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. 1998 Feb 16;17(4):868–876. doi: 10.1093/emboj/17.4.868

Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes.

P A Burrows 1, L A Sazanov 1, Z Svab 1, P Maliga 1, P J Nixon 1
PMCID: PMC1170436  PMID: 9463365

Abstract

The plastid genomes of several plants contain homologues, termed ndh genes, of genes encoding subunits of the NADH:ubiquinone oxidoreductase or complex I of mitochondria and eubacteria. The functional significance of the Ndh proteins in higher plants is uncertain. We show here that tobacco chloroplasts contain a protein complex of 550 kDa consisting of at least three of the ndh gene products: NdhI, NdhJ and NdhK. We have constructed mutant tobacco plants with disrupted ndhC, ndhK and ndhJ plastid genes, indicating that the Ndh complex is dispensible for plant growth under optimal growth conditions. Chlorophyll fluorescence analysis shows that in vivo the Ndh complex catalyses the post-illumination reduction of the plastoquinone pool and in the light optimizes the induction of photosynthesis under conditions of water stress. We conclude that the Ndh complex catalyses the reduction of the plastoquinone pool using stromal reductant and so acts as a respiratory complex. Overall, our data are compatible with the participation of the Ndh complex in cyclic electron flow around the photosystem I complex in the light and possibly in a chloroplast respiratory chain in the dark.

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Selected References

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  1. Arnon D. I. COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS. Plant Physiol. 1949 Jan;24(1):1–15. doi: 10.1104/pp.24.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bennoun P. Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci U S A. 1982 Jul;79(14):4352–4356. doi: 10.1073/pnas.79.14.4352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Diner B. A. Dependence of the deactivation reactions of photosystem II on the redox state of plastoquinone pool A varied under anaerobic conditions; Equilibria on the acceptor side of photosystem II. Biochim Biophys Acta. 1977 May 11;460(2):247–258. doi: 10.1016/0005-2728(77)90211-0. [DOI] [PubMed] [Google Scholar]
  4. Fearnley I. M., Walker J. E. Conservation of sequences of subunits of mitochondrial complex I and their relationships with other proteins. Biochim Biophys Acta. 1992 Dec 7;1140(2):105–134. doi: 10.1016/0005-2728(92)90001-i. [DOI] [PubMed] [Google Scholar]
  5. Friedrich T., Steinmüller K., Weiss H. The proton-pumping respiratory complex I of bacteria and mitochondria and its homologue in chloroplasts. FEBS Lett. 1995 Jun 26;367(2):107–111. doi: 10.1016/0014-5793(95)00548-n. [DOI] [PubMed] [Google Scholar]
  6. Guedeney G., Corneille S., Cuiné S., Peltier G. Evidence for an association of ndh B, ndh J gene products and ferredoxin-NADP-reductase as components of a chloroplastic NAD(P)H dehydrogenase complex. FEBS Lett. 1996 Jan 15;378(3):277–280. doi: 10.1016/0014-5793(95)01473-x. [DOI] [PubMed] [Google Scholar]
  7. Harris G. C., Heber U. Effects of Anaerobiosis on Chlorophyll Fluorescence Yield in Spinach (Spinacia oleracea) Leaf Discs. Plant Physiol. 1993 Apr;101(4):1169–1173. doi: 10.1104/pp.101.4.1169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Heber U., Walker D. Concerning a dual function of coupled cyclic electron transport in leaves. Plant Physiol. 1992 Dec;100(4):1621–1626. doi: 10.1104/pp.100.4.1621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Horton P., Ruban A. V., Walters R. G. Regulation of Light Harvesting in Green Plants (Indication by Nonphotochemical Quenching of Chlorophyll Fluorescence). Plant Physiol. 1994 Oct;106(2):415–420. doi: 10.1104/pp.106.2.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Leif H., Sled V. D., Ohnishi T., Weiss H., Friedrich T. Isolation and characterization of the proton-translocating NADH: ubiquinone oxidoreductase from Escherichia coli. Eur J Biochem. 1995 Jun 1;230(2):538–548. doi: 10.1111/j.1432-1033.1995.tb20594.x. [DOI] [PubMed] [Google Scholar]
  11. Martín M., Casano L. M., Sabater B. Identification of the product of ndhA gene as a thylakoid protein synthesized in response to photooxidative treatment. Plant Cell Physiol. 1996 Apr;37(3):293–298. doi: 10.1093/oxfordjournals.pcp.a028945. [DOI] [PubMed] [Google Scholar]
  12. Matsubayashi T., Wakasugi T., Shinozaki K., Yamaguchi-Shinozaki K., Zaita N., Hidaka T., Meng B. Y., Ohto C., Tanaka M., Kato A. Six chloroplast genes (ndhA-F) homologous to human mitochondrial 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. 1987 Dec;210(3):385–393. doi: 10.1007/BF00327187. [DOI] [PubMed] [Google Scholar]
  13. Maxwell P. C., Biggins J. Role of cyclic electron transport in photosynthesis as measured by the photoinduced turnover of P700 in vivo. Biochemistry. 1976 Sep 7;15(18):3975–3981. doi: 10.1021/bi00663a011. [DOI] [PubMed] [Google Scholar]
  14. Nixon P. J., Gounaris K., Coomber S. A., Hunter C. N., Dyer T. A., Barber J. psbG is not a photosystem two gene but may be an ndh gene. J Biol Chem. 1989 Aug 25;264(24):14129–14135. [PubMed] [Google Scholar]
  15. Plaxton William C. THE ORGANIZATION AND REGULATION OF PLANT GLYCOLYSIS. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):185–214. doi: 10.1146/annurev.arplant.47.1.185. [DOI] [PubMed] [Google Scholar]
  16. Robinson C., Klösgen R. B. Targeting of proteins into and across the thylakoid membrane--a multitude of mechanisms. Plant Mol Biol. 1994 Oct;26(1):15–24. doi: 10.1007/BF00039516. [DOI] [PubMed] [Google Scholar]
  17. Sazanov L. A., Burrows P., Nixon P. J. Detection and characterization of a complex I-like NADH-specific dehydrogenase from pea thylakoids. Biochem Soc Trans. 1996 Aug;24(3):739–743. doi: 10.1042/bst0240739. [DOI] [PubMed] [Google Scholar]
  18. Schägger H., Cramer W. A., von Jagow G. Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal Biochem. 1994 Mar;217(2):220–230. doi: 10.1006/abio.1994.1112. [DOI] [PubMed] [Google Scholar]
  19. Shinozaki K., Ohme M., Tanaka M., Wakasugi T., Hayashida N., Matsubayashi T., Zaita N., Chunwongse J., Obokata J., Yamaguchi-Shinozaki K. The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J. 1986 Sep;5(9):2043–2049. doi: 10.1002/j.1460-2075.1986.tb04464.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Shipton C. A., Barber J. Photoinduced degradation of the D1 polypeptide in isolated reaction centers of photosystem II: evidence for an autoproteolytic process triggered by the oxidizing side of the photosystem. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6691–6695. doi: 10.1073/pnas.88.15.6691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Svab Z., Hajdukiewicz P., Maliga P. Stable transformation of plastids in higher plants. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8526–8530. doi: 10.1073/pnas.87.21.8526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Svab Z., Maliga P. High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):913–917. doi: 10.1073/pnas.90.3.913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Yu L., Zhao J., Muhlenhoff U., Bryant D. A., Golbeck J. H. PsaE Is Required for in Vivo Cyclic Electron Flow around Photosystem I in the Cyanobacterium Synechococcus sp. PCC 7002. Plant Physiol. 1993 Sep;103(1):171–180. doi: 10.1104/pp.103.1.171. [DOI] [PMC free article] [PubMed] [Google Scholar]

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