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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2000 Oct 29;355(1402):1541–1547. doi: 10.1098/rstb.2000.0714

Chlororespiration.

P J Nixon 1
PMCID: PMC1692878  PMID: 11128007

Abstract

The term 'chlororespiration' is used to describe the activity of a putative respiratory electron transler chain within the thylakoid membrane of chloroplasts and was originally proposed by Bennouon in 1982 to explain effects on the redox state of the plastoquinone pool in green algae in the absence of photosynthetic plastoquinone electrontransfer. In his original model, Bennoun suggested that the pool could be reduced through the action of a NAD(P) H dehydrogenase and could be oxidized by oxygen at an oxidase. At the same time an electrochemical gradient would be generated across the membrane. This review describes the current status of the chlororespiration model in light of the recent discoveries of novel respiratory components chloroplast thylakoid membrane.

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Selected References

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  1. Atteia A., de Vitry C., Pierre Y., Popot J. L. Identification of mitochondrial proteins in membrane preparations from Chlamydomonas reinhardtii. J Biol Chem. 1992 Jan 5;267(1):226–234. [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. Burrows P. A., Sazanov L. A., Svab Z., Maliga P., Nixon P. J. Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J. 1998 Feb 16;17(4):868–876. doi: 10.1093/emboj/17.4.868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carol P., Stevenson D., Bisanz C., Breitenbach J., Sandmann G., Mache R., Coupland G., Kuntz M. Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell. 1999 Jan;11(1):57–68. doi: 10.1105/tpc.11.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Casano L. M., Zapata J. M., Martín M., Sabater B. Chlororespiration and poising of cyclic electron transport. Plastoquinone as electron transporter between thylakoid NADH dehydrogenase and peroxidase. J Biol Chem. 2000 Jan 14;275(2):942–948. doi: 10.1074/jbc.275.2.942. [DOI] [PubMed] [Google Scholar]
  6. Cooley J. W., Howitt C. A., Vermaas W. F. Succinate:quinol oxidoreductases in the cyanobacterium synechocystis sp. strain PCC 6803: presence and function in metabolism and electron transport. J Bacteriol. 2000 Feb;182(3):714–722. doi: 10.1128/jb.182.3.714-722.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cournac L., Redding K., Ravenel J., Rumeau D., Josse E. M., Kuntz M., Peltier G. Electron flow between photosystem II and oxygen in chloroplasts of photosystem I-deficient algae is mediated by a quinol oxidase involved in chlororespiration. J Biol Chem. 2000 Jun 9;275(23):17256–17262. doi: 10.1074/jbc.M908732199. [DOI] [PubMed] [Google Scholar]
  8. Elortza F., Asturias J. A., Arizmendi J. M. Chloroplast NADH dehydrogenase from Pisum sativum: characterization of its activity and cloning of ndhK gene. Plant Cell Physiol. 1999 Feb;40(2):149–154. doi: 10.1093/oxfordjournals.pcp.a029522. [DOI] [PubMed] [Google Scholar]
  9. Endo T., Shikanai T., Takabayashi A., Asada K., Sato F. The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett. 1999 Aug 20;457(1):5–8. doi: 10.1016/s0014-5793(99)00989-8. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Feild TS, Nedbal L, Ort DR. Nonphotochemical reduction of the plastoquinone pool in sunflower leaves originates from chlororespiration . Plant Physiol. 1998 Apr;116(4):1209–1218. doi: 10.1104/pp.116.4.1209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Goyal A., Tolbert N. E. Association of glycolate oxidation with photosynthetic electron transport in plant and algal chloroplasts. Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3319–3324. doi: 10.1073/pnas.93.8.3319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Heineke D., Riens B., Grosse H., Hoferichter P., Peter U., Flügge U. I., Heldt H. W. Redox Transfer across the Inner Chloroplast Envelope Membrane. Plant Physiol. 1991 Apr;95(4):1131–1137. doi: 10.1104/pp.95.4.1131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Howitt C. A., Udall P. K., Vermaas W. F. Type 2 NADH dehydrogenases in the cyanobacterium Synechocystis sp. strain PCC 6803 are involved in regulation rather than respiration. J Bacteriol. 1999 Jul;181(13):3994–4003. doi: 10.1128/jb.181.13.3994-4003.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Howitt C. A., Vermaas W. F. Quinol and cytochrome oxidases in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry. 1998 Dec 22;37(51):17944–17951. doi: 10.1021/bi981486n. [DOI] [PubMed] [Google Scholar]
  18. Jose Quiles M, Cuello J. Association of ferredoxin-NADP oxidoreductase with the chloroplastic pyridine nucleotide dehydrogenase complex in barley leaves . Plant Physiol. 1998 May;117(1):235–244. doi: 10.1104/pp.117.1.235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kofer W., Koop H. U., Wanner G., Steinmüller K. Mutagenesis of the genes encoding subunits A, C, H, I, J and K of the plastid NAD(P)H-plastoquinone-oxidoreductase in tobacco by polyethylene glycol-mediated plastome transformation. Mol Gen Genet. 1998 Apr;258(1-2):166–173. doi: 10.1007/s004380050719. [DOI] [PubMed] [Google Scholar]
  20. Lemaire C., Wollman F. A., Bennoun P. Restoration of phototrophic growth in a mutant of Chlamydomonas reinhardtii in which the chloroplast atpB gene of the ATP synthase has a deletion: an example of mitochondria-dependent photosynthesis. Proc Natl Acad Sci U S A. 1988 Mar;85(5):1344–1348. doi: 10.1073/pnas.85.5.1344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Matsuo M., Endo T., Asada K. Properties of the respiratory NAD(P)H dehydrogenase isolated from the cyanobacterium Synechocystis PCC6803. Plant Cell Physiol. 1998 Mar;39(3):263–267. doi: 10.1093/oxfordjournals.pcp.a029366. [DOI] [PubMed] [Google Scholar]
  23. Maxwell D. P., Wang Y., McIntosh L. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci U S A. 1999 Jul 6;96(14):8271–8276. doi: 10.1073/pnas.96.14.8271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mills J. D., Crowther D., Slovacek R. E., Hind G., McCarty R. E. Electron transport pathways in spinach chloroplasts. Reduction of the primary acceptor of photosystem II by reduced nicotinamide adenine dinucleotide phosphate in the dark. Biochim Biophys Acta. 1979 Jul 10;547(1):127–137. doi: 10.1016/0005-2728(79)90101-4. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Rappaport F., Finazzi G., Pierre Y., Bennoun P. A new electrochemical gradient generator in thylakoid membranes of green algae. Biochemistry. 1999 Feb 16;38(7):2040–2047. doi: 10.1021/bi982351k. [DOI] [PubMed] [Google Scholar]
  27. Sazanov L. A., Burrows P. A., Nixon P. J. The chloroplast Ndh complex mediates the dark reduction of the plastoquinone pool in response to heat stress in tobacco leaves. FEBS Lett. 1998 Jun 5;429(1):115–118. doi: 10.1016/s0014-5793(98)00573-0. [DOI] [PubMed] [Google Scholar]
  28. Sazanov L. A., Burrows P. A., Nixon P. J. The plastid ndh genes code for an NADH-specific dehydrogenase: isolation of a complex I analogue from pea thylakoid membranes. Proc Natl Acad Sci U S A. 1998 Feb 3;95(3):1319–1324. doi: 10.1073/pnas.95.3.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shikanai T., Endo T., Hashimoto T., Yamada Y., Asada K., Yokota A. Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9705–9709. doi: 10.1073/pnas.95.16.9705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Turmel M., Otis C., Lemieux C. The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: insights into the architecture of ancestral chloroplast genomes. Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10248–10253. doi: 10.1073/pnas.96.18.10248. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wakasugi T., Tsudzuki J., Ito S., Nakashima K., Tsudzuki T., Sugiura M. Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):9794–9798. doi: 10.1073/pnas.91.21.9794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Willeford K. O., Gombos Z., Gibbs M. Evidence for Chloroplastic Succinate Dehydrogenase Participating in the Chloroplastic Respiratory and Photosynthetic Electron Transport Chains of Chlamydomonas reinhardtii. Plant Physiol. 1989 Jul;90(3):1084–1087. doi: 10.1104/pp.90.3.1084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wu D., Wright D. A., Wetzel C., Voytas D. F., Rodermel S. The IMMUTANS variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell. 1999 Jan;11(1):43–55. doi: 10.1105/tpc.11.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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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