Light-responsive metabolite and transcript levels are maintained following a dark-adaptation period in leaves of Arabidopsis thaliana

New Phytologist

Volumn 195, Issue 1, 2012, Pages 136-148

  Florez Sarasa, Igor ^a   Araújo, Wagner L ^b,c   Wallström, Sabá V ^d   Rasmusson, Allan G ^d   Fernie, Alisdair R ^b   Ribas Carbo, Miquel ^a  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^d LUND UNIVERSITY   (Sweden)

Author keywords

Arabidopsis thaliana; Isotope fractionation; Light; Oxygen metabolites; Respiration

Indexed keywords

OXYGEN;

CYTOCHROME; DICOTYLEDON; ISOTOPIC FRACTIONATION; LEAF; LIGHT AVAILABILITY; LIGHT EFFECT; LIGHT INTENSITY; METABOLITE; OXYGEN ISOTOPE; RESPIRATION;

ARABIDOPSIS; ARTICLE; CELL RESPIRATION; DARKNESS; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; PLANT LEAF;

ARABIDOPSIS; CELL RESPIRATION; DARKNESS; GENE EXPRESSION REGULATION, PLANT; LIGHT; OXYGEN; PLANT LEAVES;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84861480436     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2012.04153.x     Document Type: Article

References (64)

1. Araújo WL, Nunes-Nesi A, Trenkamp S, Bunik VI, Fernie AR. 2008. Inhibition of 2-oxoglutarate dehydrogenase in potato tuber suggests the enzyme is limiting for respiration and confirms its importance in nitrogen assimilation. Plant Physiology 148: 1782-1796.
2. Atkin OK, Millar AH, Gardeström P, Day DA. 2000. Photosynthesis, carbohydrate metabolism and respiration in leaves of higher plants. In: Leegood RC, Sharkey TD, von Caemmerer S, eds. Photosynthesis: physiology and metabolism. Dordrecht, the Netherlands: Kluwer Academic Publishers, 153-175.
3. Atkin OK, Seibke K, Evans JR. 1998. Relationship between the inhibition of leaf respiration by light and enhancement of leaf dark respiration following light treatment. Australian Journal of Plant Physiology 25: 437-443.
4. Atkin OK, Westbeek MHM, Cambridge ML, Lambers H, Pons TL. 1997. Leaf respiration in light and darkness: a comparison of slow- and fast-growing Poa species. Plant Physiology 113: 961-965.
5. 2 gas exchange in illuminated higher plant cells. Evidence for light inhibition of substrate decarboxylations. Planta 183: 150-157.
6. Azcon-Bieto J, Lambers H, Day DA. 1983. Effect of photosynthesis and carbohydrate status on respiratory rates and the involvement of the alternative pathway in leaf respiration. Plant Physiology 72: 598-603.
7. 2 production by respiration in darkened and illuminated leaves. Plant Physiology 71: 574-581.
8. Bartoli CG, Gomez F, Gergoff G, Guiamet JJ, 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.
9. Bauwe H, Hegemann M, Fernie AR. 2010. Photorespiration: players, partners and origin. Trends in Plant Science 15: 330-336.
10. Budde RJA, Randall DD. 1990. Pea leaf mitochondrial PDH complex is inactivated invivo in a light-dependent manner. Proceedings of the National Academy of Sciences, USA 87: 673-676.
11. Bykova NV, Keerberg O, Pärnik T, Bauwe H, Gardeström P. 2005. Interaction between photorespiration and respiration in transgenic potato plants with antisense reduction in glycine decarboxylase. Planta 222: 130-140.
12. 2 exchange in leaves in the light. Plant Physiology 66: 302-307.
13. Carrari F, Nunes-Nesi A, Gibon Y, Lytovchenko A, Ehlers-Loureiro M, Fernie AR. 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.
14. Dry IB, Day DA, Wiskich JT. 1983. Preferential oxidation of glycine by the respiratory chain of pea leaf mitochondria. FEBS Letters 158: 154-158.
15. Dutilleul C, Driscoll S, Cornic G, De Paepe R, Foyer CH, Noctor G. 2003. Functional mitochondrial complex I is required for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiology 131: 264-275.
16. Dutilleul C, Lelarge C, Prioul JL, De Paepe R, Foyer CH, Noctor G. 2005. Mitochondria-driven changes in leaf NAD status exert a crucial influence on the control of nitrate assimilation and the integration of carbon and nitrogen metabolism. Plant Physiology 139: 64-78.
17. Escobar MA, Franklin KA, Svensson AS, Salter MG, Whitelam GC, Rasmusson AG. 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.
18. Florez-Sarasa I, Flexas J, Rasmusson AG, Umbach AL, Siedow JN, Ribas-Carbo M. 2011. Invivo cytochrome and alternative pathway respiration in leaves of Arabidopsis thaliana plants with altered alternative oxidase under different light conditions. Plant, Cell & Environment 34: 1373-1383.
19. Florez-Sarasa I, Ostaszewska M, Galle A, Flexas J, Rychter AM, 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.
20. Florez-Sarasa ID, Bouma TJ, 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.
21. Foyer CH, Noctor G, Hodges M. 2011. Respiration and nitrogen assimilation: targeting mitochondria-associated metabolism as a means to enhance nitrogen use efficiency. Journal of Experimental Botany 62: 1467-1482.
22. 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.
23. Gardeström P, Igamberdiev AU, Raghavendra AS. 2002. Mitochondrial functions in the light and significance to carbon-nitrogen interactions. In: Foyer CH, Noctor G, eds. Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism, vol. 12. Dordrect, the Netherlands: Kluwer Academic Publishers, 151-172.
24. Gibon Y, Usadel B, Blaesing OE, Kamlage B, Hoehne M, Trethewey R, Stitt M. 2006. Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biology 7: R76.
25. Guy RD, Berry JA, Fogel ML, Hoering TC. 1989. Differential fractionation of oxygen isotopes by cyanide-resistant and cyanide-sensitive respiration in plants. Planta 177: 483-491.
26. Hurry V, Igamberdiev AU, Keerberg O, Pärnik T, Atkin OK, 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: Lambers H, Ribas-Carbo M, eds. Plant respiration: from cell to ecosystem, vol. 18. Advances in photosynthesis and respiration series. Dordrecht, the Netherlands: Springer, 43-61.
27. Igamberdiev AU, Gardeström P. 2003. Regulation of NAD- and NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleosides in mitochondria and cytosol of pea leaves. Biochimica et Biophysica Acta 1606: 117-125.
28. Igamberdiev AU, Romanowska E, Gardeström P. 2001. Photorespiratory flux and mitochondrial contribution to energy and redox balance of barley leaf protoplasts in the light and during light-dark transitions. Journal of Plant Physiology 158: 1325-1332.
29. Juszczuk IM, Flexas J, Szal B, Dabrowska Z, Ribas-Carbo M, Rychter AM. 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.
30. Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmuller E, Dormann P, Weckwerth W, Gibon Y, Stitt M et al. 2005. GMD@CSB.DB: the Golm metabolome database. Bioinformatics 21: 1635-1638.
31. 2 concentrations. Plant Physiology 102: 947-955.
32. Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR. 2006. Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols 1: 387-396.
33. Liu YJ, Nunes-Nesi A, Wallström SV, Lager I, Michalecka AM, Norberg FE, Widell S, Fredlund KM, Fernie AR, Rasmusson AG. 2009. A redox-mediated modulation of stem bolting in transgenic Nicotiana sylvestris differentially expressing the external mitochondrial NADPH dehydrogenase. Plant Physiology 150: 1248-1259.
34. Maurino VG, Peterhänsel C. 2010. Photorespiration: current status and approaches for metabolic engineering. Current Opinion in Plant Biology 13: 248-255.
35. Michalecka AM, Svensson AS, Johansson FI, Agius SC, Johanson U, Brennicke A, Binder S, Rasmusson AG. 2003. Arabidopsis genes encoding mitochondrial type II NAD(P)H dehydrogenases have different evolutionary origin and show distinct responses to light. Plant Physiology 133: 642-652.
36. Noctor G, De Paepe R, Foyer CH. 2007. Mitochondrial redox biology and homeostasis in plants. Trends in Plant Science 12: 125-134.
37. Noguchi K. 2005. Effects of light intensity and carbohydrate status on leaf and root respiration. In: Lambers H, Ribas-Carbo M, eds. Plant respiration: from cell to ecosystem, vol. 18. Advances in photosynthesis and respiration series. Dordrecht, the Netherlands: Springer, 63-83.
38. Noguchi K, Go CS, 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, Yoshida K. 2008. Interaction between photosynthesis and respiration in illuminated leaves. Mitochondrion 8: 87-99.
40. Nunes-Nesi A, Araújo WL, Fernie AR. 2011. Targeting mitochondrial metabolism and machinery as a means to enhance photosynthesis. Plant Physiology 155: 101-107.
41. Nunes-Nesi A, Carrari F, Gibon Y, Sulpice R, Lytovchenko A, Fisahn J, Graham J, Ratcliffe RG, Sweetlove LJ, Fernie AR. 2007a. Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. The Plant Journal 50: 1093-1106.
42. Nunes-Nesi A, Carrari F, Lytovchenko A, Smith AMO, Ratcliffe RG, Sweetlove LJ, Fernie AR. 2005. Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiology 137: 611-622.
43. Nunes-Nesi A, Sweetlove LJ, Fernie AR. 2007b. Operation and function of the tricarboxylic acid cycle in the illuminated leaf. Physiologia Plantarum 129: 45-56.
44. Padmasree K, Padmavathi L, Raghavendra AS. 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.
45. 2 concentrations and irradiances. Plant, Cell & Environment 30: 1535-1544.
46. Popov VN, Eprintsev AT, Fedorin DN, Igamberdiev AU. 2010. Succinate dehydrogenase in Arabidopsis thaliana is regulated by light via phytochrome A. FEBS Letters 584: 199-202.
47. Raghavendra AS, Padmasree K. 2003. Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends in Plant Science 8: 546-553.
48. Rasmusson AG, Escobar MA. 2007. Light and diurnal regulation of plant respiratory gene expression. Physiologia Plantarum 129: 57-67.
49. Reddy MM, Vani T, Raghavendra AS. 1991. Light enhanced dark respiration in mesophyll protoplasts from leaves of pea. Plant Physiology 96: 1368-1371.
50. Ribas-Carbo M, Lennon AM, Robinson SA, Giles L, Berry JA, Siedow JN. 1997. The regulation of electron partitioning between the cytochrome and alternative pathways in soybean cotyledon and root mitochondria. Plant Physiology 113: 903-911.
51. Ribas-Carbo M, Robinson SA, Giles L. 2005. The application of the oxygen-isotope technique to assess respiratory pathway partitioning. In: Lambers H, Ribas-Carbo M, eds. Plant respiration: from cell to ecosystem, vol. 18. Advances in photosynthesis and respiration series. Dordrecht, the Netherlands: Springer, 31-42.
52. Ribas-Carbo M, Robinson SA, Gonzalez-Meler MA, Lennon AM, Giles L, Siedow JN, Berry JA. 2000. Effects of light on respiration and oxygen isotope fractionation in soybean cotyledons. Plant, Cell & Environment 23: 983-989.
53. Schauer N, Steinhauser D, Strelkov S, Schomburg D, Allison G, Moritz T, Lundgren K, Roessner-Tunali U, Forbes MG, Willmitzer L et al. 2005. GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Letters 579: 1332-1337.
54. Sweetlove LJ, Lytovchenko A, Morgan M, Nunes-Nesi A, Taylor NL, Baxter CJ, Eickmeier I, Fernie AR. 2006. Mitochondrial uncoupling protein is required for efficient photosynthesis. Proceedings of the National Academy of Sciences, USA 103: 19587-19592.
55. Tcherkez G, Cornic G, Bligny R, Gout E, Ghashghaie J. 2005. Invivo respiratory metabolism of illuminated leaves. Plant Physiology 138: 1596-1606.
56. 2 conditions. Proceedings of the National Academy of Sciences, USA 105: 797-802.
57. Tovar-Mendez A, Miernyk JA, Randall DD. 2003. Regulation of pyruvate dehydrogenase complex activity in plant cells. European Journal of Biochemistry 270: 1043-1049.
58. Urbanczyk-Wochniak E, Baxter C, Kolbe A, Kopka J, Sweetlove LJ, Fernie AR. 2005. Profiling of diurnal patterns of metabolite and transcript abundance in potato (Solanum tuberosum) leaves. Planta 221: 891-903.
59. Xue X, Gauthier DA, Turpin DH, Weger HG. 1996. Interactions between photosynthesis and respiration in the green alga Chlamydomonas reinhardtii. Characterization of light-enhanced dark respiration. Plant Physiology 112: 1005-1014.
60. 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.
61. 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.
62. Yoshida K, Watanabe CK, Hachiya T, Tholen D, Shibata M, Terashima I, Noguchi K. 2011. Distinct responses of the mitochondrial respiratory chain to long- and short-term high-light environments in Arabidopsis thaliana. Plant, Cell & Environment 34: 618-628.
63. 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.
64. Zell MB, Fahnenstich H, Maier A, Saigo M, Voznesenskaya EV, Edwards GE, Andreo C, Schleifenbaum F, Zell C, Drincovich MF et al. 2010. Analysis of Arabidopsis with highly reduced levels of malate and fumarate sheds light on the role of these organic acids as storage carbon molecules. Plant Physiology 152: 1251-1262.