organelle to nucleus are roughly equivalent to the rate of single gene mutation. DNA introduced into mitochondria is transferred to the nucleus at a rate of 2 × 10–5 per generation. Experiments to measure transfer in the reverse direction, from nucleus to mitochondrion, suggest that it is much lower, <10–10 (Thorsness and Fox, 1990). When a nuclear-specific antibiotic resistance gene is introduced into chloroplasts, its transfer to the nucleus and successful expression can be followed by screening seedlings for resistance to the antibiotic. This shows that transfer occurs at a rate of 1 in 16,000 seedlings, or 6 × 10–5 (Huang, Ayliffe, and Timmis, 2003).
Transfer of a gene from an organelle to the nucleus requires physical movement of the DNA, of course, but successful expression also requires changes in the coding sequence. Organelle proteins that are coded by nuclear genes have special sequences that allow them to be imported into the organelle after they have been synthesized in the cytoplasm (see 8.17 Post-translational membrane insertion depends on leader sequences). These sequences are not required by proteins that are synthesized within the organelle. Perhaps the process of effective gene transfer occurred at a period when compartments were less rigidly defined, so that it was easier both for the DNA to be relocated, and for the proteins to be incorporated into the organelle irrespective of the site of synthesis.
Phylogenetic maps show that gene transfers have occurred independently in many different lineages. It appears that transfers of mitochondrial genes to the nucleus occurred only early in animal cell evolution, but it is possible that the process is still continuing in plant cells (Adams et al., 2000). The number of transfers can be large; there are >800 nuclear genes in Arabidopsis whose sequences are related to genes in the chloroplasts of other plants (The Arabidopsis Genome Initiative., 2000). These genes are candidates for evolution from genes that originated in the chloroplast