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NADPH recycling systems in oxidative stressed pea nodules: a key role for the NADP+-dependent isocitrate dehydrogenase

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Abstract

The symbiosis between legumes and rhizobia is characterised by the formation of dinitrogen-fixing root nodules. In natural conditions, nitrogen fixation is strongly impaired by abiotic stresses which generate over-production of reactive oxygen species. Since one of the nodule main antioxidant systems is the ascorbate–glutathione cycle, NADPH recycling that is involved in glutathione reduction is of great relevance under stress conditions. NADPH is mainly produced by glucose 6-phosphate dehydrogenase (G6PDH; EC 1.1.1.49) and 6-phosphogluconate dehydrogenase (6PGDH; EC 1.1.1.44) from the oxidative pentose phosphate pathway, and also by NADP+-dependent isocitrate dehydrogenase (ICDH; EC 1.1.1.42). In this work, 10 μM paraquat (PQ) was applied to pea roots in order to determine the in vivo relationship between oxidative stress and the activity of the NADPH-generating enzymes in nodules. Whereas G6PDH and 6PGDH activities remained unchanged, a remarkable induction of ICDH gene expression and a dramatic increase of the ICDH activity was observed during the PQ treatment. These results support that ICDH has a key role in NADPH recycling under oxidative stress conditions in pea root nodules.

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Abbreviations

2OG:

2-oxoglutarate

6PGDH:

6-phosphogluconate dehydrogenase

APX:

Ascorbate peroxidase

ASC:

Ascorbate

BNF:

Biological nitrogen fixation

CAT:

Catalase

DHA:

Dehydroascorbate

G6PDH:

Glucose-6-phosphate dehydrogenase

GSH:

Reduced glutathione

GSSG:

Oxidised glutathione

ICDH:

Isocitrate dehydrogenase

MnSOD:

Mn superoxide dismutase

OPPP:

Oxidative pentose phosphate pathway

PEPC:

Phosphoenolpyruvate carboxylase

PQ:

Paraquat

ROS:

Reactive oxygen species

SS:

Sucrose synthase

References

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Chen R (1998) Plant NADP-dependent isocitrate dehydrogenases are predominantly localized in the cytosol. Planta 207:280–285

    Article  PubMed  CAS  Google Scholar 

  • Chen RD, Gadal P (1990) Do mitochondria provide the 2-oxoglutarate needed for glutamate synthesis in higher plant chloroplasts? Plant Physiol Biochem 28:141–145

    CAS  Google Scholar 

  • Chen KM, Gong HJ, Chen GC, Wang SM, Zhang CL (2003) Up-regulation of glutathione metabolism and changes in redox status involved in adaptation of reed (Phragmites communis) ecotypes to drought-prone and saline habitats. J Plant Physiol 160:293–301

    Article  PubMed  CAS  Google Scholar 

  • Copeland L, Vella J, Hong ZQ (1989) Enzymes of carbohydrate metabolism in soybean nodules. Phytochemistry 28:57–61

    Article  CAS  Google Scholar 

  • Craig J, Barratt P, Tatge H, Dejardin A, Handley L, Gardner CD, Barber L, Wang T, Hedley C, Martin C, Smith AM (1999) Mutations at the rug4 locus alter the carbon and nitrogen metabolism of pea plants through an effect on sucrose synthase. Plant J 17:353–362

    Article  CAS  Google Scholar 

  • Dalton DA, Post CJ, Langeberg L (1991) Effects of ambient oxygen and of fixed nitrogen on concentrations of glutathione, ascorbate and associated enzymes in soybean root nodules. Plant Physiol 96:812–818

    PubMed  CAS  Google Scholar 

  • Dalton DA, Langeberg L, Treneman N (1993) Correlations between the ascorbate-glutathione pathway and effectiveness in legume root nodules. Physiol Plant 87:365–370

    Article  CAS  Google Scholar 

  • Davies MJ, Puppo A (1992) Direct detection of a globin-derived radical in leghaemoglobin treated with peroxides. Biochem J 281:197–201

    PubMed  CAS  Google Scholar 

  • Deutsch J (1978) Maleimide as an inhibitor in measurement of erythrocyte glucose-6-phosphate dehydrogenase activity. Clin Chem 24:885–889

    PubMed  CAS  Google Scholar 

  • Fahrendorf T, Ni W, Shorrosh BS, Dixon RA (1995) Stress responses in alfalfa (Medicago sativa L.) XIX. Transcriptional activation of oxidative pentose phosphate pathway genes at the onset of the isoflavonoid phytoalexin response. Plant Mol Biol 28:885–900

    Article  PubMed  CAS  Google Scholar 

  • Ferri A, Lluch C, Ocaña A (2000) Effect of salt stress on carbon metabolism and bacteroid respiration in root nodules of common bean (Phaseolus vulgaris L.). Plant Biol 2:396–402

    Article  CAS  Google Scholar 

  • Gálvez S, Lancien M, Hodges M (1999) Are isocitrate dehydrogenases and 2-oxoglutarate involved in the regulation of glutamate synthesis? Trends Plant Sci 4:484–490

    Article  PubMed  Google Scholar 

  • Gálvez L, González EM, Arrese-Igor C (2005) Evidence for carbon flux shortage and strong carbon/nitrogen interactions in pea nodules at early stages of water stress. J Exp Bot 56:2551–2561

    Article  PubMed  CAS  Google Scholar 

  • Hernández-Jiménez MJ, Lucas MM, de Felipe MR (2002) Antioxidant defence and damage in senescencing lupin nodules. Plant Physiol Biochem 40:645–657

    Article  Google Scholar 

  • Hodges M, Flesch V, Gálvez S, Bismuth E (2003) Higher plant NADP+-dependent isocitrate dehydrogenases, ammonium assimilation and NADPH production. Plant Physiol Biochem 41:577–585

    Article  CAS  Google Scholar 

  • Isin SH, Allen RD (1991) Isolation and characterization of a pea catalase cDNA. Plant Mol Biol 17:1263–1265

    Article  PubMed  CAS  Google Scholar 

  • Iturbe-Ormaetxe I, Escuredo PR, Arrese-Igor C, Becana M (1998) Oxidative damage in pea plants exposed to water deficit or paraquat. Plant Physiol 116:173–181

    Article  CAS  Google Scholar 

  • Jo SH, Son MK, Koh HJ, Lee SM, Song IH, Kim YO, Lee YS, Jeong KS, Kim WB, Park JW, Song BJ, Huhe TL (2001) Control of mitochondrial redox balance and cellular defence against oxidative damage by mitochondrial NADP+-dependent isocitrate dehydrogenase. J Biol Chem 276:16168–16176

    Article  PubMed  CAS  Google Scholar 

  • Kim SY, Park JW (2003) Cellular defence against singlet oxygen-induced oxidative damage by cytosolic NADP+-dependent isocitrate dehydrogenase. Free Radic Res 37:309–316

    Article  PubMed  CAS  Google Scholar 

  • Kim HJ, Kang BS, Park JW (2005) Cellular defence against heat shock-induced oxidative damage by mitochondrial NADP+-dependent isocitrate dehydrogenase. Free Radic Res 39:441–448

    Article  PubMed  CAS  Google Scholar 

  • Kruse A, Fieuw S, Heineke D, Müller-Röber B (1998) Antisense inhibition of cytosolic NADP-dependent isocitrate dehydrogenase in transgenic potato plants. Planta 205:82–91

    Article  CAS  Google Scholar 

  • Labhilili M, Joudrier P, Gautier MF (1995) Characterization of cDNAs encoding Triticum durum dehydrins and their expression patterns in cultivars that differ in drought tolerance. Plant Sci 112:219–230

    Article  CAS  Google Scholar 

  • León AM, Palma JM, Corpas FJ, Gómez M, Romero-Puertas MC, Chatterjee D, Mateos RM, del Río LA, Sandalio LM (2002) Antioxidative enzymes in cultivars of pepper plants with different sensitivity to cadmium. Plant Physiol Biochem 40:813–820

    Article  Google Scholar 

  • Leterrier M, del Río LA, Corpas FJ (2004). Pisum sativum NADP-dependent isocitrate dehydrogenase I gene, complete cds. (Accesion No. AY730588)

  • Marino D, González EM, Arrese-Igor C (2006) Drought effects on carbon and nitrogen metabolism of pea nodules can be mimicked by paraquat: evidence for the occurrence of two regulation pathways under oxidative stresses. J Exp Bot 57:665–673

    Article  PubMed  CAS  Google Scholar 

  • Matamoros MA, Baird LM, Escuredo PR, Dalton DA, Minchin FR, Iturbe-Ormaetxe I, Rubio MC, Moran JF, Gordon AJ, Becana M (1999). Stress-induced legume root nodule senescence. Physiological, biochemical, and structural alterations. Plant Physiol 121:97–111

    Article  PubMed  CAS  Google Scholar 

  • Mattioni C, Gabbrielli R, Vangronsveld J, Clijsters H (1997) Nickel and cadmium toxicity and enzymatic activity in Ni-tolerant and non-tolerant populations of Silene italica Pers. J Plant Physiol 150:173–177

    CAS  Google Scholar 

  • Mittler R, Zilinskas BA (1991) Molecular cloning and nucleotide sequence analysis of a cDNA encoding pea cytosolic ascorbate peroxidase. FEBS Lett 289:257–259

    Article  PubMed  CAS  Google Scholar 

  • Moran JF, Becana M, Iturbe-Ormaetxe I, Frechilla S, Klucas RV, Aparicio-Tejo PM (1994) Drought induces oxidative stress in pea plants. Planta 194:346–352

    Article  CAS  Google Scholar 

  • Moreau S, Davies MJ, Mathieu C, Herouart D, Puppo A (1996) Lb derived radicals. Evidence for multiple protein-derived radicals and the initiation of peribacteroid membrane damage. J Biol Chem 271:32557–32562

    Article  PubMed  CAS  Google Scholar 

  • Pandolfi PP, Sonati F, Rivi R, Mason P, Grosveld F, Luzzato L (1995) Targeted disruption of the housekeeping gene encoding glucose-6-phosphate dehydrogenase (G6PD): G6PD is dispensable for pentose synthesis but essential for defence against oxidative stress. EMBO J 14:5209–5215

    PubMed  CAS  Google Scholar 

  • Prasad TK, Anderson MD, Martín BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6:65–74

    Article  PubMed  CAS  Google Scholar 

  • Puppo A, Herrada G, Rigaud J (1991) Lipid peroxidation in peribacteroid membranes from French bean nodules. Plant Physiol 96:826–830

    Article  PubMed  CAS  Google Scholar 

  • Puppo A, Groten K, Bastian F, Carzaniga R, Soussi M, Lucas MM, de Felipe MR, Harrison J, Vanacker H, Foyer CH (2005) Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol 165:683–701

    Article  PubMed  CAS  Google Scholar 

  • Rigaud J, Puppo A (1975) Indole-3-acetic catabolism by soybean bacteroids. J Gen Microbiol 88:223–228

    Google Scholar 

  • Romero-Puertas MC, McCarthy I, Sandalio LM, Palma JM, Corpas VJ, Gómez M, del Río LA (1999) Cadmium toxicity and oxidative metabolism of pea leaf peroxisomes. Free Radic Res 31:S25-S32

    Article  PubMed  CAS  Google Scholar 

  • Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    PubMed  CAS  Google Scholar 

  • Su ML, Koh JJ, Park DC, Song BJ, Huh TL, Park JW (2002) Cytosolic NADP+-dependent isocitrate dehydrogenase status modulates oxidative damage to cells. Free Radic Biol Med 32:1185–1196

    Article  Google Scholar 

  • Suganuma N, Okada Y, Kanayama Y (1997) Isolation of a cDNA for nodule-enhanced phosphoenolpyruvate carboxylase from pea and its expression in effective and plant-determined ineffective pea nodules. J Exp Bot 48:1165–1173

    CAS  Google Scholar 

  • Wong-Vega L, Burke JJ, Allen RD (1991) Isolation and sequence analysis of a cDNA that encodes pea manganese superoxide dismutase. Plant Mol Biol 17:1271–1274

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Gustavo Garijo, Elena Denia and Regina Galarza for technical assistance and Bonduelle SA for providing pea seeds. Daniel Marino is the holder of a funding grant from the Basque Government. Nitrogenase antibody was kindly provided by Dr. Paul Ludden. This work was supported by DGI-MEC (Spain) funding grant AGL2005-00274 and its associated FEDER funding.

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Authors and Affiliations

  1. Departamento de Ciencias del Medio Natural, Universidad Pública de Navarra, Campus Arrosadía, 31006, Pamplona, Spain

    Daniel Marino, Esther M. González & Cesar Arrese-Igor

  2. Interactions Plantes-Microorganismes et Santé Végétale, UMR CNRS 6192 – INRA 1064 – Université de Nice – Sophia Antipolis, 400, Route des Chappes, BP167, 06903, Sophia Antipolis Cedex, France

    Pierre Frendo & Alain Puppo

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  1. Daniel Marino
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  2. Esther M. González
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  3. Pierre Frendo
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  4. Alain Puppo
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  5. Cesar Arrese-Igor
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Correspondence to Cesar Arrese-Igor.

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Marino, D., González, E.M., Frendo, P. et al. NADPH recycling systems in oxidative stressed pea nodules: a key role for the NADP+-dependent isocitrate dehydrogenase. Planta 225, 413–421 (2007). https://doi.org/10.1007/s00425-006-0354-5

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