Abstract
Background and aims
The potential use of a metal-tolerant sunflower mutant line for both biomonitoring and phytoremediating a Cu-contaminated soil series was investigated.
Methods
The soil series (21–1,170 mg Cu kg−1) was sampled in field plots at control and wood preservation sites. Sunflowers were cultivated 1 month in potted soils under controlled conditions.
Results
pH and dissolved organic matter influenced Cu concentration in the soil pore water. Leaf chlorophyll content and root growth decreased as Cu exposure rose. Their EC10 values corresponded to 104 and 118 μg Cu L−1 in the soil pore water, 138 and 155 mg Cu kg−1 for total soil Cu, and 16–18 mg Cu kg−1 DW shoot. Biomass of plant organs as well as leaf area, length and asymmetry were well correlated with Cu exposure, contrary to the maximum stem height and leaf water content.
Conclusions
Physiological parameters were more sensitive to soil Cu exposure than the morphological ones. Bioconcentration and translocation factors and distribution of mineral masses for Cu highlighted this mutant as a secondary Cu accumulator. Free Cu2+ concentration in soil pore water best predicted Cu phytoavailability. The usefulness of this sunflower mutant line for biomonitoring and Cu phytoextraction was discussed.
Similar content being viewed by others
Abbreviations
- BCF:
-
Bioconcentration factor
- Carot:
-
Carotenoid content
- CCA:
-
Chromated copper arsenate
- CEC:
-
Cation exchange capacity
- Chl:
-
Chlorophyll
- CTRL:
-
Control soil
- Cu-ISE:
-
Copper ion selective electrode
- ChlTOT:
-
Total chlorophyll content
- CuMM:
-
Shoot Cu removal
- CuRT:
-
Root Cu concentration
- CuSH:
-
Shoot Cu concentration
- CuSPW:
-
Total Cu concentration in the soil pore water
- CuTOT:
-
Total soil Cu
- DL:
-
Dolomitic limestone
- DMF:
-
N,N-dimethylformamide
- DOM:
-
Dissolved organic matter
- DW:
-
Dry weight
- DWSH:
-
Shoot DW yield
- EC10 :
-
in a graded dose response curve, the concentration of a compound where 10 % of its maximal effect is observed
- EMS:
-
Ethyl methanesulphonate
- INRA LAS:
-
French National Institute for Agricultural Research - Laboratory of soil analysis Arras France
- ISE:
-
Ion selective electrode
- LA:
-
Leaf asymmetry
- OM:
-
Organic matter
- RPI:
-
Relative parameter index
- RTEI:
-
Relative treatment efficiency index
- SL:
-
Stem length
- TE:
-
Trace element
- TF:
-
Translocation factor
- TI:
-
Tolerance index
- TLA:
-
Total leaf area
- TOC:
-
Total organic carbon
- UNT:
-
Untreated soil
- WC:
-
Water content
References
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. doi:10.1007/s11270-009-0128-3
Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals, 2nd edn. Springer Verlag, New-York, 871 p
Adriano DC, Wenzel WW, Vangronsveld J, Bolan NS (2004) Role of assisted natural remediation in environmental cleanup. Geoderma 122:121–142. doi:10.1016/j.geoderma.2004.01.003
Alaoui-Sosse B, Genet P, Vinit-Dunand F, Toussaint ML, Epron D, Badot PM (2004) Effect of copper on growth in cucumber plants (Cucumis sativus) and its relationships with carbohydrate accumulation and changes in ion contents. Plant Sci 166:1213–1218. doi:10.1016/j.plantsci.2003.12.032
Ambo-Rappe R, Lajus DL, Schreider MJ (2008) Increased heavy metal and nutrient contamination does not increase fluctuating asymmetry in the seagrass Halophila ovalis. Ecol Indic 8:100–103. doi:10.1016/j.ecolind.2006.12.004
Arellano JB, Lazaro JJ, Lopez-Gorgé J, Baron M (1995) The donor side of photosystem-II as the copper-inhibitory binding-site - fluorescence and polarografic studies. Photosynth Res 45:127–134. doi:10.1007/bf00032584
Ashworth DJ, Alloway BJ (2007) Complexation of copper by sewage sludge-derived dissolved organic matter: Effects on soil sorption behaviour and plant uptake. Water Air Soil Pollut 182:187–196. doi:10.1007/s11270-006-9331-7
Baker A, Tipping E, Thacker SA, Gondar D (2008) Relating dissolved organic matter fluorescence and functional properties. Chemosphere 73:1765–1772. doi:10.1016/j.chemosphere.2008.09.018
Barcelo J, Poschenrieder C (1990) Plant water relations as affected by heavy-metal stress - a review. J Plant Nutr 13:1–37. doi:10.1080/01904169009364057
Basol (2013) Base de données Basol sur les sites et sols pollués ou potentiellement pollués appelant une action des pouvoirs publics, à titre préventif ou curatif. http://basol.environnement.gouv.fr/. Accessed 11 March 2013
Beesley L, Dickinson N (2011) Carbon and trace element fluxes in the pore water of an urban soil following greenwaste compost, woody and biochar amendments, inoculated with the earthworm Lumbricus terrestris. Soil Biol Biochem 43:188–196. doi:10.1016/j.soilbio.2010.09.035
Bes C, Mench M (2008) Remediation of copper-contaminated topsoils from a wood treatment facility using in situ stabilisation. Environ Pollut 156:1128–1138. doi:10.1016/j.envpol.2008.04.006
Bes CM, Mench M, Aulen M, Gaste H, Taberly J (2010) Spatial variation of plant communities and shoot Cu concentrations of plant species at a timber treatment site. Plant Soil 330:267–280. doi:10.1007/s11104-009-0198-4
Bravin MN, Michaud AM, Larabi B, Hinsinger P (2010a) RHIZOtest: a plant-based biotest to account for rhizosphere processes when assessing copper bioavailability. Environ Pollut 158:3330–3337. doi:10.1016/j.envpol.2010.07.029
Bravin MN, Le Merrer B, Denaix L, Schneider A, Hinsinger P (2010b) Copper uptake kinetics in hydroponically-grown durum wheat (Triticum turgidum durum L.) as compared with soil’s ability to supply copper. Plant Soil 331:91–104. doi:10.1007/s11104-009-0235-3
Buck RP, Cosofret VV (1993) Recommended procedures for calibration of ion-selective electrodes. Pure Appl Chem 65:1849–1858. doi:10.1351/pac199365081849
Calabrese EJ, Blain RB (2009) Hormesis and plant biology. Environ Pollut 157:42–48. doi:10.1016/j.envpol.2008.07.028
Carrillo-Gonzalez R, Simunek J, Sauvé S, Adriano D (2006) Mechanisms and pathways of trace element mobility in soils. Adv Agron 91:111–178
CETIOM (1995) Les stades repères du tournesol (détails). Available at http://www.cetiom.fr/tournesol/cultiver-du-tournesol/atouts-points-cles/stades-reperes/stades-reperes-detailles/?print=1. Access on 12 March 2013
Chaignon V, Quesnoit M, Hinsinger P (2009) Copper availability and bioavailability are controlled by rhizosphere pH in rape grown in an acidic Cu-contaminated soil. Environ Pollut 157:3363–3369. doi:10.1016/j.envpol.2009.06.032
Chatterjee J, Chatterjee C (2000) Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ Pollut 109:69–74. doi:10.1016/s0269-7491(99)00238-9
Clemente R, Hartley W, Riby P, Dickinson NM, Lepp NW (2010) Trace element mobility in a contaminated soil two years after field-amendment with a greenwaste compost mulch. Environ Pollut 158:1644–1651. doi:10.1016/j.envpol.2009.12.006
Cook CM, Vardaka E, Lanaras T (1997) Concentrations of Cu, growth and chlorophyll content of field-cultivated wheat growing in naturally enriched Cu soil. Bull Environ Contam Toxicol 58:248–253, Available at http://link.springer.com/article/10.1007%2Fs001289900327#page-1. Access on July 4, 2013
Cuypers A, Vangronsveld J, Clijsters H (2000) Biphasic effect of copper on the ascorbate-glutathione pathway in primary leaves of Phaseolus vulgaris seedlings during the early stages of metal assimilation. Physiol Plant 110:512–517. doi:10.1111/j.1399-3054.2000.1100413.x
da Silva RF, Antoniolli ZI, Lupatini M, Trindade LL, da Silva AS (2010) Tolerance of canafistula (Peltophorum dubium (Spreng) Taub.) seedlings inoculated with Pisolithus microcarpus to copper contaminated soil. Ciencia Florestal 20:147–156, Available at http://www.researchgate.net/publication/44188992_Tolerncia_De_Mudas_De_Canafstula_(_Peltophorum_dubium_(Spreng.)_Taub.)_Inoculada_Com_Pisolithus_microcarpus_A_Solo_Com_Excesso_De_Cobre/file/9fcfd50b34e54a967f.pdf. Access on July 4, 2013
Datta SP, Young SD (2005) Predicting metal uptake and risk to the human food chain from leaf vegetables grown on soils amended by long-term application of sewage sludge. Water Air Soil Pollut 163:119–136. doi:10.1007/s11270-005-0006-6
Degryse F, Smolders E, Zhang H, Davison W (2009) Predicting availability of mineral elements to plants with the DGT technique: a review of experimental data and interpretation by modelling. Environ Chem 6:198–218. doi:10.1071/EN09010
Dickinson NM, Baker AJM, Doronila A, Laidlaw S, Reeves RD (2009) Phytoremediation of inorganics: realism and synergies. Int J Phytorem 11:97–114. doi:10.1080/15226510802378368
Ernst WHO, Peterson PJ (1994) The role of biomarkers in environmental assessment. 4. Terrestrial plants. Ecotoxicology 3:180–192. doi:10.1007/bf00117083
Faessler E, Robinson BH, Stauffer W, Gupta SK, Papritz A, Schulin R (2010) Phytomanagement of metal-contaminated agricultural land using sunflower, maize and tobacco. Agric Ecosyst Environ 136:49–58. doi:10.1016/j.agee.2009.11.007
Fellet G, Marchiol L, Perosa D, Zerbi G (2007) The application of phytoremediation technology in a soil contaminated by pyrite cinders. Ecol Eng 31:207–214. doi:10.1016/j.ecoleng.2007.06.011
Forsberg LS, Kleja DB, Greger M, Ledin S (2009) Effects of sewage sludge on solution chemistry and plant uptake of Cu in sulphide mine tailings at different weathering stages. Appl Geochem 24:475–482. doi:10.1016/j.apgeochem.2008.12.030
Fritsch C, Cosson RP, Coeurdassier M, Raoul F, Giraudoux P, Crini N, de Vaufleury A, Scheifler R (2010) Responses of wild small mammals to a pollution gradient: host factors influence metal and metallothionein levels. Environ Pollut 158:827–840. doi:10.1016/j.envpol.2009.09.027
Gunkel P, Roth E, Fabre B (2003) Copper distribution in chemical soil fractions and relationships with maize crop yield. Environ Chem Lett 1:92–97. doi:10.1007/s10311-002-0003-6
Hernandez AJ, Pastor J (2008) Relationship between plant biodiversity and heavy metal bioavailability in grasslands overlying an abandoned mine. Environ Geochem Health 30:127–133. doi:10.1007/s10653-008-9150-4
Hewitt E (1966) Sand and water culture methods used in the study of plant nutrition. The Eastern press Ltd, London
HiPerTOC (2004) Total organic carbon analyzer. Available at http://www.ankersmid-lab.be/AutoFiles/doc/4266_HiPerTOC_specsheet__PS42033[1].pdf. Accessed on 12 March 2013
Inaba S, Takenaka C (2005) Effects of dissolved organic matter on toxicity and bioavailability of copper for lettuce sprouts. Environ Int 31:603–608. doi:10.1016/S1001-0742(09)60346-6
INRA LAS (2013) Méthodes applicables aux sols. http://www5.lille.inra.fr/las/methodes_d_analyse/Sols. Accessed on 12 March 2013
ISO (2005) Soil quality - determination of the effects of pollutants on soil flora in part 2: effects of chemicals on the emergence and growth of higher plants, Geneva
Japenga J, Koopmans GF, Song J, Romkens PFAM (2007) A feasibility test to estimate the duration of phytoextraction of heavy metals from polluted soils. Int J Phytorem 9:115–132. doi:10.1080/15226510701232773
Jiang WS, Liu DH, Li HF (2000) Effects of Cu2+ on root growth, cell division, and nucleolus of Helianthus annuus L. Sci Total Environ 256:59–65
Jiang LY, Yang XE, He ZL (2004) Growth response and phytoextraction of copper at different levels in soils by Elsholtzia splendens. Chemosphere 55:1179–1187
Jung HI, Gayomba SR, Rutzke MA, Craft E, Kochian LV, Vatamaniuk OK (2012) COPT6 Is a plasma membrane transporter that functions in copper homeostasis in Arabidopsis and is a novel target of SQUAMOSA promoter-binding protein-like 7. J Biol Chem 287:33252–33267. doi:10.1074/jbc.M112.397810
Ke W, Xiong Z-T, Chen S, Chen J (2007) Effects of copper and mineral nutrition on growth, copper accumulation and mineral element uptake in two Rumex japonicus populations from a copper mine and an uncontaminated field sites. Environ Exp Bot 59:59–67. doi:10.1016/j.envexpbot.2005.10.007
Kidd P, Barcelo J, Pilar Bernal M, Navari-Izzo F, Poschenrieder C, Shilev S, Clemente R, Monterroso C (2009) Trace element behaviour at the root-soil interface: implications in phytoremediation. Environ Exp Bot 67:243–259. doi:10.1016/j.envexpbot.2009.06.013
Knezevic SZ, Streibig JC, Ritz C (2007) Utilizing R software package for dose–response studies: the concept and data analysis. Weed Technol 21:840–848. doi:10.1614/wt-06-161.1
Kolbas A, Mench M, Herzig R, Nehnevajova E, Bes CM (2011) Copper phytoextraction in tandem with oilseed production using commercial cultivars and mutant lines of sunflower. Int J Phytorem 13(Suppl 1):55–76. doi:10.1080/15226514.2011.568536
Korpe DA, Aras S (2011) Evaluation of copper-induced stress on eggplant (Solanum melongena L.) seedlings at the molecular and population levels by use of various biomarkers. Muta Res Gen Tox En 719:29–34. doi:10.1016/j.mrgentox.2010.10.003
Kryazheva NG, Chistyakova EK, Zakharov VM (1996) Analysis of development stability of Betula pendula under conditions of chemical pollution. Russ J Ecol 27:422–424
Kuepper H, Goetz B, Mijovilovich A, Kuepper FC, Meyer-Klaucke W (2009) Complexation and toxicity of copper in higher plants. I. Characterization of copper accumulation, speciation, and toxicity in Crassula helmsii as a new copper accumulator. Plant Physiol 151:702–714. doi:10.1104/pp. 109.139717
Lagadic L, Caquet T, Amiard JC, Ramade F (1997) Biomarqueurs en écotoxicologie. Aspects fondamentaux. Masson, Paris, p 419
Lagomarsino A, Mench M, Marabottini R, Pignataro A, Grego S, Renella G, Stazi SR (2011) Copper distribution and hydrolase activities in a contaminated soil amended with dolomitic limestone and compost. Ecotoxicol Environ Saf 74:2013–2019. doi:10.1016/j.ecoenv.2011.06.013
Lagriffoul A, Mocquot B, Mench M, Vangronsveld J (1998) Cadmium toxicity effects on growth, mineral and chlorophyll contents, and activities of stress related enzymes in young maize plants (Zea mays L.). Plant Soil 200:241–250. doi:10.1023/a:1004346905592
Leduc F, Whalen JK, Sunahara GI (2008) Growth and reproduction of the earthworm Eisenia fetida after exposure to leachate from wood preservatives. Ecotoxicol Environ Saf 69:219–226. doi:10.1016/j.ecoenv.2007.01.006
Lequeux H, Hermans C, Lutts S, Verbruggen N (2010) Response to copper excess in Arabidopsis thaliana: impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiol Biochem 48:673–682. doi:10.1016/j.plaphy.2010.05.005
Li Z, Tang S, Deng X, Wang R, Song Z (2010) Contrasting effects of elevated CO2 on Cu and Cd uptake by different rice varieties grown on contaminated soils with two levels of metals: implication for phytoextraction and food safety. J Hazard Mater 177:352–361. doi:10.1016/j.jhazmat.2009.12.039
Lin JX, Jiang WS, Liu DH (2003) Accumulation of copper by roots, hypocotyls, cotyledons and leaves of sunflower (Helianthus annuus L.). Bioresour Technol 86:151–155. doi:10.1016/s0960-8524(02)00152-9
Liu D, Xue P, Meng Q, Zou J, Gu J, Jiang W (2009) Pb/Cu effects on the organization of microtubule cytoskeleton in interphase and mitotic cells of Allium sativum L. Plant Cell Rep 28:695–702. doi:10.1007/s00299-009-0669-3
Luna CM, Gonzalez CA, Trippi VS (1994) Oxidative damage caused by an excess of copper in oat leaves. Plant Cell Physiol 35:11–15
Luo XS, Zhou DM, Wang YJ (2006) Free cupric ions in contaminated agricultural soils around a copper mine in eastern Nanjing City, China. J Environ Sci (China) 18:927–931. doi:10.1016/s1001-0742(06)60016-8
Macnicol RD, Beckett PHT (1985) Critical tissue concentrations of potentially toxic elements. Plant Soil 85:107–129. doi:10.1007/bf02197805
Madejon P, Murillo JM, Maranon T, Cabrera F, Soriano MA (2003) Trace element and nutrient accumulation in sunflower plants two years after the Aznalcollar mine spill. Sci Total Environ 307:239–257. doi:10.1016/s0048-9697(02)00609-5
Maderova L, Watson M, Paton GI (2011) Bioavailability and toxicity of copper in soils: Integrating chemical approaches with responses of microbial biosensors. Soil Biol Biochem 43:1162–1168. doi:10.1016/j.soilbio.2011.02.004
Marchand L, Mench M, Jacob DL, Otte ML (2010) Metal and metalloid removal in constructed wetlands, with emphasis on the importance of plants and standardized measurements: a review. Environ Pollut 158:3447–3461. doi:10.1016/j.envpol.2010.08.018
Marchand L, Mench M, Marchand C, Le Coustumer P, Kolbas A, Maalouf JP (2011) Phytotoxicity testing of lysimeter leachates from aided phytostabilized Cu-contaminated soils using duckweed (Lemna minor L.). Sci Total Environ 410:146–153. doi:10.1016/j.scitotenv.2011.09.049
McBride M, Sauvé S, Hendershot W (1997) Solubility control of Cu, Zn, Cd and Pb in contaminated soils. Eur J Soil Sci 48:337–346. doi:10.1111/j.1365-2389.1997.tb00554.x
Meers E, Ruttens A, Geebelen W, Vangronsveld J, Samson R, Vanbroekhoven K, Vandegehuchte M, Diels L, Tack FMG (2006) 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
Mench M, Bes C (2009) Assessment of ecotoxicity of topsoils from a wood treatment site. Pedosphere 19:143–155. doi:10.1016/S1002-0160(09)60104-1
Mench M, Lepp N, Bert V, Schwitzguebel JP, Gawronski SW, Schroeder P, Vangronsveld J (2010) Successes and limitations of phytotechnologies at field scale: outcomes, assessment and outlook from COST Action 859. J Soil Sediment 10:1039–1070. doi:10.1007/s11368-010-0190-x
Mendoza-Soto AB, Sanchez F, Hernandez G (2012) MicroRNAs as regulators in plant metal toxicity response. Front Plant Sci 3:105. doi:10.3389/fpls.2012.00105
Mocquot B, Vangronsveld J, Clijsters H, Mench M (1996) Copper toxicity in young maize (Zea mays L) plants: effects on growth, mineral and chlorophyll contents, and enzyme activities. Plant Soil 182:287–300
Moreno-Jimenez E, Beesley L, Lepp NW, Dickinson NM, Hartley W, Clemente R (2011) Field sampling of soil pore water to evaluate trace element mobility and associated environmental risk. Environ Pollut 159:3078–3085. doi:10.1016/j.envpol.2011.04.004
Navari-Izzo F, Cestone B, Cavallini A, Natali L, Giordani T, Quartacci MF (2006) Copper excess triggers phospholipase D activity in wheat roots. Phytochemistry 67:1232–1242. doi:10.1016/j.phytochem.2006.04.006
Nehnevajova E, Herzig R, Federer G, Erismann KH, Schwitzguébel JP (2005) Screening of sunflower cultivars for metal phytoextraction in a contaminated field prior to mutagenesis. Int J Phytorem 7:337–349. doi:10.1080/16226510500327210
Nehnevajova E, Herzig R, Bourigault C, Bangerter S, Schwitzguebel JP (2009) Stability of enhanced yield and metal uptake by sunflower mutants for improved phytoremediation. Int J Phytorem 11:329–346. doi:10.1080/15226510802565394
Nehnevajova E, Lyubenova L, Herzig R, Schroeder P, Schwitzguébel JP, Schmuelling T (2012) Metal accumulation and response of antioxidant enzymes in seedlings and adult sunflower mutants with improved metal removal traits on a metal-contaminated soil. Environ Exp Bot 76:39–48. doi:10.1016/j.envexpbot.2011.10.005
Palmer CM, Guerinot ML (2009) Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat Chem Biol 5:333–340. doi:10.1038/nchembio.166
Panou-Filotheou H, Bosabalidis AM (2004) Root structural aspects associated with copper toxicity in oregano (Origanum vulgare subsp hirtum). Plant Sci 166:1497–1504. doi:10.1016/j.plantsci.2004.01.026
Parsons PA (1992) Fluctuating asymmetry - a biological monitor of environmental and genomic stress. Heredity 68:361–364
Patsikka E, Kairavuo M, Sersen F, Aro EM, Tyystjarvi E (2002) Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiol 129:1359–1367. doi:10.1104/pp. 004788
Poschenrieder C, Bech J, Llugany M, Pace A, Fenes E, Barcelo J (2001) Copper in plant species in a copper gradient in Catalonia (North East Spain) and their potential for phytoremediation. Plant Soil 230:247–256. doi:10.1023/a:1010374732486
Posmyk MM, Kontek R, Janas KM (2009) Antioxidant enzymes activity and phenolic compounds content in red cabbage seedlings exposed to copper stress. Ecotoxicol Environ Saf 72:596–602. doi:10.1016/j.ecoenv.2008.04.024
Qi XM, Li PJ, Liu W, Xie LJ (2006) Multiple biomarkers response in maize (Zea mays L.) during exposure to copper. J Environ Sci (China) 18:1182–1188. doi:10.1016/s1001-0742(06)60059-4
Rivelli AR, de Maria S, Puschenreiter M, Gherbin P (2012) Accumulation of cadmium, zinc, and copper by Helianthus annuus L.: impact on plant growth and uptake of nutritional elements. Int J Phytorem 14:320–334. doi:10.1080/15226514.2011.620649
Rousos PA, Harrison HC, Steffen KL (1989) Physiological-responses of cabbage to incipient copper toxicity. J Am Soc Hortic Sci 114:149–152
Santra GH, Das DK, Mandal BK (1989) Relationship of boron with iron, manganese, copper and zinc with respect to their availability in rice soil. Environ Ecol 7:874–877
Sauvé S (2003) Modelling trace element exposure and effects on plants. In: Mench M, Mocquot B (eds) Risk assessment and sustainable land management using plants in trace element-contaminated soils. Centre INRA Bordeaux-Aquitaine, Villenave d’Ornon, pp 69–70, Available at http://w3.gre.ac.uk/cost859/book/Livre_COST837_2003_session_2.pdf. Access on July 4, 2013
Sauvé S, McBride MB, Norvell WA, Hendershot WH (1997) Copper solubility and speciation of in situ contaminated soils: effects of copper level, pH and organic matter. Water Air Soil Pollut 100:133–149. doi:10.1023/a:1018312109677
Singh S, Saxena R, Pandey K, Bhatt K, Sinha S (2004) Response of antioxidants in sunflower (Helianthus annuus L.) grown on different amendments of tannery sludge: its metal accumulation potential. Chemosphere 57:1663–1673. doi:10.1016/j.chemosphere.2004.07.049
Smeets K, Opdenakker K, Remans T, Forzani C, Hirt H, Vangronsveld J, Cuypers A (2013) The role of the kinase OXI1 in cadmium- and copper-induced molecular responses in Arabidopsis thaliana. Plant Cell Environ 36:1228–1238. doi:10.1111/pce.12056
Song J, Zhao FJ, Luo YM, McGrath SP, Zhang H (2004) Copper uptake by Elsholtzia splendens and Silene vulgaris and assessment of copper phytoavailability in contaminated soils. Environ Pollut 128:307–315. doi:10.1016/j.envpol.2003.09.019
Tahsin N, Yankov B (2007) Research on accumulation of zinc (Zn) and cadmium (Cd) in sunflower oil. J Tekirdag Agric Fac 4:109–112
Temminghoff EJM, Van der Zee S, deHaan FAM (1997) Copper mobility in a copper-contaminated sandy soil as affected by pH and solid and dissolved organic matter. Environ Sci Technol 31:1109–1115. doi:10.1021/es9606236
Thakali S, Allen HE, Di Toro DM, Ponizovsky AA, Rooney CP, Zhao FJ, McGrath SP (2006) A terrestrial biotic ligand model. 1. Development and application to Cu and Ni toxicities to barley root elongation in soils. Environ Sci Technol 40:7085–7093. doi:10.1021/es061171s
Vamerali T, Bandiera M, Mosca G (2010) Field crops for phytoremediation of metal-contaminated land. A review. Environ Chem Lett 8:1–17. doi:10.1007/s10311-009-0268-0
Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E, van der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794. doi:10.1007/s11356-009-0213-6
Vassilev A, Schwitzguebel JP, Thewys T, Van Der Lelie D, Vangronsveld J (2004) The use of plants for remediation of metal-contaminated soils. Sci World J 4:9–34
Waraich EA, Ahmad R, Saifullah, Ashraf MY, Ehsanullah (2011) Role of mineral nutrition in alleviation of drought stress in plants. Aust J Crop Sci 5:764–777
Warne MSJ, Heemsbergen D, McLaughlin M, Bell M, Broos K, Whatmuff M, Barry G, Nash D, Pritchard D, Penney N (2008) Models for the field-based toxicity of copper and zinc salts to wheat in 11 Australian soils and comparison to laboratory-based models. Environ Pollut 156:707–714. doi:10.1016/j.envpol.2008.06.012
Yruela I (2009) Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36:409–430. doi:10.1071/fp08288
Acknowledgments
This work was financially supported by ADEME, Department of Urban Brownfields and Polluted Sites, Angers, France (Mrs F. Cadière as supervisor), the University of Bordeaux 1, Department of International Relationships, through European Commission Erasmus Mundus Lot 6, and the European Commission under the Seventh Framework Programme for Research (FP7-KBBE-266124, GREENLAND). Thanks to Dr. Christophe Barnier (Institut EGID University Bordeaux 3, France), Dr. Anne Serani-Loppinet (ICMCB, University Bordeaux 1, France), and Pr. Mikael Motelica (University of Orléans, France) for their help in the analysis of soil pore waters. Special thanks to Dr. Jean-Paul Maalouf and Galina Brutcova for their technical assistance.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Juan Barcelo.
Highlights
A metal-tolerant sunflower mutant can be used for monitoring and phytoremediating soil Cu contamination at a wood preservation site.
Rights and permissions
About this article
Cite this article
Kolbas, A., Marchand, L., Herzig, R. et al. 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 (2014). https://doi.org/10.1007/s11104-013-1974-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-013-1974-8