Summary
The vestigial plastid genome of Epifagus virginiana (beechdrops), a nonphotosynthetic parasitic flowering plant, is functional but lacks six ribosomal protein and 13 tRNA genes found in the chloroplast DNAs of photosynthetic flowering plants. Import of nuclear gene products is hypothesized to compensate for many of these losses. Codon usage and amino acid usage patterns in Epifagus plastic genes have not been affected by the tRNA gene losses, though a small shift in the base composition of the whole genome (toward A + T -richness) is apparent. The ribosomal protein and tRNA genes that remain have had a high rate of molecular evolution, perhaps due to relaxation of constraints on the translational apparatus. Despite the compactness and extensive gene loss, one translational gene (infA, encoding initiation factor 1) that is a pseudogene in tobacco has been maintained intact in Epifagus.
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Andachi Y, Yamao F, Muto A, Osawa S (1989) Codon recognition patterns as deduced from sequences of the complete set of transfer RNA species in Mycoplasma capricolum. Resemblance to mitochondria. J Mol Biol 209:37–54
Baldauf SL, Palmer JD (1990) Evolutionary transfer of the chloroplast tufA gene to the nucleus. Nature 344:262–265
Borst P, Grivell LA (1981) Small is beautiful—portrait of a mitochondrial genome. Nature 290: 443–444
Brown WM (1983) Evolution of animal mitochondrial DNA. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Sinauer, Sunderland, MA, pp 62–88
Butler JS, Springer M, Grunberg-Manago M (1987) AUU-toAUG mutation in the initiator codon of the translation initiation factor IF3 abolishes translational autocontrol of its own gene (infC) in vivo. Proc Natl Acad Sci USA 84:4022–4025
Cann RL, Brown WM, Wilson AC (1984) Polymorphic sites and the mechanism of evolution in human mitochondrial DNA. Genetics 106:479–499
dePamphilis CW, Palmer JD (1990) Loss of photosynthetic and chlororespiratory genes from the plastid genome of a parasitic flowering plant. Nature 348:337–339
Downie SR, Palmer JD (1992) Use of chloroplast DNA rearrangements in reconstructing plant phylogeny. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants. Chapman and Hall, New York, pp 14–35
Gantt JS, Baldauf SL, Calie PJ, Weeden NF, Palmer JD (1991) Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron. EMBO J 10:3073–3078
Gray MW, Boer PH (1988) Organization and expression of algal (Chlamydomonas reinhardtii) mitochondrial DNA. Phil Trans Roy Soc Lond Ser B 319:135–147
Hancock K, Hajduk SL (1990) The mitochondrial tRNAs of Trypanosoma brucei are nuclear encoded. J Biol Chem 265: 19208–19215
Harris EH, Gillham NW, Boynton JE (1993) Chloroplast ribosomes: genetics, biogenesis and evolutionary relationships. Microbiol Rev, submitted
Hill WE, Dahlberg A, Garrett RA, Moore PB, Schlessinger D, Warner JR (eds) (1990) The ribosome. Am Soc Microbiol, Washington, DC, pp 1–678
Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun C-R, Meng B-Y, Li Y-Q, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete nucleotide 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
Hoch B, Maier RM, Appel K, Igloi GL, Koessel H (1991) Editing of a chloroplast mRNA by creation of an initiation codon. Nature 353:178–180
Isono K, Isono S (1976) Lack of ribosomal protein S1 in Bacillus stearothermophilus. Proc Nall Acad Sci USA 73:767–770
Joyce PBM, Gray MW (1989) Chloroplast-like transfer RNA genes expressed in wheat mitochondria. Nucleic Acids Res 17:5461–5476
Kudla J, Igloi GL, Metzlaff M, Hagemann R, Koessel H (1992) RNA editing in tobacco chloroplasts leads to the formation of a translatable psbL mRNA by a C to U substitution within the initiation codon. EMBO J 11:1099–1103
Li W-H, Wu C-I, Luo C-C (1985) A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 2:150–174
Marechal-Drouard L, Weil J-H, Guillemaut P (1988) Import of several tRNAs from the cytoplasm into the mitochondria in bean Phaseolus vulgaris. Nucleic Acids Res 16:4777–4788
Martin RP, Schneller J-M, Stahl AJC, Dirheimer G (1979) Import of nuclear deoxyribonucleic acid coded lysin-accepting transfer ribonucleic acid (anticodon C-U-U) into yeast mitochondria. Biochemistry 18:4600–4605
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
Michel F, Umesono K, Ozeki H (1989) Comparative and functional anatomy of group II catalytic introns—a review. Gene 82:5–30
Morden CW, Wolfe KH, dePamphilis CW, Palmer JD (1991) Plastid translation and transcription genes in a non-photosynthetic plant: intact, missing and pseudo genes. EMBO J 10:3281–3288
Nagano Y, Ishikawa H, Matsuno R, Sasaki Y (1991) Nucleotide sequence and expression of the ribosomal protein L2 gene in pea chloroplasts. Plant Mol Biol 17:541–545
Nugent JM, Palmer JD (1991) RNA-mediated transfer of the gene coxII from the mitochondrion to the nucleus during flowering plant evolution. Cell 66:473–481
Ohto C, Torazawa K, Tanaka M, Shinozaki K, Sugiura M (1988) Transcription of ten ribosomal protein genes from tobacco chloroplasts: a compilation of ribosomal protein genes found in the tobacco chloroplast genome. Plant Mol Biol 11: 589–600
Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H (1986) Chloroplast gene organization deduced from complete nucleotide sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:572–574
Okimoto R, Wolstenholme DR (1990) A set of RRNAs that lack either the TψC arm or the dihydrouridine arm: towards a minimal tRNA adaptor. EMBO J 9:3405–3411
Osawa S, Ohama T, Yamao F, Muto A, Jukes TH, Ozeki H, Umesono K (1988) Directional mutation pressure and transfer RNA in choice of the third nucleotide of synonymous two-codon sets. Proc Natl Acad Sci USA 85:1124–1128
Ozeki H, Ohyama K, Inokuchi H, Fukuzawa H, Kohchi T, Sano T, Nakahigashi K, Umesono K (1987) Genetic system of chloroplasts. Cold Spring Harbor Symp Quant Biol 52:791–804
Pfanner N, Pfaller R, Nupert W (1988) How finicky is mitochondria protein import? Trends Biochem Sci 13:165–167
Pfitzinger H, Guillemaut P, Weil J-H, Pillay DTN (1987) Adjustment of the tRNA population to the codon usage in chloroplasts. Nucleic Acids Res 15:1377–1386
Pritchard AE, Seilhamer JE, Mahalingham R, Sable CL, Venuti SE, Cummings DJ (1990) Nucleotide sequence of the mitochondrial genome of Paramecium. Nucleic Acids Res 18: 173–180
Schimmel P (1991) RNA minihelices and the decoding of genetic information. FASEB J 5:2180–2187
Schulman LH, Pelka H (1988) Anticodon switching changes the identity of methionine and valine transfer RNAs. Science 242:765–768
Schuster W, Wissinger B, Hiesel R, Unseld M, Gerold E, Knoop V, Marchfelder A, Binder S, Schobel W, Scheike R, Gronger P, Ternes R, Brennicke A (1991) Between DNA and protein—RNA editing in plant mitochondria. Physiol Plant 81: 437–445
Shih M-C, Lazar G, Goodman HM (1986) Evidence in favor of the symbiotic origin of chloroplasts: primary structure and evolution of tobacco glyceraldehyde-3-phosphate dehydrogenases. Cell 47:73–80
Shinozaki K, Ohme M, Tanaka T, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5: 2043–2049
Sijben-Mueller G, Hallick RB, Alt J, Westhoff P, Herrmann RG (1986) Spinach plastid genes coding for initiation factor IF-1, ribosomal protein 811 and RNA polymerase alpha-subunit. Nucleic Acids Res 14:1029–1044
Simpson AM, Suyama Y, Dewes H, Campbell DA, Simpson L (1989) Kinetoplastid mitochondria contain functional tRNAs which are encoded in nuclear DNA and also contain small minicircle and maxicircle transcripts of unknown function. Nucleic Acids Res 17:5427–5445
Sprinzl M, Hartmann T, Weber J, Blank J, Zeidler R (1989) Compilation of tRNA sequences and sequences of tRNA genes. Nucl Acids Res 17 (suppl):r1-r172
Steinmetz A, Weil J-H (1986) Isolation and characterization of chloroplast and cytoplasmic transfer RNAs. Methods Enzymol 118:212–231
Subramanian AR, Stahl D, Prombona A (1991) Ribosomal proteins, ribosomes, and translation in plastids. In: Bogorad L, Vasil IK (eds) Molecular biology of plastids, vol 7A of Vasil IK (ed-in-chief), Cell culture and somatic cell genetics of plants. Academic Press, San Diego, pp 191–215
Sugiura M (1987) Structure and function of the tobacco chloroplast genome. Bot Mag Tokyo 100:407–436
Sugiura M, Shinozaki K, Zaita N, Kusuda M, Kumano M (1986) Clone bank of the tobacco (Nicotiana tabacum) chloroplast genome as a set of overlapping restriction endonuclease fragments: mapping of eleven ribosomal protein genes. Plant Sci 44:211–216
Surguchov AP (1987) Common genes for mitochondrial and cytoplasmic proteins. Trends Biochem Sci 12:335–338
Taylor GW, Wolfe KH, Mordent CW, dePamphilis CW, Palmer JD (1991) Lack of a functional plastid tRNACys gene is associated with loss of photosynthesis in a lineage of parasitic plants. Curr Genet 20:515–518
Timmis JN, Scott NS (1983) Sequence homology between spinach nuclear and chloroplast genomes. Nature 305:65–67
Tingey SV, Tsai FY, Edwards JW, Walker EL, Coruzzi GM (1988) Chloroplast and cytoplasmic glutamine synthetase are encoded by homologous nuclear genes which are differentially expressed in vivo. J Biol Chem 263:9651–9657
Toukifimpa R, Romby P, Rozier C, Ehresmann C, Ehresmann B, Mache R (1989) Characterization and footprint analysis of two 5S rRNA binding proteins from spinach chloroplast ribosomes. Biochemistry 28:5840–5846
Wakasugi T, Ohme M, Shinozaki K, Sugiura M (1986) Structures of tobacco chloroplast genes for tRNAIle (CAU), tRNALeu (CAA), tRNACys (GCA), tRNASer (UGA) and tRNAThr (GGU): a compilation of tRNA genes from tobacco chloroplasts. Plant Mol Biol 7:385–392
Walsh MA, Rechel EA, Popovich TM (1980) Observations on plastid fine-structure in the holoparasitic angiosperm Epifagus virginiana. Am J Bot 67:833–837
Wegloehner W, Subramanian AR (1991) A heptapeptide repeat contributes to the unusual length variation of chloroplast ribosomal protein S18. FEBS Lett 279:193–197
Wimpee CF, Morgan R, Wrobel R (1992) An aberrant plastid ribosomal RNA gene cluster in the root parasite Conopholis americana. Plant Mol Biol 18:275–285
Wolfe KH, Li W-H, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058
Wolfe KH, Morden CW, Palmer JD (1992a) Small single-copy region of plastid DNA in the non-photosynthetic angiosperm Epifagus virginiana contains only two genes: differences among dicots, monocots and bryophytes in gene organization at a non-bioenergetic locus. J Mol Biol 223:95–104
Wolfe KH, Katz-Downie DS, Morden CW, Palmer JD (1992b) Evolution of the plastid ribosomal RNA operon in a nongreen parasitic plant: accelerated sequence evolution, altered promoter structure, and tRNA pseudogenes. Plant Mol Biol 18:1037–1048
Yokoi F, Vassileva A, Hayashida N, Torazawa N, Wakasugi T, Sugiura M (1990) Chloroplast ribosomal protein L32 is encoded in the chloroplast genome. FEBS Lett 276:88–90
Yokoi F, Tanaka M, Wakasugi T, Sugiura M (1991) The chloroplast gene for ribosomal protein CL23 is functional in tobacco. FEBS Lett 281:64–66
Ziaie Z, Suyama Y (1987) The cytochrome oxidase subunit I gene of Tetrahymena: a 57 amino acid NH2- terminal extension and a 108 amino acid insert. Curr Genet 12:357–368
Zurawski G, Clegg MT (1987) Evolution of higher-plant chloroplast DNA-encoded genes: implications for structure-function and phylogenetic studies. Ann Rev Plant Physiol 38:391–418
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Wolfe, K.H., Mordent, C.W., Ems, S.C. et al. Rapid evolution of the plastid translational apparatus in a nonphotosynthetic plant: Loss or accelerated sequence evolution of tRNA and ribosomal protein genes. J Mol Evol 35, 304–317 (1992). https://doi.org/10.1007/BF00161168
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DOI: https://doi.org/10.1007/BF00161168