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Regulation of Electron Transport in the Respiratory Chain of Plant Mitochondria

  • Francis E. Sluse
  • Wieslawa Jarmuszkiewicz
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 17)

Summary

The aim of this chapter is to gather updated understanding of electron flow and H+ flux-linked processes in plant mitochondria. New understanding of molecular mechanisms of redox pumps and ATP synthase are described. Special attention is paid to the non-phosphorylating electron flow pathways and to H+ electrochemical gradient consumers. Partitioning of electrons between ubiquinol oxidizing pathways (alternative oxidase, AOX, and cytochrome pathway) is analyzed at the level of methodological aspects and interpreted in terms of energy conservation efficiency and of cell metabolism regulation. Partitioning of H+ electrochemical gradient between ATP synthase and uncoupling protein (UCP) is tackled through the ADP/O method. It is shown how efficiently UCP activity can divert energy from oxidative phosphorylation. It is also stressed that AOX and UCP are not redundant as cnergy-dissipating proteins because AOX is inhibited by free fatty acids that stimulate UCP and because AOX and UCP have completely different kinetic behavior regarding the redox State of ubiquinone. It is concluded that we are still very far from having a clear idea about the physiological role and interplay of energy-wasting and energy-conserving Systems.

Keywords

Linoleic Acid Tomato Fruit Uncouple Protein Alternative Oxidase Plant Mitochondrion 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

AOX

alternative oxidase

BHAM

benzohydroxamic acid

complex I

NADH: ubiquinone oxidoreductase

complex II

succinate: ubiquinone oxidoreductase

complex III

ubiquinol: ubiquinone cytochrome c oxidoreductase

complex IV

cytochrome c oxidoreductase

ΔµH+

H+ electrochemical gradient

ΔpH

pH difference between the intermembrane and matrix spaces

ΔΨ

mitochondrial transmembrane electrical potential, Ψin—Ψout

ETF

electron transfer flavoprotein

FFA

free fatty acid

FMN

flavin mononucleotide

ISP

Rieske iron-sulfur protein

LA

linoleic acid

MACP family

mitochondrial anion carrier protein family

mtDNA

mitochondrial

NAD+, NADH

nicotinamide adenine dinucleotide and its reduced form

NADP+

nicotinamide adenine dinucleotide

NADPH

phosphate and its reduced form

nor

non-ripening

Q

ubiquinone

QH2

ubiquinol

TCA

cycle: tricarboxylic acid cycle

UCP

uncoupling protein

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References

  1. Abrahams JP, Leslie AG, Lutter R and Walker JE (1994) Structure at 2.8 Å resolution of F1ATPase from bovine heart mitochondria. Nature 370: 621–628PubMedCrossRefGoogle Scholar
  2. Affourtit C, Krab K and Moore AL (2001) Control of plant mitochondrial respiration. Biochim Biophys Acta 1504: 58–69PubMedCrossRefGoogle Scholar
  3. Almeida AM, Jarmuszkiewicz W, Khomsi H, Arruda P, Vercesi AE and Sluse FE (1999) Cyanide-resistant, ATP-synthesis-sustained, and uncoupling protein-sustained respiration during postharvest ripening of tomato fruit. Plant Physiol 119: 1323–1329Google Scholar
  4. Almeida AM, Navet R, Jarmuszkiewicz W, Vercesi AE, Sluse-Goffart CM and Sluse FE (2002) The energy-conserving and energy-dissipating processes in mitochondria isolated from wild type and non-ripening tomato fruits during development on the plant. J Bioenerg Biomembr 34: 487–498PubMedCrossRefGoogle Scholar
  5. Babcock GT and Wikstrom M (1992) Oxygen activation and the conservation of energy in cell respiration. Nature 356: 301–309PubMedCrossRefGoogle Scholar
  6. Bernardi P (1999) Mitochondrial transport of cations: Channels, exchangers, and permeability transition. Physiol Rev 79: 1127–1155PubMedGoogle Scholar
  7. Boyer PD (1997) The ATP synthase—a splendid molecular machine. Annu Rev Biochem 66: 717–749PubMedCrossRefGoogle Scholar
  8. Brandt U (1996) Energy conservation by bifurcated electron-transfer in the cytochrome-bc 1 complex. Biochim Biophys Acta 1275: 41–46PubMedCrossRefGoogle Scholar
  9. Brandt U (1997) Proton-translocation by membrane-bound NADH: ubiquinone-oxidoreductase (complex I) through redox-gated ligand conduction. Biochim Biophys Acta 1318: 79–91PubMedCrossRefGoogle Scholar
  10. Duncan TM, Bulygin VV, Zhou Y, Hutcheon ML and Cross RL (1995) Rotation of subunits during catalysis by Escherichia coli F1-ATPase. Proc Natl Acad Sci USA 92:10964–10968PubMedCrossRefGoogle Scholar
  11. Dutton PL, Moser CC, Sled VD, Daldal F and Ohnishi T (1998) A reductant-induced oxidation mechanism for complex I. Biochim Biophys Acta 1364: 245–257PubMedCrossRefGoogle Scholar
  12. Echtay KS, Winkler E and Klingenberg M (2000) Coenzyme Q is an obligatory cofactor for uncoupling protein function. Nature 408: 609–613PubMedCrossRefGoogle Scholar
  13. Elston T, Wang H and Oster G (1998) Energy transduction in ATP synthase. Nature 391:510–513PubMedCrossRefGoogle Scholar
  14. Garlid KD, Orosz DE, Modriansky M, Vassanelli S and Jezek P (1996) On the mechanism of fatty acid-induced proton trans­port by mitochondrial uncoupling protein. J Biol Chem 271: 2615–2620PubMedCrossRefGoogle Scholar
  15. Guy RG, Berry JA, Fogel ML and Hoerinng TC (1989) Differential fractionation of oxygen isotopes by cyanide-resistant and cyanide-insensitive respiration in plants. Planta 177:483–491CrossRefGoogle Scholar
  16. Jarmuszkiewicz W, Hryniewiecka L, Sluse-Goffart CM and Sluse FE (1998a) Electron partitioning between the two branching quinol-oxidizing pathways in Acanthamoeba castellanii mitochondria during steady-state state 3 respira­tion. J Biol Chem 273: 10174–10180PubMedCrossRefGoogle Scholar
  17. Jarmuszkiewicz W, Almeida AM, Sluse-Goffart CM, Sluse FE and Vercesi AE (1998b) Linoleic acid-induced activity of plant uncoupling mitochondrial protein in purified tomato fruit mitochondria during resting, phosphorylating, and progres­sively uncoupled respiration. J Biol Chem 273: 34882–34886PubMedCrossRefGoogle Scholar
  18. Jarmuszkiewicz W, Almeida AM, Vercesi AE, Sluse FE and Sluse-Goffart CM (2000) Proton re-uptake partitioning between uncoupling protein and ATP synthase during benzo-hydroxamic acid resistant state 3 respiration in tomato fruit mitochondria. J Biol Chem 275: 13315–13320PubMedCrossRefGoogle Scholar
  19. Jarmuszkiewicz W, Sluse-Goffart CM, Vercesi AE and Sluse FE (2001) Alternative oxidase and uncoupling protein: thermogenesis versus cell energy balance. Biosci Reports 21: 213–222CrossRefGoogle Scholar
  20. Jarmuszkiewicz W, Berendt M, Navet R and Sluse FE (2002a) Uncoupling protein and alternative oxidase of Dictyostelium discoideum: occurrence, properties and protein expression during vegetative life and starvation-induced early development. FEBS Lett 532: 459–564PubMedCrossRefGoogle Scholar
  21. Jarmuszkiewicz W, Sluse FE, Hryniewiecka L and Sluse-Goffart CM (2002b). Interactions between the cytochrome pathway and the alternative oxidase in isolated Acanthamoeba castellanii mitochondria. J Bioenerg Biomembr 34: 31–40PubMedCrossRefGoogle Scholar
  22. Laloi M (1999) Plant mitochondrial carriers: an overview. Cell Mol Life Sci 56: 918–944PubMedCrossRefGoogle Scholar
  23. Mackenzie S and Mcintosh L (1999) Higher plant mitochondria. Plant Cell 11:571–585PubMedGoogle Scholar
  24. Michel H (1998) The mechanism of proton pumping by cytochrome c oxidase. Proc Natl Acad Sci USA 95: 12819–12824PubMedCrossRefGoogle Scholar
  25. Mitchell P (1961) Coupling of phosphorylation to electron and proton transfer by a chemi-osmotic type of mechanism. Nature 191: 144–148PubMedCrossRefGoogle Scholar
  26. Mitchell P (1976) Possible molecular mechanisms of the pro-tonmotive function of cytochrome systems. J Theor Biol 62: 327–367PubMedCrossRefGoogle Scholar
  27. Considine M, Daley DO and Whelan J (2001)The expression of alternative oxidase and uncoupling protein during fruit ripening in mango. Plant Physiol 126:1619–1629PubMedCrossRefGoogle Scholar
  28. Navet R, Jarmuszkiewicz W, Almeida AM, Sluse-Goffart CM and Sluse FE (2003) Energy conservation and dissipation in mitochondria from developing tomato fruit of ethylene defective mutants failing normal ripening. The effect of ethephon, a chemical precursor of ethylene. J Bioenerg Biomembr 35: 157–168PubMedCrossRefGoogle Scholar
  29. Rasmusson AG, Heiser V, Zabaleta E, Brennicke A and Grohmann L (1998) Physiological, biochemical and molecular aspects of mitochondrial complex I in plants. Biochim Biophys Acta 1364: 101–111PubMedCrossRefGoogle Scholar
  30. Saraste M (1999) Oxidative phosphorylation at the fin de siecle. Science 283:1488–1493PubMedCrossRefGoogle Scholar
  31. Sluse FE (1996) Mitochondrial metabolite carrier family, topology, structure and functional properties: an overview. Acta Biochem Polonica 43: 349–360Google Scholar
  32. Sluse FE and Jarmuszkiewicz W (1998) Alternative oxidase in the branched mitochondrial respiratory network: an overview on structure, function, regulation, and role. Braz J Med Biol Res 31:733–747PubMedCrossRefGoogle Scholar
  33. Sluse FE and Jarmuszkiewicz W (2000) Activity and functional interaction of alternative oxidase and uncoupling protein in mitochondria from tomato fruit. Braz J Med Biol Res 33: 259–268PubMedCrossRefGoogle Scholar
  34. Sluse FE and Jarmuszkiewicz W (2002) Uncoupling proteins outside the animal and plant kingdoms: functional and evolutionary aspects. FEBS Lett 510: 117–120PubMedCrossRefGoogle Scholar
  35. Sluse FE, Almeida AM, Jarmuszkiewicz W and Vercesi AE (1998) Free fatty acids regulate the uncoupling protein and the alternative oxidase activities in plant mitochondria. FEBS Lett 433: 237–240PubMedCrossRefGoogle Scholar
  36. Soole KL and Menz RI (1995) Functional molecular aspects of the NADH dehydrogenases of plant mitochondria. J Bioenerg Biomembr 27: 397–406PubMedCrossRefGoogle Scholar
  37. Tielens AG, Rotte C, van Hellemond JJ and Martin W (2002) Mitochondria as we don’t know them. Trends Biochem Sci 27:564–572PubMedCrossRefGoogle Scholar
  38. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R and Yoshikawa S (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 272: 1136–1144PubMedCrossRefGoogle Scholar
  39. Winkler E and Klingenberg M (1994) Effect of fatty acids on H+ transport activity of the reconstituted uncoupling protein. J Biol Chem 269: 2508–2515PubMedGoogle Scholar
  40. Van den Bergen CWM, Wagner AM, Krab K and Moore AL (1994) The relationship between electron flux and the redox poise of the quinone pool in plant mitochondria. Eur J Biochem 226: 1071–1078PubMedCrossRefGoogle Scholar
  41. Vedel F, Lalanne E, Sabar M, Chetrit P and De Paepe R (1999) The mitochondrial respiratory chain and ATP synthase complexes: composition, structure and mutational studies. Plant Physiol Biochem 37: 629–643CrossRefGoogle Scholar
  42. Vercesi AE, Martins IS, Silva MAP, Leite HMF, Cuccovia IM and Chaimovich H (1995) PUMPing plants. Nature 375: 24CrossRefGoogle Scholar
  43. Yasuda R, Noji H, Jr, Kinosita K and Yoshida M (1998) Fl-ATPase is a highly efficient molecular motor that rotates with discrete 120 degree steps. Cell 93: 1117–1124PubMedCrossRefGoogle Scholar
  44. Zhang Z, Huang L, Shulmeister VM, Chi YI, Kim KK, Hung LW, Crofts AR, Berrt EA and Kim SH (1998) Electron transfer by domain movement in cytochrome bc x. Nature 392: 677–684PubMedCrossRefGoogle Scholar
  45. Zhou Y, Duncan TM and Cross RL (1997) Subunit rotation in Escherichia coli F0F1-ATP synthase during oxidative phos­phorylation. Proc Natl Acad Sci USA 94: 10583–10587PubMedCrossRefGoogle Scholar
  46. Zottini M and Zannoni D (1993) The use of fura-2 fluorescence to monitor the movement of free calcium ions into the matrix of plant mitochondria (Pisum sativum and Helianthus tuberosus). Plant Physiol 102: 573–578PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2004

Authors and Affiliations

  • Francis E. Sluse
    • 1
  • Wieslawa Jarmuszkiewicz
    • 2
  1. 1.Laboratory of Bioenergetics, Centre of Oxygen Research and Development, Department of Life Sciences, Institute of Chemistry B6cUniversity of LiegeLiegeBelgium
  2. 2.Laboratory of Bioenergetics, Institute of Molecular Biology and BiotechnologyAdam Mickiewicz UniversityPoznanPoland

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