Abstract
Previous work suggested that the tufA gene, encoding protein synthesis elongation factor Tu, was transferred from the chloroplast to the nucleus within the green algal lineage giving rise to land plants. In this report we investigate the timing and mode of transfer by examining chloroplast and nuclear DNA from the three major classes of green algae, with emphasis on the class Charophyceae, the proposed sister group to land plants. Filter hybridizations reveal a chloroplast tufA gene in all Ulvophyceae and Chlorophyceae and in some but not all Charophyceae. One charophycean alga, Coleochaete orbicularis, is shown to contain an intact but highly divergent chloroplast tufA gene, whose product is predicted to be non-functional in protein synthesis. We propose that a copy of the tufA gene was functionally transferred from the chloroplast to the nucleus early in the evolution of the Charophyceae, with chloroplast copies of varying function being retained in some but not all of the subsequently diverging lineages. This proposal is supported by the demonstration of multiple tufA-like sequences in Coleochaete nuclear DNA and in nuclear DNA from all other Charophyceae examined.
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- Attardi G., Schatz G. Biogenesis of mitochondria. Annu Rev Cell Biol. 1988;4:289–333. doi: 10.1146/annurev.cb.04.110188.001445. [DOI] [PubMed] [Google Scholar]
- Bachleitner M., Ludwig W., Stetter K. O., Schleifer K. H. Nucleotide sequence of the gene coding for the elongation factor Tu from the extremely thermophilic eubacterium Thermotoga maritima. FEMS Microbiol Lett. 1989 Jan 1;48(1):115–120. doi: 10.1016/0378-1097(89)90157-2. [DOI] [PubMed] [Google Scholar]
- Baldauf S. L., Palmer J. D. Evolutionary transfer of the chloroplast tufA gene to the nucleus. Nature. 1990 Mar 15;344(6263):262–265. doi: 10.1038/344262a0. [DOI] [PubMed] [Google Scholar]
- Brown S., Blumenthal T. Function and structure in ribonucleic acid phage Qbeta ribonucleic acid replicase. Effect of inhibitors of EF-Tu on ribonucleic acid synthesis and renaturation of active enzyme. J Biol Chem. 1976 May 10;251(9):2749–2753. [PubMed] [Google Scholar]
- Buttarelli F. R., Calogero R. A., Tiboni O., Gualerzi C. O., Pon C. L. Characterization of the str operon genes from Spirulina platensis and their evolutionary relationship to those of other prokaryotes. Mol Gen Genet. 1989 May;217(1):97–104. doi: 10.1007/BF00330947. [DOI] [PubMed] [Google Scholar]
- Froman B. E., Tait R. C., Gottlieb L. D. Isolation and characterization of the phosphoglucose isomerase gene from Escherichia coli. Mol Gen Genet. 1989 May;217(1):126–131. doi: 10.1007/BF00330951. [DOI] [PubMed] [Google Scholar]
- Grantham R. Amino acid difference formula to help explain protein evolution. Science. 1974 Sep 6;185(4154):862–864. doi: 10.1126/science.185.4154.862. [DOI] [PubMed] [Google Scholar]
- Hori H., Lim B. L., Osawa S. Evolution of green plants as deduced from 5S rRNA sequences. Proc Natl Acad Sci U S A. 1985 Feb;82(3):820–823. doi: 10.1073/pnas.82.3.820. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jacquet E., Parmeggiani A. Structure-function relationships in the GTP binding domain of EF-Tu: mutation of Val20, the residue homologous to position 12 in p21. EMBO J. 1988 Sep;7(9):2861–2867. doi: 10.1002/j.1460-2075.1988.tb03142.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jurnak F. Structure of the GDP domain of EF-Tu and location of the amino acids homologous to ras oncogene proteins. Science. 1985 Oct 4;230(4721):32–36. doi: 10.1126/science.3898365. [DOI] [PubMed] [Google Scholar]
- Kolodner R., Tewari K. K. Physicochemical characterization of mitochondrial DNA from pea leaves. Proc Natl Acad Sci U S A. 1972 Jul;69(7):1830–1834. doi: 10.1073/pnas.69.7.1830. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lapadat M. A., Spremulli L. L. Effect of guanine nucleotides on the conformation and stability of chloroplast elongation factor Tu. J Biol Chem. 1989 Apr 5;264(10):5510–5514. [PubMed] [Google Scholar]
- Manhart J. R., Palmer J. D. The gain of two chloroplast tRNA introns marks the green algal ancestors of land plants. Nature. 1990 May 17;345(6272):268–270. doi: 10.1038/345268a0. [DOI] [PubMed] [Google Scholar]
- Martin W., Cerff R. Prokaryotic features of a nucleus-encoded enzyme. cDNA sequences for chloroplast and cytosolic glyceraldehyde-3-phosphate dehydrogenases from mustard (Sinapis alba). Eur J Biochem. 1986 Sep 1;159(2):323–331. doi: 10.1111/j.1432-1033.1986.tb09871.x. [DOI] [PubMed] [Google Scholar]
- Meng B. Y., Shinozaki K., Sugiura M. Genes for the ribosomal proteins S12 and S7 and elongation factors EF-G and EF-Tu of the cyanobacterium, Anacystis nidulans: structural homology between 16S rRNA and S7 mRNA. Mol Gen Genet. 1989 Mar;216(1):25–30. doi: 10.1007/BF00332226. [DOI] [PubMed] [Google Scholar]
- Meyerowitz E. M. Arabidopsis thaliana. Annu Rev Genet. 1987;21:93–111. doi: 10.1146/annurev.ge.21.120187.000521. [DOI] [PubMed] [Google Scholar]
- Montandon P. E., Stutz E. Nucleotide sequence of a Euglena gracilis chloroplast genome region coding for the elongation factor Tu; evidence for a spliced mRNA. Nucleic Acids Res. 1983 Sep 10;11(17):5877–5892. doi: 10.1093/nar/11.17.5877. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nagata S., Tsunetsugu-Yokota Y., Naito A., Kaziro Y. Molecular cloning and sequence determination of the nuclear gene coding for mitochondrial elongation factor Tu of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1983 Oct;80(20):6192–6196. doi: 10.1073/pnas.80.20.6192. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ohama T., Yamao F., Muto A., Osawa S. Organization and codon usage of the streptomycin operon in Micrococcus luteus, a bacterium with a high genomic G + C content. J Bacteriol. 1987 Oct;169(10):4770–4777. doi: 10.1128/jb.169.10.4770-4777.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ohyama K., Kohchi T., Sano T., Yamada Y. Newly identified groups of genes in chloroplasts. Trends Biochem Sci. 1988 Jan;13(1):19–22. doi: 10.1016/0968-0004(88)90013-8. [DOI] [PubMed] [Google Scholar]
- Palmer J. D. Comparative organization of chloroplast genomes. Annu Rev Genet. 1985;19:325–354. doi: 10.1146/annurev.ge.19.120185.001545. [DOI] [PubMed] [Google Scholar]
- Prager E. M., Wilson A. C. Ancient origin of lactalbumin from lysozyme: analysis of DNA and amino acid sequences. J Mol Evol. 1988;27(4):326–335. doi: 10.1007/BF02101195. [DOI] [PubMed] [Google Scholar]
- Reddy P., Miller D., Peterkofsky A. Stimulation of Escherichia coli adenylate cyclase activity by elongation factor Tu, a GTP-binding protein essential for protein synthesis. J Biol Chem. 1986 Sep 5;261(25):11448–11451. [PubMed] [Google Scholar]
- Seidler L., Peter M., Meissner F., Sprinzl M. Sequence and identification of the nucleotide binding site for the elongation factor Tu from Thermus thermophilus HB8. Nucleic Acids Res. 1987 Nov 25;15(22):9263–9277. doi: 10.1093/nar/15.22.9263. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siemeister G., Buchholz C., Hachtel W. Genes for the plastid elongation factor Tu and ribosomal protein S7 and six tRNA genes on the 73 kb DNA from Astasia longa that resembles the chloroplast DNA of Euglena. Mol Gen Genet. 1990 Feb;220(3):425–432. doi: 10.1007/BF00391749. [DOI] [PubMed] [Google Scholar]
- Sugiura M. The chloroplast chromosomes in land plants. Annu Rev Cell Biol. 1989;5:51–70. doi: 10.1146/annurev.cb.05.110189.000411. [DOI] [PubMed] [Google Scholar]
- Thompson R. C. EFTu provides an internal kinetic standard for translational accuracy. Trends Biochem Sci. 1988 Mar;13(3):91–93. doi: 10.1016/0968-0004(88)90047-3. [DOI] [PubMed] [Google Scholar]
- Travers A. Control of ribosomal RNA synthesis in vitro. Nature. 1973 Jul 6;244(5410):15–18. doi: 10.1038/244015a0. [DOI] [PubMed] [Google Scholar]
- Vijgenboom E., Bosch L. Translational frameshifts induced by mutant species of the polypeptide chain elongation factor Tu of Escherichia coli. J Biol Chem. 1989 Aug 5;264(22):13012–13017. [PubMed] [Google Scholar]
- Vijgenboom E., Nilsson L., Bosch L. The elongation factor EF-Tu from E. coli binds to the upstream activator region of the tRNA-tufB operon. Nucleic Acids Res. 1988 Nov 11;16(21):10183–10197. doi: 10.1093/nar/16.21.10183. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yokota T., Sugisaki H., Takanami M., Kaziro Y. The nucleotide sequence of the cloned tufA gene of Escherichia coli. Gene. 1980 Dec;12(1-2):25–31. doi: 10.1016/0378-1119(80)90012-8. [DOI] [PubMed] [Google Scholar]
- van den Boogaart P., Samallo J., Agsteribbe E. Similar genes for a mitochondrial ATPase subunit in the nuclear and mitochondrial genomes of Neurospora crassa. Nature. 1982 Jul 8;298(5870):187–189. doi: 10.1038/298187a0. [DOI] [PubMed] [Google Scholar]