Phyto-management of Cr-contaminated soils by sunflower hybrids: physiological and biochemical response and metal extractability under Cr stress

Abstract

Chromium (Cr) is a biologically non-essential, carcinogenic and toxic heavy metal. The cultivation of Cr-tolerant genotypes seems the most favorable and environment friendly strategy for rehabilitation and remediation of Cr-contaminated soils. To prove this hypothesis and identify the Cr tolerance, the present study was performed to assess the physiological and biochemical response of sunflower genotypes to Cr stress. The seeds of six sunflower hybrids, namely FH-425, FH-600, FH-612, FH-614, FH-619, and FH-620, were grown in spiked soil for 12 weeks under increasing concentrations of Cr (0, 5, 10, and 20 mg kg−1). A seed germination test was also run under different concentrations of Cr (0, 5, 10, 200 mM) in petri dishes. Plants were harvested after 12 weeks of germination. Different plant attributes such as growth; biomass; photosynthesis; gas exchange; activity of antioxidant enzymes, i.e., superoxide dismutase (SOD), guaiacol peroxidase (POD), ascorbate (APX), and catalases (CAT); reactive oxygen species (ROS); lipid peroxidation; electrolyte leakage; and Cr concentration as well as accumulations in all plant parts were studied for the selection of the most Cr-tolerant genotype. Increasing concentration of Cr in soil triggered the reduction of all plant parameters in sunflower. Cr stress increased electrolyte leakage and production of reactive oxygen species which stimulated the activities of antioxidant enzymes and gas exchange attributes of sunflower. Chromium accumulation in the root and shoot increased gradually with increasing Cr treatments and caused reduction in overall plant growth. The accumulation of Cr was recorded in the order of FH-614 > FH-620 > FH-600 > FH-619 > FH-612 > FH-425. The differential uptake and accumulation of Cr by sunflower hybrids may be useful in selection and breeding for Cr-tolerant genotypes.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Adesodun JK, Atayese MO, Agbaje TA, Osadiaye BA, Mafe OF, Soretire AA (2010) Phytoremediation potentials of sunflowers (Tithonia diversifolia and Helianthus annuus) for metals in soils contaminated with zinc and lead nitrates. Water Air Soil Pollut 207:195–201

    CAS  Article  Google Scholar 

  2. Adrees M, Ali S, Rizwan M, Ibrahim M, Abbas F, Farid M, Zia-ur-Rehman M, Irshad MK, Bharwana SA (2015a) The effect of excess copper on growth and physiology of important food crops: a review. Environ Sci Pollut Res 22:8148–8162. doi:10.1007/s11356-015-4496-5

    CAS  Article  Google Scholar 

  3. Adrees M, Ali S, Rizwan M, Zia-ur-Rehman M, Ibrahim M, Abbas F, Farid M, Qayyum MF, Irshad MK (2015b) Mechanisms of silicon-mediated alleviation of heavy metal toxicity in plants: a review. Ecotoxicol Environ Safe 119:186–197. doi:10.1016/j.ecoenv.2015.05.011

    CAS  Article  Google Scholar 

  4. Adrees M, Saleem F, Jabeen F, Rizwan M, Ali S, Khalid S, Ibrahim M, Iqbal N, Abbas F (2016) Effects of ambient gaseous pollutants on photosynthesis, growth, yield and grain quality of selected crops grown at different sites varying in pollution levels. Arch Agron Soil Sci 62:1195–1207

    CAS  Article  Google Scholar 

  5. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    CAS  Article  Google Scholar 

  6. Afshan S, Ali S, Bharwana SA, Rizwan M, Farid M, Abbas F, Ibrahim M, Mehmood MA, Abbasi GH (2015) Citric acid enhances the phytoextraction of chromium, plant growth, and photosynthesis by alleviating the oxidative damages in Brassica napus L. Environ Sci Pollut Res 22:11679–11689

    CAS  Article  Google Scholar 

  7. Akhtar T, Zia-ur-Rehman M, Naeem A, Nawaz R, Ali S, Murtaza G, Maqsood MA, Azhar M, Khalid H, Rizwan M (2017) Photosynthesis and growth response of maize (Zea mays L.) hybrids exposed to cadmium stress. Environ Sci Pollut Res 24:5521–5529

  8. Ali S, Farooq MA, Yasmeen T, Hussain S, Arif MS, Abbas F, Bharwana SA, Zhang G (2013) The influence of silicon on barley growth, photosynthesis and ultra-structure under chromium stress. Ecotoxicol Environ Saf 89:66–72

    CAS  Article  Google Scholar 

  9. Ali S, Bharwana SA, Rizwan M, Farid M, Kanwal S, Ali Q, Ibrahim M, Gill RA, Khan MD (2015) Fulvic acid mediates chromium (Cr) tolerance in wheat (Triticum aestivum L.) through lowering of Cr uptake and improved antioxidant defense system. Environ Sci Pollut Res 22:10601–10609

    CAS  Article  Google Scholar 

  10. Anjum SA, Tanveer M, Hussain S, Bao M, Wang L, Khan I, Ullah E, Tung SA, Samad RA, Shahzad B (2015) Cadmium toxicity in maize (Zea mays L.): consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environ Sci Pollut Res 22:17022–17030. doi:10.1007/s11356-015-4882-z

    CAS  Article  Google Scholar 

  11. Anjum SA, Ashraf U, Khan I, Tanveer M, Saleem MF, Wang L (2016a) Aluminum and chromium toxicity in maize: implications for agronomic attributes, net photosynthesis, physio-biochemical oscillations, and metal accumulation in different plant parts. Water Air Soil Pollut 227:326. doi:10.1007/s11270-016-3013-x

    Article  Google Scholar 

  12. Anwaar SA, Ali S, Ali S, Ishaque W, Farid M, Farooq MA, Najeeb U, Abbas F, Sharif M (2015) Silicon (Si) alleviates cotton (Gossypium hirsutum L.) from zinc (Zn) toxicity stress by limiting Zn uptake and oxidative damage. Environ Sci Pollut Res 22:3441–3450

    CAS  Article  Google Scholar 

  13. Arshad M, Ali S, Noman A, Ali Q, Rizwan M, Farid M, Irshad MK (2016) Phosphorus amendment decreased cadmium (Cd) uptake and ameliorates chlorophyll contents, gas exchange attributes, antioxidants, and mineral nutrients in wheat (Triticum aestivum L.) under Cd stress. Arch Agron Soil Sci 62:533–546

    CAS  Article  Google Scholar 

  14. Artiushenko T, Syshchykov D, Gryshko V, Čiamporová M, Fiala R, Repka V, Martinka M, Pavlovkin J (2014) Metal uptake, antioxidant status and membrane potential in maize roots exposed to cadmium and nickel. Biologia 69:1142–1147

    CAS  Article  Google Scholar 

  15. Atta MI, Bokhari TZ, Malik SA, Wahid A, Saeed S, Gulshan AB (2013) Assessing some emerging effects of hexavalent chromium on leaf physiological performance in sunflower (Helianthus annuus L.) Int J Sci Eng Res 4:945–949

    Google Scholar 

  16. Azad HN, Shiva AH, Malekpour R (2011) Toxic effects of lead on growth and some biochemical and ionic parameters of sunflower (Helianthus annuus L.) seedlings. Curr Res J Biol Sci 3:398–403

    CAS  Google Scholar 

  17. Baker AJ, Whiting SN (2002) In search of the Holy Grail—a further step in understanding metal hyperaccumulation. New Phytol 155:1–4

    Article  Google Scholar 

  18. Barceló JU, Poschenrieder C (1990) Plant water relations as affected by heavy metals stress: a review. J Plant Nutr 13:1–37

    Article  Google Scholar 

  19. Belhaj D, Jerbi B, Medhioub M, Zhou J, Kallel M, Ayadi H (2016) Impact of treated urban wastewater for reuse in agriculture on crop response and soil ecotoxicity. Environ Sci Pollut Res 23:15877-15887

  20. 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

    CAS  Article  Google Scholar 

  21. Bukhari SA, Shang S, Zhang M, Zheng W, Zhang G, Wang TZ, Shamsi IH, Wu F (2015) Genome-wide identification of chromium stress-responsive microRNAs and their target genes in tobacco (Nicotiana tabacum) roots. Environ Toxicol Chem 34:2573–2582

    CAS  Article  Google Scholar 

  22. Bukhari SA, Wang R, Wang W, Ahmed IM, Zheng W, Cao F (2016a) Genotype-dependent effect of exogenous 24-epibrassinolide on chromium-induced changes in ultrastructure and physicochemical traits in tobacco seedlings. Environ Sci Pollut Res 23:18229–18238

    CAS  Article  Google Scholar 

  23. Bukhari SA, Zheng W, Xie L, Zhang G, Shang S, Wu F (2016b) Cr-induced changes in leaf protein profile, ultrastructure and photosynthetic traits in the two contrasting tobacco genotypes. Plant Growth Regul 79:147–156

    CAS  Article  Google Scholar 

  24. Chae MJ, Jung GB, Kang SS, Kong MS, Kim YH, Lee DB (2014) Evaluation of the feasibility of phytoremediation of soils contaminated with Cd, Pb and Zn using sunflower, corn and castor plants. Korean J Soil Sci Fert 47:491–495

    CAS  Article  Google Scholar 

  25. Chen TH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20

    Article  Google Scholar 

  26. Cornuet JY, Bakoto R, Bonnard O, Bussière S, Coriou C, Sirguey C, Sterckeman T, Thunot S, Visse MI, Nguyen C (2016) Cadmium uptake and partitioning during the vegetative growth of sunflower exposed to low Cd2C concentrations in hydroponics. Plant Soil. doi:10.1007/s11104-016-2839-8

  27. Cutright T, Gunda N, Kurt F (2010) Simultaneous hyperaccumulation of multiple heavy metals by Helianthus annuus grown in a contaminated sandy-loam soil. Int J Phytoremediation 12:562–573

    CAS  Article  Google Scholar 

  28. De Maria S, Puschenreiter M, Rivelli AR (2013) Cadmium accumulation and physiological response of sunflower plants to Cd during the vegetative growing cycle. J Plant Soil Environ 59:254–261

    CAS  Google Scholar 

  29. Del Gatto A, Mengarelli C, Pedretti EF, Duca D, Pieri S, Mangoni L, Signor M, Raccuia SA, Melilli MG (2015) Adaptability of sunflower (Helianthus annuus L.) high oleic hybrids to different Italian areas for biodiesel production. Ind Crop Prod 75:108–117

    CAS  Article  Google Scholar 

  30. Demidchik V (2012) Reactive oxygen species and oxidative stress in plants. In: Shabala S (ed) Plant stress physiol. CAB International, Wallingford, pp 24–58

    Google Scholar 

  31. Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V (2014) Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. J Exp Bot 65:1259–1270

    CAS  Article  Google Scholar 

  32. Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased level of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    CAS  Article  Google Scholar 

  33. Di Cagno R, Guidi L, De Gara L, Soldatini GF (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    Article  Google Scholar 

  34. Di Cagno R, Guidi L, De Gara L, Soldatini GF (2001) Combined cadmium and ozone treatments affect photosynthesis and ascorbate-dependent defences in sunflower. New Phytol 151:627–636. doi:10.1046/j.1469-8137.2001.00217.x

    CAS  Article  Google Scholar 

  35. Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    CAS  Article  Google Scholar 

  36. Doncheva S, Moustakas M, Ananieva K, Chavdarova M, Gesheva E, Vassilevska R, Mateev P (2013) Plant response to lead in the presence or absence EDTA in two sunflower genotypes (cultivated H. annuus cv. 1114 and interspecific line H. annuus H. argophyllus). Environ Sci Pollut Res 20:823-833

  37. Dong CH, Zolman BK, Bartel B, Lee BH, Stevenson B, Agarwal M, Zhu JK (2009) Disruption of Arabidopsis CHY1 reveals an important role of metabolic status in plant cold stress signaling. MolePlant 2:59–72

    CAS  Google Scholar 

  38. Edreva A, Yordanov I, Kardjieva R, Gesheva E (1998) Heat shock responses of bean plants: involvement of free radicals, antioxidants and free radical/active oxygen scavenging systems. Biol Plantarum 41:185–191

    CAS  Article  Google Scholar 

  39. Ehsan S, Ali S, Noureen S, Farid M, Shakoor MB, Aslam A, Bharwana SA, Tauqeer HM (2013) Comparative assessment of different heavy metals in urban soil and vegetables irrigated with sewage/industrial waste water. Ecoterra 35:37–53

    Google Scholar 

  40. Ehsan S, Ali S, Noureen S, Mahmood K, Farid M, Ishaque W, Shakoor MB, Rizwan M (2014) Citric acid assisted phytoremediation of cadmium by Brassica napus L. Ecotoxicol Environ Saf 106:164–172. doi:10.1016/j.ecoenv.2014.03.007

    CAS  Article  Google Scholar 

  41. Farid M, Ali S, Ishaque W, Shakoor MB, Niazi NK, Bibi I, Dawood M, Gill RA, Abbas F (2015) Exogenous application of ethylenediamminetetraacetic acid enhanced phytoremediation of cadmium by Brassica napus L. IJEST 12:3981–3992

    CAS  Google Scholar 

  42. Farooq MA, Ali S, Hameed A, Ishaque W, Mahmood K, Iqbal Z (2013) Alleviation of cadmium toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes; suppressed cadmium uptake and oxidative stress in cotton. Ecotoxicol Environ Saf 96:242–249

    CAS  Article  Google Scholar 

  43. Farooq MA, Ali S, Hameed A, Bharwana SA, Rizwan M, Ishaque W, Farid M, Mahmood K, Iqbal Z (2016) Cadmium stress in cotton seedlings: physiological, photosynthesis and oxidative damages alleviated by glycinebetaine. S Afr J Bot 104:61–68

    CAS  Article  Google Scholar 

  44. Fozia A, Muhammad AZ, Muhammad A, Zafar MK (2008) Effect of chromium on growth attributes in sunflower (Helianthus annuus L.) J Environ Sci 20:1475–1480

    CAS  Article  Google Scholar 

  45. Gallego SM, Kogan MJ, Azpilicueta CE, Peña C, Tomaro ML (2005) Glutathionemediated antioxidative mechanisms in sunflower (Helianthus annuus L.) cells in response to cadmium stress. Plant Growth Regul 46:267–276. doi:10.1007/s10725-005-0163-z

    CAS  Article  Google Scholar 

  46. Ghani A (2011) Varietal differences in canola (Brassic anapus L.) for the growth, yield and yield components exposed to cadmium stress. J Anim Plant Sci 21:57–59

    CAS  Google Scholar 

  47. Gill RA, Zang L, Ali B, Farooq MA, Cui P, Yang S, Ali S, Zhou W (2015) Chromium-induced physio-chemical and ultrastructural changes in four cultivars of Brassica napus L. Chemosphere 120:154–164

    CAS  Article  Google Scholar 

  48. Gill RA, Ali B, Cui P, Shen E, Farooq MA, Islam F, Ali S, Mao B, Zhou W (2016a) Comparative transcriptome profiling of two Brassica napus cultivars under chromium toxicity and its alleviation by reduced glutathione. BMC Genomics 17:885

    Article  Google Scholar 

  49. Gill RA, Zhang N, Ali B, Farooq MA, Xu J, Gill MB, Mao B, Zhou W (2016b) Role of exogenous salicylic acid in regulating physio-morphic and molecular changes under chromium toxicity in black-and yellow-seeded Brassica napus L. Environ Sci Pollut Res 23:20483–20496

    CAS  Article  Google Scholar 

  50. Giovanini MP, Puthoff DP, Nemacheck JA, Mittapalli O, Saltzmann KD, Ohm HW, Shukle RH, Williams CE (2006) Gene-for-gene defense of wheat against the Hessian fly lacks a classical oxidative burst. Mol Plant Microbe In 19:1023–1033

    CAS  Article  Google Scholar 

  51. Gopal R, Khurana N (2011) Effect of heavy metal pollutants on sunflower. African J Plant Sci 5:531–536

    CAS  Google Scholar 

  52. Gupta DK, Nicoloso FT, Schetinger MR, Rossato LV, Pereira LB, Castro GY, Srivastava S, Tripathi RD (2009) Antioxidant defense mechanism in hydroponically grown Zea mays seedlings under moderate lead stress. J Hazard Mater 172:479–484

    CAS  Article  Google Scholar 

  53. Habiba U, Ali S, Farid M, Shakoor MB, Rizwan M, Ibrahim M, Abbasi GH, Hayat T, Ali B (2015) EDTA enhanced plant growth, antioxidant defense system, and phytoextraction of copper by Brassica napus L. Environ. Sci Pollut Res 22:1534–1544. doi:10.1007/s11356-014-3431-5

    CAS  Article  Google Scholar 

  54. Halliwell B, Gutteridge JM (1999) Free radicals in biology and medicine. Oxford University Press, Oxford

    Google Scholar 

  55. Harris TM, Hottle TA, Soratana K, Klane J, Landis AE (2016) Life cycle assessment of sunflower cultivation on abandoned mine land for biodiesel production. J Clean Prod 112:182–195

    Article  Google Scholar 

  56. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    CAS  Article  Google Scholar 

  57. Imran MA, Khan RM, Ali Z, Mahmood T (2013) Toxicity of arsenic (As) on seed germination of sunflower (Helianthus annuus L.) Int J Phys Sci 8:840–847

    CAS  Article  Google Scholar 

  58. Jabeen N, Abbas Z, Iqbal M, Rizwan M, Jabbar A, Farid M, Ali S, Ibrahim M, Abbas F (2016) Glycinebetaine mediates chromium tolerance in mung bean through lowering of Cr uptake and improved antioxidant system. Arch Agron Soil Sci 62:648–662. doi:10.1080/03650340.2015.1082032

    CAS  Article  Google Scholar 

  59. Jana S, Choudhuri MA (1981) Glycolate metabolism of three submerged aquatic angiosperms during aging. Aquat Bot 12:345–354

    Article  Google Scholar 

  60. Jiang W, Liu D, Li H (2000) Effects of Cu2C on root growth, cell division, and nucleolus of Helianthus annuus L. Sci Total Environ 256:59–65. doi:10.1016/S0048-9697(00)00470-8

    CAS  Article  Google Scholar 

  61. Júnior CA, Mazzafera P, Arruda MA (2014) A comparative ionomic approach focusing on cadmium effects in sunflowers (Helianthus annuus L.) Environ Exp Bot 107:180–186. doi:10.1016/j.envexpbot.2014.06.002

    Article  Google Scholar 

  62. Júnior CA, de Sousa BH, Galazzi RM, Koolen HH, Gozzo FC, Arruda MA (2015) Evaluation of proteome alterations induced by cadmium stress in sunflower (Helianthus annuus L.) cultures. Ecotoxicol Environ Saf 119:170–177

    Article  Google Scholar 

  63. Junior CAL, Oliveira SR, Mazzafera P, Arruda MAZ (2016) Expanding the information about the influence of cadmium on the metabolism of sunflowers: evaluation of total, bioavailable, and bioaccessible content and metallobiomolecules in sunflower seeds. Environ Exp Bot 125:87–97. doi:10.1016/j.envexpbot.2016.02.003

    CAS  Article  Google Scholar 

  64. Kanwal U, Ali S, Shakoor MB, Farid M, Hussain S, Yasmeen T, Adrees M, Bharwana SA, Abbas F (2014) EDTA ameliorates phytoextraction of lead and plant growth by reducing morphological and biochemical injuries in Brassica napus L. under lead stress. Environ Sci Pollut Res 21:9899–9910

    CAS  Article  Google Scholar 

  65. Kastori R, Plesničar M, Sakač Z, Panković D, Arsenijević-Maksimović I (1998) Effect of excess lead on sunflower growth and photosynthesis. J Plant Nutr 21:75–85. doi:10.1080/01904169809365384

    CAS  Article  Google Scholar 

  66. Khaliq A, Ali S, Hameed A, Farooq MA, Farid M, Shakoor MB, Mahmood K, Ishaque W, Rizwan M (2016) Silicon alleviates nickel toxicity in cotton seedlings through enhancing growth, photosynthesis, and suppressing Ni uptake and oxidative stress. Arch Agron Soil Sci 62:633–647

    CAS  Article  Google Scholar 

  67. Kolbas A, Marchand L, Herzig R, Nehnevajova E, Mench M (2014) Phenotypic seedling responses of a metal-tolerant mutant line of sunflower growing on a Cu-contaminated soil series: potential uses for biomonitoring of Cu exposure and phytoremediation. Plant Soil 376:377–397. doi:10.1007/s11104-013-1974-8

    CAS  Article  Google Scholar 

  68. Kolbas A, Kidd P, Guinberteau J, Jaunatre R, Herzig R, Mench M (2015) Endophytic bacteria take the challenge to improve Cu phytoextraction by sunflower. Environ Sci Pollut Res 22:5370–5382. doi:10.1007/s11356-014-4006-1

    CAS  Article  Google Scholar 

  69. Kötschau A, Büchel G, Einax JW, Fischer C, Von Tümpling W, Merten D (2013) Mapping of macro and micro elements in the leaves of sunflower (Helianthus annuus) by laser ablation-ICP-MS. Microchem J 110:783–789. doi:10.1016/j.microc.2012.12.011

    Article  Google Scholar 

  70. Lee KK, Cho HS, Moon YC, Ban SJ, Kim JY (2013) Cadmium and lead uptake capacity of energy crops and distribution of metals within the plant structures. KSCE J Civ Eng 17:44–50. doi:10.1007/s12205-013-1633-x

    Article  Google Scholar 

  71. Lichtenthaler HK (1987) Chlorophylls and carotenoids pigments of photosynthetic biomembranes In: Colowick SP, Kaplan NO (ed) Methods Enzymol vol 148, pp 350–382

  72. Meers E, Ruttens A, Geebelen W, Vangronsveld J, Samson R, Vanbroekhoven K, Vandegehuchte M, Diels L, Tack FM (2005a) Potential use of the plant antioxidant network for environmental exposure assessment of heavy metals in soils. Environ Monit Assess 120:243–267. doi:10.1007/s10661-005-9059-7

    Article  Google Scholar 

  73. Metzner H, Rau H, Senger H (1965) Untersuchungen zur Synchronisierbakeit einzelner Pigmentmangel-Mutation von Chlorella. Planta 65:186–194 (in German)

    CAS  Article  Google Scholar 

  74. Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216

    CAS  Article  Google Scholar 

  75. Najeeb U, Jilani G, Ali S, Sarwar M, Xu L, Zhou WJ (2011) Insight into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. J Hazard Mater 186:565–574

    CAS  Article  Google Scholar 

  76. 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 

  77. Nehnevajova E, Herzig R, Federer G, Erismann KH, Schwitzguébel JP (2007) Chemical mutagenesis—a promising technique to increase metal concentration and extraction in sunflowers. Int J Phytoremediation 9:149–165

    CAS  Article  Google Scholar 

  78. Noman A, Ali S, Naheed F, Ali Q, Farid M, Rizwan M, Irshad MK (2015) Foliar application of ascorbate enhances the physiological and biochemical attributes of maize (Zea mays L.) cultivars under drought stress. Arch Agron Soil Sci 61:1659–1672

    CAS  Article  Google Scholar 

  79. Park J, Kim JY, Kim KW (2012) Phytoremediation of soil contaminated with heavy metals using Brassica napus. Geosyst Eng 15:10–18

    Article  Google Scholar 

  80. Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 32:539–548

    CAS  Article  Google Scholar 

  81. Qadir S, Qureshi MI, Javed S, Abdin MZ (2004) Genotypic variation in phytoremediation potential of Brassica juncea cultivars exposed to Cd stress. Plant Sci 167:1171–1181

    CAS  Article  Google Scholar 

  82. Ramzani PMA, Khan WD, Iqbal M, Kausar S, Ali S, Rizwan M, Virk ZA (2016) Effect of different amendments on rice (Oryza sativa L.) growth, yield, nutrient uptake and grain quality in Ni-contaminated soil. Environ Sci Pollut Res doi:10.1007/s11356-016-7038-x

  83. Rehman MZ, Rizwan M, Ghafoor A, Naeem A, Ali S, Sabir M, Qayyum MF (2015) Effect of inorganic amendments for in situ stabilization of cadmium in contaminated soils and its phyto-availability to wheat and rice under rotation. Environ Sci Pollut Res 22:16897–16906. doi:10.1007/s11356-015-4883-y

    CAS  Article  Google Scholar 

  84. Rivelli AR, Puschenreiter M, De Maria S (2014) Assessment of cadmium uptake and nutrient content in sunflower plants grown under Cd stress. Plant Soil Environ 60:80–86

    CAS  Google Scholar 

  85. Rizwan M, Ali S, Ibrahim M, Farid M, Adrees M, Bharwana SA, Zia-ur-Rehman M, Qayyum MF, Abbas F (2015) Mechanisms of silicon-mediated alleviation of drought and salt stress in plants: a review. Environ Sci Pollut Res 22:15416–15431. doi:10.1007/s11356-015-5305-x

    CAS  Article  Google Scholar 

  86. Rizwan M, Ali S, Qayyum MF, Ok YS, Zia-ur-Rehman M, Abbas Z, Hannan F (2016a) Use of maize (Zea mays L.) for phytomanagement of Cd-contaminated soils: a critical review. Environ Geochem Health doi:10.1007/s10653-016-9826-0

  87. Rizwan M, Ali S, Rizvi H, Rinklebe J, Tsang DC, Meers E, Ok YS, Ishaque W (2016b) Phytomanagement of heavy metals in contaminated soils using sunflower: a review. Crit Rev Environ Sci Technol 46:1498–1528

    CAS  Article  Google Scholar 

  88. Rizwan M, Ali S, Abbas F, Adrees M, Zia-ur-Rehman M, Farid M, Gill RA, Ali B (2017) Role of organic and inorganic amendments in alleviating heavy metal stress in oil seed crops. In: Ahmad P (ed) Oil Seed Crops: Yield and Adaptations under Environmental Stress, 1st edn, vol. 12. John Wiley & Sons, Ltd., 224–235

  89. Saleem M, Asghar HN, Khan MY, Zahir ZA (2015) Gibberellic acid in combination with pressmud enhances the growth of sunflower and stabilizes chromium(VI)-contaminated soil. Environ Sci Pollut Res 22:10610–10617. doi:10.1007/s11356-015-4275-3

    CAS  Article  Google Scholar 

  90. Schützendübel 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

    Article  Google Scholar 

  91. Shaheen SM, Rinklebe J (2015) Phytoextraction of potentially toxic elements by Indian mustard, rapeseed, and sunflower from a contaminated riparian soil. Environ Geochem Health 37:953–967. doi:10.1007/s10653-015-9718-8

    CAS  Article  Google Scholar 

  92. Shakoor MB, Ali S, Hameed A, Farid M, Hussain S, Yasmeen T, Najeeb U, Bharwana SA, Abbasi GH (2014) Citric acid improves lead (Pb) phytoextraction in Brassica napus L. by mitigating Pb-induced morphological and biochemical damages. Ecotoxicol Environ Saf 109:38–47

    Article  Google Scholar 

  93. Shamsi IH, Zhang GP, Hu HL, Xue QY, Hussain N, Ali E, Shen QF, Zheng W, Zhang QC, Liu XX, Jabeen Z (2014) Assessment of the hazardous effects of Cd on physiological and biochemical characteristics of soybean genotypes. Int J Agric Biol 16:41–48

    CAS  Google Scholar 

  94. Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11:229–254

    CAS  Article  Google Scholar 

  95. Song NH, Yin XL, Chen GF, Yang H (2007) Biological responses of wheat (Triticum aestivum) plants to the herbicide chlorotoluron in soils. Chemosphere 68:1779–1787

    CAS  Article  Google Scholar 

  96. SPSS I (2009) PASW statistics release 18. IBM Corp, Armonk

  97. Tauqeer HM, Ali S, Rizwan M, Ali Q, Saeed R, Iftikhar U, Ahmad R, Farid M, Abbasi GH (2016) Phytoremediation of heavy metals by Alternanthera bettzickiana: growth and physiological response. Ecotoxicol Environ Saf 126:138–146

    CAS  Article  Google Scholar 

  98. Wahid A, Ghani A, Javed F (2008) Effect of cadmium on photosynthesis, nutrition and growth of mung bean. Agron Sustain Dev 28:273–280

    CAS  Article  Google Scholar 

  99. Wang C, Wang X, Tian Y, Xue Y, Xu X, Sui Y, Yu H (2008) Oxidative stress and potential biomarkers in tomato seedlings subjected to soil lead contamination. Ecotoxicol Environ Saf 71:685–691

    Article  Google Scholar 

  100. Zaheer IE, Ali S, Muhammad R, Farid M, Shakoor MB, Gill RA, Najeeb U, Iqbal N, Ahmad R (2015) Citric acid assisted phytoremediation of copper by Brassica napus L. Ecotoxicol Environ Saf 120:310–317. doi:10.1016/j.ecoenv.2014.03.007

    CAS  Article  Google Scholar 

  101. Zhang XZ (1992) The measurement and mechanism of lipid peroxidation and SOD, POD and CAT activities in biological system. In: Zhang XZ (ed) Research methodology of crop physiology. Agriculture Press, Beijing, pp 208–211

    Google Scholar 

  102. Zhang JX, Kirham MB (1994) Drought stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol 35:785–791

    CAS  Article  Google Scholar 

Download references

Acknowledgments

This study is the part of PhD dissertation of Mr. Mujahid Farid. The authors are highly thankful to the Government College University, Faisalabad, Pakistan, and the Higher Education Commission of Pakistan for the financial and technical support during this study.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Shafaqat Ali.

Additional information

Responsible editor: Philippe Garrigues

Electronic supplementary material

Supplementary Fig. 1

(DOCX 42 kb)

Supplementary Fig. 2

(DOCX 50 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Farid, M., Ali, S., Akram, N.A. et al. Phyto-management of Cr-contaminated soils by sunflower hybrids: physiological and biochemical response and metal extractability under Cr stress. Environ Sci Pollut Res 24, 16845–16859 (2017). https://doi.org/10.1007/s11356-017-9247-3

Download citation

Keywords

  • Chromium
  • Gas exchange parameters
  • Growth
  • Antioxidant enzymes
  • Sunflower hybrids
  • Reactive oxygen species