Skip to main content
SpringerLink
Log in

Glutathione and transpiration as key factors conditioning oxidative stress in Arabidopsis thaliana exposed to uranium

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Although oxidative stress has been previously described in plants exposed to uranium (U), some uncertainty remains about the role of glutathione and tocopherol availability in the different responsiveness of plants to photo-oxidative damage. Moreover, in most cases, little consideration is given to the role of water transport in shoot heavy metal accumulation. Here, we investigated the effect of uranyl nitrate exposure (50 μM) on PSII and parameters involved in water transport (leaf transpiration and aquaporin gene expression) of Arabidopsis wild type (WT) and mutant plants that are deficient in tocopherol (vte1: null α/γ-tocopherol and vte4: null α-tocopherol) and glutathione biosynthesis (high content: cad1.3 and low content: cad2.1). We show how U exposure induced photosynthetic inhibition that entailed an electron sink/source imbalance that caused PSII photoinhibition in the mutants. The WT was the only line where U did not damage PSII. The increase in energy thermal dissipation observed in all the plants exposed to U did not avoid photo-oxidative damage of mutants. The maintenance of control of glutathione and malondialdehyde contents probed to be target points for the overcoming of photoinhibition in the WT. The relationship between leaf U content and leaf transpiration confirmed the relevance of water transport in heavy metals partitioning and accumulation in leaves, with the consequent implication of susceptibility to oxidative stress.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Araus JL, Villegas D, Aparicio N, García del Moral LF, El Hani S, Rharrabti Y, Ferrio JP, Royo C (2003) Environmental factors determining carbon isotope discrimination and yield in durum wheat under Mediterranean conditions. Crop Sci 43:170–180

    Article  Google Scholar 

  • Aroca R, Porcel R, Ruiz-Lozano JM (2012) Regulation of root water uptake under abiotic stress conditions. J Exp Bot 63:43–57

    Article  CAS  PubMed  Google Scholar 

  • Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Biol 50:601–639

    Article  CAS  Google Scholar 

  • Bartoli F, Coinchelin D, Robin C, Echevarria G (2012) Impact of active transport and transpiration on nickel and cadmium accumulation in the leaves of the Ni-hyperaccumulator Leptoplax emarginata: a biophysical approach. Plant Soil 350:99–115

    Article  CAS  Google Scholar 

  • Battarbee R, Anderson N, Appleby P, Flower RG, Fritz S, Haworth E, Higgit S, Jones V, Kreiser A, Munro MA, Natkanski J, Oldfield F, Patrick ST, Richardson N, Rippey B, Stevenson AC (1988) Lake acidification in the United Kingdom ENSIS, London

  • Cela J, Chang C, Munné-Bosch S (2011) Accumulation of γ-rather than α-tocopherol alters ethylene signaling gene expression in the vte4 mutant of Arabidopsis thaliana. Plant Cell Physiol 52:1389–1400

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chaudhary N, Khurana P (2009) Vitamin E biosynthesis genes in rice: molecular characterization, expression profiling and comparative phylogenetic analysis. Plant Sci 177:479–491

    Article  CAS  Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen Z, Gallie DR (2004) The ascorbic acid redox state controls guard cell signaling and stomatal movement. Plant Cell 16:1143–1162

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Claus J, Bohmann A, Chavarría-Krauser A (2013) Zinc uptake and radial transport in roots of Arabidopsis thaliana: a modelling approach to understand accumulation. Ann Bot 112:369–380

    Article  CAS  PubMed  Google Scholar 

  • Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719

    Article  CAS  PubMed  Google Scholar 

  • Collin VC, Eymery F, Genty B, Rey P, Havaux M (2008) Vitamin E is essential for the tolerance of Arabidopsis thaliana to metal-induced oxidative stress. Plant Cell Environ 31:244–257

    CAS  PubMed  Google Scholar 

  • European Environment Agency (1999) Environment in the European Union at the turn of the century”. pp 446, ISBN 92-9157-202-0

  • Fahrenholzt SR, Doleiden FH, Tozzolo AM, Lamola AA (1974) On the quenching of singlet oxygen by alpha-tocopherol. Photochem Photobiol 20:505–509

    Article  Google Scholar 

  • Falk J, Munné-Bosch S (2010) Tocochromanol functions in plants: antioxidation and beyond. J Exp Bot 61:1549–1566

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Ribas-Carbó M, Hanson DT, Bota J, Otto B, Cifre J, McDowell N, Medrano H, Kaldenhoff R (2006) Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. The Plant J 48:427–439

    Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Galmés J, Abadía A, Cifre J, Medrano H, Flexas J (2007) Photoprotection processes under water stress and recovery in Mediterranean plants with different growth forms and leaf habits. Physiol Plantarum 130:495–510

    Article  Google Scholar 

  • Harley PC, Loreto F, Marco GD, Sharkey TD (1992) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiol 98:1429–1436

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Howden R, Andersen CR, Goldsbrough PB, Cobbett CC (1995) A cadmium-sensitive, glutathione-deficient mutant of Arabidopsis thaliana. Plant Physiol 107:1067–1073

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Janik E, Bednarska J, Zubik M, Puzio M, Luchowski R, Grudzinski W, Mazur R, Garstka M, Maksymiec W, Kulik A, Dietler G, Gruszecki WI (2013) Molecular architecture of plant thylakoids under physiological and light stress conditions: a study of lipid–light-harvesting complex II model membranes. Plant Cell 25:2155–2170

    Article  CAS  PubMed  Google Scholar 

  • Kadioglu A, Saruhan N, Saglam A, Terzi R, Acet T (2011) Exogenous salicylic acid alleviates effects of long term drought stress and delays leaf rolling by inducing antioxidant system. Plant Growth Regul 64:27–37

    Article  CAS  Google Scholar 

  • Kay R, Chau A, Daly M (1987) Duplication of CaMV 35S promoter sequences creates a strong enhancer for plants genes. Science 236:1299–1302

    Article  CAS  PubMed  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lawlor DW, Tezara W (2009) Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes. Ann Bot 103:561–579

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophyll and carotenoids: pigments of photosynthetic biomembranes. In: Douce R, Packer L (eds) Methods in enzymology. Plant cell membranes. Academic Press, USA, pp 350–382

    Chapter  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • López-Millán A, Sagardoy R, Solanas M, Abadía A, Abadía J (2009) Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. Environ Exp Bot 65:376–385

    Article  Google Scholar 

  • Maksymiec W, Wójcik M, Krupa Z (2007) Variation in oxidative stress and photochemical activity in Arabidopsis thaliana leaves subjected to cadmium and excess copper in the presence or absence of jasmonate and ascorbate. Chemosphere 66:421–427

    Article  CAS  PubMed  Google Scholar 

  • Maurel C (1997) Aquaporins and water permeability of plant membranes. Annu Rev Plant Biol 48:399–429

    Article  CAS  Google Scholar 

  • May MJ, Vernoux T, Leaver C, Van Montagu M, Inzé D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 321:649–667

    Google Scholar 

  • Mène-Saffrané L, Jones AD, DellaPenna D (2010) Plastochromanol-8 and tocopherols are essential lipid-soluble antioxidants during seed desiccation and quiescence in Arabidopsis. Proc Natl Acad Sci USA 107:17815–17820

    Article  PubMed Central  PubMed  Google Scholar 

  • Minotti G, Aust D (1987) The requirement for iron (III) in the initiation of lipid peroxidation by iron (II) and hydrogen peroxide. J Biol Chem 262:1098–1104

    CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Morillon R, Chrispeels MJ (2001) The role of ABA and the transpiration stream in the regulation of the osmotic water permeability of leaf cells. Proc Natl Acad Sci USA 98:14138–14143

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Müller M, Munné-Bosch S (2011) Rapid and sensitive hormonal profiling of complex plant samples by liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Plant Methods 7:37

    Article  PubMed Central  PubMed  Google Scholar 

  • Munné-Bosch S (2005) Linking tocopherols with cellular signaling in plants. New Phytol 166:363–366

    Article  PubMed  Google Scholar 

  • Munné-Bosch S (2007) α-Tocopherol: a multifaceted molecule in plants. Vitam Horm 76:375–392

    Article  PubMed  Google Scholar 

  • Munné-Bosch S, Alegre L (2002) The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 21:31–57

    Article  Google Scholar 

  • Munné-Bosch S, Falara V, Pateraki I, López-Carbonell M, Cela J, Kanellis AK (2009) Physiological and molecular responses of the isoprenoid biosynthetic pathway in a drought-resistant Mediterranean shrub, Cistus creticus exposed to water deficit. J Plant Physiol 166:136–145

    Article  PubMed  Google Scholar 

  • Neves MO, Abreu MM, Figueiredo V (2012) Uranium in vegetable foodstuffs: should residents near the Cunha Baixa uranium mine site (Central Northern Portugal) be concerned? Environ Geochem Health 34:181–189

    Article  CAS  PubMed  Google Scholar 

  • Niinemets U, Kull O (2001) Sensitivity of photosynthetic electron transport to photoinhibition in a temperate deciduous forest canopy: photosystem II center openness, non-radiative energy dissipation and excess irradiance under field conditions. Tree Physiol 21:899–914

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time PCR. Nucleic Acids Res 29:2002–2007

    Article  Google Scholar 

  • Porfirova S, Bergmüller E, Tropf S, Lemke R, Dörmann P (2002) Isolation of an Arabidopsis mutant lacking vitamin E and identification of a cyclase essential for all tocopherol biosynthesis. Proc Natl Acad Sci U S A 99:12495–12500

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Przedpelska-Wasowicz EM, Wierzbicka M (2011) Gating of aquaporins by heavy metals in Allium cepa L. epidermal cells. Protoplasma 248:663–671

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Renkema H, Koopmans A, Kersbergen L, Kikkert J, Hale B, Berkelaar E (2012) The effect of transpiration on selenium uptake and mobility in durum wheat and spring canola. Plant Soil 354:239–250

    Article  CAS  Google Scholar 

  • Ribera D, Labrot F, Tisnerat G, Narbonne JF (1996) Uranium in the environment: occurrence, transfer, and biological effects. Rev Environ Contam Toxicol 146:53–89

    CAS  PubMed  Google Scholar 

  • Ricciarelli R, Zingg J, Azzi A (2001) Vitamin E 80th anniversary: a double life, not only fighting radicals. IUBMB Life 52:71–76

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez E, Santos C, Azevedo R, Moutinho-Pereira J, Correia C, Dias MC (2012) Chromium (VI) induces toxicity at different photosynthetic levels in pea. Plant Physiol Biochem 53:94–100

    Article  CAS  PubMed  Google Scholar 

  • Sakurai-Ishikawa J, Murai-Hatano M, Hayashi H, Ahamed A, Fukushi K, Matsumoto T, Kitagawa Y (2011) Transpiration from shoots triggers diurnal changes in root aquaporin expression. Plant Cell Environ 34:1150–1163

    Article  CAS  PubMed  Google Scholar 

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    Article  PubMed  Google Scholar 

  • Subrahmanyam D (2008) Effects of chromium toxicity on leaf photosynthetic characteristics and oxidative changes in wheat (Triticum aestivum L.). Photosynthetica 46:339–345

    Article  CAS  Google Scholar 

  • Szymanska R, Kruk J (2010) Plastoquinol is the main prenyllipid synthesized during acclimation to high light conditions in Arabidopsis and is converted to plastochromanol by tocopherol cyclase. Plant Cell Physiol 5:537–545

    Article  Google Scholar 

  • Turcsányi E, Lyons T, Plochl M, Barnes J (2000) Does ascorbate in the mesophyll cell walls form the first line of defence against ozone? Testing the concept using broad bean (Vicia faba L.). J Exp Bot 51:901–910

    Article  PubMed  Google Scholar 

  • Uehlein N, Sperling H, Heckwolf M, Kaldenhoff R (2012) The Arabidopsis aquaporin PIP1;2 rules cellular CO2 uptake. Plant Cell Environ 35:1077–1083

    Google Scholar 

  • Vanhoudt N, Vandenhove H, Smeets K, Remans T, Van Hees M, Wannijn J, Vangronsveld J, Cuypers A (2008) Effects of uranium and phosphate concentrations on oxidative stress related responses induced in Arabidopsis thaliana. Plant Physiol Biochem 46:987–996

    Article  CAS  PubMed  Google Scholar 

  • Vanhoudt N, Cuypers A, Horemans N, Remans T, Opdenakker K, Smeets K, Bello DM, Havaux M, Wannijn J, Van Hees M, Vangronsveld J, Vandenhove H (2011a) Unraveling uranium induced oxidative stress related responses in Arabidopsis thaliana seedlings. Part II: responses in the leaves and general conclusions. J Environ Radioact 102:638–645

    Article  CAS  PubMed  Google Scholar 

  • Vanhoudt N, Vandenhove H, Horemans N, Bello DM, Van Hees M, Wannijn J, Carleer R, Vangronsveld J, Cuypers A (2011b) Uranium induced effects on development and mineral nutrition of Arabidopsis Thaliana. J Plant Nutr 34:1940–1956

    Article  CAS  Google Scholar 

  • Vanhoudt N, Vandenhove H, Horemans N, Remans T, Opdenakker K, Smeets K, Bello DM, Wannijn J, Van Hees M, Vangronsveld J, Cuypers A (2011c) Unraveling uranium induced oxidative stress related responses in Arabidopsis thaliana seedlings. Part I: responses in the roots. J Environ Radioact 102:630–637

    Article  CAS  PubMed  Google Scholar 

  • Verhoeven AS, Adams WW III, Demmig-Adams B, Croce R, Bassi R (1999) Xanthophyll cycle pigment localization and dynamics during exposure to low temperatures and light stress in Vinca major. Plant Physiol 120:727–737

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Viehweger K, Geipel G, Bernhard G (2011) Impact of uranium (U) on the cellular glutathione pool and resultant consequences for the redox status of U. Biometals 24:1197–1204

    Article  CAS  PubMed  Google Scholar 

  • Villiers F, Ducruix C, Hugouvieux V, Jarno N, Ezan E, Garin J, Junot C, Bourguignon J (2011) Investigating the plant response to cadmium exposure by proteomic and metabolomic approaches. Proteomics 11:1650–1663

    Article  CAS  PubMed  Google Scholar 

  • Villiers F, Jourdain A, Bastien O, Leonhardt N, Fujioka S, Tichtincky G, Parcy F, Bourguignon J, Hugouvieux V (2012) Evidence for functional interaction between brassinosteroids and cadmium response in Arabidopsis thaliana. J Exp Bot 63:1185–1200

    Article  CAS  PubMed  Google Scholar 

  • von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387

    Article  Google Scholar 

  • Wedepohl HK (1995) The composition of the continental crust. Geochimica et Cosmochim. Acta 59:1217–1232

    CAS  Google Scholar 

  • Yamaguchi H, Fukuoka H, Arao T, Ohyama A, Nunome T, Miyatake K, Negoro S (2010) Gene expression analysis in cadmium-stressed roots of a low cadmium-accumulating solanaceous plant, Solanum torvum. J Exp Bot 61:423–437

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song C (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work has been funded by the Région Rhône-Alpes CMIRA program and by the CEA program of Toxicology. RA and RP were supported by Ministry of Economy and Competitiveness of Spain (AGL2011-25403 project). The authors would like to thank Serge Berthet for his help with the ICP-MS measurements.

Author information

Authors and Affiliations

  1. Instituto de Agrobiotecnología, Universidad Pública de Navarra-CSIC-Gobierno de Navarra, Campus de Arrosadía, 31192, Mutilva Baja, Spain

    Iker Aranjuelo

  2. CEA, iRTSV, Laboratoire Physiologie Cellulaire Végétale (PCV), CEA, CNRS (UMR 5168) UJF, INRA (USC1359), CEA-Grenoble, 17 rue des Martyrs, 38054, Grenoble Cedex 9, France

    Iker Aranjuelo, Fany Doustaly & Jacques Bourguignon

  3. PCV, Université Grenoble Alpes, 38041, Grenoble, France

    Iker Aranjuelo, Fany Doustaly & Jacques Bourguignon

  4. CNRS, UMR5168, PCV, 38054, Grenoble, France

    Iker Aranjuelo, Fany Doustaly & Jacques Bourguignon

  5. INRA, USC1359, PCV, 38054, Grenoble, France

    Iker Aranjuelo, Fany Doustaly & Jacques Bourguignon

  6. Unitat de Fisologia Vegetal, Facultat de Biologia, Universitat de Barcelona, Av. Diagonal 643, 08028, Barcelona, Spain

    Jana Cela, Maren Müller & Sergi Munné-Bosch

  7. Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín (CSIC), Profesor Albareda 1, 18008, Granada, Spain

    Rosa Porcel & Ricardo Aroca

Authors
  1. Iker Aranjuelo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fany Doustaly
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jana Cela
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rosa Porcel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maren Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ricardo Aroca
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sergi Munné-Bosch
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jacques Bourguignon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Iker Aranjuelo or Jacques Bourguignon.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 42 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aranjuelo, I., Doustaly, F., Cela, J. et al. Glutathione and transpiration as key factors conditioning oxidative stress in Arabidopsis thaliana exposed to uranium. Planta 239, 817–830 (2014). https://doi.org/10.1007/s00425-013-2014-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-013-2014-x

Keywords

Search

Navigation