Gene transfer from organelles to the nucleus: Frequent and in big chunks

Abstract

Chloroplasts arose >1.2 billion years ago (1) when a free-living cyanobacterium became an endosymbiont in a eukaryotic host. Since that time, chloroplast genomes have undergone severe reduction, because chloroplast genomes encode between 50 and 200 proteins, whereas cyanobacterial genomes encode several thousand. Accordingly, endosymbiotic theories have always assumed that the cyanobacterial ancestor of plastids relinquished much of its genetic autonomy: “it is not surprising that chloroplasts lost their ability to live independently long ago,” as Mereschkowsky put it in 1905 (2). In today's terms, that means that during the course of evolution, genes must have been transferred from the ancestral chloroplast to the nucleus, where they acquired the proper expression and targeting signals to allow the encoded proteins to be synthesized on cytosolic ribosomes and reimported into the organelle with the help of a transit peptide. This process, a special kind of lateral gene transfer called endosymbiotic gene transfer (3), appears to be very widespread in nature: ≈18% of the nuclear genes in Arabidopsis seem to come from cyanobacteria (4), and obvious remnants of the chloroplast DNA have been found in higher plant nuclear chromosomes (5). Evolutionary biologists have long been able to infer endosymbiotic gene transfer from evolutionary sequence comparisons but have not been able to watch it happen in the lab until now. In this issue of PNAS, Stegemann et al. (6) report gene transfer from the tobacco chloroplast genome to nuclear chromosomes under laboratory conditions. Their findings, together with other recent developments, open up new chapters in our understanding of organelle–nuclear DNA dynamics and have far-reaching evolutionary implications. The experimental design used by Stegemann et al. (6) was simple and effective. Using a technology called chloroplast transformation (7), they introduced a cassette containing two foreign genes into tobacco chloroplast DNA. The first one encoded spectinomycin resistance ( aad …