Skip to main content
Log in

Cadmium stress alters the redox reaction and hormone balance in oilseed rape (Brassica napus L.) leaves

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

In order to understand the physiological response of oilseed rape (Brassica napus L.) leaves to cadmium (Cd) stress and exploit the physiological mechanisms involved in Cd tolerance, macro-mineral and chlorophyll concentrations, reactive oxygen species (ROS) accumulation, activities of enzymatic antioxidants, nonenzymatic compounds metabolism, endogenous hormonal changes, and balance in leaves of oilseed rape exposed to 0, 100, or 200 μM CdSO4 were investigated. The results showed that under Cd exposure, Cd concentrations in the leaves continually increased while macro-minerals and chlorophyll concentrations decreased significantly. Meanwhile, with increased Cd stress, superoxide anion (O • −2 ) production rate and hydrogen peroxide (H2O2) concentrations in the leaves increased significantly, which caused malondialdehyde (MDA) accumulation and oxidative stress. For scavenging excess accumulated ROS and alleviating oxidative injury in the leaves, the activity of enzymatic antioxidants, such as superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT), was increased significantly at certain stress levels. However, with increased Cd stress, the antioxidant enzyme activities all showed a trend towards reduction. The nonenzymatic antioxidative compounds, such as proline and total soluble sugars, accumulated continuously with increased Cd stress to play a long-term role in scavenging ROS. In addition, ABA levels also increased continuously with Cd stress while ZR decreased and the ABA/ZR ratio increased, which might also be providing a protective role against Cd toxicity.

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

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

Car:

Carotenoid

Cd:

Cadmium

Chl:

Chlorophyll

Chl a:

Chlorophyll a

Chl b:

Chlorophyll b

Ca:

Calcium

CAT:

Catalase

CK:

Cytokinin

H2O2 :

Hydrogen peroxide

K:

Potassium

MDA:

Malondialdehyde

Mg:

Magnesium

Na:

Sodium

O • −2 :

Superoxide anion

POD:

peroxidase

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

Total Chl:

Total chlorophyll

ZR:

Zeatin-riboside

References

  • Agarwal S, Sairam RK, Srivastava GC, Tyagi A, Meena RC (2005) Role of ABA, salicylic acid, calcium and hydrogen peroxide on antioxidant enzymes induction in wheat seedlings. Plant Sci 169:559–570

    Article  CAS  Google Scholar 

  • Asada K (1996) Radical production and scavenging in the chloroplasts. In: Photosynthesis and the Environment. Springer, Netherlands, pp 123–150

    Google Scholar 

  • Asada K, Foyer CH, Mullineaux PM (1994) Production and action of active oxygen species in photosynthetic tissues. Causes of photooxidative stress and amelioration of defense systems in plants., pp 77–104

    Google Scholar 

  • Azevedo H, Glória Pinto CG, Fernandes J, Loureiro S, Santos C (2005) Cadmium effects on sunflower growth and photosynthesis. J Plant Nutr 28:2211–2220

    Article  CAS  Google Scholar 

  • Bhattacharjee S (1997) Membrane lipid peroxidation, free radical scavengers and ethylene evolution in Amaranthus as affected by lead and cadmium. Biol Plantarum 40:131–135

    Article  CAS  Google Scholar 

  • Brugière N, Jiao S, Hantke S, Zinselmeier C, Roessler JA, Niu X, Jones RJ, Habben JE (2003) Cytokinin oxidase gene expression in maize is localized to the vasculature, and is induced by cytokinins, abscisic acid, and abiotic stress. Plant Physiol 132:1228–1240

    Article  CAS  Google Scholar 

  • Carrier P, Baryla A, Havaux M (2003) Cadmium distribution and microlocalization in oilseed rape (Brassica napus) after long-term growth on cadmium-contaminated soil. Planta 216:939–950

    CAS  Google Scholar 

  • Chaves MM (1991) Effects of water deficits on carbon assimilation. J Exp Bot 42:1–16

    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-London 103:551–560

    Article  CAS  Google Scholar 

  • Chen SL, Wang SS, Altman A, Hüttermann A (1996) Cytokinins: moderators of stomatal movement in poplar genotypes. J Beijing For Univ (Einglish Ed) 5:9–22

    Google Scholar 

  • Couée I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459

    Article  CAS  Google Scholar 

  • Dermont G, Bergeron M, Mercier G, Richer-Laflèche M (2008) Soil washing for metal removal: a review of physical/chemical technologies and field applications. J Hazard Mater 152:1–31

    Article  CAS  Google Scholar 

  • Dodd IC (2005) Root-to-shoot signalling: assessing the roles of ‘up’ in the up and down world of long-distance signalling in planta. Plant Soil 274:251–270

    Article  CAS  Google Scholar 

  • Ekmekçi Y, Tanyolac D, Ayhan B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J Plant Physiol 165:600–611

    Article  CAS  Google Scholar 

  • Elin RJ (1987) Assessment of magnesium status. Clin Chem 33:1965–1970

    CAS  Google Scholar 

  • Esfandiari E, Shakiba MR, Mahboob SA, Alyari H, Toorchi M (2007) Water stress, antioxidant enzyme activity and lipid peroxidation in wheat seedling. J Food Agric Environ 5:149–153

    CAS  Google Scholar 

  • Fang Z, Bouwkamp JC, Solomos T (1998) Chlorophyllase activities and chlorophyll degradation during leaf senescence in non-yellowing mutant and wild type of Phaseolus vulgaris L. J Exp Bot 49:503–510

    CAS  Google Scholar 

  • Fodor E, Szabó-Nagy A, Erdei L (1995) The effects of cadmium on the fluidity and H+-ATPase activity of plasma membrane from sunflower and wheat roots. J Plant Physiol 147:87–92

    Article  CAS  Google Scholar 

  • Fryer MJ, Andrews JR, Oxborough K, Blowers DA, Baker NR (1998) Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature. Plant Physiol 116:571–580

    Article  CAS  Google Scholar 

  • Gao Y, Miao C, Wang Y, Xia J, Zhou P (2012) Metal-resistant microorganisms and metal chelators synergistically enhance the phytoremediation efficiency of Solanum nigrum L. in Cd-and Pb-contaminated soil. Environ Technol 33:1383–1389

    Article  CAS  Google Scholar 

  • Ghanem ME, Albacete A, Martínez-Andújar C, Acosta M, Romero-Aranda R, Dodd IC, Lutts S, Pérez-Alfocea F (2008) Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.). J Exp Bot 59:3039–3050

    Article  CAS  Google Scholar 

  • Gonçalves JF, Antes FG, Maldaner J, Pereira LB, Tabaldi LA, Rauber R, Rossato LV, Bisognin DA, Dressler VL, de Moraes Flores ÉM (2009) Cadmium and mineral nutrient accumulation in potato plantlets grown under cadmium stress in two different experimental culture conditions. Plant Physiol Bioch 47:814–821

    Article  CAS  Google Scholar 

  • Guo T, Zhang G, Zhou M, Wu F, Chen J (2004) Effects of aluminum and cadmium toxicity on growth and antioxidant enzyme activities of two barley genotypes with different Al resistance. Plant Soil 258:241–248

    Article  CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  CAS  Google Scholar 

  • Hassan M, Mansoor S (2014) Oxidative stress and antioxidant defense mechanism in mung bean seedlings after lead and cadmium treatments. Turk J Agric For 38:55–61

    Article  CAS  Google Scholar 

  • He Z (1993) A laboratory guide to chemical control technology on field crop. Beijing Agricultural University Press, Beijing, China, pp 60–68

    Google Scholar 

  • He J, Qin J, Long L, Ma Y, Li H, Li K, Jiang X, Liu T, Polle A, Liang Z (2011) Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus × canescens. Physiol Plantarum 143:50–63

    Article  CAS  Google Scholar 

  • He J, Ma C, Ma Y, Li H, Kang J, Liu T, Polle A, Peng C, Luo Z (2013) Cadmium tolerance in six poplar species. Environ Sci Pollut R 20:163–174

    Article  CAS  Google Scholar 

  • Hermans C, Chen J, Coppens F, Inzé D, Verbruggen N (2011) Low magnesium status in plants enhances tolerance to cadmium exposure. New Phytol 192:428–436

    Article  CAS  Google Scholar 

  • Hou Z, Wang L, Liu J, Hou L, Liu X (2013) Hydrogen sulfide regulates ethylene-induced stomatal closure in Arabidopsis thaliana. J Integr Plant Biol 55:277–289

    Article  CAS  Google Scholar 

  • Hsu YT, Kao CH (2003) Role of abscisic acid in cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Cell Environ 26:867–874

    Article  CAS  Google Scholar 

  • Hsu YT, Kao CH (2005) Abscisic acid accumulation and cadmium tolerance in rice seedlings. Physiol Plantarum 124:71–80

    Article  CAS  Google Scholar 

  • Huaiman C, Chunrong Z, Shenqiang W, Cong T (2000) Combined pollution and pollution index of heavy metals in red soil. Pedosphere 10:117–124

    Google Scholar 

  • Janicka-Russak M, Kabała K, Burzyński M (2012) Different effect of cadmium and copper on H+-ATPase activity in plasma membrane vesicles from Cucumis sativus roots. J Exp Bot 63:4133–4142

    Article  CAS  Google Scholar 

  • Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273

    Article  CAS  Google Scholar 

  • Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410

    Article  CAS  Google Scholar 

  • Kishor K, Polavarapu B, Sreenivasulu N (2014) Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant Cell Environ 37:300–311

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lei Y, Yin C, Li C (2006) Differences in some morphological, physiological, and biochemical responses to drought stress in two contrasting populations of Populus przewalskii. Physiol Plantarum 127:182–191

    Article  CAS  Google Scholar 

  • Li P, Wang XX, Zhang TL, Zhou DM, He YQ (2008) Effects of several amendments on rice growth and uptake of copper and cadmium from a contaminated soil. J Environ Sci 20:449–455

    Article  Google Scholar 

  • Llamas A, Ullrich CI, Sanz A (2000) Cd2+ effects on transmembrane electrical potential difference, respiration and membrane permeability of rice (Oryza sativa L) roots. Plant Soil 219:21–28

    Article  CAS  Google Scholar 

  • Meng H, Hua S, Shamsi IH, Jilani G, Li Y, Jiang L (2009) Cadmium-induced stress on the seed germination and seedling growth of Brassica napus L., and its alleviation through exogenous plant growth regulators. Plant Growth Regul 58:47–59

    Article  CAS  Google Scholar 

  • Mohanty P, Matysik J (2001) Effect of proline on the production of singlet oxygen. Amino Acids 21:195–200

    Article  Google Scholar 

  • Nazar R, Iqbal N, Masood A, Khan MIR, Syeed S, Khan NA (2012) Cadmium toxicity in plants and role of mineral nutrients in its alleviation. American Journal of Plant Sciences 3:1476–1489

    Article  CAS  Google Scholar 

  • Nebauer SG, Renau-Morata B, Guardiola JL, Molina RV (2011) Photosynthesis down-regulation precedes carbohydrate accumulation under sink limitation in Citrus. Tree Physiol 31:169–177

    Article  CAS  Google Scholar 

  • Novo LA, Manousaki E, Kalogerakis N, González L (2013) The effect of cadmium and salinity on germination and early growth of Brassica Juncea (L.) var. juncea. Fresenius Environ Bull 22:3709–3717

    CAS  Google Scholar 

  • Radotić K, Dučić T, Mutavdžić D (2000) Changes in peroxidase activity and isoenzymes in spruce needles after exposure to different concentrations of cadmium. Environ Exp Bot 44:105–113

    Article  Google Scholar 

  • Ru SH, Wang JQ, Su DC (2004) Characteristics of Cd uptake and accumulation in two Cd accumulator oilseed rape species. J Environ Sci–China 16:594–598

    CAS  Google Scholar 

  • Salt DE, Blaylock M, Kumar NP, Dushenkov V, Ensley BD, Chet I, Raskin I (1995a) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Nat Biotechnol 13:468–474

    Article  CAS  Google Scholar 

  • Salt DE, Prince RC, Pickering IJ, Raskin I (1995b) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Santos CV (2004) Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Sci Hortic-Amsterdam 103:93–99

    Article  CAS  Google Scholar 

  • Sharma SS, Dietz KJ (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  Google Scholar 

  • Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060

    Article  CAS  Google Scholar 

  • Souza RP, Machado EC, Silva JAB, Lagôa AMMA, Silveira JAG (2004) Photosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recovery. Environ Exp Bot 51:45–56

  • Stobart AK, Griffiths WT, Ameen-Bukhari I, Sherwood RP (1985) The effect of Cd2+ on the biosynthesis of chlorophyll in leaves of barley. Physiol Plantarum 63:293–298

  • Su DC, Wong JWC (2004) Selection of mustard oilseed rape (Brassica juncea L.) for phytoremediation of cadmium contaminated soil. B Environ Contam Tox 72:991–998

    Article  CAS  Google Scholar 

  • Sun SC, Wang HX, Li QR (1985) Preliminary studies on physiological changes and injury mechanism in aquatic vascular plants treated with cadmium. Acta Photophysiologica Sinica 11:113–121

    CAS  Google Scholar 

  • Uraguchi S, Fujiwara T (2012) Cadmium transport and tolerance in rice: perspectives for reducing grain cadmium accumulation. Rice 5:1–8

    Article  Google Scholar 

  • Veselov D, Kudoyarova G, Symonyan M, Veselov S (2003) Effect of cadmium on ion uptake, transpiration and cytokinin content in wheat seedlings. Bulg J Plant Physiol 353–359

  • Wang YL, Wang XD, Zhao B, Wang YC (2007) Reduction of hyperhydricity in the culture of Lepidium meyenii shoots by the addition of rare earth elements. Plant Growth Regul 52:151–159

    Article  CAS  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    Article  CAS  Google Scholar 

  • Yan H, Hu X, Li F (2012) Leaf photosynthesis, chlorophyll fluorescence, ion content and free amino acids in Caragana korshinskii Kom exposed to NaCl stress. Acta Physiol Plant 34:2285–2295

    Article  CAS  Google Scholar 

  • Yoneyama T, Gosho T, Kato M, Goto S, Hayashi H (2010) Xylem and phloem transport of Cd, Zn and Fe into the grains of rice plants (Oryza sativa L.) grown in continuously flooded Cd-contaminated soil. Soil Sci Plant Nutr 56:445–453

    Article  CAS  Google Scholar 

  • Zayneb C, Bassem K, Zeineb K, Grubb CD, Noureddine D, Hafedh M, Amine E (2015) Physiological responses of fenugreek seedlings and plants treated with cadmium. Environ Sci Pollut R, 22:1–11

Download references

Acknowledgments

This study was financially supported by the National Natural Science Foundation of China (51409131) and Jiangxi Province Science and Technology Support Program, China (20151BBF60013).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to DongHui Fu.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yan, H., Filardo, F., Hu, X. et al. Cadmium stress alters the redox reaction and hormone balance in oilseed rape (Brassica napus L.) leaves. Environ Sci Pollut Res 23, 3758–3769 (2016). https://doi.org/10.1007/s11356-015-5640-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-5640-y

Keywords

Navigation