Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase

Hebbelmann I, Selinski J, Wehmeyer C, Goss T, Voss I, Mulo P, Kangasjarvi S, Aro E-M, Oelze M-L, Dietz K-J, Nunes-Nesi A, et al. (2012)
Journal of Experimental Botany 63(3): 1445-1459.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Autor*in
Hebbelmann, Inga; Selinski, Jennifer; Wehmeyer, Corinna; Goss, Tatjana; Voss, Ingo; Mulo, Paula; Kangasjarvi, Saijaliisa; Aro, Eva-Mari; Oelze, Marie-LuiseUniBi; Dietz, Karl-JosefUniBi; Nunes-Nesi, Adriano; Do, Phuc T
Alle
Abstract / Bemerkung
The nuclear-encoded chloroplast NADP-dependent malate dehydrogenase (NADP-MDH) is a key enzyme controlling the malate valve, to allow the indirect export of reducing equivalents. Arabidopsis thaliana (L.) Heynh. T-DNA insertion mutants of NADP-MDH were used to assess the role of the light-activated NADP-MDH in a typical C(3) plant. Surprisingly, even when exposed to high-light conditions in short days, nadp-mdh knockout mutants were phenotypically indistinguishable from the wild type. The photosynthetic performance and typical antioxidative systems, such as the Beck-Halliwell-Asada pathway, were barely affected in the mutants in response to high-light treatment. The reactive oxygen species levels remained low, indicating the apparent absence of oxidative stress, in the mutants. Further analysis revealed a novel combination of compensatory mechanisms in order to maintain redox homeostasis in the nadp-mdh plants under high-light conditions, particularly an increase in the NTRC/2-Cys peroxiredoxin (Prx) system in chloroplasts. There were indications of adjustments in extra-chloroplastic components of photorespiration and proline levels, which all could dissipate excess reducing equivalents, sustain photosynthesis, and prevent photoinhibition in nadp-mdh knockout plants. Such metabolic flexibility suggests that the malate valve acts in concert with other NADPH-consuming reactions to maintain a balanced redox state during photosynthesis under high-light stress in wild-type plants.
Erscheinungsjahr
2012
Zeitschriftentitel
Journal of Experimental Botany
Band
63
Ausgabe
3
Seite(n)
1445-1459
ISSN
0022-0957
eISSN
1460-2431
Page URI
https://pub.uni-bielefeld.de/record/2471721

Zitieren

Hebbelmann I, Selinski J, Wehmeyer C, et al. Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase. Journal of Experimental Botany. 2012;63(3):1445-1459.
Hebbelmann, I., Selinski, J., Wehmeyer, C., Goss, T., Voss, I., Mulo, P., Kangasjarvi, S., et al. (2012). Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase. Journal of Experimental Botany, 63(3), 1445-1459. doi:10.1093/jxb/err386
Hebbelmann, Inga, Selinski, Jennifer, Wehmeyer, Corinna, Goss, Tatjana, Voss, Ingo, Mulo, Paula, Kangasjarvi, Saijaliisa, et al. 2012. “Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase”. Journal of Experimental Botany 63 (3): 1445-1459.
Hebbelmann, I., Selinski, J., Wehmeyer, C., Goss, T., Voss, I., Mulo, P., Kangasjarvi, S., Aro, E. - M., Oelze, M. - L., Dietz, K. - J., et al. (2012). Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase. Journal of Experimental Botany 63, 1445-1459.
Hebbelmann, I., et al., 2012. Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase. Journal of Experimental Botany, 63(3), p 1445-1459.
I. Hebbelmann, et al., “Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase”, Journal of Experimental Botany, vol. 63, 2012, pp. 1445-1459.
Hebbelmann, I., Selinski, J., Wehmeyer, C., Goss, T., Voss, I., Mulo, P., Kangasjarvi, S., Aro, E.-M., Oelze, M.-L., Dietz, K.-J., Nunes-Nesi, A., Do, P.T., Fernie, A.R., Talla, S.K., Raghavendra, A.S., Linke, V., Scheibe, R.: Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase. Journal of Experimental Botany. 63, 1445-1459 (2012).
Hebbelmann, Inga, Selinski, Jennifer, Wehmeyer, Corinna, Goss, Tatjana, Voss, Ingo, Mulo, Paula, Kangasjarvi, Saijaliisa, Aro, Eva-Mari, Oelze, Marie-Luise, Dietz, Karl-Josef, Nunes-Nesi, Adriano, Do, Phuc T, Fernie, Alisdair R, Talla, Sai K, Raghavendra, Agepati S, Linke, Vera, and Scheibe, Renate. “Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase”. Journal of Experimental Botany 63.3 (2012): 1445-1459.

49 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Toward an Integrated Understanding of Retrograde Control of Photosynthesis.
Dietz KJ, Wesemann C, Wegener M, Seidel T., Antioxid Redox Signal 30(9), 2019
PMID: 29463103
Malate valves: old shuttles with new perspectives.
Selinski J, Scheibe R., Plant Biol (Stuttg) 21 Suppl 1(), 2019
PMID: 29933514
Small RNA sequencing reveals dynamic microRNA expression of important nutrient metabolism during development of Camellia oleifera fruit.
Liu XX, Luo XF, Luo KX, Liu YL, Pan T, Li ZZ, Duns GJ, He FL, Qin ZD., Int J Biol Sci 15(2), 2019
PMID: 30745831
Comparative analysis of constitutive proteome between resistant and susceptible tomato genotypes regarding to late blight.
Laurindo BS, Laurindo RDF, Fontes PP, Vital CE, Delazari FT, Baracat-Pereira MC, da Silva DJH., Funct Integr Genomics 18(1), 2018
PMID: 28856505
Plastidial NAD-Dependent Malate Dehydrogenase: A Moonlighting Protein Involved in Early Chloroplast Development through Its Interaction with an FtsH12-FtsHi Protease Complex.
Schreier TB, Cléry A, Schläfli M, Galbier F, Stadler M, Demarsy E, Albertini D, Maier BA, Kessler F, Hörtensteiner S, Zeeman SC, Kötting O., Plant Cell 30(8), 2018
PMID: 29934433
Interorganelle Communication: Peroxisomal MALATE DEHYDROGENASE2 Connects Lipid Catabolism to Photosynthesis through Redox Coupling in Chlamydomonas.
Kong F, Burlacot A, Liang Y, Légeret B, Alseekh S, Brotman Y, Fernie AR, Krieger-Liszkay A, Beisson F, Peltier G, Li-Beisson Y., Plant Cell 30(8), 2018
PMID: 29997239
Ferredoxin/thioredoxin system plays an important role in the chloroplastic NADP status of Arabidopsis.
Hashida SN, Miyagi A, Nishiyama M, Yoshida K, Hisabori T, Kawai-Yamada M., Plant J 95(6), 2018
PMID: 29920827
The chloroplast 2-cysteine peroxiredoxin functions as thioredoxin oxidase in redox regulation of chloroplast metabolism.
Vaseghi MJ, Chibani K, Telman W, Liebthal MF, Gerken M, Schnitzer H, Mueller SM, Dietz KJ., Elife 7(), 2018
PMID: 30311601
The redox control of photorespiration: from biochemical and physiological aspects to biotechnological considerations.
Keech O, Gardeström P, Kleczkowski LA, Rouhier N., Plant Cell Environ 40(4), 2017
PMID: 26791824
Thioredoxins Play a Crucial Role in Dynamic Acclimation of Photosynthesis in Fluctuating Light.
Thormählen I, Zupok A, Rescher J, Leger J, Weissenberger S, Groysman J, Orwat A, Chatel-Innocenti G, Issakidis-Bourguet E, Armbruster U, Geigenberger P., Mol Plant 10(1), 2017
PMID: 27940305
Specific Arabidopsis thaliana malic enzyme isoforms can provide anaplerotic pyruvate carboxylation function in Saccharomyces cerevisiae.
Badia MB, Mans R, Lis AV, Tronconi MA, Arias CL, Maurino VG, Andreo CS, Drincovich MF, van Maris AJ, Gerrard Wheeler MC., FEBS J 284(4), 2017
PMID: 28075062
Chloroplast proteome response to drought stress and recovery in tomato (Solanum lycopersicum L.).
Tamburino R, Vitale M, Ruggiero A, Sassi M, Sannino L, Arena S, Costa A, Batelli G, Zambrano N, Scaloni A, Grillo S, Scotti N., BMC Plant Biol 17(1), 2017
PMID: 28183294
The multigenerational effects of water contamination and endocrine disrupting chemicals on the fitness of Drosophila melanogaster.
Quesada-Calderón S, Bacigalupe LD, Toro-Vélez AF, Madera-Parra CA, Peña-Varón MR, Cárdenas-Henao H., Ecol Evol 7(16), 2017
PMID: 28861253
Partial protective immunity against toxoplasmosis in mice elicited by recombinant Toxoplasma gondii malate dehydrogenase.
Liu Z, Yuan F, Yang Y, Yin L, Liu Y, Wang Y, Zheng K, Cao J., Vaccine 34(7), 2016
PMID: 26514423
The origin of cytosolic ATP in photosynthetic cells.
Gardeström P, Igamberdiev AU., Physiol Plant 157(3), 2016
PMID: 27087668
Redox- and Reactive Oxygen Species-Dependent Signaling into and out of the Photosynthesizing Chloroplast.
Dietz KJ, Turkan I, Krieger-Liszkay A., Plant Physiol 171(3), 2016
PMID: 27255485
Comparative proteomics of cucurbit phloem indicates both unique and shared sets of proteins.
Lopez-Cobollo RM, Filippis I, Bennett MH, Turnbull CG., Plant J 88(4), 2016
PMID: 27472661
The metabolomics of oxidative stress.
Noctor G, Lelarge-Trouverie C, Mhamdi A., Phytochemistry 112(), 2015
PMID: 25306398
Proteomic analysis of Citrus sinensis roots and leaves in response to long-term magnesium-deficiency.
Peng HY, Qi YP, Lee J, Yang LT, Guo P, Jiang HX, Chen LS., BMC Genomics 16(), 2015
PMID: 25887480
2-Hydroxy Acids in Plant Metabolism.
Maurino VG, Engqvist MK., Arabidopsis Book 13(), 2015
PMID: 26380567
Arabidopsis tic62 trol mutant lacking thylakoid-bound ferredoxin-NADP+ oxidoreductase shows distinct metabolic phenotype.
Lintala M, Schuck N, Thormählen I, Jungfer A, Weber KL, Weber AP, Geigenberger P, Soll J, Bölter B, Mulo P., Mol Plant 7(1), 2014
PMID: 24043709
The plastid-localized NAD-dependent malate dehydrogenase is crucial for energy homeostasis in developing Arabidopsis thaliana seeds.
Selinski J, König N, Wellmeyer B, Hanke GT, Linke V, Neuhaus HE, Scheibe R., Mol Plant 7(1), 2014
PMID: 24198233
Plastidial NAD-dependent malate dehydrogenase is critical for embryo development and heterotrophic metabolism in Arabidopsis.
Beeler S, Liu HC, Stadler M, Schreier T, Eicke S, Lue WL, Truernit E, Zeeman SC, Chen J, Kötting O., Plant Physiol 164(3), 2014
PMID: 24453164
Putative role of the malate valve enzyme NADP-malate dehydrogenase in H2O2 signalling in Arabidopsis.
Heyno E, Innocenti G, Lemaire SD, Issakidis-Bourguet E, Krieger-Liszkay A., Philos Trans R Soc Lond B Biol Sci 369(1640), 2014
PMID: 24591715
Metabolic control of redox and redox control of metabolism in plants.
Geigenberger P, Fernie AR., Antioxid Redox Signal 21(9), 2014
PMID: 24960279
The spatial organization of metabolism within the plant cell.
Sweetlove LJ, Fernie AR., Annu Rev Plant Biol 64(), 2013
PMID: 23330793
Emerging concept for the role of photorespiration as an important part of abiotic stress response.
Voss I, Sunil B, Scheibe R, Raghavendra AS., Plant Biol (Stuttg) 15(4), 2013
PMID: 23452019
Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress.
Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V, Molassiotis A., Plant J 72(4), 2012
PMID: 22780834
Action of gibberellins on growth and metabolism of Arabidopsis plants associated with high concentration of carbon dioxide.
Ribeiro DM, Araújo WL, Fernie AR, Schippers JH, Mueller-Roeber B., Plant Physiol 160(4), 2012
PMID: 23090585

62 References

Daten bereitgestellt von Europe PubMed Central.

Noncompetitive RT-PCR
Ahn JH., 2002
Reductive modification and nonreductive activation of purified spinach chloroplast NADP-dependent glyceraldehyde-3-phosphate dehydrogenase.
Baalmann E, Backhausen JE, Rak C, Vetter S, Scheibe R., Arch. Biochem. Biophys. 324(2), 1995
PMID: 8554310
Rapid determination of free proline for water-stress studies
Bates LS, Waldren RP, Teare ID., 1973
Purification of chloroplasts from fruits of green-pepper (Capsicum annuum L.) and characterization of starch synthesis. Evidence for a functional hexose-phosphate translocator
Batz O, Scheibe R, Neuhaus HE., 1995
Photorespiration: players, partners and origin.
Bauwe H, Hagemann M, Fernie AR., Trends Plant Sci. 15(6), 2010
PMID: 20403720
Influence of the photoperiod on redox regulation and stress responses in Arabidopsis thaliana L. (Heynh.) plants under long- and short-day conditions.
Becker B, Holtgrefe S, Jung S, Wunrau C, Kandlbinder A, Baier M, Dietz KJ, Backhausen JE, Scheibe R., Planta 224(2), 2006
PMID: 16435132
Proline accumulation in higher plants: a redox buffer?
Bellinger Y, Larher F., 1987
Antioxidant defences under hyperoxygenic and hyperosmotic conditions in leaves of two lines of maize with differential sensitivity to drought
Del OT, González CA, Pastori GM, Trippi VS., 1993
The function of peroxiredoxins in plant organelle redox metabolism.
Dietz KJ, Jacob S, Oelze ML, Laxa M, Tognetti V, de Miranda SM, Baier M, Finkemeier I., J. Exp. Bot. 57(8), 2006
PMID: 16606633
Redox equilibria between the regulatory thiols of light/dark-modulated chloroplast enzymes and dithiothreitol: fine-tuning by metabolites.
Faske M, Holtgrefe S, Ocheretina O, Meister M, Backhausen JE, Scheibe R., Biochim. Biophys. Acta 1247(1), 1995
PMID: 7873583
The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism
Foyer CH, Halliwell B., 1976
Photorespiratory metabolism: genes, mutants, energetics, and redox signaling.
Foyer CH, Bloom AJ, Queval G, Noctor G., Annu Rev Plant Biol 60(), 2009
PMID: 19575589
The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence
Genty B, Briantais J-M, Baker NR., 1989
The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress.
Giraud E, Ho LH, Clifton R, Carroll A, Estavillo G, Tan YF, Howell KA, Ivanova A, Pogson BJ, Millar AH, Whelan J., Plant Physiol. 147(2), 2008
PMID: 18424626
Use of transgenic plants to uncover strategies for maintenance of redox-homeostasis during photosynthesis
Hanke GT, Holtgrefe S, König N, Strodtkötter I, Voss I, Scheibe R., 2009
Proline synthesis and degradation: a model system for elucidating stress-related signal transduction
Hare PD, Cress WA, van J., 1999
Diverse roles for chloroplast stromal and thylakoid-bound ascorbate peroxidases in plant stress responses.
Kangasjarvi S, Lepisto A, Hannikainen K, Piippo M, Luomala EM, Aro EM, Rintamaki E., Biochem. J. 412(2), 2008
PMID: 18318659
The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux
König J, Baier M, Horling F, Kahmann U, Harris G, Schürmann P, Dietz KJ., 2002
Rates and roles of cyclic and alternative electron flow in potato leaves.
Laisk A, Eichelmann H, Oja V, Talts E, Scheibe R., Plant Cell Physiol. 48(11), 2007
PMID: 17938131
EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana
Lee KP, Kim C, Landgraf F, Apel K., 2007
Chloroplast NADPH-thioredoxin reductase interacts with photoperiodic development in Arabidopsis.
Lepisto A, Kangasjarvi S, Luomala EM, Brader G, Sipari N, Keranen M, Keinanen M, Rintamaki E., Plant Physiol. 149(3), 2009
PMID: 19151130
Gas chromatography mass spectrometry-based metabolite profiling in plants.
Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR., Nat Protoc 1(1), 2006
PMID: 17406261
The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development.
Narendra S, Venkataramani S, Shen G, Wang J, Pasapula V, Lin Y, Kornyeyev D, Holaday AS, Zhang H., J. Exp. Bot. 57(12), 2006
PMID: 16873450
Safety valves for photosynthesis.
Niyogi KK., Curr. Opin. Plant Biol. 3(6), 2000
PMID: 11074375
Ascorbate and glutathione: keeping active oxygen under control
Noctor G, Foyer CH., 1998
Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants.
Nunes-Nesi A, Carrari F, Lytovchenko A, Smith AM, Loureiro ME, Ratcliffe RG, Sweetlove LJ, Fernie AR., Plant Physiol. 137(2), 2005
PMID: 15665243
Response of photosynthetic carbon assimilation in mesophyll protoplasts to restriction on mitochondrial oxidative metabolism: metabolites related to the redox status and sucrose biosynthesis
Padmasree K, Raghavendra AS., 1999
Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage.
Perez-Ruiz JM, Spinola MC, Kirchsteiger K, Moreno J, Sahrawy M, Cejudo FJ., Plant Cell 18(9), 2006
PMID: 16891402
Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress.
Piippo M, Allahverdiyeva Y, Paakkarinen V, Suoranta UM, Battchikova N, Aro EM., Physiol. Genomics 25(1), 2006
PMID: 16403842
Functional analysis of the pathways for 2-Cys peroxiredoxin reduction in Arabidopsis thaliana chloroplasts.
Pulido P, Spinola MC, Kirchsteiger K, Guinea M, Pascual MB, Sahrawy M, Sandalio LM, Dietz KJ, Gonzalez M, Cejudo FJ., J. Exp. Bot. 61(14), 2010
PMID: 20616155
Preparation of Arabidopsis mesophyll protoplasts with high rates of photosynthesis
Riazunnisa K, Padmavathi L, Scheibe R, Raghavendra AS., 2007
Malate valves to balance cellular energy supply.
Scheibe R., Physiol Plant 120(1), 2004
PMID: 15032873
Strategies to maintain redox homeostasis during photosynthesis under changing conditions.
Scheibe R, Backhausen JE, Emmerlich V, Holtgrefe S., J. Exp. Bot. 56(416), 2005
PMID: 15851411
Reduction–oxidation network for flexible adjustment of cellular metabolism in photoautotrophic cells
Scheibe R, Dietz KJ., 2011
NADP regulates the light activation of NADP-dependent malate dehydrogenase
Scheibe R, Jacquot JP., 1983
Comparison of NADP-malate dehydrogenase activation, Q reduction and O evolution in spinach leaves
Scheibe R, Stitt M., 1988
Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer
Schreiber U, Schliwa U, Bilger W., 1986
Relationship between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages
Sims DA, Gamon JA., 2002
Statistical issues in cDNA microarray data analysis.
Smyth GK, Yang YH, Speed T., Methods Mol. Biol. 224(), 2003
PMID: 12710670
NTRC new ways of using NADPH in the chloroplast.
Spinola MC, Perez-Ruiz JM, Pulido P, Kirchsteiger K, Guinea M, Gonzalez M, Cejudo FJ., Physiol Plant 133(3), 2008
PMID: 18346073
Induction of the AOX1D isoform of alternative oxidase in A. thaliana T-DNA insertion lines lacking isoform AOX1A is insufficient to optimize photosynthesis when treated with antimycin A.
Strodtkotter I, Padmasree K, Dinakar C, Speth B, Niazi PS, Wojtera J, Voss I, Do PT, Nunes-Nesi A, Fernie AR, Linke V, Raghavendra AS, Scheibe R., Mol Plant 2(2), 2009
PMID: 19825614
Proline: a multifunctional amino acid.
Szabados L, Savoure A., Trends Plant Sci. 15(2), 2009
PMID: 20036181
Mitochondrial malate dehydrogenase lowers leaf respiration and alters photorespiration and plant growth in Arabidopsis.
Tomaz T, Bagard M, Pracharoenwattana I, Linden P, Lee CP, Carroll AJ, Stroher E, Smith SM, Gardestrom P, Millar AH., Plant Physiol. 154(3), 2010
PMID: 20876337

Walker D., 1988
Photorespiration: metabolic pathways and their role in stress protection
Wingler A, Lea PJ, Quick WP, Leegood RC., 2000
A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid
Wilson AK, Pickett FB, Turner JC, Estelle M., 1990
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 22140244
PubMed | Europe PMC

Suchen in

Google Scholar