Abstract
The plastid genomes of higher plants contain eleven reading frames (ndhA-K) that are homologous to genes encoding subunits of the mitochondrial NADH-ubiquinone-oxidoreductase (complex I). The carboxyterminal end of the NDH-H subunit from rice (Oryza sativa L.) was expressed as a fusion protein in Escherichia coli and antibodies against the fusion protein were generated in rabbits. The antibody was used to study the expression of NDH-H, and the following results were obtained: (i) NDH-H is expressed in mono- and dicotyledonous plants, (ii) NDH-H is localized on the stroma lamellae of the thylakoid membrane and (iii) NDH-H is expressed in etioplasts. Together with the finding that two other ndh genes (ndhI and ndhK) are expressed in plastids, these results point to the existence of an NAD(P)H-plastoquinone-oxidoreductase on the thylakoid membrane. The possible function of the enzyme in plastids is discussed and it is suggested that it works in balancing the ATP/ADP and the NADPH/NADP ratios during changing external (i.e. light) or internal (i.e. ATP and NADPH demands of biosynthetic pathways of the plastid) conditions.
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Abbreviations
- PVDF:
-
polyvinylidene difluoride
- SDS:
-
sodium dodecyl sulfate
References
Anderson, J.M., Andersson, B. (1982) The architecture of photosynthetic membranes: lateral and transverse organization. Trends Biochem. Sci. 7, 288–292
Arizmendi, J.M., Runswick, M.J., Skehel, J.M., Walker, J.E. (1992) NADH:ubiquinone oxidoreductase from bovine heart mitochondria. A fourth nuclear encoded subunit with a homologue encoded in chloroplast genomes. FEBS Lett 301, 237–242
Bartlett, S.G., Grossman, A.R., Chua, N.H. (1982) In vitro synthesis and uptake of cytoplasmically-synthesized chloroplast proteins. In: Methods in chloroplast molecular biology, pp. 1081–1090, Edelman, M., Hallick, R.B., Chua, N.-H., eds., Elsevier, Amsterdam
Bennoun, P. (1982) Evidence for a respiratory chain in the chloroplast. Proc. Natl. Acad. Sci. USA 79, 4342–4356
Berger, S., Ellersiek, U., Steinmüller, K. (1991) Cyanobacteria contain a mitochondrial complex I-homologous NADH-dehydrogenase. FEBS Lett, 286, 129–132
Berthold, D.A., Babcock, G.T., Yocum, C.F. (1981) A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes. FEBS Lett. 134, 231–234
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of proteins utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254
Chomyn, A., Mariottini, P., Cleeter, M.W.J., Ragan, C.I., Mat-suno-Yagi, A., Hatefi, Y., Doolittle, R.F., Attardi, G. (1985) Six unidentified reading frames of human mitochondrial DNA encode components of the respiratory-chain NADH dehydrogenase. Nature 314, 592–597
Chomyn A., Cleeter, M.W.J., Ragan, C.I., Riley, M., Doolittle, R.F., Attardi, G. (1986) URF6, last unidentified reading frame of human mtDNA, codes for an NADH dehydrogenase sub-unit. Science 234, 614–618
dePamphilis, C.W., Palmer, J.D. (1990) Loss of photosynthetic and chlororespiratory genes from the plastid genome of a parasitic flowering plant. Nature 348, 337–339
Douce, R., Joyard J (1982) Purification of the chloroplast envelope. In: Methods in chloroplast molecular biology, pp. 239–256, Edelman, M., Hallick, R.B., Chua, N.-H., eds., Elsevier, Amsterdam
Douce, R., Holtz, R.B., Benson A.A. (1973) Isolation and properties of the envelope of spinach chloroplasts. J. Biol. Chem. 248, 7215–722
Dupuis, A., Skehel, J.M., Walker J.E. (1991) A homologue of a nuclear-coded iron-sulfur protein subunit of bovine mitochondrial complex I is encoded in chloroplast genomes. Biochemistry 30, 2954–2960
Ellersiek, U., Steinmüller, K. (1992) Cloning and transcription analysis of the ndh(A-I-G-E) gene cluster and the ndhD gene in the cyanobacterium Synechocystis sp. PCC6803. Plant Mol. Biol. 20, 1097–1110
Fearnley, I.M., Runswick, M.J., Walker, J.E. (1989) A homologue of the nuclear coded 49 kd subunit of bovine mitochondrial NADH-ubiquinone reductase is coded in chloroplast DNA. EMBO J. 8, 665–672
Foyer, C., Furbank, R., Harbinson, J., Horton, P. (1990) The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves. Photosynth. Res. 25, 83–100
Ghanotakis, D.F., Babcock, G.T., Yocum, C.F. (1984) Structural and catalytic properties of the oxygen-evolving complex. Biochim. Biophys. Acta 765, 388–398
Harlow, E., Lane, D.P. (1988) Antibodies, a laboratory manual. Cold Spring Harbor Symp. Quant. Biol., Cold Spring Harbor, New York
Hatefi, Y., Ragan, C.I., Galante Y.M. (1985) The enzymes and the enzyme complexes of the mitochondrial oxidative phosphorylation system. In: The enzymes of biological membranes, pp. 1–70, Martonosi, A.N., ed. Plenum Press, New York
Herrmann, R.G. (1982) The preparation of circular DNA from plastids. In: Methods in chloroplast molecular biology, pp. 259–280, Edelman, M., Hallick, R.B., Chua, N.-H., eds. Elsevier, Amsterdam
Horton, P. (1985) Interactions between electron transfer and carbon assimilation. In: Photosynthetic mechanisms and the environment, pp. 135–187, Barber, J., Baker, N.R., eds. Elsevier, Amsterdam
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 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
Kraushaar, H., Hager, S., Wastyn, M., Peschek, G.A. (1990) Immunologically cross-reactive and redox-competent cytochrome b6/f-complexes in the chlorophyll-free plasma membrane of cyanobacteria. FEBS Lett. 273, 227–231
Kreuz, K., Dehesh, K., Apel, K. (1986) The light-dependent accumulation of the P700 chlorophyll a protein of the photosystem I reaction center in barley: evidence for translational control. Eur. J. Biochem. 159, 459–467
Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685
Maier, R.M., Döry, I., Igloi, G., Kössel, H. (1990) The ndhH genes of graminean plastomes are linked with the junctions between small single copy and inverted repeat regions. Curr. Genet. 18, 245–250
Maniatis, T., Fritsch, E.F., Sambrook, J. (1982) Molecular Cloning, a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Marder, J.B., Barber, J. (1989) The molecular anatomy and function of thylakoid proteins. Plant, Cell Envir 12, 595–614
Masui, R., Wakabayashi, S., Matsubara, H., Hatefi, Y. (1991) The amino acid sequence of the 9 kDa polypeptide and partial amino acid sequence of the 20 kDa polypeptide of mitochondrial NADH:ubiquinone oxidoreductase. J. Biochem. 110, 575–582
Matsubayashi, T., Wakasugi, T., Shinozaki, K., Yamaguchi-Shinozaki, K., Zaita, N., Hidaka, T., Meng, B.Y., Ohto, C., Tanaka, M., Kato, A., Maruyama, T., Sugiura M. (1987) Six chloroplast genes (ndhA-F) homologous to human mitochodrial genes encoding components of the respiratory chain NADH dehydrogenase are actively expressed: Determination of the splice sites in ndhA and ndhB pre-mRNAs. Mol. Gen. Genet. 210, 385–393
Molitor, V., Peschek, G.A. (1986) Respiratory electron transport in plasma and thylakoid membrane preparations from the cyanobacterium Anacystis nidulans. FEBS Lett. 195, 145–150
Moran, R. (1982) Formulae for determination of chlorophyllous pigments extracted with N,N-dimethylformamide. Plant Physiol. 69, 1371–1381
Nixon, P.J., Gounaris, K., Coomber, S.A., Hunter, C.N., Dyer T.A., Barber, J. (1989) psbG is not a photosystem two gene but may be an ndh gene. J. Biol. Chem. 264, 14129–14135
Ohyama, K., Fukuzawa, H., Kohchi, T., Shirai, H., Sano, T., Sano, S., Umesono, K., Shiki, Y., Takeuchi, M., Chang, Z., Aota, S.I., Inokuchi, H., Ozeki, H. (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322, 572–574
Ohyama, K., Kohchi, T., Sano, T., Yamada, Y. (1988) Newly identified groups of genes in chloroplasts. Trends Biochem. Sci. 13, 19–22
Oswald, A., Streubel, M., Ljungberg, U., Hermans, J., Eskins, K., Westhoff (1990) Differential biogenesis of photosystem II in mesophyll- and bundle sheath cells of NADP malic enzyme-type C4 plants. A comparative protein and RNA analysis. Eur. J. Biochem. 190, 185–194
Peschek, G.A. (1987) Respiratory electron transport. In: The Cyanobacteria, pp. 119–161, Fay, P., Van Baalen, eds. Elsevier, Amsterdam
Peschek, G.A., Molitor, V., Trnka, M., Wastyn, M., Erber, W. (1988) Characterization of cytochrome-c oxidase in isolated and purified plasma and thylakoid membranes from cyanobacteria. Methods Enzymol. 167, 437–449
Pilkington, S.J., Skehel, J.M., Walker, J.E. (1991) The 30 kilodalton subunit of bovine mitochondrial complex I is homologous to a protein coded in chloroplast DNA. Biochemistry 30, 1901–1908
Preis, D., van der Pas, J.C., Nehls, U., Röhlen, D.A., Sackmann, U., Jahnke, U., Weiss, H. (1990) The 49 K subunit of NADH: ubiquinone reductase (complex I) from Neurosora crassa mitochondria: primary structure of the gene and the protein. Curr. Genet. 18, 59–64
Ragan, C.I. (1987) Structure of NADH-ubiquinone reductase (Complex I). Curr. Top. Bioenerget. 15, 1–36
Robinson, J.M. (1988) Does O2 photoreduction occur within the chloroplast in vivo? Physiol. Plant. 72, 666–680
Schägger, H., von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368–379
Schantz, R., Bogorad, L. (1988) Maize chloroplast genes ndhD, ndhE, and psaC. Sequences, transcripts and transcript pools. Plant Mol. Biol. 11, 239–247
Schnepf, E., Brown jr., R.M. (1971) On relationships between endosymbiosis and the origin of plastids and mitochondria. In: Origin and continuity of cell organelles, vol. 2, pp. 299–322, Reinert, J., Ursprung, H., eds. Springer, Berlin
Schrubar, H., Wanner, G., Westhoff, P. (1990) Transcriptional control of plastid gene expression in greening Sorghum seedlings. Planta 183, 101–111
Shimada, H., Whittier, R.F., Hiratsuka, J., Maeda, Y., Hirai, A., Sugiura, M. (1989) A physical map and clone bank of the rice (Oryza sativa) chloroplast genome. Plant Mol. Biol. Rep. 7, 284–291
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, B.Y., 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
Staehelin, L.A., DeWit, M. (1984) Correlation of structure and function of chloroplast membranes at the supramolecular level. J. Cell. Biochem. 24, 261–269
Strebel, K., Beck, E., Stohmaier, K., Schaller, H. (1986) Characterization of Foot-and-Mouth Disease virus gene products with antisera against bacterially synthesized fusion proteins. J. Virol. 57, 983–991
Steinmetz, A.A., Castroviejo, M., Sayre, R.T., Bogorad, L. (1986) Protein PSII-G. An additional component of photosystem II identified through its plastid gene in maize. J. Biol. Chem. 261, 2485–2488
Steinmüller, K., Ley, A.C., Steinmetz, A.A., Sayre, R.T., Bogorad, L. (1989) Characterization of the ndhC-psbG-ORF157/159 operon of maize plastid DNA and of the cyanobacterium Synechocystis sp. PCC6803. Mol. Gen. Genet. 216, 60–69
Steinmüller, K. (1992) Nucleotide sequence and expression of the ndhH gene of the cyanobacterium Synechocystis sp. PC6803. Plant Mol. Biol. 18, 135–137
Sutton, A., Sieburth, L.E., Bennet, J. (1987) Light-dependent accumulation and localization of photosystem II proteins in maize. Eur. J. Biochem. 164, 571–578
Videira, A., Tropschug., M., Werner, S. (1990) Primary structure and expression of a nuclear-encoded subunit of complex I homologous to proteins specified by the chloroplast genome. Biochem. Biophys. Res. Comm. 171, 1168–1174
Weiss, H., Friedrich, T., Hofhaus, G., Preis, D. (1991) The respiratory-chain NADH dehydrogenase (complex I) of mitochondria. Eur. J. Biochem. 197, 563–576
Westhoff, P., Jansson, C., Klein-Hitpaß, L., Berzborn, R., Larsson, C., Bartlett, S.G. (1985) Intracellular coding sites of polypeptides associated with photosynthetic oxygen evolution of photosystem II. Plant Mol. Biol. 4, 109–120
Wu, M., Nie, Z.Q., Yang, I. (1989) The 18-kD protein that binds to the chloroplast DNA replicative origin is an iron-sulfur protein related to a subunit of NADH-dehydrogenase. Plant Cell 1, 551–557
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We thank Professor M. Sugiura for the rice plastid DNA clone bank, Oliver Buchholz for Sorghum plastid membranes, Pioneer Hi-Bred Inc. for maize and Sorghum seeds and the Deutsche Forschungsgemeinschaft for financial support (SFB189).
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Berger, S., Ellersiek, U., Westhoff, P. et al. Studies on the expression of NDH-H, a subunit of the NAD(P)H-plastoquinone-oxidoreductase of higher-plant chloroplasts. Planta 190, 25–31 (1993). https://doi.org/10.1007/BF00195671
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DOI: https://doi.org/10.1007/BF00195671