Skip to main content
Log in

Cadmium-induced stress on the seed germination and seedling growth of Brassica napus L., and its alleviation through exogenous plant growth regulators

  • Original Paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Because of its prolific growth, oilseed rape (Brassica napus L.) can be grown advantageously for phytoremediation of the lands contaminated by industrial wastes. Therefore, toxic effect of cadmium on the germination of oilseed rape, the capability of plants for cadmium phytoextraction, and the effect of exogenous application of plant growth regulators to mitigate phytotoxicity of cadmium were investigated. For the lab study of seedlings at early stage, seeds were grown on filter papers soaked in different solutions of Cd2+ (0, 10, 50, 100, 200 and 400 μM). In greenhouse study, seedlings were grown in soil for 8 weeks, transferred to hydroponic pots for another 6 weeks growth, and then treated with plant growth regulators and cadmium. Four plant growth regulators viz. jasmonic acid (12.5 μM), abscisic acid (10 μM), gibberellin (50 μM) and salicylic acid (50 μM); and three levels of Cd2+ (0, 50 and 100 μM) were applied. Data indicated that lower concentration of Cd2+ (10 μM) promoted the root growth, whereas the severe stresses (200 or 400 μM) had negative effect on the establishment of germinating seedlings. Plants treated with any of the tested plant growth regulators alleviated cadmium toxicity symptoms, which were reflected by more fresh weight, less malondialdehyde concentration in leaves and lower antioxidant enzyme activities. The application of abscisic acid to the plants cultivated in the medium containing 100 μM Cd2+ resulted in significantly lower plant internal cadmium accumulation.

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
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

PGRs:

Plant growth regulators

MDA:

Malondialdehyde

APX:

Ascorbate peroxidase

CAT:

Catalase

POD:

Peroxidase

SOD:

Superoxide dismutase

ICL:

Isocitrate lyase

JA:

Jasmonic acid

ABA:

Abscisic acid

GA:

Gibberellin

SA:

Salicylic acid

ROS:

Reactive oxygen species

References

  • Afroz S, Mohammad F, Hayat S, Siddiqui MH (2005) Exogenous application of gibberellic acid counteracts the ill effect of sodium chloride in mustard. Turk J Biol 29:233–236

    CAS  Google Scholar 

  • Anjum NA, Umar S, Ahmad A, Iqbal M, Khan NA (2008) Sulphur protects mustard (Brassica campestris L.) from cadmium toxicity by improving leaf ascorbate and glutathione. Plant Growth Regul 54(3):271–279. doi:10.1007/s10725-007-9251-6

    Article  CAS  Google Scholar 

  • Asada K (1984) Chloroplasts: formation of active oxygen and its scavenging. Methods Enzymol 105:422–429. doi:10.1016/S0076-6879(84)05059-X

    Article  CAS  Google Scholar 

  • Baker A, Graham IA, Holdsworth M, Smith SM, Theodoulou FL (2006) Chewing the fat: β-oxidation in plant signaling and development. Trends Plant Sci 11:124–132. doi:10.1016/j.tplants.2006.01.005

    Article  PubMed  CAS  Google Scholar 

  • Banyal S, Rai VK (1983) Reversal of osmotic stress effects by gibberellic acid in Brassica campestris. Recovery of hypocotyl growth, protein and RNA levels in the presence of GA. Physiol Plant 59:111–114. doi:10.1111/j.1399-3054.1983.tb06580.x

    Article  CAS  Google Scholar 

  • Bartels D, Schneider K, Terstappen G, Piatowiski D, Salamani F (1990) Molecular cloning of ABA-modulated genes from the resurrection plant Craterostigma plantagineum which are induced during desiccation. Planta 181:27–34. doi:10.1007/BF00202321

    Article  CAS  Google Scholar 

  • Battal P, Erez ME, Turker M, Berber I (2008) Molecular and physiological changes in maize (Zea mays) induced by exogeneous NAA, ABA and MeJA during cold stress. Ann Bot Fenn 45:173–185

    Google Scholar 

  • Biemelt S, Keetman V, Albrecht G (1998) Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings. Plant Physiol 116:651–658. doi:10.1104/pp.116.2.651

    Article  PubMed  CAS  Google Scholar 

  • Bornman CH, Jansson E (1980) Nicotiana tabacum callus studies. X. ABA increases resistance to cold damage. Physiol Plant 48:491–493. doi:10.1111/j.1399-3054.1980.tb03292.x

    Article  CAS  Google Scholar 

  • Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030. doi:10.1104/pp.126.3.1024

    Article  PubMed  CAS  Google Scholar 

  • Budde CO, Polenta G, Pagani A, Gabilondo J, Fussi M, Murray R (2005) The high temperature stress and exogenous applications of methyl jasmonate on peaches. In: Proceedings 5th International postharvest symposium, Verona, pp 682

  • Cakmak I, Strboe D, Marschner H (1993) Activities of hydrogen peroxide-scavenging enzymes in germinating wheat seeds. J Exp Bot 44:127–132. doi:10.1093/jxb/44.1.127

    Article  CAS  Google Scholar 

  • Cao D, Cheng H, Wu W, Soo HM, Peng J (2006) Gibberellin mobilizes distinct DELLA-dependent transcriptomes to regulate seed germination and floral development in Arabidopsis. Plant Physiol 142:509–525. doi:10.1104/pp.106.082289

    Article  PubMed  CAS  Google Scholar 

  • Cheng W, Zhang G, Yao H, Zhang H (2008) Genotypic difference of germination and early seedling growth response to Cd stress and its relation to Cd accumulation. J Plant Nutr 11:702–715. doi:10.1080/01904160801926764

    Article  CAS  Google Scholar 

  • Choudhary M, Bailey LD, Grant CA, Leisle D (1995) Effect of Zn on the concentration of Cd and Zn in plant tissue of two Durum wheat lines. Can J Plant Sci 75:445–448

    CAS  Google Scholar 

  • Creelman RA, Mullet JE (1995) Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc Natl Acad Sci USA 92:4114–4119. doi:10.1073/pnas.92.10.4114

    Article  PubMed  CAS  Google Scholar 

  • Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (1998) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351–1357. doi:10.1104/pp.116.4.1351

    Article  PubMed  CAS  Google Scholar 

  • Dhindsa RS, Dhindsa PP, Thorpe TA (1980) Leaf senescence correlated with increased levels of membrane permeability and lipid-peroxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101. doi:10.1093/jxb/32.1.93

    Article  Google Scholar 

  • Edreva A (2005) Generation and scavenging of reactive oxygen species in chloroplasts: a submolecular approach. Agric Ecosyst Environ 106:119–133. doi:10.1016/j.agee.2004.10.022

    Article  CAS  Google Scholar 

  • Focks N, Benning C (1998) wrinkled1: a novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiol 118:91–101. doi:10.1104/pp.118.1.91

    Article  PubMed  CAS  Google Scholar 

  • Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki F, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442. doi:10.1016/j.pbi.2006.05.014

    Article  PubMed  Google Scholar 

  • Graham IA, Eastmond PJ (2002) Pathways of straight and branched chain fatty acid catabolism in higher plants. Prog Lipid Res 41:156–181. doi:10.1016/S0163-7827(01)00022-4

    Article  PubMed  CAS  Google Scholar 

  • Harberd NP (2003) Relieving DELLA restraint. Science 299:1853–1854. doi:10.1126/science.1083217

    Article  PubMed  CAS  Google Scholar 

  • Hassan MJ, Shao G, Zhang G (2005a) Influence of cadmium toxicity on antioxidant enzymes activity in rice cultivars with different grain Cd accumulation. J Plant Nutr 28:1259–1270. doi:10.1081/PLN-200063298

    Article  CAS  Google Scholar 

  • Hassan MJ, Wang F, Ali S, Zhang G (2005b) Toxic effect of cadmium on rice as affected by nitrogen fertilizer form. Plant Soil 277:359–365. doi:10.1007/s11104-005-8160-6

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. doi:10.1016/0003-9861(68)90654-1

    Article  PubMed  CAS  Google Scholar 

  • Hendrix DL (1993) Rapid extraction and analysis of nonstructural carbohydrates in plant tissues. Crop Sci 33:1306–1311

    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. doi:10.1046/j.1365-3040.2003.01018.x

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa S, Noriharu AE, Murakami M, Wagatsuma T (2006) Is Brassica juncea a suitable plant for phytoremediation of cadmium in soils with moderately low cadmium contamination? Possibility of using other plant species for Cd-phytoextraction. Soil Sci Plant Nutr 52:32–42

    Article  CAS  Google Scholar 

  • Janda T, Szalai G, Antunovics Z, Horváth E, Páldi E (2000) Effect of benzoic acid and aspirin on chilling tolerance and photosynthesis in young maize plants. Maydica 45:29–33

    Google Scholar 

  • Kuriakose SV, Prasad MNV (2008) Cadmium stress affects seed germination and seedling growth in Sorghum bicolor (L.) Moench by changing the activities of hydrolyzing enzymes. Plant Growth Regul 54(2):143–156. doi:10.1007/s10725-007-9237-4

    Article  CAS  Google Scholar 

  • Li YM, Channey LR, Schneiter AA (1995) Genotypic variation in kernel cadmium concentration in sunflower germplasm under varying soil conditions. Crop Sci 35:137–141

    Article  Google Scholar 

  • Li W, Khan MA, Yamaguchi S, Kamiya Y (2005) Effects of heavy metals on seed germination and early seedling growth of Arabidopsis thaliana. Plant Growth Regul 46(1):45–50. doi:10.1007/s10725-005-6324-2

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. doi:10.1016/0076-6879(87)48036-1

    Article  CAS  Google Scholar 

  • Lu Y, Wu YR, Han B (2005) Anaerobic induction of isocitrate lyase and malate synthase in submerged rice seedlings indicates the important metabolic role of the glyoxylate cycle. Acta Biochim Biophys Sin (Shanghai) 37:406–414. doi:10.1111/j.1745-7270.2005.00060.x

    Article  CAS  Google Scholar 

  • Maksymiec W, Wianowska D, Dawidowicz A, Radkiewicz S, Mardarowicz M, Krupa Z (2005) The level of jasmonic acid in Arabidopsis thaliana and Phaseolus coccineus plants under heavy metal stress. J Plant Physiol 162:1338–1346. doi:10.1016/j.jplph.2005.01.013

    Article  PubMed  CAS  Google Scholar 

  • Metwally A, Finkemeier I, Georgi M, Dietz K (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272–281. doi:10.1104/pp.102.018457

    Article  PubMed  CAS  Google Scholar 

  • Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970

    Article  PubMed  CAS  Google Scholar 

  • Ohto MA, Fischer RL, Goldberg RB, Nakamura K, Harada JJ (2005) Control of seed mass by APETALA2. Proc Natl Acad Sci USA 102:3123–3128. doi:10.1073/pnas.0409858102

    Article  PubMed  CAS  Google Scholar 

  • Overmyer K, Brosche M, Kangasja J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342. doi:10.1016/S1360-1385(03)00135-3

    Article  PubMed  CAS  Google Scholar 

  • Pái M, Szalai G, Horváth E, Janda T, Páldi E (2002) Effect of salicylic acid during heavy metal stress. In: Proceedings of the 7th Hungarian congress plant physiology, vol 46, pp 119–120

  • Papoyan A, Piñeros M, Kochian LV (2007) Plant Cd2+ and Zn2+ status effects on root and shoot heavy metal accumulation in Thlaspi caerulescens. New Phytol 175:51–58. doi:10.1111/j.1469-8137.2007.02073.x

    Article  PubMed  CAS  Google Scholar 

  • Penner GA, Clarke J, Bezte LJ, Leisle D (1995) Identification of RAPD markers linked to a gene governing cadmium uptake in durum wheat. Genome 38:543–547

    PubMed  CAS  Google Scholar 

  • Ranaldi F, Vanni P, Giachetti E (2000) Multisite inhibition of Pinus pinea isocitrate lyase by phosphate. Plant Physiol 124:1131–1138. doi:10.1104/pp.124.3.1131

    Article  PubMed  CAS  Google Scholar 

  • Shah SH (2007) Effect of salt stress on mustard as affected by gibberellic acid application. Gen Appl Plant Physiol 33:97–106

    CAS  Google Scholar 

  • Shamsi IH, Wei K, Zhang GP, Jilani G, Hassan MJ (2008a) Interactive effects of cadmium and aluminum on growth and antioxidative enzymes in soybean. Biol Plant 52:165–169. doi:10.1007/s10535-008-0036-1

    Article  CAS  Google Scholar 

  • Shamsi IH, Jilani G, Zhang GP, Kang W (2008b) Cadmium stress tolerance through potassium nutrition in soybean. Asian J Chem 20:1099–1108

    CAS  Google Scholar 

  • Swamy PM, Smith BN (1999) Role of abscisic acid in plant stress tolerance. Curr Sci 96:1220–1228

    Google Scholar 

  • Tang QY, Feng MG (2001) Data processing system. http://www.chinadps.net

  • Vettakkorumakankav NN, Falk D, Saxena P, Fletcher RA (1999) A crucial role for gibberellins in stress protection of plants. Plant Cell Physiol 40:542–548

    CAS  Google Scholar 

  • Wang H, Huang AHC (1984) Inhibitors of lipase activities in soybean and other oil seeds. Plant Physiol 76:929–934

    Article  PubMed  CAS  Google Scholar 

  • Wasternack C, Miersch O, Kramell R, Hause B, Ward J, Beale M, Boland W, Parthier B, Feussner I (1998) Jasmonic acid: biosynthesis, signal transduction, gene expression. Fett Lipid 100:139–146. doi:10.1002/(SICI)1521-4133(19985)100:4/5<139::AID-LIPI139>3.0.CO;2-5

    Article  CAS  Google Scholar 

  • Wu FB, Zhang GP (2004) Effect of cadmium on free amino acids, glutathione and ascorbic acid content in two barley genotypes differing in Cd tolerance. Chemosphere 57:447–454. doi:10.1016/j.chemosphere.2004.06.042

    Article  PubMed  CAS  Google Scholar 

  • Yarushnykov VV, Blanke MM (2005) Alleviation of frost damage to pear flowers by application of gibberellin. Plant Growth Regul 45:21–27. doi:10.1007/s10725-004-6893-5

    Article  CAS  Google Scholar 

  • Yin H, Chen Q, Yi M (2008) Effects of short-term heat stress on oxidative damage and responses of antioxidant system in Lilium longiflorum. Plant Growth Regul 54:45–54. doi:10.1007/s10725-007-9227-6

    Article  CAS  Google Scholar 

  • Yuan S, Lin HH (2008) Role of salicylic acid in plant abiotic stress. Z Naturfosch 63:313–320

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by National Science Foundation of China (the program code: 30671339) and The Science and Technology Bureau of Zhejiang province (the program code: 2006R10002). The financial support by both of these organizations is highly acknowledged. We thank Ms. Siu-Wei Huang from Berkeley University of California for the correction of language mistakes on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lixi Jiang.

Additional information

Huabing Meng and Shujin Hua contributed equally to this paper.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meng, H., Hua, S., Shamsi, I.H. et al. 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 (2009). https://doi.org/10.1007/s10725-008-9351-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-008-9351-y

Keywords

Navigation