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Discovery of the rpl10 gene in diverse plant mitochondrial genomes and its probable replacement by the nuclear gene for chloroplast RPL10 in two lineages of angiosperms.

Kubo N, Arimura S - DNA Res. (2009)

Bottom Line: In two of them (Brassicaceae and monocots), no nuclear copy of mitochondrial rpl10 is identifiably present, and instead a second copy of nuclear-encoded chloroplast rpl10 is present.Transient assays using green fluorescent protein indicate that this duplicate gene is dual targeted to mitochondria and chloroplasts.We infer that mitochondrial rpl10 has been functionally replaced by duplicated chloroplast counterparts in Brassicaceae and monocots.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Seika, Kyoto, Japan. nk0103@kab.seika.kyoto.jp

ABSTRACT
Mitochondrial genomes of plants are much larger than those of mammals and often contain conserved open reading frames (ORFs) of unknown function. Here, we show that one of these conserved ORFs is actually the gene for ribosomal protein L10 (rpl10) in plant. No rpl10 gene has heretofore been reported in any mitochondrial genome other than the exceptionally gene-rich genome of the protist Reclinomonas americana. Conserved ORFs corresponding to rpl10 are present in a wide diversity of land plant and green algal mitochondrial genomes. The mitochondrial rpl10 genes are transcribed in all nine land plants examined, with five seed plant genes subject to RNA editing. In addition, mitochondrial-rpl10-like cDNAs were identified in EST libraries from numerous land plants. In three lineages of angiosperms, rpl10 is either lost from the mitochondrial genome or a pseudogene. In two of them (Brassicaceae and monocots), no nuclear copy of mitochondrial rpl10 is identifiably present, and instead a second copy of nuclear-encoded chloroplast rpl10 is present. Transient assays using green fluorescent protein indicate that this duplicate gene is dual targeted to mitochondria and chloroplasts. We infer that mitochondrial rpl10 has been functionally replaced by duplicated chloroplast counterparts in Brassicaceae and monocots.

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Alignment of amino acid sequences between previously characterized RPL10 proteins and the ORFs conserved in plant mitochondria. Upper: RPL10 from Reclinomonas mitochondrion and four eubacteria. Lower: proteins predicted from the Marchantia orf168 and its homologues in plant mitochondria. Identical or similar amino acid residues conserved in >50% sequences are highlighted. Amino acids conserved in two or more non-plant species are marked with asterisks. Gaps are indicated by dashes. Amino acid changes caused by RNA editing events, which were detected by RT–PCR analysis (Cycas, Carica, Nicotiana, Solanum, and Vitis) (this study), or computationally predicted (Megaceros) (accession no. EU660574), are denoted with red letters. Especially, amino acid positions in which the homologies were clearly improved by RNA editing are indicated with filled triangles. Positions of frame-shifts in Bambusa and Oryza are shown with slashes. Note that Brassica lacks two-thirds of the C-terminal conserved region, which is replaced by an unrelated 23 amino acid sequence (shown by lower case letters). The length of each ORF is given in parentheses.
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DSP024F2: Alignment of amino acid sequences between previously characterized RPL10 proteins and the ORFs conserved in plant mitochondria. Upper: RPL10 from Reclinomonas mitochondrion and four eubacteria. Lower: proteins predicted from the Marchantia orf168 and its homologues in plant mitochondria. Identical or similar amino acid residues conserved in >50% sequences are highlighted. Amino acids conserved in two or more non-plant species are marked with asterisks. Gaps are indicated by dashes. Amino acid changes caused by RNA editing events, which were detected by RT–PCR analysis (Cycas, Carica, Nicotiana, Solanum, and Vitis) (this study), or computationally predicted (Megaceros) (accession no. EU660574), are denoted with red letters. Especially, amino acid positions in which the homologies were clearly improved by RNA editing are indicated with filled triangles. Positions of frame-shifts in Bambusa and Oryza are shown with slashes. Note that Brassica lacks two-thirds of the C-terminal conserved region, which is replaced by an unrelated 23 amino acid sequence (shown by lower case letters). The length of each ORF is given in parentheses.

Mentions: An alignment of protein sequences predicted from the orf168-homologues is shown in Fig. 2. These sequences are relatively well conserved despite a few insertions/deletions in their central region. The C-terminal region is more divergent with respect to both sequence and length variation. The sequences in Bambusa, Brassica, and Oryza (and possibly Raphanus) are probably pseudogenes, as they have frame-shift mutations or are severely truncated (Fig. 2, slashes and lower case letters, and also see Supplementary Fig. S1 for Raphanus). Chaetosphaeridium and Tripsacum were omitted from the sequence alignment of Fig. 2 and from further analysis because the homologous sequence in Chaetosphaeridium was greatly diverged and because Tripsacum retains only a short stretch of rpl10 (Table 1).


Discovery of the rpl10 gene in diverse plant mitochondrial genomes and its probable replacement by the nuclear gene for chloroplast RPL10 in two lineages of angiosperms.

Kubo N, Arimura S - DNA Res. (2009)

Alignment of amino acid sequences between previously characterized RPL10 proteins and the ORFs conserved in plant mitochondria. Upper: RPL10 from Reclinomonas mitochondrion and four eubacteria. Lower: proteins predicted from the Marchantia orf168 and its homologues in plant mitochondria. Identical or similar amino acid residues conserved in >50% sequences are highlighted. Amino acids conserved in two or more non-plant species are marked with asterisks. Gaps are indicated by dashes. Amino acid changes caused by RNA editing events, which were detected by RT–PCR analysis (Cycas, Carica, Nicotiana, Solanum, and Vitis) (this study), or computationally predicted (Megaceros) (accession no. EU660574), are denoted with red letters. Especially, amino acid positions in which the homologies were clearly improved by RNA editing are indicated with filled triangles. Positions of frame-shifts in Bambusa and Oryza are shown with slashes. Note that Brassica lacks two-thirds of the C-terminal conserved region, which is replaced by an unrelated 23 amino acid sequence (shown by lower case letters). The length of each ORF is given in parentheses.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2818186&req=5

DSP024F2: Alignment of amino acid sequences between previously characterized RPL10 proteins and the ORFs conserved in plant mitochondria. Upper: RPL10 from Reclinomonas mitochondrion and four eubacteria. Lower: proteins predicted from the Marchantia orf168 and its homologues in plant mitochondria. Identical or similar amino acid residues conserved in >50% sequences are highlighted. Amino acids conserved in two or more non-plant species are marked with asterisks. Gaps are indicated by dashes. Amino acid changes caused by RNA editing events, which were detected by RT–PCR analysis (Cycas, Carica, Nicotiana, Solanum, and Vitis) (this study), or computationally predicted (Megaceros) (accession no. EU660574), are denoted with red letters. Especially, amino acid positions in which the homologies were clearly improved by RNA editing are indicated with filled triangles. Positions of frame-shifts in Bambusa and Oryza are shown with slashes. Note that Brassica lacks two-thirds of the C-terminal conserved region, which is replaced by an unrelated 23 amino acid sequence (shown by lower case letters). The length of each ORF is given in parentheses.
Mentions: An alignment of protein sequences predicted from the orf168-homologues is shown in Fig. 2. These sequences are relatively well conserved despite a few insertions/deletions in their central region. The C-terminal region is more divergent with respect to both sequence and length variation. The sequences in Bambusa, Brassica, and Oryza (and possibly Raphanus) are probably pseudogenes, as they have frame-shift mutations or are severely truncated (Fig. 2, slashes and lower case letters, and also see Supplementary Fig. S1 for Raphanus). Chaetosphaeridium and Tripsacum were omitted from the sequence alignment of Fig. 2 and from further analysis because the homologous sequence in Chaetosphaeridium was greatly diverged and because Tripsacum retains only a short stretch of rpl10 (Table 1).

Bottom Line: In two of them (Brassicaceae and monocots), no nuclear copy of mitochondrial rpl10 is identifiably present, and instead a second copy of nuclear-encoded chloroplast rpl10 is present.Transient assays using green fluorescent protein indicate that this duplicate gene is dual targeted to mitochondria and chloroplasts.We infer that mitochondrial rpl10 has been functionally replaced by duplicated chloroplast counterparts in Brassicaceae and monocots.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Seika, Kyoto, Japan. nk0103@kab.seika.kyoto.jp

ABSTRACT
Mitochondrial genomes of plants are much larger than those of mammals and often contain conserved open reading frames (ORFs) of unknown function. Here, we show that one of these conserved ORFs is actually the gene for ribosomal protein L10 (rpl10) in plant. No rpl10 gene has heretofore been reported in any mitochondrial genome other than the exceptionally gene-rich genome of the protist Reclinomonas americana. Conserved ORFs corresponding to rpl10 are present in a wide diversity of land plant and green algal mitochondrial genomes. The mitochondrial rpl10 genes are transcribed in all nine land plants examined, with five seed plant genes subject to RNA editing. In addition, mitochondrial-rpl10-like cDNAs were identified in EST libraries from numerous land plants. In three lineages of angiosperms, rpl10 is either lost from the mitochondrial genome or a pseudogene. In two of them (Brassicaceae and monocots), no nuclear copy of mitochondrial rpl10 is identifiably present, and instead a second copy of nuclear-encoded chloroplast rpl10 is present. Transient assays using green fluorescent protein indicate that this duplicate gene is dual targeted to mitochondria and chloroplasts. We infer that mitochondrial rpl10 has been functionally replaced by duplicated chloroplast counterparts in Brassicaceae and monocots.

Show MeSH
Related in: MedlinePlus