The Cyanelles of Cyanophora paradoxa

Critical Reviews in Plant Sciences

Volumn 16, Issue 4, 1997, Pages 393-413

  Loffelhardt W ^a   Bohnert, H J ^b   Bryant, D A ^c  

^a LUDWIG BOLTZMANN INSTITUTE FOR LUNG VASCULAR RESEARCH   (Austria)

^b University of Arizona   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Conservative sorting; Endosymbiosis; Peptidoglycan; Plastid evolution; Protein translocation

Indexed keywords

ALGAE; CYANOBACTERIA; CYANOPHORA; CYANOPHORA PARADOXA; EMBRYOPHYTA; ESCHERICHIA COLI; GLAUCOCYSTIS NOSTOCHINEARUM; GLAUCOCYSTOPHYCEAE; PISUM SATIVUM; PROKARYOTA; PROTISTA;

EID: 0000275443     PISSN: 07352689     EISSN: None     Source Type: Journal    
DOI: 10.1080/07352689709701955     Document Type: Article

References (79)

1. Aitken, A. and Stanier, R. Y. 1979. Characterization of peptidoglycan from cyanelles of Cyanophora paradoxa. J. Gen. Microbiol., 112: 219-223.
2. Apt, K. E., Hoffmann, N. E., and Grossman, A. R. 1993. The γ subunit of R-phycoerythrin and its possible mode of transport into the plastid of red algae. J. Biol. Chem., 268: 16208-16215.
3. Asai, K., Fujisaki, S., Nishimura, Y., Nishino, T., Okada, K., Nakagawa, T., Kawamukai, M., and Matsuda, H. 1994. The identification of Escherichia coli ispB (cel) gene encoding the octaprenyl diphosphate synthase. Biochem. Biophys. Res. Commun., 202: 340-354.
4. Ashby, M. N. and Edwards, P. 1990. Elucidation of the deficiency in two yeast coenzyme Q mutants. Characterization of the structural gene encoding hexaprenyl pyrophosphate synthetase. J. Biol. Chem., 365: 13157-13164.
5. Bartsevich, V. V. and Pakrasi, H. 1995. Molecular identification of an ABC transporter complex for mangenese: analysis of a cyanobacterial mutant strain impaired in the photosynthetic oxygen evolution process. EMBO J., 14: 1845-1853.
6. Baum, M. and Schön, A. 1996. Localization and expression of the closely linked cyanelle genes for RNase P RNA and two transfer RNAs. FEBS Lett., 382: 60-64.
7. Baum, M., Cordier, A., and Schön, A. 1996. RNase P from a photosynthetic organelle contains an RNA homologous to the cyanobacterial counter-part. J. Mol. Biol., 257: 43-52.
8. Berenguer, J., Rojo, F., de Pedro, M. A., Pfanzagl, B., and Löffelhardt, W. 1987. Penicillin-binding proteins in the cyanelles of Cyanophora paradoxa, an eukaryotic photoautotroph sensitive to β-lactam antibiotics. FEBS Lett., 224: 401-405.
9. Bhattacharya, D., Helmchen, T., Bibeau, C., and Melkonian, M. 1995. Comparisons of nuclear-encoded small subunit ribosomal RNAs reveal the evolutionary position of the Glaucocystophyta. Mol. Biol. Evol., 12: 415-420.
10. Boston, R. S., Viitanen, P. V., and Vierling, E. 1996. Molecular chaperones and protein folding in plants. Plant Mol. Biol., 32: 191-222.
11. Bryant, D. A. 1992. Puzzles of chloroplast ancestry. Curr. Biol., 2: 240-242.
12. Dolganov, N. A. M., Bhaya, D., and Grossman, A. R. 1995. Cyanobacterial protein with similarity to the chlorophyll a/b binding proteins of higher plants: evolution and regulation. Proc. Natl. Acad. Sci. U.S.A., 92: 636-640.
13. Donachie, W. D. 1993. The cell cycle of Escherichia coli Ann. Rev. Microbiol., 47: 199-230.
14. Douglas, S. E. 1994. Chloroplast origins and evolution. In: The Molecular Biology of the Cyanobacteria. Bryant, D. A., Ed., Kluwer Academic Publishers, Dordrecht, pp. 91-118.
15. Flachmann, R., Michalowski, C. B., Löffelhardt, W., and Bohnert, H. J. 1993. SecY, an integral subunit of the bacterial preprotein translocase is encoded by a plastid genome. J. Biol. Chem., 268: 7514-7519.
16. Giddings, T. H., Jr., Wasmann, C., and Staehelin, L. A. 1983. Structure of the thylakoids and envelope membranes of the cyanelles of Cyanophora paradoxa. Plant Physiol., 71: 409-419.
17. Gilson, P. R. and McFadden, G. I. 1996. The miniaturized genome of a eukaryotic endosymbiont contains genes that overlap, genes that are cotranscribed, and the smallest known spliceosomal introns. Proc. Natl. Acad. Sci. U.S.A., 93: 7737-7742.
18. Green, B. R. and Durnford, D. G. 1996. The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol., 47: 685-712.
19. Grossman, A. R., Bhaya, D., Apt, K. E., and Kehoe, D. M. 1995. Light-harvesting complexes in oxygenic photosynthesis: diversity, control, and evolution. Annu. Rev. Genet., 29: 231-288.
20. Hallick, R. B. 1989. Proposals for the naming of chloroplast genes. II. Update to the nomenclature of genes for thylakoid membrane polypeptides. Plant Mol. Biol. Reptr., 7: 266-275.
21. Hallick, R. B. and Bottomley, W. 1983. Proposals for the naming of chloroplast genes. Plant Mol. Biol. Reptr., 1: 38-43.
22. Hallick, R. B. and Bairoch, A. 1994. Proposals for the naming of chloroplast genes. III. Nomenclature for open reading frames encoded in chloroplast genomes. Plant Mol. Biol. Reptr., 12: S29-30.
23. Hallick, R. B., Hong, L., Drager, R. G., Favreau, M. R., Montfort, A., Orsat, B., Spielmann, A., and Stutz, E. 1993. Complete sequence of Euglena gracilis chloroplast DNA. Nucleic Acids Res., 21: 3537-3544.
24. Hartl, F. U. and Neupert, W. 1990. Protein sorting to mitochondria: evolutionary conservation of folding and assembly. Science, 247: 930-938.
25. Hayes, S. A. and Dice, J. F. 1996. Roles of molecular chaperones in protein degradation. J. Cell Biol., 132: 255-258.
26. Helmchen, T. A., Bhattacharya, D., and Melkonian, M. 1995. Analyses of ribosomal RNA sequences from glaucocystophyte cyanelles provide new insights into evolutionary relationships of plastids. J. Mol. Evol., 41: 203-210.
27. Hess, W. R., Partensky, F., van der Staay, G. W. M., Garcia-Fernandez, J. M., Börner, T., and Vaulot, D. 1996. Coexistence of phycoerythrin and a chlorophyll a/b antenna in a marine prokaryote. Proc. Natl. Acad. Sci. U.S.A., 93: 11126-11130.
28. +-reductase cDNA from Cyanophora paradoxa specifying a precursor for a nucleus-encoded cyanelle polypeptide. Plant Mol. Biol., 21: 1023-1033.
29. +-oxidoreductase from Cyanophora paradoxa into cyanelles and into pea chloroplasts. FEBS Lett., 381: 153-155.
30. Kaneko, T., Tanaka, A., Sato, S., Kotani, H., Sazuka, T., Miyajima, N., Sugiura, M., and Tabata, S. 1995. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. I. Sequence features in the 1 Mb region from map positions 64 to 92% of the genome. DNA Res., 2: 153-166.
31. Kies, L. 1988. The effect of penicillin on the morphology and ultrastructure of Cyanophora, Gloeochaete and Glaucocystis (Glaucocystophyceae) and their cyanelles. Endocyt. Cell Res., 5: 361-372.
32. Kies, L. 1992. Glaucocystophyceae and other protists harboring prokaryotic endocytobionts. In: Algae and Symbioses. Reisser, W., Ed., Biopress Limited, Bristol, pp. 353-377.
33. Kihara, A., Akiyama, Y., and Ito, K. 1995. FtsH is required for proteolytic elimination of uncomplexed SecY, an essential protein translocase subunit. Proc. Natl. Acad. Sci. U.S.A. 92: 4532-4536.
34. Klösgen, R. B. 1997. Protein transport into and across the thylakoid membrane. Photochem. Photobiol., in press.
35. Kowallik, K. V., Stoebe, B., Schaffran, I., and Freier, U. 1995. The chloroplast genome of a chlorophyll a+c containing alga, Odontella sinensis. Plant Mol. Biol. Rptr., 13: 336-342.
36. Krantz, R. G. and Beckman, D. L. 1995. Cytochrome biogenesis. In: Anoxygenic Photosynthetic Bacteria. Blankenship, R. E., Madigan, M. T., and Bauer, C. E., Eds., Kluwer, Dordrecht, pp. 709-723.
37. Kuntz, M., Römer, S., Suire, C., Hugueney, P., Weil, J.-H., Schantz, R., and Camara, B. 1992. Identification of a cDNA for the plastid-located geranylgeranyl pyrophosphate synthase from Capsicum annuum: correlative increase in enzyme activity and transcript level during ripening. Plant J., 2: 25-34.
38. Laudenbach, D. and Grossman, A. 1991. Characterization and mutagenesis of sulfur-regulated genes in a cyanobacterium: evidence for a function in sulfate transport. J. Bacteriol., 173: 2739-2750.
39. Lehel, C., Los, D., Wada, H., Györgyei, J., Horváth, I., Kovács, E., Murata, N., and Vigh, L. 1993. A second groEL-like gene, organized in a groESL operon is present in the genome of Synechocystis sp. PCC 6803. J. Biol. Chem., 268: 1799-1804.
40. Löffelhardt, W. 1995. Molecular analysis of plastid evolution. In: Molecular Ecology of Aquatic Microbes, NATO ASI Series G, Vol. 138, Joint, I., Ed., Springer-Verlag, Berlin-Heidelberg, pp. 265-278.
41. Löffelhardt, W. and Kindl, H. 1979. Conversion of 4-hydroxyphenylpyruvic acid into homogentisic acid at the thylakoid membrane of Lemna gibba. FEBS Lett., 104: 332-334.
42. Löffelhardt, W. and Bohnert, H.J. 1994. Molecular biology of cyanelles. In: The Molecular Biology of Cyanobacteria. Bryant, D. A., Ed., Kluwer Academic Publishers, Dordrecht, pp. 65-89.
43. Löffelhardt, W., and Bohnert, H. J. 1994. Structure and function of the cyanelle genome. In: International Review of Cytology. Vol. 151, Jeon, K. W. and Jarvik, J., Eds., Academic Press, Orlando, pp. 29-65.
44. Löffelhardt, W., Stirewalt, V. L., Michalowski, C. B., Annarella, M., Farley, J. Y., Schluchter, W. M., Chung, S., Neumann-Spallart, C., Steiner, J. M., Jakowitsch, J., Bohnert, H. J., and Bryant, D. A. 1996. The complete sequence of the cyanelle genome from Cyanophora paradoxa: the genetic complexity of a primitive plastid. In: Endocytobiology VI. Schenk, H. E. A., Ed., Springer-Verlag, Berlin-Heidelberg, in press.
45. Mackle, M. M. and Zylinskas, B. A. 1994. Role of signal peptides in targeting of proteins in cyanobacteria. J. Bacteriol., 176: 1857-1864.
46. Mangeney, E. and Gibbs, S. P. 1987. Immunocytochemical localization of ribulose-1,5-bisphosphate carboxylase/oxygenase in the cyanelles of Cyanophora paradoxa and Glaucocystis nostochinearum. Eur. J. Cell Biol., 43: 65-70.
47. Maurizi, M. R., Clark, W. P., Kim, S.-H., and Gottesman, S. 1990. ClpP represents a unique family of serine proteinases. J. Biol.Chem., 265: 12546-12552.
48. McFadden, G., and Gilson, P. 1995. Something borrowed, something green: lateral transfer of chloroplasts by secondary endosymbiosis. Trends Ecol. Evol., 10: 12-17.
49. Michalowski, C. B., Bohnert, H. J., and Löffelhardt, W. 1991. An ORF with homology to crtE, specifying prephytoene pyrophosphate dehydrogenase, is encoded by cyanelle DNA in the eukaryotic alga Cyanophora paradoxa. J. Biol. Chem., 266: 11866-11870.
50. Nakai, M., Sugita, D., Omata, T., and Endo, T. 1993. SecY protein is localized in both the cytoplasmic and thylakoid membranes in the cyanobacterium Synechococcus PCC 7942. Biochem. Biophys. Res. Commun., 193: 228-234.
51. Nakai, M., Nohara, T., Sugita, D., and Endo, T. 1994. Identification and characterization of the SecA protein homologue in the cyanobacterium Synechococcus PCC 7942. Biochem. Biophys. Res. Commun., 200: 844-851.
52. Omer, C. A. and Gibbs, J. B. 1994. Protein prenylation in eukaryotic microorganisms: genetics, biology and biochemistry. Mol. Microbiol., 11: 219-225.
53. Osteryoung, C. M. and Vierung, E. 1995. Conserved cell and organelle division. Nature, 376: 473-174.
54. Palenik, B. and Haselkorn, R. 1991. Multiple evolutionary origins of prochlorophytes, the chlorophyll b-containing prokaryotes. Nature, 355: 265-267.
55. Palmer, J. D. 1991. Plastid chromosomes: structure and evolution. In: The Molecular Biology of Plastids: Cell Culture and Somatic Cell Genetics of Plants, Vol. 7A. Vasil, I. K. and Bogorad, L., Eds., Academic Press, San Diego, 5-53.
56. Palmer, J. D. and Delwiche, C. F. 1996. Second-hand chloroplasts and the case of the disappearing nucleus. Proc. Natl. Acad. Sci. U.S.A., 93: 7432-7435.
57. Pascual, A. and Vioque, A. 1996. The protein subunit of RNase P from the cyanobacterium Synechocystis sp. PCC 6803. Cloning, purification and characterization. Eur. J. Biochem., 241: 17-24.
58. Pfanzagl, B., Pittenauer, E., Allmaier, G., Martinez, J., Berenguer, J., Schmid, E. R., de Pedro, M. A., and Löffelhardt W. 1993. Investigations on structure and biosynthesis of cyanelle murein from Cyanophora paradoxa. In: Bacterial Growth and Lysis, de Pedro, M. A., Höltje J.-V., and Löffelhardt, W., Eds., Plenum Press, London-New York, pp. 47-55.
59. PfanzagI, B., Zenker, A., Pittenauer, E., Allmaier, G., Martinez-Torrecuadrada, J., Schmid, E. R., de Pedro, M. A., and Löffelhardt, W. 1996a. Primary structure of cyanelle peptidoglycan of Cyanophora paradoxa: a prokaryotic cell wall as part of an organelle envelope. J. Bacteriol., 178: 332-339.
60. Pfanzagl,B., Allmaier, G., Schmid, E. R., de Pedro, M. A., and Löffelhardt, W. 1996b. N-Acetyl-putrescine as a characteristic constituent of cyanelle peptidoglycan in glaucocystophyte algae. J. Bacteriol., 178: 6994-6997.
61. 252Cf-plasma desorption mass spectrometry and fast atom bombardment/tandem mass spectrometry. Biol. Mass Spectr., 22: 524-536.
62. Plaimauer, B., Pfanzagl, B., Berenguer, J., de Pedro, M. A., and Löffelhardt, W. 1991. Subcellular distribution of enzymes involved in the biosynthesis of cyanelle murein in the protist Cyanophora paradoxa. FEBS Lett., 284: 169-172.
63. Raven, P. H. 1970. A multiple origin for plastids and mitochondria. Science, 169: 641-646.
64. Reith, M. 1995. Molecular biology of rhodophyte and chromophyte plastids. Annu. Rev Plant Physiol Plant Mol. Biol., 46: 549-575.
65. Reith, M. and Munholland, J. 1993. A high-resolution gene map of the chloroplast genome of the red alga Porphyra purpurea. Plant Cell, 5: 465-475.
66. Reith, M. and Munholland, J. 1995. Complete nucleotide sequence of the Porphyra purpurea chloroplast genome. Plant Mol. Biol. Rptr., 13: 332-335.
67. Schenk, H. E. A. 1970. Nachweis einer lysozymempfindlichen Stützmembran der Endocyanellen von Cyanophora paradoxa (Korschikoff). Z. Naturforsch. 25b: 656.
68. Schenk, H. E. A. 1992. Cyanobacterial symbioses. In: The Prokaryotes, Vol. 4. Ballows, A., Trüper, H. G., Dworkin, M., Harder, W., and Schleifer, K. H., Eds., Springer, New York, 3819-3854.
69. Schlichting, R., Zimmer, W., and Bothe, H. 1990. Exchange of metabolites in Cyanophora paradoxa and its cyanelles. Bot. Acta, 103: 392-398.
70. Schlichting, R. and Bothe, H. 1993. The cyanelles (organelles of a low evolutionary scale) possess a phosphate translocator and a glucose carrier in Cyanophora paradoxa. Bot. Acta, 106: 428-434.
71. Shevelev, E., Bryant, D. A., Löffelhardt, W., and Bohnert, H. J. 1995. Ribonuclease-P RNA gene of the plastid chromosome from Cyanophora paradoxa. DNA Res., 2: 231-234.
72. Smeekens, S., Weisbeek, P., and Robinson, C. 1990. Protein transport into and within chloroplasts. Trends Biochem. Sci., 15: 73-76.
73. Stirewalt, V. L., Michalowski, C. B., Löffelhardt, W., Bohnert, H. J., and Bryant, D. A. 1995. Nucleotide sequence of the cyanelle genome from Cyanophora paradoxa. Plant Mol. Biol. Rptr., 13: 327-332.
74. Sugiura, M. 1992. The chloroplast genome. Plant Mol. Biol., 19: 149-169.
75. Sulli, C. and Schwartzbach, S. D. 1996. A soluble protein is imported into Euglena chloroplasts as a membrane-bound precursor. Plant Cell, 8: 43-53.
76. Swiezewska, E., Dallner, G., Andersson, B., and Ernster, L. 1993. Biosynthesis of ubiquinone and plastoquinone in the endoplasmic reticulum-Golgi membranes of spinach leaves. J. Biol. Chem., 268: 1494-1499.
77. Thöny-Meyer, L., Ritz, D., and Hennecke, H. 1994. Cytochrome c biogenesis in bacteria: a possible pathway begins to emerge. Mol. Microbiol., 12: 1-9.
78. von Heijne, G. 1991. Chloroplast transit peptides: the perfect random coil? FEBS Lett, 278: 1-3.
79. Xie, Z. and Merchant, S. 1996. The plastid-encoded ccsA gene is required for heme attachment to chloroplastc-typecytochromes. J. Biol. Chem., 271: 4632-4639.