Dynamic changes in the mitochondrial electron transport chain underpinning cold acclimation of leaf respiration

Plant, Cell and Environment

Volumn 31, Issue 8, 2008, Pages 1156-1169

  Armstrong, Anna F ^a   Badger, Murray R ^b   Day, David A ^d   Barthet, Michelle M ^d   Smith, Penelope M C ^d   Millar, A Harvey ^e   Whelan, Jim ^e   Atkin, Owen K ^c  

^a UNIVERSITY OF YORK   (United Kingdom)

^b LA TROBE UNIVERSITY   (Australia)

^c AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Alternative oxidase; Arabidopsis; Cytochrome oxidase; Gene expression; Temperature; Uncoupling protein

Indexed keywords

ALTERNATIVE OXIDASE; ARABIDOPSIS PROTEIN; CYTOCHROME C OXIDASE; MESSENGER RNA; OXIDOREDUCTASE; OXYGEN;

ACCLIMATION; CYTOCHROME; DICOTYLEDON; ELECTRON; ENZYME ACTIVITY; GENE EXPRESSION; MITOCHONDRION; PROTEIN; RESPIRATION; TEMPERATURE EFFECT;

ACCLIMATIZATION; ARABIDOPSIS; ARTICLE; CELL RESPIRATION; COLD; CYTOLOGY; ELECTRON TRANSPORT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MITOCHONDRION; PLANT LEAF; TEMPERATURE;

ACCLIMATIZATION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL RESPIRATION; COLD; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; GENE EXPRESSION REGULATION, PLANT; MITOCHONDRIA; OXIDOREDUCTASES; OXYGEN ISOTOPES; PLANT LEAVES; RNA, MESSENGER; TEMPERATURE;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 46949106176     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2008.01830.x     Document Type: Article

References (81)

1. Amthor J.S. (1994) Plant respiratory responses to the environment and their effects on the carbon balance. In Plant-Environment Interactions (ed. R.E. Wilkinson pp. 501 554. Marcel Dekker, New York, NY, USA.
2. Armstrong A.F., Logan D.C., O'Toole P., Tobin A.K. Atkin O.K. (2006) Heterogeneity of plant mitochondrial responses underpinning respiratory acclimation to the cold in Arabidopsis thaliana leaves. Plant, Cell & Environment 29, 940 949.
3. Atkin O.K. Day D.A. (1990) A comparison of the respiratory p rocesses and growth rates of selected alpine and lowland plant species. Australian Journal of Plant Physiology 17, 517 526.
4. Atkin O.K. Tjoelker M.G. (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science 8, 343 351.
5. Atkin O.K., Edwards E.J. Loveys B.R. (2000a) Response of root respiration to changes in temperature and its relevance to global warming. New Phytologist 147, 141 154.
6. Atkin O.K., Holly C. Ball M.C. (2000b) Acclimation of snow gum (Eucalyptus pauciflora) leaf respiration to seasonal and diurnal variations in temperature: the importance of changes in the capacity and temperature sensitivity of respiration. Plant, Cell & Environment 23, 15 26.
7. Atkin O.K., Zhang Q. Wiskich J.T. (2002) Effect of temperature on rates of alternative and cytochrome pathway respiration and their relationship with the redox poise of the quinone pool. Plant Physiology 128, 212 222.
8. Atkin O.K., Bruhn D., Hurry V.M. Tjoelker M.G. (2005) The hot and the cold: unravelling the variable response of plant respiration to temperature. Functional Plant Biology 32, 87 105.
9. Azcón-Bieto J. (1992) Relationships between photosynthesis and respiration in the dark in plants. In Trends in Photosynthesis Research (eds J. Barber, M.G. Guerrero H. Medrano pp. 241 253. Intercept Ltd, Andover, Hampshire, UK.
10. Azcón-Bieto J., Day D.A. Lambers H. (1983) Respiratory properties of developing bean and pea leaves. Australian Journal of Plant Physiology 10, 237 245.
11. Berry J.A. Raison J.K. (1981) Responses of macrophytes to temperature. In Physiological Plant Ecology I. Responses to the Physical Environment (eds O.L. Lange, P.S. Nobel, C.B. Osmond H. Zeigler pp. 277 338. Springer-Verlag, Berlin, Germany.
12. Billings W.D., Godfrey P.J., Chabot B.F. Bourque D.P. (1971) Metabolic acclimation to temperature in Arctic and alpine ecotypes of Oxyria digyna. Arctic and Alpine Research 3, 277 289.
13. Bolstad P.V., Reich P. Lee T. (2003) Rapid temperature acclimation of leaf respiration rates in Quercus alba and Quercus rubra. Tree Physiology 23, 969 976.
14. Campbell C., Atkinson L., Zaragosa-Castells J., Lundmark M., Atkin O. Hurry V. (2007) Acclimation of photosynthesis and respiration is asynchronous in response to changes in temperature regardless of plant functional group. New Phytologist 176, 375 389.
15. Clifton R., Lister R., Parker K.L., Sappl P.G., Elhafez D., Millar A.H., Day D.A. Whelan J 2005) Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Molecular Biology 58, 193 212.
16. 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. Biochim Biophys Acta - Bioenergetics 1757, 730 741.
17. Collier D.E. (1996) No difference in leaf respiration rates among temperate, subarctic, and arctic species grown under controlled conditions. Canadian Journal of Botany 74, 317 320.
18. Collier D.E. Cummins W.R. (1990) The effects of low growth and measurement temperature on the respiratory properties of five temperate species. Annals of Botany 65, 533 538.
19. Considine M.J., Daley D.O. Whelan J. (2001) The expression of alternative oxidase and uncoupling protein during fruit ripening in mango. Plant Physiology 126, 1619 1629.
20. Considine M.J., Goodman M., Echtay K.S., Laloi M., Whelan J., Brand M.D. Sweetlove L.J. (2003) Superoxide stimulates a proton leak in potato mitochondria that is related to the activity of uncoupling protein. Journal of Biological Chemistry 278, 22298 22302.
21. Covey-Crump E.M., Bykova N.V., Affourtit C., Hoefnagel M.H.N., Gardeström P. Atkin O.K. (2007) Temperature-dependent changes in respiration rates and redox poise of the ubiquinone pool in protoplasts and isolated mitochondria of potato leaves. Physiologia Plantarum 129, 174 184.
22. Czechowski T., Stitt M., Altmann T., Udvardi M.K. Scheible W.R. (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology 139, 5 17.
23. Day D.A. Lambers H. (1983) Regulation of glycolysis and electron transport in roots. Physiologia Plantarum 58, 155 160.
24. Elthon T.E., Stewart C.R., McCoy C.A. Bonner W.D. (1986) Alternative respiratory path capacity in plant mitochondria. Effect of growth temperature, the electrochemical gradient, and assay pH. Plant Physiology 80, 378 383.
25. 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.
26. Fitter A.H., Graves J.D., Self G.K., Brown T.K., Bogie D.S. Taylor K. (1998) Root production, turnover and respiration under two grassland types along an altitudinal gradient - influence of temperature and solar radiation. Oecologia 114, 20 30.
27. Florez-Sarasa I.D., Bouma T.J., Medrano H., Azcón-Bieto J. Ribas-Carbó M 2007) Contribution of the cytochrome and alternative pathways to growth respiration and maintenance respiration in Arabidopsis thaliana. Physiologia Plantarum 129, 143 151.
28. Forward D.F. (1960) Effect of temperature on respiration. In Encyclopedia of Plant Physiology, Vol. 12 (ed. W. Ruhland pp. 234 258. Springer-Verlag, Berlin, Germany.
29. Gonzàlez-Meler M.A., Ribas-Carbó 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.
30. Gutierres S., Sabar M., Lelandais C., Chétrit P., Diolez P., Degand H., Boutry M., Vedel F., de Kouchkovsky Y. De Paepe R. (1997) Lack of mitochondrial and nuclear-encoded subunits of complex I and alteration of the respiratory chain in Nicotiana sylvestris mitochondrial deletion mutants. Proceedings of the National Academy of Sciences of the United States of America 94, 3436 3441.
31. 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.
32. Guy R.D., Berry J.A., Fogel M.L. Hoering T.C. (1989) Differential fractionation of oxygen isotopes by cyanide-resistant and cyanide-sensitive respiration in plants. Planta 177, 483 491.
33. Henry B.K., Atkin O.K., Day D.A., Millar A.H., Menz R.I. Farquhar G.D. (1999) Calculation of the oxygen isotope discrimination factor for studying plant respiration. Australian Journal of Plant Physiology 26, 773 780.
34. Hoefnagel M.H.N. Wiskich J.T. (1998) Activation of the plant alternative oxidase by high reduction levels of the Q-pool and pyruvate. Archives of Biochemistry and Biophysics 335, 262 270.
35. 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.
36. Hoefnagel M.H.N., Rich P.R., Zhang Q. Wiskich J.T. (1997) Substrate kinetics of the plant mitochondrial alternative oxidase and the effects of pyruvate. Plant Physiology 115, 1145 1153.
37. Hoefnagel M.H.N., Atkin O.K. Wiskich J.T. (1998) Interdependence between chloroplasts and mitochondria in the light and the dark. Biochimica et Biophysica Acta - Bioenergetics 1366, 235 255.
38. Ito Y., Saisho D., Nakazono M., Tsutsumi N. Hirai A. (1997) Transcript levels of tandem-arranged alternative oxidase genes in rice are increased by low temperature. Gene 203, 121 129.
39. James W.O. (1953) Plant Respiration. Clarendon Press, Oxford, UK.
40. Kiener C.M. Bramlage W.J. (1981) Temperature effects on the activity of the alternative respiratory pathway in chill-sensitive Cucumis sativus. Plant Physiology 68, 1474 1478.
41. Kurimoto K., Millar A.H., Lambers H., Day D.A. Noguchi K. (2004) Maintenance of growth rate at low temperature in rice and wheat cultivars with a high degree of respiratory homeostasis is associated with a high efficiency of respiratory ATP production. Plant Cell Physiology 45, 1015 1022.
42. Laloi M., Klein M., Riesmeier J.W., Müller-Röber B., Fleury C., Bouillaud F. Ricquier D 1997) A plant cold-induced uncoupling protein. Nature 389, 135 136.
43. Lambers H., Szaniawski R.K. de Visser R. (1983) Respiration for growth, maintenance and ion uptake. An evaluation of concepts, methods, values and their significance. Physiologia Plantarum 58, 556 563.
44. Larigauderie A. Körner C. (1995) Acclimation of leaf dark respiration to temperature in alpine and lowland plant species. Annals of Botany 76, 245 252.
45. Lennon A.M., Pratt J., Leach G. Moore A.L. (1995) Developmental regulation of respiratory activity in pea leaves. Plant Physiology 107, 925 932.
46. Loveys B.R., Atkinson L.J., Sherlock D.J., Roberts R.L., Fitter A.H. Atkin O.K. (2003) Thermal acclimation of leaf and root respiration: an investigation comparing inherently fast- and slow-growing plant species. Global Change Biology 9, 895 910.
47. McNulty A.K. Cummins W.R. (1987) The relationship between respiration and temperature in leaves of the arctic plant Saxifraga cernua. Plant, Cell & Environment 10, 319 325.
48. Maia I.G., Benedetti C.E., Leite A., Turcinelli S.R., Vercesi A.E. Arruda P. (1998) AtPUMP: an Arabidopsis gene encoding a plant uncoupling mitochondrial protein. FEBS Letters 429, 403 406.
49. 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.
50. Millar A.H. Day D.A. (1997) Alternative solutions to radical problems. Trends in Plant Science 2, 289 290.
51. 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.
52. Millar A.H., Atkin O.K., Menz R.I., Henry B., Farquhar G. Day D.A. (1998) Analysis of respiratory chain regulation in roots of soybean seedlings. Plant Physiology 117, 1083 1093.
53. Millenaar F.F. Lambers H. (2003) The alternative oxidase: in vivo regulation and function. Plant Biology 5, 2 15.
54. Millenaar F.F., Benschop J.J., Wagner A.M. Lambers H. (1998) The role of the alternative oxidase in stabilizing the in vivo reduction state of the ubiquinone pool and the activation state of the alternative oxidase. Plant Physiology 118, 599 607.
55. Moore A.L. Siedow J.N. (1991) The regulation and nature of the cyanide resistant alternative oxidase of plant mitochondria. Biochim Biophys Acta - Bioenergetics 1059, 121 140.
56. 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.
57. Noguchi K.O., Taylor N.L., Millar A.H., Lambers H.A.N.S. Day D.A. (2005) Response of mitochondria to light intensity in the leaves of sun and shade species. Plant, Cell & Environment 28, 760 771.
58. 2 production in plant mitochondria. FEBS Letters 415, 87 90.
59. Purvis A.C. Shewfelt R.L. (1993) Does the alternative pathway ameliorate chilling injury in sensitive plant tissues? Physiologia Plantarum 88, 712 718.
60. Rasmusson A.G., Soole K.L. Elthon T.E. (2004) Alternative NAD(P)H dehydrogenases of plant mitochondria. Annual Review of Plant Biology 55, 23 39.
61. Ribas-Carbó 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.
62. Ribas-Carbó 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.
63. Ribas-Carbó M., Aroca R., Gonzàlez-Meler M.A., Irigoyen J.J. Sanchezdiaz M. (2000) The electron partitioning between the cytochrome and alternative respiratory pathways during chilling recovery in two cultivars of maize differing in chilling sensitivity. Plant Physiology 122, 199 204.
64. Ribas-Carbó 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.
65. Robinson S.A., Ribas-Carbó M., Yakir D., Giles L., Reuveni Y. Berry J.A. (1995) Beyond SHAM and cyanide - opportunities for studying the alternative oxidase in plant respiration using oxygen isotope discrimination. Australian Journal of Plant Physiology 22, 487 496.
66. Savitch L.V., Barker-Åstrom J., Ivanov A.G., Hurry V., Öquist G., Huner N.P.A. Gardeström P. (2001) Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity, associated with an increased reduction of the chloroplast stroma. Planta 214, 295 303.
67. Shane M.W., Cramer M.D., Funayama-Noguchi S., Cawthray G.R., Millar A.H., Day D.A. Lambers H. (2004) Developmental physiology of cluster-root carboxylate synthesis and exudation in harsh hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase. Plant Physiology 135, 549 560.
68. Sluse F.E. Jarmuszkiewicz W. (2002) Uncoupling proteins outside the animal and plant kingdoms: functional and evolutionary aspects. FEBS Letters 510, 117 120.
69. Smith A.M.O., Ratcliffe R.G. Sweetlove L.J. (2004) Activation and function of mitochondrial uncoupling protein in plants. Journal of Biological Chemistry 279, 51944 51952.
70. Stewart C.R., Martin B.A., Reding L. Cerwick S. (1990a) Respiration and alternative oxidase in corn seedlings during germination at different temperatures. Plant Physiology 92, 755 760.
71. Stewart C.R., Martin B.A., Reding L. Cerwick S. (1990b) Seedling growth, mitochondrial characteristics, and alternative respiratory capacity of corn genotypes differing in cold tolerance. Plant Physiology 92, 761 766.
72. Stupnikova I., Benamar A., Tolleter D., Grelet J., Borovskii G., Dorne A.J. Macherel D. (2006) Pea seed mitochondria are endowed with a remarkable tolerance to extreme physiological temperatures. Plant Physiology 140, 326 335.
73. Takumi S., Tomioka M., Eto K., Naydenov N. Nakamura C. (2002) Characterization of two non-homologous nuclear genes encoding mitochondrial alternative oxidase in common wheat. Genes Genetics Systems 77, 81 88.
74. Talts P., Pärnik T., Gardeström P. Keerberg O. (2004) Respiratory acclimation in Arabidopsis thaliana leaves at low temperature. Journal of Plant Physiology 161, 573 579.
75. Umbach A.L. Siedow J.N. (1993) Covalent and noncovalent dimers of the cyanide-resistant alternative oxidase protein in higher plant mitochondria and their relationship to enzyme activity. Plant Physiology 103, 845 854.
76. Umbach A.L. Siedow J.N. (1996) The reaction of the soybean cotyledon mitochondrial cyanide-resistant oxidase with sulfhydryl reagents suggests that α-keto acid activation involves the formation of a thiohemiacetal. Journal of Biological Chemistry 271, 25019 25026.
77. 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.
78. Vanlerberghe G.C. McIntosh L 1992) Lower growth temperature increases alternative pathway capacity and alternative oxidase protein in tobacco. Plant Physiology 100, 115 119.
79. Wagner A.M. Krab K. (1995) The alternative respiration pathway in plants. Role and regulation. Physiologia Plantarum 95, 318 325.
80. Xiong F.S., Mueller E.C. Day T.A. (2000) Photosynthetic and respiratory acclimation and growth response of Antarctic vascular plants to contrasting temperature regimes. American Journal of Botany 87, 700 710.
81. Yoshida S. Tagawa F. (1979) Alteration of the respiratory function in chill-sensitive callus due to low-temperature stress. I. Involvement of the alternative pathway. Plant Physiology 20, 1243 1250.