New insights into photorespiration obtained from metabolomics

Plant Biology

Volumn 15, Issue 4, 2013, Pages 656-666

  Florian, A ^a   Araujo W L ^b   Fernie, A R ^a  

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

^b FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

Author keywords

Metabolite profiles; Metabolomics; Photorespiration; Tricarboxylic acid cycle

Indexed keywords

NITROGEN; OXYGEN; RIBULOSEBISPHOSPHATE CARBOXYLASE;

ENZYME ACTIVITY; GENE EXPRESSION; GROWTH RATE; METABOLITE; OXYGEN; PHOTOSYNTHESIS; PHYTOCHEMISTRY; PROTEIN; RESPIRATION;

CELL RESPIRATION; CITRIC ACID CYCLE; LIGHT; METABOLISM; METABOLOMICS; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PLANT; RADIATION EXPOSURE; REVIEW;

CELL RESPIRATION; CITRIC ACID CYCLE; LIGHT; METABOLOMICS; NITROGEN; OXIDATION-REDUCTION; OXYGEN; PHOTOSYNTHESIS; PLANTS; RIBULOSE-BISPHOSPHATE CARBOXYLASE;

EID: 84879502170     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/j.1438-8677.2012.00704.x     Document Type: Review

References (81)

1. Anderson L.E. (1971) Chloroplast and cytoplasmic enzymes. II. Pea leaf triose phosphate isomerases. Biochimica et Biophysica Acta, 235, 237-244.
2. Araújo W.L., Nunes-Nesi A., Trenkamp S., Bunik V.I., Fernie A.R. (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.
3. Araújo W.L., Ishizaki K., Nunes-Nesi A., Larson T.R., Tohge T., Krahnert I., Witt S., Obata T., Schauer N., Graham I.A., Leaver C.J., Fernie A.R. (2010) Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. The Plant Cell, 22, 1549-1563.
4. Araújo W.L., Ishizaki K., Nunes-Nesi A., Tohge T., Larson T.R., Krahnert I., Balbo I., Witt S., Doermann P., Graham I.A., Leaver C.J., Fernie A.R. (2011a) Analysis of a range of catabolic mutants provides evidence that phytanoyl-coenzyme A does not act as a substrate of the electron-transfer flavoprotein/electron-transfer flavoprotein: ubiquinone oxidoreductase complex in Arabidopsis during dark-induced senescence. Plant Physiology, 157, 55-69.
5. Araújo W.L., Tohge T., Ishizaki K., Leaver C.J., Fernie A.R. (2011b) Protein degradation - an alternative respiratory substrate for stressed plants. Trends in Plant Science, 16, 489-498.
6. Araújo W.L., Nunes-Nesi A., Nikoloski Z., Sweetlove L.J., Fernie A.R. (2012a) Metabolic control and regulation of the tricarboxylic acid cycle in photosynthetic and heterotrophic plant tissues. Plant, Cell & Environment, 35, 1-21.
7. Araújo W.L., Tohge T., Osorio S., Lohse M., Balbo I., Krahnert I., Sienkiewicz-Porzucek A., Usadel B., Nunes-Nesi A., Fernie A.R. (2012b) Antisense inhibition of the 2-oxoglutarate dehydrogenase complex in tomato demonstrates its importance for plant respiration and during leaf senescence and fruit maturation. The Plant Cell, 24, 2328-2351.
8. Barak S., Nejidat A., Heimer Y., Volokita M. (2001) Transcriptional and posttranscriptional regulation of the glycolate oxidase gene in tobacco seedlings. Plant Molecular Biology, 45, 399-407.
9. Bauwe H., Hagemann M., Fernie A.R. (2010) Photorespiration: players, partners and origin. Trends in Plant Science, 15, 330-336.
10. Bauwe H., Hagemann M., Kern R., Timm S. (2012) Photorespiration has a dual origin and manifold links to central metabolism. Current Opinion in Plant Biology, 15, 269-275.
11. Black S., Wright N.G. (1956) Enzymatic formation of glyceryl and phosphoglyceryl methylthiol esters. Journal of Biological Chemistry, 221, 171-180.
12. Blackwell R.D., Murray A.J.S., Lea P.J. (1990) Photorespiratory mutants of the mitochondrial conversion of glycine to serine. Plant Physiology, 94, 1316-1322.
13. Bloom A.J., Burger M., Asensio J.S.R., Cousins A.B. (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science, 328, 899-903.
14. Boldt R., Edner C., Kolukisaoglu U., Hagemann M., Weckwerth W., Wienkoop S., Morgenthal K., Bauwe H. (2005) D-Glycerate 3-kinase, the last unknown enzyme in the photorespiratory cycle in Arabidopsis, belongs to a novel kinase family. The Plant Cell, 17, 2413-2420.
15. Boyes D.C., Zayed A.M., Ascenzi R., McCaskill A.J., Hoffman N.E., Davis K.R., Gorlach J. (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. The Plant Cell, 13, 1499-1510.
16. Bräutigam A., Weber A.P.M. (2011) Do metabolite transport processes limit photosynthesis? Plant Physiology, 155, 43-48.
17. Bykova N., 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.
18. Caldana C., Degenkolbe T., Cuadros-Inostroza A., Klie S., Sulpice R., Leisse A., Steinhauser D., Fernie A.R., Willmitzer L., Hannah M.A. (2011) High-density kinetic analysis of the metabolomic and transcriptomic response of Arabidopsis to eight environmental conditions. Plant Journal, 67, 869-884.
19. Chaouch S., Queval G., Vanderauwera S., Mhamdi A., Vandorpe M., Langlois-Meurinne M., Van Breusegem F., Saindrenan P., Noctor G. (2010) Peroxisomal hydrogen peroxide is coupled to biotic defense responses by isochorismate synthase1 in a daylength-related manner. Plant Physiology, 153, 1692-1705.
20. Chaouch S., Queval G., Noctor G. (2012) AtRbohF is a crucial modulator of defence-associated metabolism and a key actor in the interplay between intracellular oxidative stress and pathogenesis responses in Arabidopsis. Plant Journal, 69, 613-627.
21. Collakova E., Goyer A., Naponelli V., Krassovskaya I., Gregory J.F., Hanson A.D., Shachar-Hill Y. (2008) Arabidopsis 10-formyl tetrahydrofolate deformylases are essential for photorespiration. The Plant Cell, 20, 1818-1832.
22. Cossins E. (2000) The fascinating world of folate and one-carbon metabolism. Canadian Journal of Botany, 78, 691-708.
23. 2 release. Plant Physiology, 148, 786-795.
24. Douce R., Bourguignon J., Neuburger M., Rebeille F. (2001a) The glycine decarboxylase system: a fascinating complex. Trends in Plant Science, 6, 167-176.
25. Douce R., Bourguignon J., Neuburger M., Rébeillé F. (2001b) The glycine decarboxylase system: a fascinating complex. Trends in Plant Science, 6, 167-176.
26. Dutilleul C., Driscoll S., Cornic G., De Paepe R., Foyer C.H., Noctor G. (2003a) Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiology, 131, 264-275.
27. Dutilleul C., Garmier M., Noctor G., Mathieu C., Chétrit P., Foyer C.H., de Paepe R. (2003b) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. The Plant Cell, 15, 1212-1226.
28. Engel N., van den Daele K., Kolukisaoglu Ü., Morgenthal K., Weckwerth W., Pärnik T., Keerberg O., Bauwe H. (2007) Deletion of glycine decarboxylase in Arabidopsis is lethal under nonphotorespiratory conditions. Plant Physiology, 144, 1328-1335.
29. Engel N., Ewald R., Gupta K.J., Zrenner R., Hagemann M., Bauwe H. (2011) The presequence of Arabidopsis serine hydroxymethyltransferase SHM2 selectively prevents import into mesophyll mitochondria. Plant Physiology, 157, 1711-1720.
30. Fahnenstich H., Scarpeci T.E., Valle E.M., Fluegge U.-I., Maurino V.G. (2008) Generation of hydrogen peroxide in chloroplasts of Arabidopsis overexpressing glycolate oxidase as an inducible system to study oxidative stress. Plant Physiology, 148, 719-729.
31. Fait A., Fromm H., Walter D., Galili G., Fernie A.R. (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends in Plant Science, 13, 14-19.
32. Foyer C.H., Noctor G. (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiology, 155, 2-18.
33. Foyer C.H., Bloom A.J., Queval G., Noctor G. (2009) Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annual Review of Plant Biology, 60, 455-484.
34. Foyer C.H., 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.
35. Hanson A.D., Roje S. (2001) One-carbon metabolism in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology, 52, 119-137.
36. Ichihara A., Greenberg D.M. (1957) Studies on the purification and properties of D-glyceric acid kinase of liver. Journal of Biological Chemistry, 225, 949-958.
37. Igamberdiev A.U., Gardeström P. (2003) Regulation of NAD- and NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves. Biochimica et Biophysica Acta, 1606, 117-125.
38. Igarashi D., Miwa T., Seki M., Kobayashi M., Kato T., Tabata S., Shinozaki K., Ohsumi C. (2003) Identification of photorespiratory glutamate: glyoxylate aminotransferase (GGAT) gene in Arabidopsis. Plant Journal, 33, 975-987.
39. Intergovernmental Panel on Climate Change (2007) Climate Change 2007: Synthesis Report. http://www.ipcc.ch/publications_and_data_publications_ipcc_fourth_assessment_report_synthesis_report.htm.
40. 2 specificity of ribulose-1, 5-bisphosphate carboxylase/oxygenase: dependence on ribulose bisphosphate concentration, pH and temperature. Planta, 161, 308-313.
41. Kelly G.J., Latzko E. (1976) Inhibition of spinach leaf phosphofructokinase by 2-phosphoglycolate. FEBS Letters, 68, 55-58.
42. 3 higher plants. Photosynthesis Research, 87, 165-175.
43. Leegood R.C., Lea P.J., Adcock M.D., Hausler R.E. (1995) The regulation and control of photorespiration. Journal of Experimental Botany, 46, 1397-1414.
44. Liepman A.H., Olsen L.J. (2001) Peroxisomal alanine:glyoxylate aminotransferase (AGT1) is a photorespiratory enzyme with multiple substrates in Arabidopsis thaliana. Plant Journal, 25, 487-498.
45. Liepman A.H., Olsen L.J. (2003) Alanine aminotransferase homologs catalyze the glutamate:glyoxylate aminotransferase reaction in peroxisomes of Arabidopsis. Plant Physiology, 131, 215-227.
46. Linka N., Esser C. (2012) Transport proteins regulate the flux of metabolites and cofactors across the membrane of plant peroxisomes. Frontiers in Plant Science, 3, 3.
47. Long S.P., Zhu X.G., Naidu S.L., Ort D.R. (2006) Can improvement in photosynthesis increase crop yields? Plant, Cell & Environment, 29, 315-330.
48. Maurino V.G., Peterhansel C. (2010) Photorespiration: current status and approaches for metabolic engineering. Current Opinion in Plant Biology, 13, 249-256.
49. Murray A.J.S., Blackwell R.D., Joy K.W., Lea P.J. (1987) Photorespiratory N donors, aminotransferase specificity and photosynthesis in a mutant of barley deficient in serine:glyoxylate aminotransferase activity. Planta, 172, 106-113.
50. Niessen M., Krause K., Horst I., Staebler N., Klaus S., Gaertner S., Kebeish R., Araujo W.L., Fernie A.R., Peterhansel C. (2012) Two alanine aminotranferases link mitochondrial glycolate oxidation to the major photorespiratory pathway in Arabidopsis and rice. Journal of Experimental Botany, 63, 2705-2716.
51. Noctor G., Arisi A.C.M., Jouanin L., Foyer C.H. (1999) Photorespiratory glycine enhances glutathione accumulation in both the chloroplastic and cytosolic compartments. Journal of Experimental Botany, 50, 1157-1167.
52. Noctor G., Mhamdi A., Chaouch S., Han Y.I., Neukermans J., Marquez-Garcia B., Queval G., Foyer C.H. (2012) Glutathione in plants: an integrated overview. Plant, Cell & Environment, 35, 454-484.
53. Novitskaya L., Trevanion S.J., Driscoll S., Foyer C.H., Noctor G. (2002) How does photorespiration modulate leaf amino acid contents? A dual approach through modelling and metabolite analysis. Plant, Cell & Environment, 25, 821-835.
54. Nunes-Nesi A., Fernie A.R., Stitt M. (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon-nitrogen interactions. Molecular Plant, 3, 973-996.
55. Osorio S., Do P.T., Fernie A.R. (2012) Profiling primary metabolites of tomato fruit with gas chromatography/mass spectrometry. Methods in Molecular Biology, 860, 101-109.
56. Palmieri F., Pierri C.L., De Grassi A., Nunes-Nesi A., Fernie A.R. (2011) Evolution, structure and function of mitochondrial carriers: a review with new insights. Plant Journal, 66, 161-181.
57. Potters G., De Gara L., Asard H., Horemans N. (2002) Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiology and Biochemistry, 40, 537-548.
58. 2-induced cell death. Plant Journal, 52, 640-657.
59. Rachmilevitch S., Cousins A.B., Bloom A.J. (2004) Nitrate assimilation in plant shoots depends on photorespiration. Proceedings of the National Academy of Sciences of the United States of America, 101, 11506-11510.
60. 2 cycle have become filled - others remain. Biochimica et Biophysica Acta, 1763, 1496-1510.
61. Rontein D., Rhodes D., Hanson A.D. (2003) Evidence from engineering that decarboxylation of free serine is the major source of ethanolamine moieties in plants. Plant and Cell Physiology, 44, 1185-1191.
62. Schwacke R., Schneider A., van der Graaff E., Fischer K., Catoni E., Desimone M., Frommer W.B., Flügge U.-I., Kunze R. (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiology, 131, 16-26.
63. Schwarte S., Bauwe H. (2007) Identification of the photorespiratory 2-phosphoglycolate phosphatase, PGLP1, in Arabidopsis. Plant Physiology, 144, 1580-1586.
64. Sienkiewicz-Porzucek A., Sulpice R., Osorio S., Krahnert I., Leisse A., Urbanczyk-Wochniak E., Hodges M., Fernie A.R., Nunes-Nesi A. (2010) Mild reductions in mitochondrial NAD-dependent isocitrate dehydrogenase activity result in altered nitrate assimilation and pigmentation but do not impact growth. Molecular Plant, 3, 156-173.
65. Somerville C.R., Ogren W.L. (1980) Photorespiration mutants of Arabidopsis thaliana deficient in serine-glyoxylate aminotransferase activity. Proceedings of the National Academy of Sciences of the United States of America, 77, 2684-2687.
66. Somerville C.R., Ogren W.L. (1981) Photorespiration-deficient mutants of Arabidopsis thaliana lacking mitochondrial serine transhydroxymethylase activity. Plant Physiology, 67, 666-671.
67. Studart-Guimarães C., Fait A., Nunes-Nesi A., Carrari F., Usadel B., Fernie A.R. (2007) Reduced expression of succinyl-coenzyme A ligase can be compensated for by up-regulation of the gamma-aminobutyrate shunt in illuminated tomato leaves. Plant Physiology, 145, 626-639.
68. Sweetlove L.J., Lytovchenko A., Morgan M., Nunes-Nesi A., Taylor N.L., Baxter C.J., Eickmeier I., Fernie A.R. (2006) Mitochondrial uncoupling protein is required for efficient photosynthesis. Proceedins of the National Academy of Sciences of the United States of America, 103, 19587-19592.
69. Sweetlove L.J., Beard K.F.M., Nunes-Nesi A., Fernie A.R., Ratcliffe R.G. (2010) Not just a circle: flux modes in the plant TCA cycle. Trends in Plant Science, 15, 462-470.
70. 2 conditions. Proceedings of the National Academy of Sciences of the United States of America, 105, 797-802.
71. Timm S., Nunes-Nesi A., Pärnik T., Morgenthal K., Wienkoop S., Keerberg O., Weckwerth W., Kleczkowski L.A., Fernie A.R., Bauwe H. (2008) A cytosolic pathway for the conversion of hydroxypyruvate to glycerate during photorespiration in Arabidopsis. The Plant Cell, 20, 2848-2859.
72. Timm S., Florian A., Jahnke K., Nunes-Nesi A., Fernie A.R., Bauwe H. (2011) The hydroxypyruvate-reducing system in Arabidopsis: multiple enzymes for the same end. Plant Physiology, 155, 694-705.
73. 2 acclimation reveals plasticity of the photorespiratory pathway and indicates regulatory links to cellular metabolism of Arabidopsis. PLoS ONE, 7, e42809.
74. Timm S., Florian A., Arrivault S., Stitt M., Fernie A.R., Bauwe H. (2012b) Glycine decarboxylase controls photosynthesis and plant growth. FEBS Letters, 586, 3692-3697.
75. Voll L.M., Jamai A., Renne P., Voll H., McClung C.R., Weber A.P.M. (2006) The photorespiratory Arabidopsis shm1 mutant is deficient in SHM1. Plant Physiology, 140, 59-66.
76. Waller J.C., Ellens K.W., Alvarez S., Loizeau K., Ravanel S., Hanson A.D. (2012) Mitochondrial and plastidial COG0354 proteins have folate-dependent functions in iron-sulphur cluster metabolism. Journal of Experimental Botany, 63, 403-411.
77. Wingler A., Lea P.J., Quick W.P., Leegood R.C. (2000) Photorespiration: metabolic pathways and their role in stress protection. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 355, 1517-1529.
78. 2 fixation in C3 plants. Annual Review of Plant Physiology and Plant Molecular Biology, 39, 533-594.
79. Xu H., Zhang J., Zeng J., Jiang L., Liu E., Peng C., He Z., Peng X. (2009) Inducible antisense suppression of glycolate oxidase reveals its strong regulation over photosynthesis in rice. Journal of Experimental Botany, 60, 1799-1809.
80. Yu Q.-B., Li G., Wang G., Sun J.-C., Wang P.-C., Wang C., Mi H.-L., Ma W.-M., Cui J., Cui Y.-L., Chong K., Li Y.-X., Li Y.-H., Zhao Z., Shi T.-L., Yang Z.-N. (2008) Construction of a chloroplast protein interaction network and functional mining of photosynthetic proteins in Arabidopsis thaliana. Cell Research, 18, 1007-1019.
81. Zelitch I., Schultes N.P., Peterson R.B., Brown P., Brutnell T.P. (2009) High glycolate oxidase activity is required for survival of maize in normal air. Plant Physiology, 149, 195-204.