Summary
The nucleotide sequences of the ribosomal protein genesrps18, rps19, rpl2, rpl33, and partial sequence ofrpl22 from cyanelles, the photosynthetic organelles of the protistCyanophora paradoxa, have been determined. These genes form two clusters oriented in opposite and divergent directions. One cluster contains therpl33 andrps18 genes; the other contains therpl2, rps19, andrpl22 genes, in that order. Phylogenetic trees were constructed from both the DNA sequences and the deduced protein sequences of cyanelles,Euglena gracilis and land plant chloroplasts, andEscherichia coli, using parsimony or maximum likelihood methods. In addition, a phylogenetic tree was built from a distance matrix comparing the number of nucleotide substitutions per site. The phylogeny inferred from all these methods suggests that cyanelles fall within the chloroplast line of evolution and that the evolutionary distances between cyanelles and land plant chloroplasts are shorter than betweenE. gracilis chloroplasts and land plant chloroplasts.
Similar content being viewed by others
References
Banks MP (1970) Evolution and plants of the past. Wadsworth, Belmont CA
Bohnert HJ, Michalowski C, Bevacqua S, Mucke H, Löffelhardt W (1985) Cyanelle DNA fromCyanophora paradoxa: physical mapping and location of protein coding regions. Mol Gen Genet 201:565–574
Breiteneder H, Seiser C, Löffelhardt W, Michalowski C, Bohnert H (1988) Physical map and protein gene map of cyanelle DNA from the second known isolate ofCyanophora paradoxa (Kies-strain). Curr Genet 13:199–206
Bryant DA, De Lorimier R, Lambert DH, Dubbs J, Stirewalt VL, Stevens SE, Porter RD, Tam J, Jay E (1985) Molecular cloning and nucleotide sequence of theα and β subunits of allophycocyanin from the cyanelle genome ofCyanophora paradoxa. Proc Natl Acad Sci USA 82:3242–3246
Burger-Wiersma T, Veenhuis M, Korthals HJ, Van de Wiel CCM, Mur LR (1986) A new prokaryote containing chlorophylls a and b. Nature 320:262–264
Cech TR (1986) The generality of self-splicing RNA: relationship to nuclear mRNA splicing. Cell 44:207–210
Chisholm SW, Olson RJ, Zettler ER,. Goericke R, Waterbury JB, Welschmeyer NA (1988) A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334:340–343
Christopher DA, Cushman JC, Price CA, Hallick RB (1988) Organization of ribosomal protein genesrpl23, rpl2, rps19, rpl22 andrps3 on theEuglena gracilis chloroplast genome. Curr Genet 14:275–286
Dayhoff MO, Eck RV (1978) Atlas of protein sequence and structure. National Biomedical Research Foundation, Silver Spring MD
Dereveux J, Haeberli P, Smithies O (1984) A comprehensive set of sequences and analysis programs for the VAX. Nucleic Acids Res 12:387–395
Emberger L (1968) Les plantes fossiles dans leurs rapports avec les végétaux vivants. Masson et Cie, Paris, France
Evrard JL, Kuntz M, Straus NA, Weil JH (1988) A class-I intron in a cyanelle tRNA gene fromCyanophora paradoxa: phylogenetic relationship between cyanelles and plant chloroplasts. Gene 71:115–122
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Felsenstein J (1988) Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet 22:521–565
Floener L, Bothe H (1982) Metabolic activities inCyanophora paradoxa and its cyanelles: II. Photosynthesis and respiration. Planta 156:78–83
Floener L, Danneberg G, Bothe H (1982) Metabolic activities inCyanophora paradoxa and its cyanelles: I. The enzymes of assimilatory nitrate reduction. Planta 156:70–77
Gray MW, Doolittle WF (1982) Has the endosymbiont hypothesis been proven? Microbiol Rev 46:1–42
Heinhorst S, Shively JM (1983) Encoding of both subunits of ribulose 1,5 bisphosphate carboxylase by organelle genome ofCyanophora paradoxa. Nature 304:373–374
Hiratsuka J, Shimada H, Whittier RF, Ishibashi T, Sakamoto M, Mori M, Kondo M, Honji Y, Sun CR, Meng BY, Li YQ, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (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
Jaynes JM, Vernon LP (1982) The cyanelle ofCyanophora paradoxa: almost a cyanobacterial chloroplast. Trends Biochem Sci 7:22–24
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Ko K, Jaynes JM, Straus NA (1985) Homology between the cyanelle DNA ofCyanophora paradoxa and the chloroplast DNA ofVicia faba. Plant Sci 42:115–123
Kuntz M, Crouse EJ, Mubumbila M, Burkard G, Weil JH, Bohnert HJ, Mucke H, Löffelhardt W (1984) Transfer RNA gene mapping studies on cyanelle DNA fromCyanophora paradoxa. Mol Gen Genet 194:508–512
Kuntz M, Evrard JL, Weil JH (1988) Nucleotide sequence of the tRNASerGGA and tRNAGlyGCC genes from cyanelles ofCyanophora paradoxa. Nucleic Acids Res 16:8733
Lambert HL, Bryant DA, Stirewalt VL, Dubbs JM, Stevens SE, Porter RD (1985) Gene map for theCyanophora paradoxa cyanelle genome. J Bacteriol 164:659–664
Lemaux PG, Grossman AR (1985) Major light-harvesting polypeptides encoded in polycistronic transcripts in a eukaryotic alga. EMBO J 4:1911–1919
Lewin RA (1976) Prochlorophyta as a proposed new division of algae. Nature 261:697–698
Morden CW, Golden SS (1989)psbA genes indicate common ancestry of prochlorophytes and chloroplasts. Nature 337: 382–385
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 sequence of liverwortMarchantia polymorpha chloroplast DNA. Nature 322:572–574
Shinozaki K, Ohme M, Tanaka M, 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
Tanaka M, Wakasugi T, Sugita M, Shinozaki K, Sugiura M (1986) Genes for the eight ribosomal proteins are clustered on the chloroplast genome of tobacco (Nicotiana tabacum): similarity to the S10 and spc operons ofEscherichia coli. Proc Natl Acad Sci USA 83:6030–6034
Thomas F, Massenet O, Dorne AM, Briat JF, Mache R (1988) Expression of therpl23, rpl2 andrps19 genes in spinach chloroplasts. Nucleic Acids Res 16:2461–2472
Turner S, Burger-Wiersma T, Giovannoni SJ, Mur LR, Pace NR (1989) The relationship of a prochlorophyteProchlorothrix hollandica to green chloroplasts. Nature 337:380–382
Van den Eynde H, De Baere R, De Roeck E, Van de Peer Y, Vandenberghe A, Willekens P, De Wachter R (1988) The 5S ribosomal RNA sequences of a red algal rhodoplast and a gymnosperm chloroplast. Implications for the evolution of plastids and cyanobacteria. J Mol Evol 27:126–132
Whatley JM, Whatley FR (1981) Chloroplast evolution. New Phytol 87:233–247
White ME (1986) The greening of Gondwana: the 400 million years story of Australia's plants. Reed Book Ltd Frenchs Forest, Australia
Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058
Zhang H, Scholl R, Browse J, Somerville C (1988) Double stranded DNA sequencing as a choice for DNA sequencing. Nucleic Acids Res 16:1220
Zurawski S, Marvo-Zurawski S (1985) Structure of theEscherichia coli S10 ribosomal operon. Nucleic Acids Res 13: 4521–4526
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Evrard, J.L., Kuntz, M. & Weil, J.H. The nucleotide sequence of five ribosomal protein genes from the cyanelles ofCyanophora paradoxa: Implications concerning the phylogenetic relationship between cyanelles and chloroplasts. J Mol Evol 30, 16–25 (1990). https://doi.org/10.1007/BF02102449
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF02102449