Decreased glycolate oxidase activity leads to altered carbon allocation and leaf senescence after a transfer from high CO2 to ambient air in Arabidopsis thaliana

Journal of Experimental Botany

Volumn 67, Issue 10, 2016, Pages 3149-3163

  Dellero, Younès ^a   Jossier, Mathieu ^a   Glab, Nathalie ^a   Oury, Céline ^a   Tcherkez, Guillaume ^a,b   Hodges, Michael ^a  

^a CNRS   (France)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Arabidopsis; Carbon allocation; Mutant; Photorespiration; Photosynthesis; Senescence

Indexed keywords

ALCOHOL DEHYDROGENASE; ARABIDOPSIS PROTEIN; CARBON DIOXIDE; CHLOROPHYLL; GOX1 PROTEIN, ARABIDOPSIS; GOX3 PROTEIN, ARABIDOPSIS; HYDROXY ACID OXIDASE A;

AGING; ARABIDOPSIS; ENZYMOLOGY; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF;

AGING; ALCOHOL OXIDOREDUCTASES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARBON DIOXIDE; CHLOROPHYLL; PHOTOSYNTHESIS; PLANT LEAVES;

EID: 84970024114     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erw054     Document Type: Article

References (56)

1. Anderson LE. 1971. Chloroplast and cytoplasmic enzymes II. Pea leaf triose phosphate isomerases. Biochimica et Biophysica Acta 235, 237-244
2. Avice J-C, Etienne P. 2014. Leaf senescence and nitrogen remobilization efficiency in oilseed rape (Brassica napus L). Journal of Experimental Botany 65, 3813-3824
3. Avila-Ospina L, Marmagne A, Talbotec J, Krupinska K, Masclaux-Daubresse C. 2015. The identification of new cytosolic glutamine synthetase and asparagine synthetase genes in barley (Hordeum vulgare L), and their expression during leaf senescence. Journal of Experimental Botany 66, 2013-2026
4. Bauwe H, Hagemann M, Fernie AR. 2010. Photorespiration: players, partners and origin. Trends in Plant Science 15, 330-336
5. Bensmihen S, To A, Lambert G, Kroj T, Giraudat J, Parcy F. 2004. Analysis of an activated ABI5 allele using a new selection method for transgenic Arabidopsis seeds. FEBS Letters 561, 127-131
6. Bloom AJ. 2015. Photorespiration and nitrate assimilation: a major intersection between plant carbon and nitrogen. Photosynthesis Research 123, 117-128
7. Boex-Fontvieille E, Gauthier P, Gilard F, Hodges M, Tcherkez G. 2013. A new anaplerotic respiratory pathway involving lysine biosynthesis in isocitrate dehydrogenase-deficient Arabidopsis mutants. New Phytologist 199, 673-682
8. Boldt R. 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
9. Campbell WJ, Ogren WL. 1990. Glyoxylate inhibition of ribulosebisphosphate carboxylase/oxygenase activation in intact, lysed, and reconstituted chloroplasts. Photosynthesis Research 23, 257-268
10. Chastain CJ, Ogren WL. 1989. Glyoxylate inhibition of ribulosebisphosphate carboxylase/oxygenase activation state in vivo. Plant and Cell Physiology 30, 937-944
11. Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735-743
12. Dellero Y, Lamothe-Sibold M, Jossier M, Hodges M. 2015a. Arabidopsis thaliana ggt1 photorespiratory mutants maintain leaf carbon/ nitrogen balance by reducing RuBisCO content and plant growth. The Plant Journal 83, 1005-1018
13. Dellero Y, Mauve C, Boex-Fontvieille E, Flesch V, Jossier M, Tcherkez G, Hodges M. 2015b. Experimental evidence for a hydrid transfer mechanism in plant glycolate oxidase catalysis. Journal of Biological Chemistry 290, 1689-1698
14. Diaz C, Saliba-Colombani V, Loudet O, Belluomo P, Moreau L, Daniel-Vedele F, Morot-Gaudry JF, Masclaux-Daubresse C. 2005. Leaf yellowing and anthocyanin accumulation are two genetically independent strategies in response to nitrogen limitation in Arabidopsis thaliana. Plant and Cell Physiology 47, 74-83
15. Edwards K, Johnstone C, Thompson C. 1991. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Research 19, 1349
16. Engel N, Ewald R, Gupta KJ, 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
17. Engel N, van den Daele K, Kolukisaoglu U, Morgenthal K, Weckwerth W, Parnik T, Keerberg O, Bauwe H. 2007. Deletion of glycine decarboxylase in Arabidopsis is lethal under nonphotorespiratory conditions. Plant Physiology 144, 1328-1335
18. Engqvist MKM, Kuhn A, Wienstroer J, Weber K, Jansen EEW, Jakobs C, Weber APM, Maurino VG. 2011. Plant d-2-Hydroxyglutarate Dehydrogenase Participates in the Catabolism of Lysine Especially during Senescence. Journal of Biological Chemistry 286, 11382-11390
19. Engqvist MK, Schmitz J, Gertzmann A, Florian A, Jaspert N, Arif M, Balazadeh S, Mueller-Roeber B, Fernie AR, Maurino VG. 2015. GLYCOLATE OXIDASE3, a glycolate oxidase homolog of yeast l-lactate cytochrome c oxidoreductase, supports l-lactate oxidation in roots of Arabidopsis. Plant Physiology 169, 1042-1061
20. Esser C, Kuhn A, Groth G, Lercher MJ, Maurino VG. 2014. Plant and animal glycolate oxidases have a common eukaryotic ancestor and convergently duplicated to evolve long-chain 2-hydroxy acid oxidases. Molecular Biology and Evolution 31, 1089-1101
21. Fahnenstich H, Saigo M, Niessen M, Zanor MI, Andreo CS, Fernie AR, Drincovich MF, Flugge U-I, Maurino VG. 2007. Alteration of organic acid metabolism in Arabidopsis overexpressing the maize C4 NADP-malic enzyme causes accelerated senescence during extended darkness. Plant Physiology 145, 640-652
22. 2 assimilation in illuminated leaves of Brassica napus. New Phytologist 185, 988-999
23. Hanson AD, Gregory JF. 2011. Folate biosynthesis, turnover, and transport in plants. Annual Review of Plant Biology 62, 105-125
24. Jossier M, Bouly JP, Meimoun P, Ajrmand A, Lessard P, Hawley S, Grahame Hardie D, Thomas M. 2009. SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signaling in Arabidopsis thaliana. The Plant Journal 59, 316-328
25. Keech O, Pesquet E, Gutierrez L, Ahad A, Bellini C, Smith SM, Gardestrom P. 2010. Leaf senescence is accompanied by an early disruption of the microtubule network in Arabidopsis. Plant Physiology 154, 1710-1720
26. Kuhn A, Engqvist MKM, Jansen EEW, Weber APM, KJakobs C, Maurino VG. 2013. D-2-hydroxyglutarate metabolism is linked to photorespiration in the shm1-1 mutant. Plant Biology 15, 776-784
27. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
28. Lu Y, Li Y, Yang Q, Zhang Z, Chen Y, Zhang S, Peng X-X. 2013. Suppression of glycolate oxidase causes glyoxylate accumulation that inhibits photosynthesis through deactivating Rubisco in rice. Physiologia Plantarum 150, 463-476
29. Noctor G, Bergot G, Mauve C, Thominet D, Lelarge-Trouverie C, Prioul J-L. 2007, A comparative study of amino acid measurement in leaf extracts by gas chromatography-time of flight-mass spectrometry and high performance liquid chromatography with fluorescence detection. Metabolomics 3, 161-174
30. Nölke G, Houdelet M, Kreuzaler F, Peterhänsel C, Schillberg S. 2014. The expression of a recombinant glycolate dehydrogenase polyprotein in potato (Solanum tuberosum) plastids strongly enhances photosynthesis and tuber yield. Plant Biotechnology Journal 12, 734-742
31. Pick TR, Brautigam A, Schulz MA, Obata T, Fernie AR, Weber APM. 2013. PLGG1, a plastidic glycolate glycerate transporter, is required for photorespiration and defines a unique class of metabolite transporters. Proceedings of the National Academy of Sciences, USA 110, 3185-3190
32. Porra RJ, Thompson WA, Kriedemann PE. 1989. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384-394
33. Reumann S, Babujee L, Ma C, Wienkoop S, Siemsen T, Antonicelli GE, Rasche N, Lüder F, Weckwerth W, Jahn O. 2007. Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. The Plant Cell 19, 3170-3193
34. Rojas CM, Senthil-Kumar M, Wang K, Ryu C-M, Kaundal A, Mysore KS. 2012. Glycolate oxidase modulates reactive oxygen species-mediated signal transduction during nonhost resistance in Nicotiana benthamiana and Arabidopsis. The Plant Cell 24, 336-352
35. Ros R, Muñoz-Bertomeu J, Krueger S. 2014. Serine in plants: biosynthesis, metabolism, and functions. Trends in Plant Science 19, 564-569
36. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D. 2006. Highly specific gene silencing by artificial microRNAs in Arabidopsis. The Plant Cell 18, 1121-1133
37. 2 enrichment and elevated growth temperatures on metabolites in soybean leaflets: evidence for dynamic changes of TCA cycle intermediates. Planta 238, 369-380
38. Somerville CR, Ogren WL. 1979. A phosphoglycolate phosphatasedeficient mutant of Arabidopsis. Mutants of the cruciferous plant Arabidopsis thaliana lacking glycine decarboxylase activity. Nature 280, 833-835
39. Somerville CR, Ogren WL. 1980. Photorespiration mutants of Arabidopsis thaliana deficient in serine-glyoxylate aminotransferase activity. Proceedings of the National Academy of Sciences, USA 77, 2684-2687
40. Somerville CR, Ogren WL. 1981. Photorespiration-deficient mutants of Arabidopsis thaliana lacking mitochondrial serine transhydroxymethylase activity. Plant Physiology 67, 666-671
41. Somerville CR, Ogren WL. 1982. Mutants of the cruciferous plant Arabidopsis thaliana lacking glycine decarboxylase activity. Biochemical Journal 202, 373-380
42. Sweetlove LJ, Beard KFM, Nunes-Nesi A, Fernie AR, Ratcliffe RG. 2010. Not just a circle: flux modes in the plant TCA cycle. Trends in Plant Science 15, 462-470
43. 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 Physiology 144, 487-494
44. 2 and O2 conditions. Proceedings of the National Academy of Sciences, USA 105, 797-802
45. Tcherkez G, Mahé A, Gauthier P, Mauve C, Gout E, Bligny R, Cornic G, Hodges M. 2009. In folio respiratory fluxomics revealed by 13C isotopic labeling and H/D isotope effects highlight the noncyclic nature of the tricarboxylic acid 'cycle' in illuminated leaves. Plant Physiology 151, 620-630
46. 2 and O2 on citrate metabolism in illuminated leaves. Plant, Cell and Environment 35, 2208-2220
47. Timm S, Bauwe H. 2013. The variety of photorespiratory phenotypes-employing the current status for future research directions on photorespiration. Plant Biology 15, 737-747
48. Timm S, Florian A, Arrivault S, Stitt M, Fernie AR, Bauwe H. 2013. Glycine decarboxylase controls photosynthesis and plant growth. FEBS Letters 586, 3692-3697
49. Timm S, Florian A, Jahnke K, Nunes-Nesi A, Fernie AR, Bauwe H. 2011. The hydroxypyruvate-reducing system in Arabidopsis: multiple enzymes for the same end. Plant Physiology 155, 694-705
50. 2 acclimation reveals plasticity of the photorespiratory pathway and indicates regulatory links to cellular metabolism of Arabidopsis. PLoS One 7, e42809
51. Timm S, Wittmiß M, Gamlien S, Ewald R, Florian A, Frank M, Wirtz M, Hell R, Fernie AR, Bauwe H. 2015. Mitochondrial dihydrolipoyl dehydrogenase activity shapes photosynthesis and photorespiration of Arabidopsis thaliana. The Plant Cell 27, 1968-1984
52. Watanabe M, Balazadeh S, Tohge T, Erban A, Giavalisco P, Kopka J, Mueller-Roeber B, Fernie AR, Hoefgen R. 2013. Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiology 162, 1290-1310
53. 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
54. Yamaguchi K, Nishimura M. 2000. Reduction to below threshold levels of glycolate oxidase activities in transgenic tobacco enhances photoinhibition during irradiation. Plant and Cell Physiology 41, 1397-1406
55. 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 Physiology 149, 195-204
56. Zhang N, Portis AR. 1999. Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. Proceedings of the National Academy of Sciences, USA 96, 9438-9443