Skip to main content
Log in

Differences in Al tolerance between Plantago algarbiensis and P. almogravensis reflect their ability to respond to oxidative stress

  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

We evaluated the impact of low pH and aluminum (Al) on the leaves and roots of Plantago almogravensis Franco and Plantago algarbiensis Samp., focusing on energy partitioning in photosystem II, H2O2 levels, lipid peroxidation, electrolyte leakage (EL), protein oxidation, total soluble protein content and antioxidant enzyme activities. In both species, Al triggered more changes in oxidative metabolism than low pH alone, particularly in the roots. We found that Al increased the levels of H2O2 in P. algarbiensis roots, but reduced the levels of H2O2 in P. almogravensis leaves and roots. Neither low pH nor Al affected the spatial heterogeneity of chlorophyll fluorescence, the maximum photochemical efficiency of PSII (Fv/Fm), the actual quantum efficiency of PSII (ϕPSII) or the quantum yields of regulated (ϕNPQ) and nonregulated (ϕNO) energy dissipation, and there was no significant change in total soluble protein content and EL. In P. algarbiensis, Al increased the carbonyl content and the activities of superoxide dismutase (SOD) and catalase (CAT) in the roots, and also CAT, ascorbate peroxidase and guaiacol peroxidase activities in the leaves. In P. almogravensis, Al reduced the level of malondialdehyde in the roots as well as SOD activity in the leaves and roots. We found that P. almogravensis plantlets could manage the oxidative stress caused by low pH and Al, whereas the P. algarbiensis antioxidant system was unable to suppress Al toxicity completely, leading to the accumulation of H2O2 and consequential protein oxidation in the roots.

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
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

APX:

Ascorbate peroxidase

CAT:

Catalase

EL:

Electrolyte leakage

Fv/Fm :

Maximum photochemical efficiency of PSII

FW:

Fresh weight

GPX:

Guaiacol peroxidase

MDA:

Malondialdehyde

MS:

Murashige and Skoog

NBT:

Nitroblue tetrazolium

PSII:

Photosystem II

PVPP:

Polyvinylpolypyrrolidone

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

TBA:

Thiobarbituric acid

TCA:

Trichloroacetic acid

ϕNPQ :

Quantum yield of regulated energy dissipation

ϕNO :

Quantum yield of nonregulated energy dissipation

ϕPSII :

Actual quantum efficiency of PSII

References

  • Achary VMM, Patnaik AR, Panda BB (2012) Oxidative biomarkers in leaf tissue of barley seedlings in response to aluminum stress. Ecotoxicol Environ Saf 75:16–26

    Article  Google Scholar 

  • Aebi HE (1983) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Chemie, Berlin, pp 273–286

    Google Scholar 

  • Ali S, Bai P, Zeng F, Cai S, Shamsi IH, Qiu B, Wu F, Zhang G (2011) The ecotoxicological and interactive effects of chromium and aluminum on growth, oxidative damage and antioxidant enzymes on two barley genotypes differing in Al tolerance. Environ Exp Bot 70:185–191

    Article  CAS  Google Scholar 

  • Basu U, Good AG, Taylor GJ (2001) Transgenic Brassica napus plants overexpressing aluminium-induced mitochondrial manganese superoxide dismutase cDNA are resistant to aluminium. Plant Cell Environ 24:1269–1278

    Article  CAS  Google Scholar 

  • Beauchamp CO, Fridovich I (1971) Superoxide dismutase: improved assays and assays applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194

    Article  CAS  PubMed  Google Scholar 

  • Boscolo PRS, Menossi M, Jorge RA (2003) Aluminum-induced oxidative stress in maize. Phytochemistry 62:181–189

    Article  CAS  PubMed  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cargnelutti D, Tabaldi LA, Spanevello RM, Jucoski GO, Battisti V, Redin M, Linares CEB, Dressler VL, Flores EMM, Nicoloso FT, Morsch VM, Schetinger MRC (2006) Mercury toxicity induces oxidative stress in growing cucumber seedlings. Chemosphere 65:999–1006

    Article  CAS  PubMed  Google Scholar 

  • Chen LS, Qi YP, Liu XH (2005) Effects of aluminum on light energy utilization and photoprotective systems in citrus leaves. Ann Bot 96:35–41

    Article  CAS  PubMed  Google Scholar 

  • Cruz FJR, Lobato AKS, Costa RCL, Lopes MJS, Neves HKB, Neto CFO, Silva MHL, Filho BGS, Junior JAL, Okumura RS (2011) Aluminum negative impact on nitrate reductase, nitrogen compounds and morphological parameters in sorghum plants. Aust J Crop Sci 5:641–645

    Google Scholar 

  • Demmig-Adams B, Adams WW (1996) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198:460–470

    Article  CAS  Google Scholar 

  • Egley GH, Paul RN, Vaughn KC, Duke SO (1983) Role of peroxidase in the development of water impermeable seed coats in Sida spinosa L. Planta 157:224–232

    Article  CAS  Google Scholar 

  • Ericson MC, Alfinito AE (1984) Proteins produced during salt stress in tobacco cell cultures. Plant Physiol 74:506–509

    Article  CAS  PubMed  Google Scholar 

  • Giannakoula A, Moustakas M, Mylona P, Papadakis I, Yupsanis T (2008) Aluminum tolerance in maize is correlated with increased levels of mineral nutrients, carbohydrates and proline, and decreased levels of lipid peroxidation and Al accumulation. J Plant Physiol 165:385–396

    Article  CAS  PubMed  Google Scholar 

  • Giannakoula A, Moustakas M, Syros T, Yupsanis T (2010) Aluminum stress induces up-regulation of an efficient antioxidant system in the Al-tolerant maize line but not in the Al-sensitive line. Environ Exp Bot 67:487–494

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Gonçalves S, Martins N, Romano A (2009) Micropropagation and conservation of endangered species Plantago algarbiensis and P. almogravensis. Biol Plant 53:774–778

    Article  Google Scholar 

  • Guo TR, Zhang GP, Zhang YH (2007) Physiological changes in barley plants under combined toxicity of aluminum, copper and cadmium. Colloids Surf B 57:182–188

    Article  CAS  Google Scholar 

  • Hodges DM, Delong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Inostroza-Blancheteau C, Reyes-Díaz M, Aquea F, Nunes-Nesi A, Alberdi M, Arce-Johnson P (2011) Biochemical and molecular changes in response to aluminium-stress in highbush blueberry (Vaccinium corymbosum L.). Plant Physiol Biochem 49:1005–1012

    Article  CAS  PubMed  Google Scholar 

  • Jiang HX, Chen LS, Zheng JG, Han S, Tang N, Smith BR (2008) Aluminum-induced effects on photosystem II photochemistry in citrus leaves assessed by the chlorophyll a fluorescence transient. Tree Physiol 28:1863–1871

    Article  CAS  PubMed  Google Scholar 

  • Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260

    Article  CAS  Google Scholar 

  • Kornyeyev D, Logan BA, Holaday AS (2010) Excitation pressure as a measure of the sensitivity of photosystem II to photoinactivation. Funct Plant Biol 37:943–951

    Article  CAS  Google Scholar 

  • Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218

    Article  CAS  PubMed  Google Scholar 

  • Levine RL, Willams JA, Stadtman ER, Shacter E (1994) Carbonyl assay for determination of oxidatively modified proteins. Methods Enzymol 233:346–363

    Article  CAS  PubMed  Google Scholar 

  • Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quences ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:781–787

    Article  Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oriza sativa L.) cultivar differing in salinity resistance. Ann Bot 78:389–398

    Article  CAS  Google Scholar 

  • Ma B, Gao L, Zhang H, Cui J, Shen Z (2012) Aluminum-induced oxidative stress and changes in antioxidant defenses in the roots of rice varieties differing in Al tolerance. Plant Cell Rep 31:687–696

    Article  CAS  PubMed  Google Scholar 

  • Martins N, Gonçalves S, Palma T, Romano A (2011) The influence of low pH on in vitro growth and biochemical parameters of Plantago almogravensis and P. algarbiensis. Plant Cell Tissue Organ Cult 107:113–121

    Article  CAS  Google Scholar 

  • Martins N, Osório ML, Gonçalves S, Osório J, Palma T, Romano A (2013a) Physiological responses of Plantago algarbiensis and P. almogravensis shoots and plantlets to low pH and aluminum stress. Acta Physiol Plant 35:615–625

    Article  Google Scholar 

  • Martins N, Gonçalves S, Andrade P, Valentão P, Romano A (2013b) Changes on organic acid secretion and accumulation in Plantago almogravensis Franco and P. algarbiensis Samp under aluminum stress. Plant Sci 198:1–6

    Article  CAS  PubMed  Google Scholar 

  • Martins N, Gonçalves S, Romano A (2013c) Metabolism and aluminum accumulation in Plantago almogravensis and P. algarbiensis in response to low pH and aluminum stress. Biol Plant 57:325–331

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Mukhopadyay M, Bantawa P, Das A, Sarkar B, Bera B, Ghosh P, Mondal TK (2012) Changes of growth, photosynthesis and alteration of leaf antioxidative defence system of tea [Camellia sinensis (L.) O. Kuntze] seedlings under aluminum stress. Biometals 25:1141–1154

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Shoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Murchie EH, Niyogi KK (2011) Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155:86–92

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Osório ML, Osório J, Vieira AC, Gonçalves S, Romano A (2011) Influence of enhanced temperature on photosynthesis, photooxidative damage, and antioxidant strategies in Ceratonia siliqua L. seedlings subjected to water deficit and rewatering. Photosynthetica 49:3–12

    Article  Google Scholar 

  • Pereira WE, Siqueira DL, Martínez CA, Puiatti M (2000) Gas exchange and chlorophyll fluorescence in four citrus rootstocks under Al stress. J Plant Physiol 157:513–520

    Article  CAS  Google Scholar 

  • Pereira LB, Mazzanti CM, Gonçalves JF, Cargnelutti D, Tabaldi LA, Becker AG, Calgaroto NS, Farias JG, Battisti V, Bohrer D, Nicoloso FT, Morsch VM, Schetinger MR (2010) Aluminum-induced oxidative stress in cucumber. Plant Physiol Biochem 48:683–689

    Article  CAS  PubMed  Google Scholar 

  • Pereira LB, Mazzanti CMA, Cargnelutti D, Rossato LV, Gonçalves JF, Calgaroto N, Dressler V, Nicoloso FT, Federizzi LC, Morsch VM, Shetinger MRC (2011) Differential responses of oat genotypes: oxidative stress provoked by aluminum. Biometals 24:73–83

    Article  CAS  PubMed  Google Scholar 

  • Ramírez-Benítez JE, Hernández-Sotomayor SMT (2008) Role of reactive oxygen species (ROS) in aluminium-induced signaling and aluminium resistance in plants. Curr Top Biochem Res 19:79–89

    Google Scholar 

  • Rinalducci S, Murgiano L, Zolla L (2008) Redox proteomics: basic principles and future perspectives for the detection of protein oxidation in plants. J Exp Bot 59:3781–3801

    Article  CAS  PubMed  Google Scholar 

  • Sgherri CLM, Navari-Izzo F (1995) Sunflower seedling subjected to increasing water deficit stress: oxidative stress and defense mechanisms. Physiol Plant 93:25–30

    Article  CAS  Google Scholar 

  • Shacter E, Williams JA, Lim M, Levine RL (1994) Differential susceptibility of plasma proteins to oxidative modification. Examination by Western blot immunoassay. Free Rad Biol Med 17:429–437

    Article  CAS  PubMed  Google Scholar 

  • Shaff JE, Schultz BA, Craft EJ, Clark RT, Kochian LV (2010) GEOCHEM-EZ: a chemical speciation program with greater power and flexibility. Plant Soil 330:207–214

    Article  CAS  Google Scholar 

  • Sharma P, Dubey RS (2007) Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Rep 26:2027–2038

    Article  CAS  PubMed  Google Scholar 

  • Tabaldi LA, Nicoloso FT, Castro GY, Cargnelutti D, Gonçalves JF, Rauber R, Skresky EC, Schetinger MRC, Morsch VM, Bisognin DA (2007) Physiological and oxidative stress responses of four potato clones to aluminum in nutrient solution. Braz J Plant Physiol 19:211–222

    Article  CAS  Google Scholar 

  • von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15

    Article  Google Scholar 

  • Wang W-B, Kim Y-H, Lee H-S, Kim K-Y, Deng X-P, Kwak S–S (2009) Analysis of antioxidant enzyme activity during germination of alfalfa under salt and drought stresses. Plant Physiol Biochem 47:570–577

    Article  CAS  PubMed  Google Scholar 

  • Wilson KE, Ivanov AG, Öquist G, Grodzinski B, Sarhan F, Huner NPA (2006) Energy balance, organellar redox status and acclimation to environmental stress. Can J Bot 84:1355–1370

    Article  CAS  Google Scholar 

  • Wu K, Xiao S, Chen Q, Wang Q, Zhang Y, Li K, Yu Y, Chen L (2013) Changes in the activity and transcription of antioxidant enzymes in response to Al stress in black soybeans. Plant Mol Biol Rep 31:141–150

    Article  CAS  Google Scholar 

  • Xu FJ, Li G, Jin CW, Liu WJ, Zhang YS, Lin XY (2012) Aluminum-induced changes in reactive oxygen species accumulation, lipid peroxidation and antioxidant capacity in wheat root tips. Biol Plant 56:89–96

    Article  CAS  Google Scholar 

  • Yin L, Mano J, Wang S, Tsuji W, Tanaka K (2010) The involvement of lipid peroxide-derived aldehydes in aluminum toxicity of tobacco roots. Plant Physiol 152:1406–1417

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

N. Martins, M.L. Osório and S. Gonçalves acknowledge grants from the Portuguese Science and Technology Foundation (FCT, SFRH/BD/48379/2008, SFRH/BPD/35410/2007 and SFRH/BPD/31534/2006, respectively). This work was supported by the FCT project PTDC/AGR-AAM/102664/2008.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anabela Romano.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martins, N., Osório, M.L., Gonçalves, S. et al. Differences in Al tolerance between Plantago algarbiensis and P. almogravensis reflect their ability to respond to oxidative stress. Biometals 26, 427–437 (2013). https://doi.org/10.1007/s10534-013-9625-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-013-9625-3

Keywords

Navigation