In vivo cytochrome and alternative pathway respiration in leaves of Arabidopsis thaliana plants with altered alternative oxidase under different light conditions

Plant, Cell and Environment

Volumn 34, Issue 8, 2011, Pages 1373-1383

  Florez Sarasa, Igor ^a   Flexas, Jaume ^a   Rasmusson, Allan G ^b   Umbach, Ann L ^c   Siedow, James N ^c   Ribas Carbo, Miquel ^a  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^b LUND UNIVERSITY   (Sweden)

^c DUKE UNIVERSITY   (United States)

Author keywords

High light; Oxygen isotope fractionation; Photoinhibition; Plant mitochondria

Indexed keywords

ALTERNATIVE OXIDASE; CYTOCHROME; MITOCHONDRIAL PROTEIN; OXIDOREDUCTASE; VEGETABLE PROTEIN;

CYTOCHROME; DICOTYLEDON; ENZYME ACTIVITY; GENE EXPRESSION; ISOTOPIC FRACTIONATION; LEAF; LIGHT EFFECT; MITOCHONDRION; OXYGEN ISOTOPE; PHOTOINHIBITION; PHOTOSYNTHESIS; RESPIRATION;

ARABIDOPSIS; ARTICLE; ELECTRON TRANSPORT; EVAPOTRANSPIRATION; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; MITOCHONDRION; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; PLANT LEAF; TRANSGENIC PLANT;

ARABIDOPSIS; CYTOCHROMES; ELECTRON TRANSPORT; GENE EXPRESSION REGULATION, PLANT; LIGHT; METABOLIC NETWORKS AND PATHWAYS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OXIDOREDUCTASES; PHOTOSYNTHESIS; PLANT LEAVES; PLANT PROTEINS; PLANT TRANSPIRATION; PLANTS, GENETICALLY MODIFIED; STRESS, PHYSIOLOGICAL;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 79960265167     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2011.02337.x     Document Type: Article

References (67)

1. Arnholdt-Schmitt B., Costa J.H. & Fernandes de Melo D. (2006) AOX - a functional marker for efficient cell reprogramming under stress? Trends in Plant Science 11, 281-287.
2. Bartoli C.G., Gomez F., Gergoff G., Guiamet J.J. & Puntarulo S. (2005) Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions. Journal of Experimental Botany 56, 1269-1276.
3. Bartoli C.G., Yu J., Gomez F., Fernandez L., McIntosh L. & Foyer C.H. (2006) Inter- relationships between light and respiration in the control of ascorbic acid synthesis and accumulation in Arabidopsis thaliana leaves. Journal of Experimental Botany 57, 1621-1631.
4. Bauwe H., Hegemann M. & Fernie A.R. (2010) Photorespiration: players, partners and origin. Trends in Plant Science 15, 330-336.
5. Carrari F., Nunes-Nesi A., Gibon Y., Lytovchenko A., Ehlers-Loureiro M. & Fernie A.R. (2003) Reduced expression of aconitase results in an enhanced rate of photosynthesis and marked shifts in carbon partitioning in illuminated leaves of wild species tomato. Plant Physiology 133, 1322-1335.
6. Clifton R., Millar A.H. & Whelan J. (2006) Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. Biochimica et Biophysica Acta 1757, 730-741.
7. Considine M.J., Goodman M., Echtay K.S., Laloi M., Whelan J., Brand M.D. & Sweetlove L.J. (2002) Superoxide stimulates a proton leak in potato mitochondria that is related to the activity of uncoupling protein. Journal of Biological Chemistry 278, 22298-22302.
8. Dry I.B., Day D.A. & Wiskich J.T. (1983) Preferential oxidation of glycine by the respiratory chain of pea leaf mitochondria. FEBS Letters 158, 154-158.
9. Elhafez D., Murcha M.W., Clifton R., Soole K.L., Day D.A. & Whelan J. (2006) Characterization of mitochondrial alternative NAD(P)H dehydrogenases in Arabidopsis: intraorganelle location and expression. Plant and Cell Physiology 47, 43-54.
10. Elthon T.E., Nickels R.L. & McIntosh L. (1989) Monoclonal antibodies to the alternative oxidase of higher plant mitochondria. Proceedings of the National Academy of Sciences of the United States of America 84, 8399-8403.
11. Escobar M.A., Franklin K.A., Svensson A.S., Salter M.G., Whitelam G.C. & Rasmusson A.G. (2004) Light regulation of the Arabidopsis respiratory chain. Multiple discrete photoreceptor responses contribute to induction of type II NAD(P)H dehydrogenase genes. Plant Physiology 136, 2710-2721.
12. Fiorani F., Umbach A.L. & Siedow J.N. (2005) The alternative oxidase of plant mitochondria is involved in the acclimation of shoot growth at low temperature. A study of Arabidopsis AOX1a transgenic plants. Plant Physiology 139, 1795-1805.
13. 2 in Arabidopsis thaliana. New Phytologist 175, 501-511.
14. Florez-Sarasa I.D., Bouma T.J., Medrano H., Azcon-Bieto J. & Ribas-Carbo M. (2007) Contribution of the cytochrome and alternative pathways to growth respiration and maintenance respiration in Arabidopsis thaliana. Physiologia Plantarum 129, 143-151.
15. Florez-Sarasa I., Ostaszewska M., Galle A., Flexas J., Rychter A.M. & Ribas-Carbo M. (2009) Changes of alternative oxidase activity, capacity and protein content in leaves of Cucumis sativus wild-type and MSC16 mutant grown under different light intensities. Physiologia Plantarum 137, 419-426.
16. Galle A., Haldimann P. & Feller U. (2007) Photosynthetic performance and water relations in young pubescent oak (quercus pubescens) trees during drought stress and recovery. New Phytologist 174, 799-810.
17. Genty B., Briantais J.M. & Baker N.R. (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87-92.
18. Giraud E., Ho L.H., Clifton R., etal. (2008) The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiology 147, 595-610.
19. Gonzalez-Meler M.A., Ribas-Carbo M., Giles L. & Siedow J.N. (1999) The effect of growth and measurement temperature on the activity of the alternative respiratory pathway. Plant Physiology 120, 765-772.
20. Gonzalez-Meler M.A., Giles L., Thomas R.B. & Siedow J.N. (2001) Metabolic regulation of leaf respiration and alternative pathway activity in response to phosphate supply. Plant, Cell & Environment 24, 205-215.
21. Grant N.M., Miller R.E., Watling J.R. & Robinson S.A. (2008) Synchronicity of thermogenic activity, alternative pathway respiratory flux, AOX protein content, and carbohydrates in receptacle tissues of sacred lotus during floral development. Journal of Experimental Botany 59, 705-714.
22. Guy R.D. & Vanlerberghe G.C. (2005) Partitioning of respiratory electrons in the dark in leaves of transgenic tobacco with modified levels of alternative oxidase. Physiologia Plantarum 125, 171-180.
23. Hoefnagel M.H.N., Millar A.H., Wiskich J.T. & Day D.A. (1995) Cytochrome and alternative respiratory pathways compete for electrons in the presence of pyruvate in soybean mitochondria. Archives of Biochemistry and Biophysics 318, 394-400.
24. Hurry V., Igamberdiev A.U., Keerberg O., Pärnik T., Atkin O.K., Zaragoza-Castells J. & Gardeström P. (2005) Respiration in photosynthetic cells: gas exchange components, interactions with photorespiration and the operation of mitochondria in the light. In Plant Respiration: From Cell to Ecosystem, Vol. 18. Advances in Photosynthesis and Respiration Series (eds H. Lambers & M. Ribas-Carbo), pp. 43-61. Springer, Dordrecht, The Netherlands.
25. Juszczuk I.M., Flexas J., Szal B., Dabrowska Z., Ribas-Carbo M. & Rychter A.M. (2007) Effect of mitochondrial genome rearrangement on respiratory activity, photosynthesis, photorespiration and energy status of MSC16 cucumber (Cucumis sativus) mutant. Physiologia Plantarum 131, 527-541.
26. Krömer S. (1995) Respiration during photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 46, 45-70.
27. 2 concentrations. Plant Physiology 102, 947-955.
28. Lambers H., Robinson S.A. & Ribas-Carbo M. (2005) Regulation of respiration in vivo. In Plant Respiration: From Cell to Ecosystem, Vol. 18. Advances in Photosynthesis and Respiration Series (eds H. Lambers & M. Ribas-Carbo), pp. 1-15. Springer, Dordrecht, The Netherlands.
29. Lennon A.M., Neuenschwander U.H., Ribas-Carbo M., Giles L., Ryals J.A. & Siedow J.N. (1997) The effects of salicylic acid and tobacco mosaic virus infection on the alternative oxidase of tobacco. Plant Physiology 115, 783-791.
30. McDonald A.E., Sieger S.M. & Vanlerberghe G.C. (2002) Methods and approaches to study plant mitochondrial alternative oxidase. Physiologia Plantarum 116, 135-143.
31. Maxwell K. & Johnson G.N. (2000) Chlorophyll fluorescence - a practical guide. Journal of Experimental Botany 51, 659-668.
32. Maxwell D.P., Wang Y. & McIntosh L. (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proceedings of the National Academy of Sciences of the United States of America 96, 8271-8276.
33. Millar A.H., Wiskich J.T., Whelan J. & Day D.A. (1993) Organic acid activation of the alternative oxidase of plant mitochondria. FEBS Letters 329, 259-262.
34. Møller I.M. (2001) Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Physiology and Plant Molecular Biology 52, 561-591.
35. Møller I.M., Berczi A., van der Plas L.H.W. & Lambers H. (1988) Measurement of the activity and capacity of the alternative pathway in intact plant tissues: identification of problems and possible solutions. Physiologia Plantarum 72, 642-649.
36. Moore A.L. & Siedow J.N. (1991) The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria. Biochimica et Biophysica Acta 1059, 121-140.
37. Noguchi K. (2005) Effects of light intensity and carbohydrate status on leaf and root respiration. In Plant Respiration: From Cell to Ecosystem, Vol. 18. Advances in Photosynthesis and Respiration Series (eds H. Lambers & M. Ribas-Carbo), pp. 63-83. Springer, Dordrecht, The Netherlands.
38. Noguchi K., Go C.S., Terashima I., Ueda S. & Yoshinari T. (2001) Activities of the cyanide-resistant respiratory pathway in leaves of sun and shade species. Australian Journal of Plant Physiology 28, 27-35.
39. Noguchi K., Taylor N.L., Millar A.H., Lambers H. & Day D.A. (2005) Response of mitochondria to light intensity in the leaves of sun and shade species. Plant, Cell & Environment 28, 760-771.
40. Padmasree K., Padmavathi L. & Raghavendra A.S. (2002) Essentiality of mitochondrial oxidative metabolism for photosynthesis: optimization of carbon assimilation and protection against photoinhibition. Critical Reviews in Biochemistry and Molecular Biology 37, 71-119.
41. Popov V.N., Eprintsev A.T., Fedorin D.N. & Igamberdiev A.U. (2010) Succinate dehydrogenase in Arabidopsis thaliana is regulated by light via phytochrome A. FEBS Letters 584, 199-202.
42. Purvis A.C. & Shewfelt R.L. (1993) Does the alternative pathway ameliorate chilling injury in sensitive plant tissues. Physiologia Plantarum 88, 712-718.
43. Rasmusson A.G. & Escobar M.A. (2007) Light and diurnal regulation of plant respiratory gene expression. Physiologia Plantarum 129, 57-67.
44. Rasmusson A.G., Geisler D.A. & Møller I.M. (2008) The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 8, 47-60.
45. Rasmusson A.G., Fernie A.R. & van Dongen J.T. (2009) Alternative oxidase: a defence against metabolic fluctuations? Physiologia Plantarum 137, 371-382.
46. Ribas-Carbo M., Berry J.A., Yakir D., Giles L., Robinson S.A., Lennon A.M. & Siedow J.N. (1995) Electron partitioning between the cytochrome and alternative pathways in plant mitochondria. Plant Physiology 109, 829-837.
47. Ribas-Carbo M., Lennon A.M., Robinson S.A., Giles L., Berry J.A. & Siedow J.N. (1997) The regulation of electron partitioning between the cytochrome and alternative pathways in soybean cotyledon and root mitochondria. Plant Physiology 113, 903-911.
48. Ribas-Carbo M., Robinson S.A., Gonzalez-Meler M.A., Lennon A.M., Giles L., Siedow J.N. & Berry J.A. (2000) Effects of light on respiration and oxygen isotope fractionation in soybean cotyledons. Plant, Cell & Environment 23, 983-989.
49. Ribas-Carbo M., Taylor N.L., Giles L., Busquets S., Finnegan P.M., Day D.A., Lambers H., Medrano H., Berry J.A. & Flexas J. (2005) Effects of water stress on respiration in soybean leaves. Plant Physiology 139, 466-473.
50. Ribas-Carbo M., Giles L., Flexas J., Briggs W. & Berry J.A. (2008) Phytochrome-driven changes in respiratory electron transport partitioning in soybean (Glycine max. L.) cotyledons. Plant Biology 10, 281-287.
51. Saisho D., Nambara E., Naito S., Tsutsumi N., Hirai A. & Nakazono M. (1997) Characterization of gene family for alternative oxidase from Arabidopsis thaliana. Plant Molecular Biology 35, 585-596.
52. Smirnoff N. (2000) Ascorbate biosynthesis and function in photoprotection. Philosophical Transactions of the Royal Society of London B 355, 1455-1464.
53. Smith C.A., Melino V.J., Sweetman C. & Soole K.L. (2009) Manipulation of alternative oxidase can influence salt tolerance in Arabidopsis thaliana. Physiologia Plantarum 137, 459-472.
54. Svensson Å.S. & Rasmusson A.G. (2001) Light-dependent gene expression for proteins in the respiratory chain of potato leaves. The Plant Journal 28, 73-82.
55. Umbach A.L. & Siedow J.N. (1993) Covalent and noncovalent dimers of the cyanide-resistant oxidase protein in higher plant mitochondria and their relationship to enzyme activity. Plant Physiology 103, 845-854.
56. Umbach A.L., Wiskich J.T. & Siedow J.N. (1994) Regulation of alternative oxidase kinetics by pyruvate and intermolecular disulfide bond redox status in soybean seedling mitochondria. FEBS Letters 348, 181-184.
57. Umbach A.L., Fiorani F. & Siedow J.N. (2005) Characterization of transformed Arabidopsis with altered alternative oxidase levels and analysis of effects on reactive oxygen species in tissue. Plant Physiology 139, 1806-1820.
58. Van Aken O., Giraud E., Clifton R. & Whelan J. (2009) Alternative oxidase: a target and regulator of stress responses. Physiologia Plantarum 137, 354-361.
59. Vanlerberghe G.C., Cvetkovska M. & Wang J. (2009) Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase? Physiologia Plantarum 137, 392-406.
60. Vercesi A.E. (2001) The discovery of an uncoupling mitochondrial protein in plants. Bioscience Reports 21, 195-200.
61. Vidal G., Ribas-Carbo M., Garmier M., Dubertret G., Rasmusson A.G., Mathieu C., Foyer C.H. & De Paepe R. (2007) Lack of respiratory chain complex I impairs alternative oxidase engagement and modulates redox signaling during elicitor-induced cell death in tobacco. The Plant Cell 19, 640-655.
62. Watanabe C.K., Hachiya T., Terachima I. & Noguchi K. (2008) The lack of alternative oxidase at low temperature leads to a disruption of the balance in carbon and nitrogen metabolism, and to an up-regulation of antioxidant defence systems in Arabidopsis thaliana leaves. Plant, Cell & Environment 31, 1190-1202.
63. Yoshida K. & Noguchi K. (2009) Differential gene expression profiles of the mitochondrial respiratory components in illuminated Arabidopsis leaves. Plant and Cell Physiology 50, 1449-1462.
64. Yoshida K., Terashima I. & Noguchi K. (2006) Distinct roles of the cytochrome pathway and alternative oxidase in leaf photosynthesis. Plant and Cell Physiology 47, 22-31.
65. Yoshida K., Terashima I. & Noguchi K. (2007) Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. Plant and Cell Physiology 48, 606-614.
66. Yoshida K., Watanabe C., Kato Y., Sakamoto W. & Noguchi K. (2008) Influence of chloroplastic photo-oxidative stress on mitochondrial alternative oxidase capacity and respiratory properties: a case study with Arabidopsis yellow variegated 2. Plant and Cell Physiology 49, 592-603.
67. Yoshida K., Shibata M., Terashima I. & Noguchi K. (2010) Simultaneous determination of in vivo plastoquinone and ubiquinone redox states by HPLC-based analysis. Plant and Cell Pysiology 51, 836-841.