Skip to main content
Log in

Abiotic stress effects on the antioxidative response profile of Albizia julibrissin Durazz. (Fabaceae)

  • Original Article
  • Published:
Brazilian Journal of Botany Aims and scope Submit manuscript

Abstract

Abiotic stresses (e.g., heavy metals, drought, cold, or combinations) induce oxidative stress with overproduction of reactive oxygen species (ROS). We have investigated the antioxidative responses of Albizia julibrissin Durazz. (silk tree, Fabaceae). Four-month-old plants grown in sand cultures were subjected to various single or sequential treatments involving exposure to cadmium (50–250 μmol L−1 Cd), lead (1000–5000 μmol L−1 Pb), chilling at 4 °C (CH), or drought (DR), for a period of 7–45 days. Leaf extracts were assayed for glutathione peroxidase (GPX), glutathione-disulfide reductase (GR), catalase (CAT), soluble proline (Pro), ascorbate peroxidase (APX), and guaiacol peroxidase (GUAPX). Cd and Pb accumulation in the leaves was also measured. CAT activity decreased strongly with increasing Pb exposure and after CH. It was also found to be reduced after Cd and DR treatments. GR activity increased highly in nearly all treatments, most strongly at high Cd or Pb, after DR + CH, and after CH followed by Cd. GUAPX and GPX showed similar trends of increase. APX activity dropped after CH, but increased after low Cd treatment and in CH + DR sequential stresses. Massive accumulation of soluble Pro occurred after 14–21 days in highly Cd- or Pb-stressed plants. CH or DR acclimation led to some alterations of antioxidative responses, particularly for CAT, GR, and APX. Our data indicate that GSH, GSH-linked redox systems, peroxidases, and Pro are possibly the more important antioxidants under severe stress.

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
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

AGFI:

Adjusted goodness-of-fit

APX:

Ascorbate peroxidase

BCF:

Bioconcentration factor

C:

Control

CAT:

Catalase

Cd 250:

250 μmol L−1 Cd

Cd 50:

50 μmol L−1 Cd

CH:

Chilling

CH + Cd 50:

Chilling 14 days + 50 μmol L−1 Cd 7 days

CH + DR:

Chilling 15 days + drought 15 days

CH + Pb 1000:

Chilling 14 days + 1000 μmol L−1 Pb 7 days

DHAR:

Dehydroascorbate reductase

DR:

Drought

DR + Cd 50:

Drought 14 days + 50 μmol L−1 Cd 7 days

DR + CH:

Drought 15 days + chilling 15 days

DR + Pb 1000:

Drought 14 days + 1000 μmol L−1 Pb 7 days

dw:

Dry weight

fw:

Fresh weight

GPX:

Glutathione peroxidase

GR:

Glutathione-disulfide reductase

GSH:

Glutathione

GSSG:

Glutathione-disulfide

GUA:

Guaiacol

GUAPX:

Guaiacol peroxidase

ND:

Not detected

Pb 1000:

1000 μmol L−1 Pb

Pb 5000:

5000 μmol L−1 Pb

PC:

Principal component

PCA:

Principal component analysis

POD:

Peroxidase

Pro:

Proline

RMSR:

Root mean square residual

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

References

  • Abdi H, Williams LJ (2010) Principal component analysis. Wiley Interdiscip Rev Comput Stat 2:433–459

    Article  Google Scholar 

  • Aebi H (1984) Catalase in vitro. Method Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • ATSDR (2015) Agency for toxic substance and disease registry. http://www.atsdr.cdc.gov/SPL/index.html. Accessed 26 Mar 2016

  • Basto M, Pereira JM (2012) An SPSS R-menu for ordinal factor analysis. J Stat Softw 46:1–29

    Article  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Baycu G, Tolunay D, Özden H, Günebakan S (2006) Ecophysiological and seasonal variations in Cd, Pb, Zn, and Ni concentrations in the leaves of urban deciduous trees in Istanbul. Environ Pollut 143:545–554

    Article  CAS  PubMed  Google Scholar 

  • Birecka H, Briber KA, Catalfama JL (1973) Comparative studies on tobacco pith and sweet potato root isoperoxidases in relation to injury, indolacetic acid and ethylene effects. Plant Physiol 52:43–49

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Filippou P, Bouchagier P, Skotti E, Fotopoulos V (2014) Proline and reactive oxygen/nitrogen species metabolism is involved in the tolerant response of the invasive plant species Ailanthus altissima to drought and salinity. Environ Exp Bot 97:1–10

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Sign 11:861–905

    Article  CAS  Google Scholar 

  • Gallego SM, Pena LB, Roberto A, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46

    Article  CAS  Google Scholar 

  • Gechev T, Willekens H, Van Montagu M, Inzé D, Van Camp W, Toneva V, Minkov I (2003) Different responses of tobacco antioxidant enzymes to light and chilling stress. J Plant Physiol 160:509–515

    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 

  • Grundy J, Stoker C, Carré IA (2015) Circadian regulation of abiotic stress tolerance in plants. Front Plant Sci. doi:10.3389/fpls.2015.00648

    PubMed  PubMed Central  Google Scholar 

  • Guo Z, Ou W, Lu S, Zhong Q (2006) Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem 44:828–836

    Article  CAS  PubMed  Google Scholar 

  • Gupta DK, Palma M, Corpas FJ (2015) Reactive oxygen species and oxidative damage in plants under stress. Springer, Berlin

    Book  Google Scholar 

  • Hossain MA, Mostofa MG, Fujita M (2013) Cross protection by cold-shock to salinity and drought stress-induced oxidative stress in mustard (Brassica campestris L.) seedlings. Mol Plant Breed 4:50–70

    Google Scholar 

  • Husson F, Josse J, Pages J (2010) Principal component methods—hierarchical clustering—partitional clustering: why would we need to choose for visualizing data? Technical Reports, Agrocampus, pp. 1–10, http://factominer.free.fr/docs/HCPC_husson_josse.pdf. Accessed Apr 2016

  • Ingestad T (1970) A definition of optimum nutrient requirements in birch seedlings I. Physiol Plant 23:1127–1138

    Article  Google Scholar 

  • Iqbal A, Yabuta Y, Takeda T, Nakano Y, Shigeoka S (2006) Hydroperoxide reduction by thioredoxin-specific glutathione peroxidase isoenzymes of Arabidopsis thaliana. FEBS J 273:5589–5597

    Article  CAS  PubMed  Google Scholar 

  • John R, Ahmad P, Gadgil K, Sharma S (2009) Cadmium and lead-induced changes in lipid peroxidation, antioxidative enzymes and metal accumulation in Brassica juncea L. at three different growth stages. Arch Agron Soil Sci 55:395–405

    Article  CAS  Google Scholar 

  • Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534

    Article  PubMed  Google Scholar 

  • Lawrence RA, Burk RF (1976) Glutathione peroxidase activity in rat liver. Biochem Biophys Res Commun 71:952–958

    Article  CAS  PubMed  Google Scholar 

  • Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Liao S-W, Chang W-L (2004) Heavy metal phytoremediation by water hyacinth at constructed wetlands in Taiwan. J Aquat Plant Manag 42:60–68

    Google Scholar 

  • Marmiroli M, Imperiale D, Maestri E, Marmiroli N (2013) The response of Populus spp. to cadmium stress: chemical, morphological and proteomics study. Chemosphere 93:1333–1344

    Article  CAS  PubMed  Google Scholar 

  • Mishra S, Srivastava S, Tripathi RD, Govindarajan R, Kuriakose SV, Prasad MNV (2006) Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L. Plant Physiol Biochem 44:25–37

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    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 

  • Opdenakker K, Remans T, Keunen E, Vangronsveld J, Cuypers A (2012) Exposure of Arabidopsis thaliana to Cd or Cu excess leads to oxidative stress mediated alterations in MAPKinase transcript levels. Environ Exp Bot 83:53–61

    Article  CAS  Google Scholar 

  • Ouzounidou G, Giannakoula A, Ilias I, Zamanidis P (2016) Alleviation of drought and salinity stresses on growth, physiology, biochemistry and quality of two Cucumis sativus L. cultivars by Si application. Braz J Bot 39:531–539

    Article  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  • Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Revelle, W (2015) Psych: procedures for personality and psychological research, Northwestern University, Evanston. http://CRAN.R-project.org/package=psych Version = 1.5.4

  • Sastre J, Sahuquillo A, Vidal M, Rauret G (2002) Determination of Cd, Cu, Pb, and Zn in environmental samples: microwave-assisted total digestion versus aqua regia and nitric acid digestion. Anal Chim Acta 462:59–72

    Article  CAS  Google Scholar 

  • Sharma SS, Dietz K-J (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726

    Article  CAS  PubMed  Google Scholar 

  • Siripornadulsil S, Traina S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14:2837–2847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5,5′-dithiobis(2-nitrobenzoic acid). Anal Biochem 175:408–413

    Article  CAS  PubMed  Google Scholar 

  • Turan Ö, Ekmekci Y (2014) Chilling tolerance of Cicer arietinum lines evaluated by photosystem II and antioxidant activities. Turk J Bot 38:499–510

    Article  CAS  Google Scholar 

  • Yücel E, Yaltırık F, Öztürk M (1995) Ornamental plants: trees and shrubs. Anadolu University, Faculty of Science Publications, Eskisehir

  • Zhang DP, Cao BH, Jia B, Tang Q (2008) Germination and physiological response of Albizia julibrissin seeds under alkali-salt stress. Sci Silvae Sin 44:157–161

    Google Scholar 

Download references

Acknowledgments

This work has been supported by Istanbul University Scientific Research Projects to G. Baycu (UDP-2681/0307208 and IRP-19869). S.E. Rognes received support from the Department of Molecular Biosciences, University of Oslo. The authors thank N.G. Kürüm, A.I. Aktürk, H. Eroglu, E. Kartal, and I. Özdemir for laboratory assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gülriz Baycu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baycu, G., Rognes, S.E., Özden, H. et al. Abiotic stress effects on the antioxidative response profile of Albizia julibrissin Durazz. (Fabaceae). Braz. J. Bot 40, 21–32 (2017). https://doi.org/10.1007/s40415-016-0318-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40415-016-0318-3

Keywords

Navigation