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Evolution of the plastid ribosomal RNA operon in a nongreen parasitic plant: Accelerated sequence evolution, altered promoter structure, and tRNA pseudogenes

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Abstract

The nucleotide sequence of a 7.4 kb region containing the entire plastid ribosomal RNA operon of the nongreen parasitic plant Epifagus virginiana has been determined. Analysis of the sequence indicates that all four rRNA genes are intact and almost certainly functional. In contrast, the split genes for tRNAIle and tRNAAla present in the 16S-23S rRNA spacer region have become pseudogenes, and deletion upstream of the 16S rRNA gene has removed a tRNAVal gene and most of the promoter region for the rRNA operon. The rate of nucleotide substitution in 16S and 23S rRNAs is several times higher in Epifagus than in tobacco, a related photosynthetic plant. Possible reasons for this, including relaxed translational constraints, are discussed.

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References

  1. Audren, H, Bisanz-Seyer, C, Briat, J-F, Mache, R: Structure and transcription of the 5S rRNA gene from spinach chloroplasts. Curr Genet 12: 263–269 (1987).

    Google Scholar 

  2. Baeza, L, Bertrand, A, Mache, R, Lerbs-Mache, S: Characterization of a protein binding sequence in the promoter region of the 16S rRNA gene of the spinach chloroplast genome. Nucl Acids Res 19: 3577–3581 (1991).

    Google Scholar 

  3. Bogorad, L: Replication and transcription of plastid DNA. 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), pp. 93–124. Academic Press, San Diego (1991).

    Google Scholar 

  4. deLanversin, G, Pillay, DTN: Primary structure and sequence organization of the 16S–23S spacer in the ribosomal operon of soybean (Glycine max L.) chloroplast DNA. Theor Appl Genet 76: 443–448 (1988).

    Google Scholar 

  5. Delp, G, Koessel, H: rRNAs and rRNA genes of 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), pp. 139–167. Academic Press, San Diego (1991).

    Google Scholar 

  6. Delp, G, Igloi, GL, Koessel, H: Identification of in vivo processing intermediates and of splice junctions of tRNAs from maize chloroplasts by amplification with the polymerase chain reaction. Nucl Acids Res 19: 713–716 (1991).

    Google Scholar 

  7. dePamphilis, CW, Palmer, JD: Loss of photosynthetic and chlororespiratory genes from the plastid genome of a parasitic flowering plant. Nature 348: 348: 337–339 (1990).

    Google Scholar 

  8. Doyle, JJ, Doyle, JL: A rapid isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19: 11–15 (1987).

    Google Scholar 

  9. Edwards, K, Koessel, H: The rRNA operon from Zea mays chloroplasts: nucleotide sequence of 23S rDNA and its homology with E. coli 23S rDNA. Nucl Acids Res 9: 2853–2869 (1981).

    Google Scholar 

  10. Gao, J, Wang, X, Wang, Q: The complete nucleotide sequence of Brassica napus chloroplast 16S rRNA gene. Acta Genet Sin 16: 263–268 (1989).

    Google Scholar 

  11. Gao, J, Wang, X, Wang, Q, Tan, J: Analysis of the primary structure of the leader sequence of the 16S rRNA gene from Vicia faba. Science in China, ser B 33: 592–598 (1990).

    Google Scholar 

  12. Gutell, RR, Fox, GE: A compilation of large subunit RNA sequences presented in a structural format. Nucl Acids Res 16: r175-r269 (1988).

    Google Scholar 

  13. Henikoff, S: Unidirectional digestion with exonuclease III in DNA sequence analysis. Meth Enzymol 155: 156–165 (1987).

    Google Scholar 

  14. Hildebrand, M, Hallick, RB, Passavant, CW, Bourque, DP: Trans-splicing in chloroplasts: the rps 12 locus of Nicotiana tabacum. Proc Natl Acad Sci USA 85: 372–376 (1988).

    Google Scholar 

  15. 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, Hiral, A, Shinozaki, K, Sugiura, M: 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 (1989).

    Google Scholar 

  16. Hu, J, Bogorad, L: Maize chloroplast RNA polymerase: The 180-, 120-, and 38-kilodalton polypeptides are encoded in chloroplast genes. Proc Natl Acad Sci USA 87: 1531–1535 (1990).

    Google Scholar 

  17. Hu, J, Troxler, RF, Bogorad, L: Maize chloroplast RNA polymerase: The 78-kilodalton polypeptide is encoded by the plastid rpoC1 gene. Nucl Acids Res 19: 3431–3434 (1991).

    Google Scholar 

  18. Janssen, I, Mucke, H, Loeffelhardt, W, Bohnert, HJ: The central part of the cyanelle rDNA unit of Cyanophora paradoxa: sequence comparisons with chloroplasts and cyanobacteria. Plant Mol Biol 9: 479–484 (1987).

    Google Scholar 

  19. Keus, RJA, Dekker, AF, vanRoon, MA, Groot, GSP: The nucleotide sequence of the regions flanking the genes coding for 23S, 16S and 4.5S ribosomal RNA on chloroplast DNA from Spirodela oligorhiza. Nucl Acids Res 11: 6465–6474 (1984).

    Google Scholar 

  20. Koch, W, Edwards, K, Koessel, H: Sequencing of the 16S–23S spacer in a ribosomal RNA operon of Zea mays chloroplast DNA reveals two split tRNA genes. Cell 25: 203–213 (1981).

    Google Scholar 

  21. Koessel, H, Edwards, K, Langridge, P, Schiefermayr, E, Schwars, Zs, Strittmatter, G, Zenke, G: Structural and functional analysis of an rRNA operon and its flanking tRNA genes from Zea mays chloroplasts. Nucl Acids Res Symp Ser 11: 117–120 (1982).

    Google Scholar 

  22. Lavin, M, Doyle, JJ, Palmer, JD: Evolutionary significance of the loss of the chloroplast-DNA inverted in the Leguminosae subfamily Papilionoideae. Evolution 44: 390–402 (1990).

    Google Scholar 

  23. Little, MC, Hallick, RB: Chloroplast rpoA, rpoB, and rpoC genes specify at least three components of a chloroplast DNA-dependent RNA polymerase active in tRNA and mRNA transcription. J Biol Chem 263: 14302–14307 (1988).

    Google Scholar 

  24. Maid, U, Zetsche, K: Structural features of the plastid ribosomal RNA operons of two red algae: Antithamnion sp. and Cyanidium caldarium. Plant Mol Biol 16: 537–546 (1991).

    Google Scholar 

  25. Manhart, JR, Palmer, JD: The gain of two chloroplast tRNA introns marks the green algal ancestors of land plants. Nature 345: 268–270 (1990).

    Google Scholar 

  26. Massenet, O, Martinez, P, Seyer, P, Briat, J-R: Sequence organization of the chloroplast ribosomal spacer of Spinacia oleracea including the 3′ end of the 16S rRNA and the 5′ end of the 23S rRNA. Plant Mol Biol 10: 53–63 (1987).

    Google Scholar 

  27. Michel, F, Umesono, K, Ozeki, H: Comparative and functional anatomy of group II catalytic introns—a review. Gene 82: 5–30 (1989).

    Google Scholar 

  28. Morden, CW, Wolfe, KH, dePamphilis, CW, Palmer, JD: Plastid translation and transcription genes in a non-photosynthetic plant: intact, missing and pseudo genes. EMBO J 10: 3281–3288 (1991).

    Google Scholar 

  29. 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: Chloroplast gene organization deduced from complete nucleotide sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322: 572–574 (1986).

    Google Scholar 

  30. Palmer, JD, Jansen, RK, Michaels, HJ, Chase, MW, Manhart, JR: Chloroplast DNA variation and plant phylogeny. Ann Missouri Bot Gard 75: 1180–1206 (1988).

    Google Scholar 

  31. Saitou, N, Nei, M: The neighbor joining method: a new method for reconstructing phylogenetic tress. Mol Biol Evol 4: 406–425 (1987).

    Google Scholar 

  32. Schwarz, Zs, Koessel, H: The primary structure of 16S rDNA from Zea mays chloroplast is homologous to E. coli 16S rRNA. Nature 283: 739–742 (1980).

    Google Scholar 

  33. 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: The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5: 2043–2049 (1986).

    Google Scholar 

  34. Strittmatter, G, Gozdzicka-Jozefiak, A, Koessel, H: Identification of an rRNA operon promoter from Zea mays chloroplasts which excludes the proximal tRNAGAC Val from the primary transcript. EMBO J 4: 599–604 (1985).

    Google Scholar 

  35. Stummann, BM, Lehmbeck, J, Bookjans, G, Henningsen, KW: Nucleotide sequence of the single ribosomal RNA operon of pea chloroplast DNA. Physiol Plant 72: 139–146 (1988).

    Google Scholar 

  36. Sun, E, Wu, B-W, Tewari, KK: In vitro analysis of the pea chloroplast 16S rRNA gene promoter. Mol Cell Biol 9: 5650–5659 (1989).

    Google Scholar 

  37. Svab, Z, Maliga, P: Mutation proximal to the tRNA binding region of the Nicotiana plastid 16S rRNA confers resistance to spectinomycin. Mol Gen Genet 228: 316–319 (1991).

    Google Scholar 

  38. Takaiwa, F, Sugiura, M: Nucleotide sequence of the 16S–23S spacer region in an rRNA gene cluster from tobacco chloroplst DNA. Nucl Acids Res 10: 2665–2676 (1982).

    Google Scholar 

  39. Takaiwa, F, Sugiura, M: The complete nucleotide sequence of a 23-S rRNA gene from tobacco chloroplasts. Eur J Biochem 124: 13–19 (1982).

    Google Scholar 

  40. Tohdoh, N, Sugiura, M: The complete nucleotide sequence of a 16S ribosomal RNA gene from tobacco chloroplasts. Gene 17: 213–218 (1982).

    Google Scholar 

  41. Toukifimpa, R, Romby, P, Rozier, C, Ehresmann, C, Ehresmann, B, Mache, R: Characterization and footprint analysis of two 5S rRNA binding proteins from spinach chloroplast ribosomes. Biochemistry 28: 5840–5846 (1989).

    Google Scholar 

  42. vonAllmen, J-M, Stutz, E: The soybean chloroplast genome: nucleotide sequence of a region containing tRNA-Val(GAC) and 16S rRNA gene. Nucl Acids Res 16: 1200 (1988).

    Google Scholar 

  43. Wimpee, CF, Wrobel, RL, Garvin, DK: A divergent plastid genome in Conopholis americana, an achlorophyllous parasitic plant. Plant Mol Biol 17: 161–166 (1991).

    Google Scholar 

  44. Wimpee CF, Morgan R, Wrobel R: An aberrant plastid ribosomal RNA gene cluster in the root parasite Conopholis americana. Plant Mol Biol, in press.

  45. Wolfe, KH: Protein-coding genes in chloroplast DNA: compilation of nucleotide sequences, data base entries, and rates of molecular evolution. In: Bogorad, L, Vasil, IK (eds) The Photosynthetic Apparatus: Molecular Biology and Operation (vol 7B of Vasil IK (ed-in-chief), Cell Culture and Somatic Cell Genetics of Plants), pp. 467–482. Academic Press, San Diego (1991).

    Google Scholar 

  46. Wolfe, KH, Li, W-H, Sharp, PM: Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84: 9054–9058 (1987).

    Google Scholar 

  47. Wolfe, KH, Gouy, M, Yang, Y-W, Sharp, PM, Li, W-H: Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86: 6201–6205 (1989).

    Google Scholar 

  48. Wolfe KH, Morden CW, Palmer JD: 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}. {jtJ Mol Biol, in press.

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Author notes

  1. Kenneth H. Wolfe

    Present address: Department of Genetics, University of Dublin, Trinity College, Dublin 2, Ireland

  2. Deborah S. Katz-Downie

    Present address: Department of Plant Biology, University of Illinois, 61801, Urbana, IL, USA

  3. Clifford W. Morden

    Present address: Department of Botany, University of Hawaii, 96822, Honolulu, HI, USA

Authors and Affiliations

  1. Department of Biology, Indiana University, 47405, Bloomington, IN, USA

    Kenneth H. Wolfe, Deborah S. Katz-Downie, Clifford W. Morden & Jeffrey D. Palmer

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Wolfe, K.H., Katz-Downie, D.S., Morden, C.W. et al. 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 (1992). https://doi.org/10.1007/BF00047707

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