Abstract
Pot experiments were conducted to evaluate the effects of gibberellic acid (GA3) and ethylenediaminetetraacetic acid (EDTA) on growth parameters, cadmium (Cd) phytoextraction, total phenolics, free proline and chlorophyll content of Parthenium hysterophorus plant grown in Cd-contaminated (100 mg/kg) soil. GA3 was applied as foliar spray (10−2, 10−4 and 10−6 M) while EDTA (40 mg/kg soil) was added to soil as single and in split doses. Results showed decrease in growth parameters due to Cd stress but P. hysterophorus plant demonstrated Cd hyperaccumulator potential based on bioconcentration factor (BCF). Lower concentration of GA3 (10−6 M) showed highest significant increase in the growth parameters while Cd concentration, accumulation (1.97 ± 0.11 mg/DBM) and bioconcentration (9.75 ± 0.34) was significantly higher in the treatment T11 (GA3 10−2 + split doses of EDTA). Cadmium significantly increased the root free proline while total phenolic concentration was significantly high in all parts of the plant. Chlorophyll contents were significantly reduced by Cd. GA3 showed significant increase in phenolic and chlorophyll contents in plant. Cadmium accumulation in plant tissues showed positive correlation with free proline (R 2 = 0.527, R 2 = 0.630) and total phenolics (R 2 = 0.554, R 2 = 0.723) in roots and leaves, respectively. Cd contents negatively correlated with biomass, chlorophyll and total water contents. Proline and phenolic contents showed positive correlation with dry biomass of plant. These findings suggest further investigation to study the role of endogenous phenolics and proline in heavy metal phytoremediation.
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Adewole MB, Sridhar MKC, Adeoye GO (2010) Removal of heavy metals from soil polluted with effluents from a paint industry using Helianthus annuus L. and Tithonia diversifolia (Hemsl.) as influenced by fertilizer applications. Biorem J 14(4):169–179
Åkesson A, Bjellerup P, Lundh T, Lidfeldt J, Nerbrand C, Samsioe G (2006) Cadmium-induced effects on bone in a population-based study of women. Environ Health Perspect 114:830–834
Alkorta I, Allica JH, Becerril JM, Amezaga I, Albizu I, Garbisu C (2004) Recent findings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and metalloids such as zinc, cadmium, lead, and arsenic. RESB 3:71–90
Allen SE (1974) Chemical analysis of ecological materials. Blackwell Scientific Publication, Oxford, London
Aloni B, Daie J, Wyse RE (1986) Enhancement of (14C)-sucrose export from source leaves of Vicia faba by gibberellic acid. Plant Physiol 82:962–966
Al-Wakeel SAM, Hamed AA, Dadoura SS (1995) Interactive effects of water stress and gibberellic acid on mineral composition of fenugreek plant. Egypt J Physiol Sci 18:269–282
Ambedkar G, Muniyan M (2013) Bioaccumulation of heavy and essential metals in the selected freshwater fish species from Perumal lake Cuddalore District, Tamilnadu, India. ISRJ 2(12):1–7
Ansari HR (1996) Effect of some phytohormones and NPK on growth and metabolism of mustard, PhD Thesis, Aligarh Muslim University, Aligarh, India
Arnon DI (1949) Copper enzymes in isolated chloroplasts, polyphenoloxidae in Beta vulgaris. Plant Physiol 24:1–15
Arteca RN (1996) Plant growth substances: principles and applications. Chapman and Hall Inc, New York
Arun KS, Carlos C, Herminia LZ, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753
Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution ecology and phytochemistry. Biorecovery 1:811–826
Barcelo J, Poschenriede C (1990) Plant water relations as affected by heavy metal stress: a review. J Plant Nutr 13:1–37
Bates LS, Waldren SP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Benjerano NR, Lips SH (1970) Hormonal regulation of nitrate reductase activity in leaves. New Phytol 69(1):165–169
Bhattacharjee S, Mukherjee AK (1994) Influence of cadmium and lead on physiological and biochemical responses of Vigna unguiculata (L). Walp. Seedling germination behaviour, total protein, proline content and protease activity. Pollut Res 13:269–277
Broughton WJ, McComb AJ (1971) Changes in the pattern of enzyme development in gibberellin-treated pea internodes. Annu Bot J 35:213–228
Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, Maryland
Chai MW, Li RL, Shi FC, Liu FC, Pan X, Cao D, Wen X (2012) Effects of cadmium stress on growth, metal accumulation and organic acids of Spartina alterniflora Loisel. Afr J Biotechnol 11(22):6091–6099
Chen H, Cutright T (2001) EDTA and HEDTA effects on Cd, Cr and Ni uptake by Helianthus annus. Chemosphere 45:21–28
Chen Y, Shen Z, Li X (2004) The use of vetiver grass (Vetiveria zizanioides) in the phytoremediation of soils contaminated with heavy metals. Appl Geo-chem 19:1553–1565
Choudhary NL, Sairam RK, Tyagi A (2005) Expression of delta1-pyrroline-5-carboxylate synthetase gene during drought in rice (Oryza sativa L.). Ind J Biochem Biophys 42:366–370
Chugh LK, Sawhney SK, Ghorbal MN, Ferjani EE (1997) Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzymes activities in bean (Phaseolus vulgaris L.). Plant Sci 127:139–147
Costa G, Morel J (1994) Water relations, gas exchange and amino acid content in Cd-treated lettuce. Plant Physiol Biochem 32:561–570
Crozier A, Turnbull CGN, (1984) Gibberellins: biochemistry and action in extension growth. What’s New in Plant Physiol 15: 9–12
De B, Mukherjee AK (1998) Mercury induced metabolic changes in seedlings and cultured cells of tomato. Geobios 23:83–88
Dhawan SR, Dhawan P (1996) Regeneration in Parthenium hysterophorus L. World Weeds 3:181–182
Diaz J, Bernal A, Pomar F, Merino F (2001) Induction of shikimate dehydrogenase and peroxidase in pepper (Capsicum annum L.) seedlings in response to copper stress and its relation to lignification. Plant Sci 1:161–179
Ekmekci 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
Elless MP, Blaylock MJ (2000) Amendment optimization to enhance lead extractability from contaminated soils for phytoremediation. Int J Phytoremed 2:75–89
Entry JA, Watrud LS, Reeves M (1999) Accumulation of 137Cs and 90Sr from contaminated soil by three grass species inoculated with mycorrhizal fungi. Int J Environ Pollut 104:449–457
Epelde L, Hernández-Allica J, Becerril JM, Blanco F, Garbisu C (2008) Effects of chelates on plants and soil microbial community: comparison of EDTA and EDDS for lead phytoextraction. Sci Total Environ 401:21–28
Evins WH, Varner JE (1972) Hormonal control of polyribosome formation in barley aleurone layers. Plant Physiol 49:348–352
Fabro G, Kovács I, Pavet V, Szabados L, Alvarez ME (2004) Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis. Mol Plant-Microbe Interact 17:343–350
Falkowska M, Pietryczuk A, Piotrowska A, Bajguz A, Grygoruk A, Czerpak R (2011) The effect of gibberellic acid (GA3) on growth, metal biosorption and metabolism of the green algae Chlorella vulgaris (Chlorophyceae) Beijerinck exposed to cadmium and lead stress. Pol J Environ Stud 20:53–59
Faller P, Kienzler K, Krieger-Liszkay A (2005) Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of photosystem II by competitive binding to the essential Ca2+ site. Biochim Biophys Acta 1706:158–164
Genrich I, Burd D, George D, Glick BR (2000) Plant growth promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbial 46:237–245
Grace SC, Logan BA (2000) Energy dissipation and radical scavenging by the plant phenylpropanoid pathway. Phil Trans R Soc Lond B 355:1499–1510
Guo CN, Liu F, Xu XM (2006) Chlorophyll-b deficiency and photosynthesis in plants. Plant Physiol Commun 42:967–973
Hadi F, Bano A (2009) Utilization of Parthenium hysterophorus for the remediation of lead-contaminated soil. Weed Biol Manag 9(4):307–314
Hadi F, Ali N, Ahmad A (2014) Enhanced phytoremediation of cadmium-contaminated soil by Parthenium hysterophorus plant: effect of gibberellic acid (GA3) and synthetic chelator, alone and in combinations. Bioremediat J 18(1):46–55
Hadi F, Bano A, Fuller MP (2010) The improved phytoextraction of lead (Pb) and the growth of maize (Zea mays L.): the role of plant growth regulators (GA3 and IAA) and EDTA alone and in combinations. Chemosphere 80:475–462
Haudecoeur E, Tannieres M, Cirou A, Raffoux A, Dessaux Y, Faure D (2009) Proline antagonizes GABA-induced quenching of quorum-sensing in Agrobacterium tumefaciens. Proc Natl Acad Sci U S A 106:14587–14592
Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7(11):1456–1466
Houshmandfar A, Moraghebi F (2011) Effect of mixed cadmium, copper, nickel and zinc on seed germination and seedling growth of safflower. Afr J Agric Res 6(5):1182–1187
John R, Ahmad P, Gadgil K, Sharma S (2009) Heavy metal toxicity: effect on plant growth, biochemical parameters and metal accumulation by Brassica juncea L. Int J Plant Prod 3:65–76
John R, Ahmad P, Gadgil K, Sharma S (2008) Effect of cadmium and lead on growth, biochemical parameters and uptake in Lemna polyrrhiza L. Plant Soil Environ 54(6):262–270
Kafel A, Rozpędek K, Szulińska E, Zawisza-Raszka A, Migula P (2014) The effects of cadmium or zinc multigenerational exposure on metal tolerance of Spodoptera exigua (Lepidoptera: Noctuidae). Environ Sci Pollut Res 21:4705–4715. doi:10.1007/s11356-013-2409-z
Kamnev AA, Van Der Lelie D (2000) Chemical and biological parameters as tools to evaluate and improve heavy metal phytoremediation. Biosci Rep 20:239–258
Khan NA, Ansari HR, Samiullah (1998) Effect of gibberellic acid spray during ontogeny of mustard on growth, nutrient uptake and yield characteristics. J Agron Crop Sci 181:61–73
Khatamipour M, Piri E, Esmaeilian Y, Tavassoli A (2011) Toxic effect of cadmium on germination, seedling growth and proline content of milk thistle (Silybum marianum). Ann Biol Res 2(5):527–532
Kidd PS, Domínguez-Rodríguez MJ, Díez J, Monterroso C (2007) Bioavailability and plant accumulation of heavy metals and phosphorus in agricultural soils amended by long-term application of sewage sludge. Chemosphere 66:1458–1467
Lakshaman KC, Surinder KS (1999) Photosynthetic activities of Pisum sativum seedlings grown in presence of cadmium. Plant Physiol Biochem 37:297–303
Lalk I, Dorfling K (1985) Hardening, ABA, proline and freezing resistance in the winter wheat varieties. Physiol Plant 63:287–29
Lavola A, Julkunen-Titto R, Delarosa TM, Lehto T, Aphalo PJ (2000) Allocation of carbon to growth and secondary metabolites in birch seedlings under UV-B radiation and CO2 exposure. Physiol Plant 109:260–267
Li YM, Chaney R, Brewer E, Roseberg R, Angle JS, Baker AJM, Reeves R, Nelkin J (2003) Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant Soil 249:107–115
Liu J, Zhu Q, Zhang Z, Xu J, Yang J, Wong MH (2005) Variations in cadmium accumulation among rice cultivars and types and the selection of cultivars for reducing cadmium in the diet. J Sci Food Agric 85:147–153
Liu Z, He X, Chen W, Yuan F, Yan K, Tao D (2009) Accumulation and tolerance characteristics of cadmium in a potential hyperaccumulator—Lonicera japonica Thunb. Water Air Soil Pollut 196:29–40
Lone MI, He Z, Stoffella PJ, Yang X (2008) Phytoremediation of heavy metal polluted soils and water: progresses and perspectives. J Zhejiang Univ Sci B 9:210–220
Lou LQ, Ye ZH, Wong MH (2007) Solubility and accumulation of metals in Chinese brake fern, vetiver and rostrate sesbania using chelating agents. Int J Phytoremediat 9:325–343
Mamindy-Pajany Y, Sayen S, Guillon E (2014) Impact of lime-stabilized biosolid application on Cu, Ni, Pb and Zn mobility in an acidic soil. Environ Sci Pollut Res 21:4473–4481
Masroor M, Khan A, Gautam C, Mohammad F, Siddiqui MH, Naeem M, Khan MN (2006) Effect of gibberellic acid spray on performance of tomato. Turk J Biol 30:11–16
Mazharia M, Homaeeb M (2012) Annual halophyte Chenopodium botrys can phytoextract cadmium from contaminated soils. J Basic Appl Sci Res 2(2):1415–1422
Meers E, Lesage E, Lamsal S, Hopgood M, Vervaekle P, Tack FMG, Verloo MG (2005) Enhanced phytoextraction: I. Effect of EDTA and citric acid on heavy metal uptake by Heliantus annuus from a calcareous soil. Int J Phytoremed 7:129–142
Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15(4):523–530
Mobin M, Nafees AK (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164:601–610
Moore TC (1989) Biochemistry and physiology of plant hormones. Springer-Verlag Inc, New York
Mubeen H, Naeem I, Taskeen A (2010) Phytoremediation of Cu(II) by Calotropis procera roots. N Y Sci J 3(3):1–5
Ngayila N, Botineau M, Baudu M, Basly JP (2008) Myriophyllum alterniflorum DC. Effect of low concentrations of copper and cadmium on somatic and photosynthetic endpoints: a chemometric approach. Ecol Indic 9:379–384
Ogawa T, Kobayashi E, Okubo Y, Suwazono Y, Kido T, Nogawa K (2004) Relationship among prevalence of patients with itai-itai disease, prevalence of abnormal urinary findings, and cadmium concentrations in rice of individual hamlets in the Jinzu river basin, Toyama prefecture of Japan. Int J Environ Health Res 14:243–252
Okedeyi OO, Dube S, Awofolu OR, Nindi MN (2014) Assessing the enrichment of heavy metals in surface soil and plant (Digitaria eriantha) around coal-fired power plants in South Africa. Environ Sci Pollut Res 21:4686–4696. doi:10.1007/s11356-013-2432-0
Parsons WT, Cuthbertson EG (1992) Noxious weeds of Australia. Inkata Press, Melbourne
Persans M, Salt DE (2000) Possible molecular mechanisms involved in nickel, zinc and selenium hyperaccumulation in plants. Biotechnol Genet Eng Rev 17:385–409
Poschenrieder C, Gunse G, Barcelo J (1989) Influence of cadmium on water relations, stomatal resistance, and abscisic acid content in expanding bean leaves. Plant Physiol 90:1365–1371
Ramadevi S, Prasad MNV (1998) Copper toxicity in Ceratophyllum demersum l. (coontail), a free floating macrophyte: response of antioxidant enzymes and antioxidants. Plant Sci. 138–157
Reeves RD, Brooks RR (1983) Hyperaccumulation of lead and zinc by two metallophytes from a mining area of Central Europe. Environ Pollut A 31:277–287
Rice-Evans CA, Miller NJ, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2:152–159
Sakihama Y, Yamasaki H (2002) Lipid peroxidation induces by phenolics in conjunction with aluminium ions. Biol Plantarum 45:249–254
Schwitzguébel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol 127:887–898
Schwitzguebel JP, Kumpiene J, Comino E, Vanek T (2009) From green to clean: a promising and sustainable approach towards environmental remediation and human health for the 21 st century. Agrochimica 53:209–237
Sharma SS, Schat H, Vooijs R (1998) In vitro alleviation of heavy metal-induced enzyme inhibition by proline. Phytochemistry 46:1531–1535
Simmons RW, Pongsakul P, Saiyasitpanich D, Klinphoklap S (2005) Elevated levels of cadmium and zinc in paddy soils and elevated levels of cadmium in rice grain downstream of a zinc mineralized area in Thailand: implications for public health. Environ Geochem Health 27:501–511
Singh OV, Labana S, Pandey G, Budhiraja R, Jain RK (2003) Phytoremediation: an overview of metallic ion decontamination from soil. Appl Microbiol Biotechnol 61:405–412
Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic—phosphotungstic acid reagents. Am J Enol Vitic 16:144–158
Sun Q, Ye ZH, Wang XR, Wong MH (2007) Cadmium hyperaccumulation leads to an increase of glutathione rather than phytochelatins in the cadmium hyperaccumulator Sedum alfredii. J Plant Physiol 164:1489–1498
Sun YB, Zhou QX, Diao CY (2008) Effects of cadmium and arsenic on growth and metal accumulation of Cd-hyperaccumulator Solanum nigrum L. Bioresour Technol 99:1103–1110
Tassi E, Pouget J, Petruzzelli G, Barbafieri M (2008) The effects of exogenous plant growth regulators in the phytoextraction of heavy metals. Chemosphere 71:66–73
Thapar R, Srivastava AK, Bhargava P, Mishra Y, Rai LC (2008) Impact of different abiotic stress on growth, photosynthetic electron transport chain, nutrient uptake and enzyme activities of Cu-acclimated Anabaena doliolum. J Plant Physiol 165:306–316
Thayalakumaran T, Robinson BH, Vogeler I, Scotter DR, Clothier BE, Percival HJ (2003) Plant uptake and leaching of copper during EDTA-enhanced phytoremediation of repacked and undisturbed soil. Plant Soil 254:415–423
Uraguchi S, Watanabe I, Yoshitomi A, Kiyono M, Kuno K (2006) Characteristics of cadmium accumulation and tolerance in novel Cd-accumulating crops, Avena strigosa and Crotalaria juncea. J Exp Bot 57:2955–2965
Vajpayee P, Tripathi RD, Rai UN, AliSingh SN (2000) Chromium (VI) accumulation reduces chlorophyll biosynthesis, nitrate reductase activity and protein content in Nymphaea alba L. Chemosphere 41:1075–1082
Wild A, Schmitt V (1995) Diagnosis of damage to Norway spruce (Picea abies) through biochemical criteria. Physiol Plant 93:357–382
Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–223
Wood A, Paleg LG (1974) Alteration of liposomal membrane fluidity by gibberellic acid. Aust J Plant Physiol 1:31–40
Xu J, Yin X, Li X (2009) Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep 28:325–333
Xue Z, Gao H, Zhao S (2014) Effects of cadmium on the photosynthetic activity in mature and young leaves of soybean plants. Environ Sci Pollut Res 21:4656–4664
Yang SL, Lan SS, Gong M (2009) Hydrogen peroxide-induced proline and metabolic pathway of its accumulation in maize seedlings. J Plant Physiol 166:1694–1699
Zengin FK, Munzuroglu O (2006) Toxic effects of cadmium (Cd++) on metabolism of sunflower (Helianthus annuus L.) seedlings. Acta Agric Scand Sect B Plant Soil Sci 56:224–229
Zheng HP, Gao LS, Wang SR (2010) Effects of cadmium on growth and antioxidant responses in Glycyrrhiza uralensis seedlings. Plant Soil Environ 56(11):508–515
Zhou WB, Qiu BS (2005) Effects of cadmium hyperaccumulation on physiological characteristics of Sedum alfredii Hance (Crassulaceae). Plant Sci 169:737–745
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The Directorate of Science and Technology, Khyber Pakhtunkhwa, Pakistan, is highly acknowledged for the full financial support. This manuscript is a part of the Ph.D. thesis of the principal author.
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Ali, N., Hadi, F. Phytoremediation of cadmium improved with the high production of endogenous phenolics and free proline contents in Parthenium hysterophorus plant treated exogenously with plant growth regulator and chelating agent. Environ Sci Pollut Res 22, 13305–13318 (2015). https://doi.org/10.1007/s11356-015-4595-3
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DOI: https://doi.org/10.1007/s11356-015-4595-3