High-to-low CO 2 acclimation reveals plasticity of the photorespiratory pathway and indicates regulatory links to cellular metabolism of Arabidopsis

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Timm, Stefan ^a   Mielewczik, Michael ^b,c   Florian, Alexandra ^d   Frankenbach, Silja ^a,e   Dreissen, Anne ^c   Hocken, Nadine ^c,f   Fernie, Alisdair R ^d   Walter, Achim ^b,c   Bauwe, Hermann ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b ETH ZURICH   (Switzerland)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

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

^e UNIVERSITY OF AVEIRO   (Portugal)

^f HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2 PHOSPHOGLYCOLIC ACID; GLYCERATE 3 KINASE; GLYCINE; GLYCINE HYDROXYMETHYLTRANSFERASE; GLYCOLIC ACID DERIVATIVE; HYDROXYPYRUVATE REDUCTASE; PHOSPHATASE; PHOSPHOGLYCOLATE PHOSPHATASE; PHOSPHOTRANSFERASE; PLANT DNA; SERINE; UNCLASSIFIED DRUG; 2 PHOSPHOGLYCOLATE PHOSPHATASE PGLP1, ARABIDOPSIS; 2-PHOSPHOGLYCOLATE PHOSPHATASE PGLP1, ARABIDOPSIS; ARABIDOPSIS PROTEIN; CARBON DIOXIDE; EMU PROTEIN, ARABIDOPSIS;

ACCLIMATIZATION; AMBIENT AIR; AMINO ACID METABOLISM; AMINO ACID SUBSTITUTION; ARABIDOPSIS; ARTICLE; BIOACCUMULATION; CARBON METABOLISM; CELL METABOLISM; CITRIC ACID CYCLE; CONTROLLED STUDY; DNA DETERMINATION; FLUORESCENCE; GAS EXCHANGE; GENE; GENOTYPE; GLYK1 GENE; HPR1 GENE; KNOCKOUT GENE; LEAF GROWTH; METABOLITE; NITROGEN METABOLISM; NONHUMAN; OXIDATION REDUCTION REACTION; PGLP1 GENE; PHENOTYPIC PLASTICITY; PHOTOCHEMISTRY; PHOTORESPIRATION; PHOTOSYNTHESIS; SHM1 GENE; WILD TYPE; ADAPTATION; CELL RESPIRATION; CHEMISTRY; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; GENE INACTIVATION; GENETICS; LIGHT; METABOLISM; MUTATION; PHOTOSYSTEM II; PLANT LEAF; RADIATION EXPOSURE;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARBON DIOXIDE; CELL RESPIRATION; CITRIC ACID CYCLE; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE KNOCKOUT TECHNIQUES; LIGHT; MUTATION; PHOSPHORIC MONOESTER HYDROLASES; PHOTOCHEMICAL PROCESSES; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT LEAVES;

EID: 84865083973     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042809     Document Type: Article

References (76)

1. Bauwe H, Hagemann M, Fernie AR, (2010) Photorespiration: players, partners and origin. Trends Plant Sci 15: 330-336.
2. Foyer CH, Bloom AJ, Queval G, Noctor G, (2009) Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu Rev Plant Biol 60: 455.
3. Troughton JH, Slatyer RO, (1969) Plant water status, leaf temperature, and calculated mesophyll resistance to carbon dioxide of cotton leaves. Aust J Biol Sci 22: 815-827.
4. Oberhuber W, Edwards GE, (1993) Temperature dependence of the linkage of quantum yield of photosystem II to CO2 fixation in C4 and C3 plants. Plant Physiol 101: 507-512.
5. Hofstra G, Hesketh JD, (1969) Effects of temperature on gas exchange of leaves in light and dark. Planta 85: 228-237.
6. Chollet R, Ogren WL, (1975) Regulation of photorespiration in C3 and C4 species. Bot Rev 41: 137-179.
7. Sage RF, (2000) C3 versus C4 photosynthesis in rice: ecophysiological perspectives. pp. 13-38.
8. Noctor G, Veljovic-Jovanovic S, Driscoll SP, Novitskaya L, Foyer CH, (2002) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot 89: 841-850.
9. Rojas CM, Senthil-Kumar M, Wang K, Ryu CM, Kaundal A, et al. (2012) Glycolate oxidase modulates reactive oxygen species-mediated signal transduction during nonhost resistance in Nicotiana benthamiana and Arabidopsis. Plant Cell 24: 226-352.
10. Eisenhut M, Ruth W, Haimovich M, Bauwe H, Kaplan A, et al. (2008) The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants. Proc Natl Acad Sci USA 105: 17199-17204.
11. Blackwell RD, Murray AJS, Lea PJ, Kendall A, Hall NP, et al. (1988) The value of mutants unable to carry out photorespiration. Photosynth Res 16: 155-176.
12. Wingler A, Lea PJ, Leegood RC, (1999) Photorespiratory metabolism of glyoxylate and formate in glycine-accumulating mutants of barley and Amaranthus edulis. Planta 207: 518-526.
13. Zelitch I, Schultes NP, Peterson RB, Brown P, Brutnell TP, (2009) High glycolate oxidase activity is required for survival of maize in normal air. Plant Physiol 149: 195-204.
14. Somerville CR, (2001) An early Arabidopsis demonstration resolving a few issues concerning photorespiration. Plant Physiol 125: 20-24.
15. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
16. Somerville CR, Ogren WL, (1982) Genetic modification of photorespiration. Trends Biochem Sci 7: 171-174.
17. Schwarte S, Bauwe H, (2007) Identification of the photorespiratory 2-phosphoglycolate phosphatase, PGLP1, in Arabidopsis. Plant Physiol 144: 1580-1586.
18. Somerville CR, Ogren WL, (1979) A phosphoglycolate phosphatase-deficient mutant of Arabidopsis. Nature 280: 833-836.
19. Hall NP, Kendall AC, Lea PJ, Turner JC, Wallsgrove RM, (1987) Characteristics of a photorespiratory mutant of barley (Hordeum vulgare L) deficient in phosphoglycollate phosphatase. Photosynth Res 11: 89-96.
20. Boldt R, Edner C, Kolukisaoglu Ü, Hagemann M, Weckwerth W, et al. (2005) D-Glycerate 3-kinase, the last unknown enzyme in the photorespiratory cycle in Arabidopsis, belongs to a novel kinase family. Plant Cell 17: 2413-2420.
21. Timm S, Nunes-Nesi A, Pärnik T, Morgenthal K, Wienkoop S, et al. (2008) A cytosolic pathway for the conversion of hydroxypyruvate to glycerate during photorespiration in Arabidopsis. Plant Cell 20: 2848-2859.
22. Murray AJS, Blackwell RD, Lea PJ, (1989) Metabolism of hydroxypyruvate in a mutant of barley lacking NADH-dependent hydroxypyruvate reductase, an important photorespiratory enzyme activity. Plant Physiol 91: 395-400.
23. Voll LM, Jamai A, Renné P, Voll H, McClung CR, et al. (2006) The photorespiratory Arabidopsis shm1 mutant is deficient in SHM1. Plant Physiol 140: 59-66.
24. Timm S, Florian A, Jahnke K, Nunes-Nesi A, Fernie AR, et al. (2011) The hydroxypyruvate-reducing system in Arabidopsis: Multiple enzymes for the same end. Plant Physiol 155: 694-705.
25. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, et al. (2001) Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants. Plant Cell 13: 1499-1510.
26. Queval G, Issakidis-Bourguet E, Hoeberichts FA, Vandorpe M, Gakiere B, et al. (2007) Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression, and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death. Plant J 52: 640-657.
27. Jansen M, Gilmer F, Biskup B, Nagel KA, Rascher U, et al. (2009) Simultaneous phenotyping of leaf growth and chlorophyll fluorescence via GROWSCREEN FLUORO allows detection of stress tolerance in Arabidopsis thaliana and other rosette plants. Funct Plant Biol 36: 902-914.
28. Takahashi S, Badger MR, (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16: 53-60.
29. Takahashi S, Bauwe H, Badger M, (2007) Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair but not acceleration of damage processes in Arabidopsis. Plant Physiol 144: 487-494.
30. Häusler RE, Bailey KJ, Lea PJ, Leegood RC, (1996) Control of photosynthesis in barley mutants with reduced activities of glutamine synthetase and glutamate synthase. 3. Aspects of glyoxylate metabolism and effects of glyoxylate on the activation state of ribulose-1,5-bisphosphate carboxylase-oxygenase. Planta 200: 388-396.
31. Wiese A, Christ MM, Virnich O, Schurr U, Walter A, (2007) Spatio-temporal leaf growth patterns of Arabidopsis thaliana and evidence for sugar control of the diel leaf growth cycle. New Phytol 174: 752-761.
32. Niittyla T, Messerli G, Trevisan M, Chen J, Smith AM, et al. (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303: 87-89.
33. Graf A, Schlereth A, Stitt M, Smith AM, (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc Natl Acad Sci USA 107: 9458-9463.
34. Weise SE, Weber AP, Sharkey TD, (2004) Maltose is the major form of carbon exported from the chloroplast at night. Planta 218: 474-482.
35. Biskup B, Scharr H, Fischbach A, Wiese-Klinkenberg A, Schurr U, et al. (2009) Diel growth cycle of isolated leaf discs analyzed with a novel, high-throughput three-dimensional imaging method is identical to that of intact leaves. Plant Physiol 149: 1452-1461.
36. Keys AJ, Bird IF, Cornelius MJ, Lea PJ, Wallsgrove RM, et al. (1978) Photorespiratory nitrogen cycle. Nature 275: 741-743.
37. Nunes-Nesi A, Araujo WL, Fernie AR, (2011) Targeting mitochondrial metabolism and machinery as a means to enhance photosynthesis. Plant Physiol 155: 101-107.
38. Pracharoenwattana I, Zhou WX, Smith SM, (2010) Fatty acid beta-oxidation in germinating Arabidopsis seeds is supported by peroxisomal hydroxypyruvate reductase when malate dehydrogenase is absent. Plant Mol Biol 72: 101-109.
39. Allan WL, Clark SM, Hoover GJ, Shelp BJ, (2009) Role of plant glyoxylate reductases during stress: a hypothesis. Biochem J 423: 15-22.
40. Sweetlove LJ, Lytovchenko A, Morgan M, Nunes-Nesi A, Taylor NL, et al. (2006) Mitochondrial uncoupling protein is required for efficient photosynthesis. Proc Natl Acad Sci USA 103: 19587-19592.
41. Noctor G, Arisi AM, Jouanin L, Foyer CH, (1999) Photorespiratory glycine enhances glutathione accumulation in both the chloroplastic and cytosolic compartments. J Exp Bot 50: 1157-1167.
42. Collakova E, Goyer A, Naponelli V, Krassovskaya I, Gregory JF, et al. (2008) Arabidopsis 10-formyl tetrahydrofolate deformylases are essential for photorespiration. Plant Cell 20: 1818-1832.
43. Tolbert NE (1963) Glycolate pathway. In: Photosynthetic Mechanisms in Green Plants. Publication 1145. Washington, DC: National Academy of Science, National Research Council. pp. 648-662.
44. Tolbert NE, (1973) Glycolate biosynthesis. Curr Top Cell Regul 7: 21-50.
45. Givan CV, Kleczkowski LA, (1992) The enzymatic reduction of glyoxylate and hydroxypyruvate in leaves of higher plants. Plant Physiol 100: 552-556.
46. Walter A, Christ MM, Barron-Gafford GA, Grieve KA, Murthy R, et al. (2005) The effect of elevated CO2 on diel leaf growth cycle, leaf carbohydrate content and canopy growth performance of Populus deltoides. Glob Change Biol 11: 1207-1219.
47. Hetherington AM, Woodward FI, (2003) The role of stomata in sensing and driving environmental change. Nature 424: 901-908.
48. Morison JIL, (1998) Stomatal response to increased CO2 concentration. J Exp Bot 49: 443-452.
49. Dodd AN, Salathia N, Hall A, Kevei E, Toth R, et al. (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309: 630-633.
50. Somerville CR, Ogren WL, (1980) Photorespiration mutants of Arabidopsis thaliana deficient in serine-glyoxylate aminotransferase activity. Proc Natl Acad Sci USA 77: 2684-2687.
51. Somerville CR, Ogren WL, (1981) Photorespiration-deficient mutants of Arabidopsis thaliana lacking mitochondrial serine transhydroxymethylase activity. Plant Physiol 67: 666-671.
52. Kofler H, Häusler RE, Schulz B, Groner F, Flügge UI, et al. (2000) Molecular characterisation of a new mutant allele of the plastid phosphoglucomutase in Arabidopsis, and complementation of the mutant with the wild-type cDNA. Mol Gen Genet 263: 978-986.
53. Bläsing OE, Gibon Y, Gunther M, Hohne M, Morcuende R, et al. (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17: 3257-3281.
54. Kleczkowski LA, (1994) Inhibitors of photosynthetic enzymes/carriers and metabolism. Ann Rev Plant Physiol 45: 339-367.
55. Anderson LE, (1971) Chloroplast and cytoplasmic enzymes. 2. Pea leaf triose phosphate isomerases. Biochim Biophys Acta 235: 237-244.
56. Johnson LN, Wolfenden R, (1970) Changes in absorption spectrum and crystal structure of triose phosphate isomerase brought about by 2-phosphoglycollate, a potential transition state analogue. J Mol Biol 47: 93-100.
57. Kelly GJ, Latzko E, (1976) Inhibition of spinach-leaf phosphofructokinase by 2-phosphoglycollate. FEBS Lett 68: 55-58.
58. Engel N, Ewald R, Gupta KJ, Zrenner R, Hagemann M, et al. (2011) The presequence of Arabidopsis serine hydroxymethyltransferase SHM2 selectively prevents import into mesophyll mitochondria. Plant Physiol 157: 1711-1720.
59. Barak S, Nejidat A, Heimer Y, Volokita M, (2001) Transcriptional and posttranscriptional regulation of the glycolate oxidase gene in tobacco seedlings. Plant Mol Biol 45: 399-407.
60. Potters G, De Gara L, Asard H, Horemans N, (2002) Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiol Biochem 40: 537-548.
61. Foyer CH, Noctor G, (2011) Ascorbate and glutathione: The heart of the redox hub. Plant Physiol 155: 2-18.
62. Novitskaya L, Trevanion SJ, Driscoll S, Foyer CH, Noctor G, (2002) How does photorespiration modulate leaf amino acid contents? A dual approach through modelling and metabolite analysis. Plant Cell Environ 25: 821-835.
63. Cousins AB, Pracharoenwattana I, Zhou W, Smith SM, Badger MR, (2008) Peroxisomal malate dehydrogenase is not essential for photorespiration in Arabidopsis but its absence causes an increase in the stoichiometry of photorespiratory CO2 release. Plant Physiol 148: 786-795.
64. Reumann S, Weber AP, (2006) Plant peroxisomes respire in the light: Some gaps of the photorespiratory C2 cycle have become filled- others remain. Biochim Biophys Acta 1763: 1496-1510.
65. Douce R, Neuburger M, (1989) The uniqueness of plant mitochondria. Ann Rev Plant Physiol 40: 371-414.
66. Dutilleul C, Driscoll S, Cornic G, De Paepe R, Foyer CH, et al. (2003) Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol 131: 264-275.
67. 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.
68. Araujo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR, (2011) Protein degradation- an alternative respiratory substrate for stressed plants. Trends Plant Sci 16: 489-498.
69. Fernie AR, Martinoia E, (2009) Malate. Jack of all trades or master of a few? Phytochemistry 70: 828-832.
70. Fait A, Fromm H, Walter D, Galili G, Fernie AR, (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci 13: 14-19.
71. Munoz-Bertomeu J, Cascales-Minana B, Mulet JM, Baroja-Fernandez E, Pozueta-Romero J, et al. (2009) Plastidial glyceraldehyde-3-phosphate dehydrogenase deficiency leads to altered root development and affects the sugar and amino acid balance in Arabidopsis. Plant Physiol 151: 541-558.
72. Ho CL, Saito K, (2001) Molecular biology of the plastidic phosphorylated serine biosynthetic pathway in Arabidopsis thaliana. Amino Acids 20: 243-259.
73. Schreiber U, Schliwa U, Bilger W, (1986) Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10: 51-62.
74. Fahnenstich H, Scarpeci TE, Valle EM, Flügge UI, Maurino VG, (2008) Generation of H2O2 in chloroplasts of Arabidopsis thaliana overexpressing glycolate oxidase as an inducible system to study oxidative stress. Plant Physiol 148: 729.
75. Jones MGK, Outlaw WH, Lowry OH, (1977) Enzymic assay of 10-7 to 10-14 moles of sucrose in plant tissues. Plant Physiol 60: 379-383.
76. Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR, (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc 1: 387-396.