Substitution of the gene for chloroplast RPS16 was assisted by generation of a dual targeting signal

Molecular Biology and Evolution

Volumn 25, Issue 8, 2008, Pages 1566-1575

  Ueda, Minoru ^a,b   Nishikawa, Tomotaro ^a   Fujimoto, Masaru ^b   Takanashi, Hideki ^b   Arimura, Shin Ichi ^b   Tsutsumi, Nobuhiro ^b   Kadowaki, Koh Ichi ^a,c  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c NATIONAL VETERINARY ASSAY LABORATORY   (Japan)

Author keywords

Dual targeting; Gene substitution; Gene transfer; Mitochondria; Plastid; Ribosomal protein

Indexed keywords

PROTEIN S 16; RIBOSOME PROTEIN;

ARABIDOPSIS; ARTICLE; ASPEN; BARREL MEDIC; CELL ORGANELLE; CHLOROPLAST; CONTROLLED STUDY; GENE LOSS; GENE TRANSFER; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; RICE; SIGNAL TRANSDUCTION; TOMATO;

AMINO ACID SEQUENCE; BASE SEQUENCE; CELL NUCLEUS; DNA PRIMERS; DNA, CHLOROPLAST; DNA, MITOCHONDRIAL; GENES, PLANT; MOLECULAR SEQUENCE DATA; PHYLOGENY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBOSOMAL PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

ARABIDOPSIS THALIANA; DICOTYLEDONEAE; EMBRYOPHYTA; EUKARYOTA; LILIOPSIDA; LYCOPERSICON ESCULENTUM; MEDICAGO TRUNCATULA; ORYZA SATIVA; POPULUS ALBA;

EID: 47649118542     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msn102     Document Type: Article

References (50)

1. Adams KL, Daley DO, Qiu YL, Whelan J, Palmer JD. 2000. Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants. Nature. 408:354-357.
2. Adams KL, Daley DO, Whelan J, Palmer JD. 2002. Genes for two mitochondrial ribosomal proteins in flowering plants are derived from their chloroplast or cytosolic counterparts. Plant Cell. 14:931-943.
3. Adams KL, Palmer JD. 2003. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogenet Evol. 29:380-395.
4. Adams KL, Song K, Roessler PG, Nugent JM, Doyle JL, Doyle JJ, Palmer JD. 1999. Intracellular gene transfer in action: dual transcription and multiple silencings of nuclear and mitochondrial cox2 genes in legumes. Proc Natl Acad Sci USA. 96:13863-13868.
5. Arimura S, Takusagawa S, Hatano S, Nakazono M, Hirai A, Tsutsumi N. 1999. A novel plant nuclear gene encoding chloroplast ribosomal protein S9 has a transit peptide related to that of rice chloroplast ribosomal protein L12. FEBS Lett. 450:231-234.
6. Arimura S, Tsutsumi N. 2002. A dynamin-like protein (ADL2b), rather than FtsZ, is involved in Arabidopsis mitochondrial division. Proc Natl Acad Sci USA. 99:5727-5731.
7. Asakura Y, Barkan A. 2006. Arabidopsis orthologs of maize chloroplast splicing factors promote splicing of orthologous and species-specific group II introns. Plant Physiol. 142:1656-1663.
8. Bonen L, Calixte S. 2006. Comparative analysis of bacterial-origin genes for plant mitochondrial ribosomal proteins. Mol Biol Evol. 23:701-712.
9. Bonnefoy E. 1997. The ribosomal S16 protein of Escherichia coli displaying a DNA-nicking activity binds to cruciform DNA. Eur J Biochem. 247:852-859.
10. Bubunenko MG, Schmidt J, Subramanian AR. 1994. Protein substitution in chloroplast ribosome evolution. A eukaryotic cytosolic protein has replaced its organelle homologue (L23) in spinach. J Mol Biol. 240:28-41.
11. Chang IF, Szick-Miranda K, Pan S, Bailey-Serres J. 2005. Proteomic characterization of evolutionarily conserved and variable proteins of Arabidopsis cytosolic ribosomes. Plant Physiol. 137:848-862.
12. Chaw SM, Chang CC, Chen HL, Li WH. 2004. Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol. 58:424-441.
13. Chiu W, Niwa Y, Zeng W, Hirano T, Kobayashi H, Sheen J. 1996. Engineered GFP as a vital reporter in plants. Curr Biol. 6:325-330.
14. Choi C, Liu Z, Adams KL. 2006. Evolutionary transfers of mitochondrial genes to the nucleus in the Populus lineage and coexpression of nuclear and mitochondrial Sdh4 genes. New Phytol. 172:429-439.
15. Christensen AC, Lyznik A, Mohammed S, Elowsky CG, Elo A, Yule R, Mackenzie SA. 2005. Dual-domain, dual-targeting organellar protein presequences in Arabidopsis can use non-AUG start codons. Plant Cell. 17:2805-2816.
16. Emanuelsson O, Nielsen H, Brunak S, von Heijne G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol. 300:1005-1016.
17. Gallois JL, Achard P, Green G, Mache R. 2001. The Arabidopsis chloroplast ribosomal protein L21 is encoded by a nuclear gene of mitochondrial origin. Gene. 274:179-185.
18. Gray MW. 1992. The endosymbiont hypothesis revisited. Int Rev Cytol. 141:233-357.
19. Guo X, Castillo-Ramirez S, Gonzalez V, Bustos P, Fernandez-Vazquez JL, Santamaria RI, Arellano J, Cevallos MA, Davila G. 2007. Rapid evolutionary change of common bean (Phaseolus vulgaris L) plastome, and the genomic diversification of legume chloroplasts. BMC Genomics. 8:228.
20. Held WA, Nomura M. 1975. Escherichia coli 30 S ribosomal proteins uniquely required for assembly. J Biol Chem. 250:3179-3184.
21. Hiratsuka J, Shimada H, Whittier R, et al. (16 co-authors). 1989. The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet. 217:185-194.
22. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP. 2001. Bayesian inference of phylogeny and its impact on evolutionary biology. Science. 294:2310-2314.
23. Jaillon O, Aury JM, Noel B, et al. (56 co-authors). 2007. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 449:463-467.
24. Kahlau S, Aspinall S, Gray JC, Bock R. 2006. Sequence of the tomato chloroplast DNA and evolutionary comparison of solanaceous plastid genomes. J Mol Evol. 63:194-207.
25. Kato T, Kaneko T, Sato S, Nakamura Y, Tabata S. 2000. Complete structure of the chloroplast genome of a legume, Lotus japonicus. DNA Res. 7:323-330.
26. Kubo N, Jordana X, Ozawa K, Zanlungo S, Harada K, Sasaki T, Kadowaki K. 2000. Transfer of the mitochondrial rps10 gene to the nucleus in rice: acquisition of the 5′ untranslated region followed by gene duplication. Mol Gen Genet. 263:733-739.
27. Liu SL, Adams KL. 2008. Molecular adaptation and expression evolution following duplication of genes for organellar ribosomal protein S13 in rosids. BMC Evol Biol. 8:25.
28. Mackenzie SA. 2005. Plant organellar protein targeting: a traffic plan still under construction. Trends Cell Biol. 15:548-554.
29. Martin W, Lagrange T, Li YF, Bisanz-Seyer C, Mache R. 1990. Hypothesis for the evolutionary origin of the chloroplast ribosomal protein L21 of spinach. Curr Genet. 18:553-556.
30. Mathur J, Szabados L, Schaefer S, Grunenberg B, Lossow A, Jonas-Straube E, Schell J, Koncz C, Koncz-Kalman Z. 1998. Gene identification with sequenced T-DNA tags generated by transformation of Arabidopsis cell suspension. Plant J. 13:707-716.
31. Mollier P, Hoffmann B, Debast C, Small I. 2002. The gene encoding Arabidopsis thaliana mitochondrial ribosomal protein S13 is a recent duplication of the gene encoding plastid S13. Curr Genet. 40:405-409.
32. Murcha MW, Rudhe C, Elhafez D, Adams KL, Daley DO, Whelan J. 2005. Adaptations required for mitochondrial import following mitochondrial to nucleus gene transfer of ribosomal protein S10. Plant Physiol. 138:2134-2144.
33. Obara K, Sumi K, Fukuda H. 2002. The use of multiple transcription starts causes the dual targeting of Arabidopsis putative monodehydroascorbate reductase to both mitochondria and chloroplasts. Plant Cell Physiol. 43:697-705.
34. Okumura S, Sawada M, Park YW, Hayashi T, Shimamura M, Takase H, Tomizawa K. 2006. Transformation of poplar (Populus alba) plastids and expression of foreign proteins in tree chloroplasts. Transgenic Res. 15:637-646.
35. Persson BC, Bylund GO, Berg DE, Wikstrom PM. 1995. Functional analysis of the ffh-trmD region of the Escherichia coli chromosome by using reverse genetics. J Bacteriol. 177:5554-5560.
36. Rand DM, Haney RA, Fry AJ. 2004. Cytonuclear coevolution: the genomics of cooperation. Trends Ecol Evol. 19:645-653.
37. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 19:1572-1574.
38. Rudhe C, Clifton R, Whelan J, Glaser E. 2002. N-terminal domain of the dual-targeted pea glutathione reductase signal peptide controls organellar targeting efficiency. J Mol Biol. 324:577-585.
39. Sandoval P, Leon G, Gomez I, Carmona R, Figueroa P, Holuigue L, Araya A, Jordana X. 2004. Transfer of RPS14 and RPL5 from the mitochondrion to the nucleus in grasses. Gene. 324:139-147.
40. Saski C, Lee SB, Daniell H, Wood TC, Tomkins J, Kim HG, Jansen RK. 2005. Complete chloroplast genome sequence of Glycine max and comparative analyses with other legume genomes. Plant Mol Biol. 59:309-322.
41. Sato S, Nakamura Y, Kaneko T, Asamizu E, Tabata S. 1999. Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Res. 6:283-290.
42. Small I, Peeters N, Legeai F, Lurin C. 2004. Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics. 4:1581-1590.
43. Steane DA. 2005. Complete nucleotide sequence of the chloroplast genome from the Tasmanian blue gum, Eucalyptus globulus (Myrtaceae). DNA Res. 12:215-220.
44. Sugiura C, Kobayashi Y, Aoki S, Sugita C, Sugita M. 2003. Complete chloroplast DNA sequence of the moss Physcomitrella patens: evidence for the loss and relocation of rpoA from the chloroplast to the nucleus. Nucleic Acids Res. 31:5324-5331.
45. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
46. Timmis JN, Ayliffe MA, Huang CY, Martin W. 2004. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet. 5:123-135.
47. Ueda M, Arimura S, Yamamoto MP, Takaiwa F, Tsutsumi N, Kadowaki K. 2006. Promoter shuffling at a nuclear gene for mitochondrial RPL27. Involvement of interchromosome and subsequent intrachromosome recombinations. Plant Physiol. 141:702-710.
48. Ueda M, Fujimoto M, Arimura S, Murata J, Tsutsumi N, Kadowaki K. 2007. Loss of the rpl32 gene from the chloroplast genome and subsequent acquisition of a preexisting transit peptide within the nuclear gene in Populus. Gene. 402:51-56.
49. Watanabe N, Che FS, Iwano M, Takayama S, Yoshida S, Isogai A. 2001. Dual targeting of spinach protoporphyrinogen oxidase II to mitochondria and chloroplasts by alternative use of two in-frame initiation codons. J Biol Chem. 276:20474-20481.
50. Whelan S, Goldman N. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol. 18:691-699.