MBE Advance Access published online on May 2, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn102
Research Article |
Substitution of the gene for chloroplast RPS16 was assisted by generation of a dual targeting signal
Institutions at which research was done: National Institute of Agrobiological Sciences; and University of Tokyo
* Genetic Diversity Department, National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8602, Japan
Laboratory of Plant Molecular Genetics, Graduate School of Agricultural and Life Sciences, University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan
Corresponding author: Dr. Koh-ichi Kadowaki, Molecular Biodiversity Lab, Genetic Diversity Department, National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8602, Japan, Tel: +81-29-838-7449, Fax: +81-29-838-7408, Email: kadowaki{at}affrc.go.jp
Received for publication January 6, 2008. Revision received March 13, 2008. Revision received April 24, 2008. Accepted for publication April 25, 2008.
Organelle (mitochondria and chloroplasts in plants) genomes lost a large number of genes after endosymbiosis occurred. Even after this major gene loss, organelle genomes still lose their own genes, even those that are essential, via gene transfer to the nucleus and gene substitution of either different organelle origin or de novo genes. Gene transfer and substitution events are important processes in the evolution of the eukaryotic cell. Gene loss is an ongoing process in the mitochondria and chloroplasts of higher plants. The gene for ribosomal protein S16 (rps16) is encoded in the chloroplast genome of most higher plants, but not in Medicago truncatula and Populus alba. Here, we show that these two species have compensated for loss of the rps16 from the chloroplast genome by having a mitochondrial rps16 that can target the chloroplasts as well as mitochondria. Furthermore, in Arabidopsis thaliana, Lycopersicon esculentum, and Oryza sativa, whose chloroplast genomes encode the rps16, we show that the product of the mitochondrial rps16 has dual targeting ability. These results suggest that the dual targeting of RPS16 to the mitochondria and chloroplasts emerged before the divergence of monocots and dicots (140–150 Myr ago). The gene substitution of the chloroplast rps16 by the nuclear-encoded rps16 in higher plants is the first report about ongoing gene substitution by dual targeting and provides evidence for an intermediate stage in the formation of this heterogeneous organelle.
Key Words: gene substitution • dual targeting • gene transfer • plastid • mitochondria • ribosomal protein
1 Present address: The Ministry of Agriculture, Forestry and Fisheries of Japan, 1-2-1 Kasumigaseki, Chiyoda-ku, Tokyo 100-8950, Japan