Transfer of the mitochondrial rps10 gene to the nucleus in rice: acquisition of the 5′ untranslated region followed by gene duplication

Abstract

Mitochondrial ribosomal protein S10 (rps10) is encoded by the mitochondrial genome in potato and pea. Here we show that the rps10 gene is absent from the mitochondrial genome of rice and has been transferred to the nucleus. Cloning and transcriptional analysis show that there are two rps10 genes in the rice nuclear genome and that their transcripts differ in abundance. Western analysis detected the RPS10 protein in the soluble fraction of rice mitochondria, although neither RPS10 has any obvious N-terminal presequence for targeting to mitochondria. This result suggests that targeting information is present in the internal region of rice RPS10. Genomic sequence analysis indicated that each rps10 gene has an intron in the 5' untranslated region (5' UTR) and that these intron sequences are homologous to each other. This result strongly suggests that a duplication event occurred after transfer of the rps10 gene to the nucleus. The duplicated rps10 genes have since been translocated to different chromosomes, because the two rps10 genes were mapped on chromosomes 6 and 12 by RFLP analysis. Interestingly, the 5' UTR and the intron of the rice rps10 genes are homologous to sequences found in several rice genes with various functions, such as osk4, EF-1beta2 and RAG1, suggesting a common origin and a functional role for the 5' UTR. Acquisition of the 5' flanking region might have accelerated the activation of the mitochondrial rps10 gene which was transferred to the nuclear genome.

Evolutionary transfers of mitochondrial genes to the nucleus in the Populus lineage and coexpression of nuclear and mitochondrial Sdh4 genes

“…None of targetp , mitoprot or predotar predicted that the N‐terminal extension of the open reading frame is a mitochondrial targeting presequence. Thus the mitochondrial targeting information may be located within the Rps10 mature coding region, as in some other species (Adams et al ., 2000; Kubo et al ., 2000). Considering the evidence for several separate transfers of Rps10 to the nucleus in other angiosperms (Adams et al ., 2000), the Rps10 gene in Populus also probably represents a separate and evolutionarily recent transfer.…”

Gene transfer from mitochondrion to nucleus: novel mechanisms for gene activation from Cox2

“…Some other cases of mitochondrial gene transfer have involved the gain of introns in the nucleus that may have played a role in functional activation. An intron located between the mitochondrial targeting sequence and the mature coding region is found in Arabidopsis Rps10 and Marchantia nad7 (Kobayashi et al ., 1997; Wischmann and Schuster, 1995); an intron is present in the 5′‐UTR of Rps10 and Sdh3 in some grass species (Adams et al ., 2000; Adams et al ., 2001; Kubo et al ., 2000); and an intron is located in the 3′‐UTR of Arabidopsis rps14 (Figueroa et al ., 1999b).…”

“…Gene transfer and functional activation appear to have ceased in animals, as evidenced by their nearly constant mitochondrial gene content (Boore, 1999). However, a number of evolutionarily recent gene transfer events from the mitochondrion to the nucleus have been identified in plants, indicating that gene transfer is still taking place (Adams et al ., 2000; Adams et al ., 2001; Covello and Gray, 1992; Figueroa et al ., 1999a; Figueroa et al ., 1999b; Grohmann et al ., 1992; Kadowaki et al ., 1996; Kobayashi et al ., 1997; Kubo et al ., 1999; Kubo et al ., 2000; Nugent and Palmer, 1991; Sanchez et al ., 1996; Wischmann and Schuster, 1995). These gene‐transfer events provide a unique window of opportunity to study gene transfer, a process of fundamental importance to the establishment and evolution of organelles in eukaryotic cells.…”

Acquisition of hydrogenosomal presequences: examples from Trichomonas vaginalis

“…Exogenous acquisition refers to presequences that originate from irrelevant genomic regions, such as fragments from other genes or noncoding regions. Events such as recombination, exon shuffling and alternative splicing are all able to mediate exogenous acquisition, and these events may occur independently or co‐operatively during acquisition of mitochondrial presequences (Kadowaki et al ., ; Long et al ., ; Kubo et al ., , , ).…”