Skip to main content

Advertisement

Log in

Involvement of nitrate reduction in the tolerance of tomato (Solanum lycopersicum L.) plants to prolonged root hypoxia

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

The putative role of nitrate and nitrate reductase in the tolerance to prolonged hypoxia was investigated in tomato plants. Nitrogen nutrition has been modified either by deprivation of nitrate or by addition of tungstate—an inhibitor of nitrate reductase (NR)—in the culture medium. In the absence of nitrate as well as in the presence of tungstate, plant growth was significantly disturbed. In the presence of nitrate, the growth of hypoxic plants maintained, nitrate absorption and NR activity increased and a significant release of nitrite into the medium was observed. This mechanism of nitrate reduction, called nitrate respiration, could be an alternative pathway to oxygen-dependent respiration during root hypoxia and a transient adaptation of tomato roots to hypoxic conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Andrews M (1986) The partitioning of nitrate assimilation between root and shoot of higher plants. Plant Cell Environ 9:511–586

    CAS  Google Scholar 

  • Arnon DI (1937) Ammonium and nitrate nitrogen nutrition of barley and rice at different seasons in relation to hydrogen-ion concentrations, manganese, copper and oxygen supplied. Soil Sci 44:91–121

    Article  CAS  Google Scholar 

  • Aschi-Smiti S, Bizid E, Hamza M (2003a) Effet de l’hydromorphie sur la croissance de 4 variétés de trèfle (Trifolium subterraneum L.). Agron 23:97–104

    Article  Google Scholar 

  • Aschi-Smiti S, Chaibi W, Brouquisse R, Ricard B, Saglio P (2003b) Assessment of enzyme induction and aerenchyma formation as mechanisms for flooding tolerance in Trifolium subterraneum ‘Park’. Ann Bot 91:195–204

    Article  CAS  PubMed  Google Scholar 

  • Beutler H-O (1984) Ethanol. In: Bergmeyer J, Grassl M (eds) Metabolites 1: carbohydrates, vol VI. Verlag Chemie, Weinheim, pp 598–606

    Google Scholar 

  • Blom CWPM, Voesenek LACJ (1996) Flooding: the survival strategies of plants. Trends Ecol Evol 11:290–295

    Article  Google Scholar 

  • Botrel A, Kaiser WM (1997) Nitrate reductase activation state in barley roots in relation to the energy and carbohydrate status. Planta 201:496–501

    Article  CAS  PubMed  Google Scholar 

  • Botrel A, Magne C, Kaiser WM (1996) Nitrate reduction, nitrite reduction and ammonium assimilation in barley roots in response to anoxia. Plant Physiol Biochem 34:645–652

    CAS  Google Scholar 

  • Bradford KJ, Yang SF (1981) Physiological responses of plants to waterlogging. Hortic Sci 16:3–8

    Google Scholar 

  • Brouquisse R, James F, Raymond P, Pradet A (1992) Asparagine metabolism and nitrogen distribution during protein degradation in sugar-starved maize root tips. Planta 188:384–395

    Article  CAS  Google Scholar 

  • Buwalda F, Greenway H (1989) Nitrogen uptake and growth of wheat during O2 deficiency in root media containing NO3 only, or NO3 plus NH4 +. New Phytol 111:161–166

    Article  CAS  Google Scholar 

  • Cataldo DA, Haroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6:71–80

    Article  CAS  Google Scholar 

  • Chrikova TV, Belonogova VA (1991) Nitrate reductase activity and productivity of grain crops under waterlogged conditions. Sov Soil Sci 22:19–29

    Google Scholar 

  • Crawford NM (1995) Nitrate: nutrient and signal for plant growth. Plant Cell 7:859–868

    Article  CAS  PubMed  Google Scholar 

  • Davies DD (1980) Anaerobic metabolism and the production of organic acids. In: Davies DD (ed) The Biochemistry of Plants, vol II. Academic Press, New York, pp 581–611

    Google Scholar 

  • Deng MD, Lamaze T, Morot-Gaudry J (1989) A new experimental approach involving the simultaneous use of tungstate and ammonium for studying the physiological effect of the absence of nitrate reduction. Plant Physiol Biochem 27:690–696

    Google Scholar 

  • Drew MC (1990) Sensing soil oxygen. Plant Cell Environ 13:681–693

    Article  CAS  Google Scholar 

  • Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol 48:223–250

    Article  CAS  PubMed  Google Scholar 

  • Drew MC, Saglio PH, Pradet A (1985) Larger adenylate energy charge and ATP/ADP ratios in aerenchymatous roots of Zea mays in anaerobic media as a consequence of improved internal oxygen transport. Planta 165:51–58

    Article  CAS  Google Scholar 

  • Ferrari TE, Yoder OC, Filner P (1973) Anaerobic nitrite production by plant cells and tissues: evidence for two nitrate pools. Plant Physiol 51:423–431

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Novo F, Crawford RMM (1973) Soil aeration, nitrate reduction and flooding tolerance in higher plants. New Phytol 72:1031–1039

    Article  CAS  Google Scholar 

  • Gharbi I, Ricard B, Rolin D, Maucourt M, Andrieu MH, Bizid E, Aschi-Smiti S, Brouquisse R (2007) Effect of hexokinase activity on tomato root metabolism during prolonged hypoxia. Plant Cell Environ 30:508–517

    Article  CAS  PubMed  Google Scholar 

  • Gharbi I, Ricard B, Aschi-Smiti S, Bizid E, Brouquisse R (2009) Increased hexose transport in the roots of tomato plants submitted to prolonged hypoxia. Planta 230:441–448

    Article  CAS  PubMed  Google Scholar 

  • Gibbs J, Greenway H (2003) Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Funct Plant Biol 30:1–47

    Article  CAS  Google Scholar 

  • Gojon A, Bussi C, Grignon C, Salsac L (1991) Distribution of NO3 reduction between roots and shoots of peach tree seedlings as affected by NO3 uptake rate. Physiol Plant 82:502–512

    Article  Google Scholar 

  • Greenway H, Gibbs J (2003) Mechanisms of anoxia tolerance in plants. II. Energy requirements for maintenance and energy distribution to essential processes. Funct Plant Biol 30:999–1036

    Article  CAS  Google Scholar 

  • Heeb A, Lundegardh B, Ericson T, Savage GP (2005) Effects of nitrate, ammonium and organic-nitrogen-based fertilizers on growth and yield of tomatoes. J Plant Nutr Soil Sci 168:123–129

    Article  CAS  Google Scholar 

  • Henshaw TL, Gilbert RA, Scholberg JMS, Sinclair TR (2007a) Soya bean (Glycine max L. Merr.) genotype response to early-season flooding: II. Aboveground growth and biomass. J Agron Crop Sci 193:189–197

    Article  Google Scholar 

  • Henshaw TL, Gilbert RA, Scholberg JMS, Sinclair TR (2007b) Soya bean (Glycine max L. Merr.) genotype response to early-season flooding: I. Root and nodule development. J Agron Crop Sci 193:177–188

    Article  Google Scholar 

  • Horchani F, Aloui A, Brouquisse R, Aschi-Smiti S (2008a) Physiological responses of tomato plants (Solanum lycopersicum) as affected by root hypoxia. J Agron Crop Sci 194:297–303

    Article  CAS  Google Scholar 

  • Horchani F, Gallusci P, Baldet P, Cabasson C, Maucourt M, Rolin D, Aschi-Smiti S, Raymond P (2008b) Prolonged root hypoxia induces ammonium accumulation and decreases the nutritional quality of tomato fruits. J Plant Physiol 165:1352–1359

    Article  CAS  PubMed  Google Scholar 

  • Horchani F, Khayati H, Raymond P, Brouquisse R, Aschi-Smiti S (2009) Contrasted effects of prolonged root hypoxia on tomato (Solanum lycopersicum) roots and fruits metabolism. J Agron Crop Sci 195:313–318

    Article  CAS  Google Scholar 

  • Irving LJ, Sheng YB, Woolley D, Matthew C (2007) Physiological effects of waterlogging on two lucerne varieties grown under glasshouse conditions. J Agron Crop Sci 193:345–356

    Article  Google Scholar 

  • Justin SHFW, Armstrong W (1987) The anatomical characteristics of roots and plant response to soil flooding. New Phytol 106:465–495

    Google Scholar 

  • Lee RB (1978) Inorganic nitrogen metabolism in barley root under poorly aerated conditions. J Exp Bot 29:693–708

    Article  CAS  Google Scholar 

  • Lee RB (1979) The release of nitrite from barley roots in response to metabolic inhibitors, uncoupling agents, and anoxia. J Exp Bot 30:119–133

    Article  CAS  Google Scholar 

  • Malavolta E (1954) Studies on the nitrogenous nutrition of rice. Plant Physiol 29:98–99

    Article  CAS  PubMed  Google Scholar 

  • Mattana M, Brambilla I, Bertani A, Reggiani R (1996) Expression of nitrogen assimilating enzymes in germinating rice under anoxia. Plant Physiol Biochem 34:653–657

    CAS  Google Scholar 

  • Menegus E, Cattaruzza L, Mattana M, Beffagna N, Ragg E (1991) Response to anoxia in rice and wheat seedlings. Plant Physiol 95:760–767

    Article  CAS  PubMed  Google Scholar 

  • Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5:62–71

    Article  CAS  PubMed  Google Scholar 

  • Mommer L, Pederson O, Visser EJW (2004) Acclimation of a terrestrial plant to submergence facilitates gas exchange under water. Plant Cell Environ 27:1281–1287

    Article  Google Scholar 

  • Morard P, Maertens C, Bertoni G, Boisseau Y (1990) Influence de la respiration racinaire sur l’absorption du potassium et du nitrate chez le blé. Compt Rend Biol 311:103–108

    CAS  Google Scholar 

  • Morard P, Lacoste L, Silvestre J (2000) The effect of oxygen deficiency on the uptake of water and mineral nutrients by tomato plants in soilless culture. J Plant Nutr 23:1063–1078

    Article  CAS  Google Scholar 

  • Morard P, Lacoste L, Silvestre J (2004) Effect of oxygen deficiency on mineral nutrition of excised tomato roots. J Plant Nutr 27:1532–4087

    Article  Google Scholar 

  • Notton BA, Hewitt EJ (1971) The role of tungsten in the inhibition of nitrate reductase activity in spinach leaves. Biochem Biophys Res Commun 44:702–710

    Article  CAS  PubMed  Google Scholar 

  • Peuke AD, Glaab J, Kaiser WM, Jeschlke WD (1996) The uptake and flow of C and N and ions between roots and shoots in Ricinus communis L. IV. Flow and metabolism of inorganic nitrogen and malate depending on nitrogen nutrient and salt treatment. J Exp Bot 47:377–385

    Article  CAS  Google Scholar 

  • Pezeshki SR (2001) Wetland plant responses to soil flooding. Environ Exp Bot 46:299–312

    Article  Google Scholar 

  • Prioul JL, Guyot C (1985) Correction par la fertilisation minérale des effets de l’ennoyage sur le blé d’hiver. I. Expérimentation sur sol. Agron 5:743–750

    Article  Google Scholar 

  • Reggiani R, Brambilla I, Bertani A (1985) Effect of exogenous nitrate on anaerobic metabolism in excised rice roots. I. Nitrate reduction and pyridine nucleotide pools. J Exp Bot 36:1193–1199

    Article  CAS  Google Scholar 

  • Ricard B, Couee I, Raymond P, Saglio P, Saint-Ges V, Pradet A (1994) Plant metabolism under hypoxia and anoxia. Plant Physiol Biochem 32:1–10

    CAS  Google Scholar 

  • Saglio P, Drew MC, Pradet A (1988) Metabolic acclimatation to anoxia induced by low (2–4 KPa partial pressure) oxygen pretreatment (hypoxia) in root tips of Zea mays. Plant Physiol 8:61–66

    Article  Google Scholar 

  • Stitt M, Muller C, Matt P, Gibon Y, Carillo P, Morcuende R, Scheible WR, Krapp A (2002) Steps towards an integrated view of nitrogen metabolism. J Exp Bot 53:959–970

    Article  CAS  PubMed  Google Scholar 

  • Stoimenova M, Hansch R, Mendel R, Gimmler H, Kaiser WM (2003) The role of nitrate reduction in the anoxic metabolism of roots. I. Characterization of root morphology and normoxic metabolism of wild type tobacco and a transformant lacking root nitrate reductase. Plant Soil 253:145–153

    Article  CAS  Google Scholar 

  • Trought MCT, Drew MC (1981) Alleviation of injury to young wheat plants in aerobic solution cultures in relation to the supply of nitrate and other inorganic nutrients. J Exp Bot 32:509–522

    Article  CAS  Google Scholar 

  • Vartapetian BB (2006) Plant anaerobic stress as a novel trend in ecological physiology, biochemistry, and molecular biology: further development of the problem. Russ J Plant Physiol 53:711–738

    Article  CAS  Google Scholar 

  • Vartapetian BB, Jackson MB (1997) Plant adaptations to anaerobic stress. Ann Bot 79:3–20

    Article  CAS  Google Scholar 

  • Visser EJW, Blom CWPM, Voesenek LACJ (1996) Flooding-induced adventitious rooting in Rumex: morphology and development in an ecological perspective. Acta Bot Neerl 45:17–28

    Google Scholar 

  • Wallace W (1986) Distribution of nitrate assimilation between the root and shoot of legumes and a comparison with wheat. Physiol Plant 66:630–636

    Article  CAS  Google Scholar 

  • Wintermans J, Mots A (1965) Spectrophotometric characteristic of chlorophylls a and b and their pheophytins in ethanol. Biochem Biophys Acta 109:448–453

    Article  CAS  PubMed  Google Scholar 

  • Younis ME, El-Shahaby SA, Abo-Hamed SA, Ibrahim AH (2000) Effects of water stress on growth, pigments and 14CO2 assimilation in three sorghum cultivars. J Agron Crop Sci 175:73–82

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Faouzi Horchani.

Additional information

Communicated by G. Klobus.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Horchani, F., Aschi-Smiti, S. & Brouquisse, R. Involvement of nitrate reduction in the tolerance of tomato (Solanum lycopersicum L.) plants to prolonged root hypoxia. Acta Physiol Plant 32, 1113–1123 (2010). https://doi.org/10.1007/s11738-010-0503-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-010-0503-0

Keywords

Navigation