Indole-acyl esters improve the effect of nitrogen and phosphorous fertilization by mitigating the phytotoxicity and concentrations of cadmium and lead in Jatropha curcas L. in contaminated soils


  • Zhirong Fang 1. College of Life Sciences, Sichuan University, Chengdu 610064; 2. Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, 610041; 3. Xichang College, Xichang 615013
  • Hongshen Wan Research Institute of Crop Science, Sichuan Academy of Agricultural Sciences, Chengdu 610066
  • Ying Xu College of Life Sciences, Sichuan University, Chengdu 610064
  • Qin Liu Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, 610041
  • Jiang Liang Xichang College, Xichang 615013
  • Xiaodong Shi College of Life Sciences, Sichuan University, Chengdu 610064
  • Fang Chen College of Life Sciences, Sichuan University, Chengdu 610064


Jatropha curcas L., Pb/Cd stress, indole-acyl esters, nitrogen, phosphorus


Paper description:

  • Indole-acyl esters (ID), nitrogen (N) or phosphorous (P) fertilizers can mitigate the toxic effects of Cd and Pb on plant growth.
  • The Box-Behnken three-variable partial factorial design was utilized to study the interaction effects of three factors on Jatropha curcas L growth. The combined effects of two or three factors on plant growth were studied using single factor experiments.
  • Combined ID, N, and P treatments increased the ability of Jatropha curcas to grow on heavy metal-contaminated soils.
  • This paper proposes a novel methodology that is related to the interaction effects of multiple factors on plants.

Abstract: The effects of indole-acyl esters (ID), NH4NO3 (N), and KH2PO4 (P), on the mitigation of the toxic effects of Cd and Pb and their concentration in Jatropha curcas L. from contaminated soils was investigated. The concentrations of ID, N, and P were optimized (0.1 mL·L-1, 7 mM, and 2.5 mM, respectively) and they were applied in various combinations to the contaminated soils of potted plants of J. curcas. The results showed that ID together with the N and P fertilizers, increased plant biomass and improved the mitigating effects of the N-P treatments on Cd and Pb toxicity. Plants growing under ID-N-IP treatments had high whole plant biomasses, high concentrations of P, N, Pb and Cd in whole plants, as well as enhanced activities of superoxide dismutase (SOD) and peroxidase (POD). These results point to the phytoremediation ability of J. curcas. We propose a new methodology that can be utilized to study the effects and interactions of multiple factors on plant growth.

Received: February 16, 2019; Revised: August 17, 2019; Accepted: August 19, 2019; Published online: August 30, 2019

How to cite this article: Fang Z, Wan H, Xu Y, Liu Q, Liang J, Shi X, Chen F. Indole-acyl esters improve the effect of nitrogen and phosphorous fertilization by mitigating the phytotoxicity and concentrations of cadmium and lead in Jatropha curcas L. in contaminated soils. Arch Biol Sci. 2019;71(4):677-86.


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Wong JWC, Selvam A. Speciation of heavy metals during co-composting of sewage sludge with lime. Chemosphere. 2006,63:980-6.

Tchounwou PB, Yedjou CG, Pallolla AK, Sutton DJ. Heavy metal toxicity and the environment. Exp Suppl. 2012;101:133-64.

Bhargava A, Carmona FF, Bhargava M, Srivastava S. Approaches for enhanced phytoextraction of heavy metals. J Environ Manage. 2012;105:103-20.

Mahawar L, Kumar R, Shekhawat GS. Evaluation of heme oxygenase 1 (HO1) in Cd and Ni induced cytotoxicity and crosstalk with ROS quenching enzymes in two to four leaf stage seedlings of Vigna radiata. Protoplasma. 2018;255:527-45.

Foidl N, Foidl G, Sanchez M, Mittelbach M, Hackel S. Jatropha curcas L. as a source for the production of biofuel in Nicaragua. Bioresource Technol. 1996;58(1):77-82.

Divakara BN, Upadhyaya HD, Wani SP, Gowda CLL. Biology and genetic improvement of Jatropha curcas L.: A review. Appl Enegr. 2010;87(3):732-42.

Prasad MNV. Jatropha curcas L. cultivation on constrained land: exploring the potential for economic growth and environmental protection. In: Warra AA, Prasad MNV, editors. Bioremediation and Bioeconomy. Elsevier; 2016. p. 129-47.

Pandey VC, Bajpai O, Singh N. Energy crops in sustainable phytoremediation. Renew Sust Enegr Rev. 2016;54:58-73.

Mangkoedihardjo S. Jatropha curcas L. for phytoremediation of lead and cadmium polluted soil. World Appl Sci J. 2008;4(4):519-22.

Yadav SK, Juwarkar AA, Kumar GP, Thawale PR, Singh SK, Chakrabarti T. Bioaccumulation and phyto-translocation of arsenic, chromium and zinc by Jatropha curcas L.: impact of dairy sludge and bio-fertilizer. Bioresour Technol. 2009;100(20):4616-22.

Jamil S, Abhilash PC, Singh N, Sharma PN. Jatropha curcas: a potential crop for phytoremediation of coal fly ash. J Hazard Mater . 2009;172(1):269-75.

Li MS, Luo YP, Su ZY. Heavy metal concentrations in soils and plant accumulation in a restored manganese mine land in Guangxi, South China. Environ Pollut. 2007;147(1):168-75.

Liang J, Yang Z, Tang L, Xu Y, Wang S, Chen F. Growth performance and tolerance responses of Jatropha (Jatropha curcas) seedling subjected to isolated or combined cadmium and lead stresses. Int J Agric Biol. 2012;14(6):861-9.

Fu J, Huang B. Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environ Exp Bot. 2001;45:105-14

Cho UH, Seo NH. Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci. 2005;168:113-20.

Zhang SS, Zhang HM, Qin R, Jjiang WS, Liu DH. Cadmium induction of lipid peroxidation and effects on root tip cells and antioxidant enzyme activities in Vicia faba L.[J]. Ecotoxicol. 2009;18(7):814-23.

Metwally A, Safronova VI, Belimov AA, Dietz KJ. Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot. 2005;56:167-78

Pandey V, Dixit V, Shyam R. Antioxidative responses in relation to growth of mustard (Brassica juncea cv. Pusa Jai Kisan) plants exposed to hexavalent chromium. Chemosphere. 2005;61:40-7.

Shaw BP. Effects of mercury and cadmium on the activities of antioxidative enzymes in the seedlings of Phaseolus aureus. Biol Plant.1995;37(4):587-96.

Sandalio L, Dalurzo H, Gomez M, Romero-Puertas M, del Rio LA. Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot. 2001;52:2115-26.

Wu FB, Zhang GP, Dominy P. Four barley genotypes respond differently to cadmium: lipid peroxidation and activities of antioxidant capacity. Environ Exp Bot. 2003;50:67-78.

Sharma SS, Kaul S, Metwally A, Goyal KC, Finkemeier I, Dietz KJ. Cadmium toxicity to barley (Hordeum vulgare) as affected by varying Fe nutritional status. Plant Sci. 2004;166:1287-95.

Mohamed Bah A, Dai H, Zhao J, Sun H, Cao F, Zhang G, Wu F. Effects of cadmium, chromium and lead on growth, metal uptake and antioxidative capacity in Typha angustifolia. Biol Trace Elem Res. 2011;142:77-92.

Panković D, Plesničar M, Arsenijević-Maksimović I, Petrović N, Sakač Z, Kastori R. Effects of nitrogen nutrition on photosynthesis in Cd-treated sunflower plants. Ann Bot. 2000;86(4):841-7.

Zhang F, Wan X, Zhong Y. Nitrogen as an important detoxification factor to cadmium stress in poplar plants. J Plant Interact. 2014;9(1):249-58.

Du J, Yan C, Li Z. Phosphorus and cadmium interactions in Kandelia obovata (S. L.) in relation to cadmium tolerance. Environ Sci Pollut R. 2014;21(1):355-65.

Fässler E, Evangelou MW, Robinson BH, Schulin R. Effects of indole-3-acetic acid (IAA) on sunflower growth and heavy metal uptake in combination with ethylene diamine disuccinic acid (EDDS). Chemosphere. 2010;80(8):901-7.

Bashri G, Prasad SM. Indole acetic acid modulates changes in growth, chlorophyll a fluorescence and antioxidant potential of Trigonella foenum-graecum L. grown under cadmium stress. Acta Physiol Plant. 2015;37(3):37-49.

He S, Wu Q, He Z. Effect of DA-6 and EDTA alone or in combination on uptake, subcellular distribution and chemical form of Pb in Lolium perenne. Chemosphere. 2013;93(11):2782-8.

He S, Wu Q, He Z.Growth-promoting hormone DA-6 assists phytoextraction and detoxification of Cd by Rye grass. Int J Phytoremediat. 2015;17(6):597-603.

Bakku RK, Terli R, Somalanka SR, Palukurty MA. Optimization of borassus flabellifer amylase extraction procedure using Box-Behnken design and development of simple affinity chromatographic technique for purification of amylases. Brit Biotechnol J. 2012;2(3):146-56.

Li HJ. Comparative Study on Determination of Phosphorus Content in Two Kinds of Plants. Mod Agr Sci Technol. 2012;11:16-17

McDonald M. A simple and improved method for the determination of microgram quantities of nitrogen in plant material. Ann Bot. 1978;42(2):363-6.

Zhang H, Tang J. Determination of Fe, Mn, Cu, Pb, and Cd in Vegetables by Atomic Absorption Spectrometry[J]. Chin J Spectrosc Lab. 2011;28(1):72-4

Li HS. The principle and measuring technique of plant physiology and chemistry. Beijing: Beijing Higher Education Press; 2000. 260-1 p.

Beauchamp C, Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem. 1971;44(1):276-87.

Lagrimini LM. Wound-induced deposition of polyphenols in transgenic plants overexpressing peroxidase. Plant Physiol. 1991;96(2):577-83.

Aebi H. Catalase in vitro. Method Enzymol. 1984;105:121-6.

Michálková Z, Martínez-Fernández D, Komárek M. Interactions of two novel stabilizing amendments with sunflower plants grown in a contaminated soil. Chemosphere. 2017;186:374-80.

Fargašová A. Phytotoxic effects of Cd, Zn, Pb, Cu and Fe on Sinapis alba L. seedlings and their accumulation in roots and shoots. Biol Plantarum. 2001;44(3):471-3.

Verma S, Dubey R. Effect of cadmium on soluble sugars and enzymes of their metabolism in rice. Biol Plantarum. 2001;44(1):117-23.

Verma S, Dubey R. Lead toxicity induced lipid per-oxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci. 2003;164:645-55.

Razaq M, Zhang P, Shen H, Salahuddin. Influence of nitrogen and phosphorous on the growth and root morphology of Acer mono. Plos ONE. 2017;12(2):e0171321.

de Groot CC, Marcelis LFM, van den Boogaard R, Kaiser WM, Lambers H. Interaction of nitrogen and phosphorus nutrition in determining growth. Plant and Soil. 2003;248:257-68.

Lippmann B, Leinhos V, Bergmann H. Influence of auxin producing rhizobacteria on root morphology and nutrient accumulation of crops, Pt. 1: Changes in root morphology and nutrient accumulation in maize (Zea mays L.) caused by inoculation with indole-3-acetic acid (IAA) producing Pseudomonas and Acinetobacter strains or IAA applied exogenously. J Appl Bot. 1995;69:31-6.

Wang HH, Shan XQ, Wen B, Owens G, Fang J, Zhang SZ. Effect of indole-3-acetic acid on lead accumulation in maize (Zea mays L.) seedlings and the relevant antioxidant response. Environ Exp Bot. 2007;61(3):246-53.

Tyburski J, Dunajska K, Mazurek P, Piotrowska B, Tretyn A. Exogenous auxin regulates H2O2 metabolism in roots of tomato (Lycopersicon esculentum Mill.) seedlings affecting the expression and activity of CuZn-superoxide dismutase, catalase, and peroxidase. Acta Physiol Plant. 2009;31:249-60.

Bashri G, Prasad SM. Exogenous IAA differentially affects growth, oxidative stress and antioxidants system in Cd stressed Trigonella foenum-graecum L. seedlings: Toxicity alleviation by up-regulation of ascorbate-glutathione cycle. Ecotoxicol Environ Saf. 2016;132:329-38.

Lee DH, Lee CB. Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Sci. 2000;159(1):75-85.

Scandalios JG. Oxygen stress and superoxide dismutases. Plant Physiol. 1993;101(1):7-12.

Ramón OC, Saúl V, Esteban E, Mercedes FP, Mara RF, Zornoza P. Cadmium-stress in white lupine: effect on nodule structure and function. Plant Physiol, 2003;161:911-9.

Kibria MG , Islam M, Osman KT . Effects of lead on growth and mineral nutrition of Amaranthus gangeticus L. and Amaranthus oleracea L. Soil Environ. 2009;28(1):1-6.

Farouk S, Mosa AA, Taha AA, El-Gahmery AM. Protective effect of humic acid and chitosan on radish (Raphanus sativus, L. var. sativus) plants subjected to cadmium stress. J Stress Physiol Biochem. 2011; 7(2):99-116.

Hussain K, Hussain M, Majeed A , Nawaz K, Nisar MF, Afghan S. Morphochemical Response of Chaksu (Cassia absus L.) to Different Concentrations of Indole Acetic Acid (IAA)[J]. Pakistan J Bot. 2010;7(3):1491-3.

Darra BL , Saxena SN. Role of IAA on the mineral composition of maize (Zea mays) crop under various osmotic stressed conditions[J]. Plant Soil. 1973;38(3):657-61.

Scheckel KG, Ryan JA, Allen D, Lescano NV. Determining speciation of Pb in phosphate-amended soils: method limitations. Sci Total Environ. 2005;350(1):261-72.

Qiu Q, Wang Y, Yang Z, Yuan J. Effects of phosphorus supplied in soil on subcellular distribution and chemical forms of cadmium in two Chinese flowering cabbage (Brassica Pdarachinensis L.) cultivars differing in cadmium accumulation. Food Chem Toxicol. 2011;49(9):2260-7.

Du RJ, He EK, Tang YT, Hu PJ, Ying RR, Morel JL, Qiu RL. How phytohormone IAA and Chelator EDTA affect lead uptake by ZN/CD Hyperaccumulator Picris divaricata. Int J Phytoremediat.2011;13(10):1024-36.




How to Cite

Fang Z, Wan H, Xu Y, Liu Q, Liang J, Shi X, Chen F. Indole-acyl esters improve the effect of nitrogen and phosphorous fertilization by mitigating the phytotoxicity and concentrations of cadmium and lead in Jatropha curcas L. in contaminated soils. Arch Biol Sci [Internet]. 2019Dec.19 [cited 2022Aug.9];71(4):677-86. Available from: