Substitution of the Gene for Chloroplast RPS16 Was Assisted by Generation of a Dual Targeting Signal

Abstract

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 2 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 MYA). 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.

Different status of the gene for ribosomal protein S16 in the chloroplast genome during evolution of the genus Arabidopsis and closely related species

“…The occurrence of gene substitution implies the emergence of a nuclear-encoded counterpart of the organellar protein. The onset of cp rps16 gene substitution is minimally estimated at 140-150 mya (Ueda et al, 2008). Considering the time of divergence of Arabidopsis thaliana and O. pumila, the nuclear genome gained an rps16 copy ~140 mya, and the chloroplast and nuclear copies have coexisted (perhaps redundantly) since then.…”

“…RPS16 is essential for cell viability (Persson et al, 1995) and plays an important role in the assembly of the 30S subunit (Held and Nomura, 1975) in Escherichia coli. It was demonstrated that chloroplast-encoded (cp) rps16 has been replaced with the nuclear-encoded rps16 which had originated from the mitochondria in M. truncatula and Populus alba, and that the present status of the rps16 gene substitution in the chloroplast genome corresponds to the intermediate stage in most angiosperms (Ueda et al, 2008). This is interesting evidence of the process of gene substitution in eukaryotes.…”

“…It is also possible that genes that have been transferred or substituted recently in evolution remain in the chloroplast genome as remnants when gene transfer or substitution has occurred. These residual genes should provide insight into the mechanistic process by which they were transferred or substituted (for example, infA (Millen et al, 2001), rpl32 (Cusack and Wolfe, 2007;Ueda et al, 2007), and rps16 (Ueda et al, 2008)). RPS16 is essential for cell viability (Persson et al, 1995) and plays an important role in the assembly of the 30S subunit (Held and Nomura, 1975) in Escherichia coli.…”

The Functional Transfer of Genes From the Mitochondria to the Nucleus: The Effects of Selection, Mutation, Population Size and Rate of Self-Fertilization

“…The complex evolution of rps16 is an illuminating case of both functional gene transfer and substitution. In some lineages, the mitochondrial rps16 is functionally expressed in the nucleus but absent from the mitochondria (functional transfer) while in a subset of taxa, the chloroplast copy is also absent and the nuclear gene is also targeted to the chloroplast [substitution (Ueda et al 2008b)].…”

Caracterização do papel da glutamil-tRNA sintetase na localização subcelular de proteínas

“…Alguns estudos especulam que as proteínas de DD evoluíram a partir de proteínas direcionadas para um único destino (UEDA et al, 2008). Neste contexto, o ganho do DD seria um mecanismo restritivo comparado ao direcionamento a uma única organela para evitar a perda do direcionamento para uma das organelas (CHEW; WHELAN, 2003;MICHALECKA et al, 2003).…”