Lack of GLYCOLATE OXIDASE1, but not GLYCOLATE OXIDASE2, attenuates the photorespiratory phenotype of CATALASE2-deficient Arabidopsis1[OPEN]

Plant Physiology

Volumn 171, Issue 3, 2016, Pages 1704-1719

  Kerchev, Pavel ^a,b   Waszczak, Cezary ^a,b,c,d,e   Lewandowska, Aleksandra ^a,b,c,d   Willems, Patrick ^a,b   Shapiguzov, Alexey ^e,f   Li, Zhen ^a,b   Alseekh, Saleh ^g   Mühlenbock, Per ^a,b   Hoeberichts, Frank A ^a,b   Huang, Jingjing ^a,c,d   Van Der Kelen, Katrien ^a,b   Kangasjärvi, Jaakko ^e,h   Fernie, Alisdair R ^g   De Smet, Riet ^a,b   Van de Peer, Yves ^a,b,i   Messens, Joris ^a,c,d   Van Breusegem, Frank ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^d Brussels Center for Redox Biology   (Belgium)

^e UNIVERSITY OF HELSINKI   (Finland)

^f TIMIRYAZEV INSTITUTE OF PLANT PHYSIOLOGY   (Russian Federation)

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

^h KING SAUD UNIVERSITY   (Saudi Arabia)

ⁱ UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL DEHYDROGENASE; ARABIDOPSIS PROTEIN; GLYCOLIC ACID DERIVATIVE; GOX1 PROTEIN, ARABIDOPSIS; HYDROXY ACID OXIDASE A;

ARABIDOPSIS; CELL RESPIRATION; GENETICS; LIGHT; METABOLISM; METABOLOME; MOLECULAR EVOLUTION; MUTATION; OXIDATION REDUCTION REACTION; PHENOTYPE; PHOTOSYNTHESIS; PHYSIOLOGY;

ALCOHOL OXIDOREDUCTASES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL RESPIRATION; EVOLUTION, MOLECULAR; GLYCOLATES; LIGHT; METABOLOME; MUTATION; OXIDATION-REDUCTION; PHENOTYPE; PHOTOSYNTHESIS;

EID: 84977490134     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00359     Document Type: Article

References (57)

1. Abat JK, Mattoo AK, Deswal R (2008) S-nitrosylated proteins of a medicinal CAM plant Kalanchoe pinnata-ribulose-1,5-bisphosphate carboxylase/oxygenase activity targeted for inhibition. FEBS J 275: 2862-2872
2. Bailey CD, Koch MA, Mayer M, Mummenhoff K, O'Kane SL, Jr., Warwick SI, Windham MD, Al-Shehbaz IA (2006) Toward a global phylogeny of the Brassicaceae. Mol Biol Evol 23: 2142-2160
3. Bauwe H, Hagemann M, Kern R, Timm S (2012) Photorespiration has a dual origin and manifold links to central metabolism. Curr Opin Plant Biol 15: 269-275
4. Birney E, Clamp M, Durbin R (2004) GeneWise and Genomewise. Genome Res 14: 988-995
5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
6. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972-1973
7. Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis-Pinheiro M (2012) Plant responses to stresses: Role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol 35: 1011-1019
8. Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27: 1164-1165
9. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17: 268-281
10. 2 to ambient air in Arabidopsis thaliana. J Exp Bot 67: 3149-3163
11. Dellero Y, Mauve C, Boex-Fontvieille E, Flesch V, Jossier M, Tcherkez G, Hodges M (2015) Experimental evidence for a hydride transfer mechanism in plant glycolate oxidase catalysis. J Biol Chem 290: 1689-1698
12. Dietz KJ (2016) Thiol-based peroxidases and ascorbate peroxidases: why plants rely on multiple peroxidase systems in the photosynthesizing chloroplast? Mol Cells 39: 20-25
13. Engqvist MKM, 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 Physiol 169: 1042-1061
14. 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. Mol Biol Evol 31: 1089-1101
15. Foyer CH, Bloom AJ, Queval G, Noctor G (2009) Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu Rev Plant Biol 60: 455-484
16. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307-321
17. Guy L, Kultima JR, Andersson SG (2010) genoPlotR: comparative gene and genome visualization in R. Bioinformatics 26: 2334-2335
18. Hartwig B, James GV, Konrad K, Schneeberger K, Turck F (2012) Fast isogenic mapping-by-sequencing of ethyl methanesulfonate-induced mutant bulks. Plant Physiol 160: 591-600
19. Hodges M, Dellero Y, Keech O, Betti M, Raghavendra AS, Sage R, Zhu XG, Allen DK, Weber AP (2016) Perspectives for a better understanding of the metabolic integration of photorespiration within a complex plant primary metabolism network. J Exp Bot 67: 3015-3026
20. Hodges M, Jossier M, Boex-Fontvieille E, Tcherkez G (2013) Protein phosphorylation and photorespiration. Plant Biol (Stuttg) 15: 694-706
21. 2 induced cell death in Arabidopsis thaliana. BMC Genomics 16: 837
22. 2-dependent cell death. Plant Cell Environ 38: 253-265
23. 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
24. Lobell DB, Gourdji SM (2012) The influence of climate change on global crop productivity. Plant Physiol 160: 1686-1697
25. Louis A, Murat F, Salse J, Crollius HR (2015) GenomicusPlants: a web resource to study genome evolution in flowering plants. Plant Cell Physiol 56: e4
26. Maruta T, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2010) Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant Cell Physiol 51: 190-200
27. Massey V (1994) Activation of molecular oxygen by flavins and flavoproteins. J Biol Chem 269: 22459-22462
28. McCarthy DJ, Chen Y, Smyth GK (2012) Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res 40: 4288-4297
29. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498
30. Narendra S, Venkataramani S, Shen G, Wang J, Pasapula V, Lin Y, Kornyeyev D, Holaday AS, Zhang H (2006) The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J Exp Bot 57: 3033-3042
31. Noctor G, Veljovic-Jovanovic S, Driscoll S, 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
32. Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmiño DM, Gupta DK, Sandalio LM, Romero-Puertas MC (2012) S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J Exp Bot 63: 2089-2103
33. Pick TR, Bräutigam 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. Proc Natl Acad Sci USA 110: 3185-3190
34. Proost S, Van Bel M, Vaneechoutte D, Van de Peer Y, Inzé D, Mueller-Roeber B, Vandepoele K (2015) PLAZA 3.0: an access point for plant comparative genomics. Nucleic Acids Res 43: D974-D981
35. Pnueli L, Liang H, Rozenberg M, Mittler R (2003) Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J 34: 187-203
36. 2-induced cell death. Plant J 52: 640-657
37. 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. Plant Cell 19: 3170-3193
38. Rochaix JD (2014) Regulation and dynamics of the light-harvesting system. Annu Rev Plant Biol 65: 287-309
39. 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. Plant Cell 24: 336-352
40. Rouhier N, Villarejo A, Srivastava M, Gelhaye E, Keech O, Droux M, Finkemeier I, Samuelsson G, Dietz KJ, Jacquot JP, Wingsle G (2005) Identification of plant glutaredoxin targets. Antioxid Redox Signal 7: 919-929
41. Sage RF, Christin PA, Edwards EJ (2011) The C(4) plant lineages of planet Earth. J Exp Bot 62: 3155-3169
42. Schäfer L, Feierabend J (2000) Photoinactivation and protection of glycolate oxidase in vitro and in leaves. Z Naturforsch C 55: 361-372
43. Schneeberger K, Ossowski S, Lanz C, Juul T, Petersen AH, Nielsen KL, Jørgensen J-E, Weigel D, Andersen SU (2009) SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nat Methods 6: 550-551
44. Timm S, Bauwe H (2013) The variety of photorespiratory phenotypes-employing the current status for future research directions on photorespiration. Plant Biol (Stuttg) 15: 737-747
45. 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 Physiol 155: 694-705
46. Timm S, Nunes-Nesi A, Pärnik T, Morgenthal K, Wienkoop S, Keerberg O, Weckwerth W, Kleczkowski LA, Fernie AR, Bauwe H (2008) A cytosolic pathway for the conversion of hydroxypyruvate to glycerate during photorespiration in Arabidopsis. Plant Cell 20: 2848-2859
47. Vanderauwera S, Suzuki N, Miller G, van de Cotte B, Morsa S, Ravanat J-L, Hegie A, Triantaphylidès C, Shulaev V, Van Montagu MCE, Van Breusegem F, Mittler R (2011) Extranuclear protection of chromosomal DNA from oxidative stress. Proc Natl Acad Sci USA 108: 1711-1716
48. Walker BJ, VanLoocke A, Bernacchi CJ, Ort DR (2016) The costs of photorespiration to food production now and in the future. Annu Rev Plant Biol 67: 107-129
49. Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F, et al; Brassica rapa Genome Sequencing Project Consortium (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43: 1035-1039
50. Waszczak C, Kerchev K, Mühlenbock P, Frank A. Hoeberichts, Van Der Kelen K, Mhamdi A, Willems P, Denecker J, Kumpf R, Noctor G, Messens J, Van Breusegem F (2016) SHORT-ROOT deficiency alleviates the cell death phenotype of the Arabidopsis catalase2 mutant under photorespiration-promoting conditions. Plant Cell, in press
51. Wheeler T, von Braun J (2013) Climate change impacts on global food security. Science 341: 508-513
52. Willems P, Mhamdi A, Stael S, Storme V, Kerchev PI, Noctor G, Gevaert K, Van Breusegem F (2016) The ROS Wheel: refining ROS transcriptional footprints in Arabidopsis. Plant Physiol 171: 1720-1733
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. J Exp Bot 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 Cell Physiol 41: 1397-1406
55. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591
56. Zhang J, Nielsen R, Yang Z (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22: 2472-2479
57. 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