Abstract
Cadmium contamination is a serious environmental problem for modern agriculture and human health. Salinity affects plant growth and development, and interactions between salt and cadmium have been reported. However, the molecular mechanisms of salinity–cadmium interactions are not fully understood. Here, we show that a low concentration of salt alleviates Cd-induced growth inhibition and increases Cd accumulation in Arabidopsis thaliana. Supplementation with low concentrations of salt reduced the reactive oxygen species level in Cd-stressed roots by increasing the contents of proline and glutathione and down-regulating the expression of RCD1, thereby protecting the plasma membrane integrity of roots under cadmium stress. Salt supplementation substantially reduces the Cd-induced elevation of IAA oxidase activity, thereby maintaining auxin levels in Cd-stressed plants, as indicated by DR5::GUS expression. Salt supply increased Cd absorption in roots and increased Cd accumulation in leaves, implying that salt enhances both Cd uptake in roots and the root-to-shoot translocation of Cd. The elevated Cd accumulation in plants in response to salt was found to be correlated with the elevated levels of phytochelatin the expression of heavy metal transporters AtHMA1-4, especially AtHMA4. Salt alleviated growth inhibition caused by Cd and increased Cd accumulation also was observed in Cd accumulator Solanum nigrum.
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Abbreviations
- CM-H2DCFDA:
-
5-(and -6)-Chloromethyl-2′,7′-dichlorodihydrofluorescein diacetate, acetylester
- PC:
-
Phytochelatin
- PI:
-
Propidium iodide
- X-Gluc:
-
5-Bromo-4-chloro-3-indolyl-β-d-glucuronic acid cyclohexyl-ammonium
- GR:
-
Glutathione reductase
References
Ahlfors R, Lang S, Overmyer K, Jaspers P, Brosche M, Tauriainen A, Kollist H, Tuominen H, Belles-Boix E, Piippo M, Inze D, Palva ET, Kangasjärvi J (2004) Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses. Plant Cell 16:1925–1937
Anderson JV, Chevone BI, Hess JL (1992) Seasonal variation in the antioxidant system of eastern white pine needles. Plant Physiol 98:501–508
Belles-Boix E, Babiychuk E, Van Montagu M, Inze D, Kushnir S (2000) CEO1, a new protein from Arabidopsis thaliana, protects yeast against oxidative damage. FEBS Lett 482:19–24
Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602
Boonsirichai K, Sedbrook JC, Chen R, Gilroy S, Masson PH (2003) ALTERED RESPONSE TO GRAVITY is a peripheral membrane protein that modulates gravity-induced cytoplasmic alkalinization and lateral auxin transport in plant statocytes. Plant Cell 15:2612–2625
Chaoui A, Ferjani EE (2005) Effects of cadmium and copper on antioxidant capacities, lignification and auxin degradation in leaves of pea (Pisum sativum L.) seedlings. C R Biol 328:23–31
Chen CT, Chen TC, Lo KF, Chiu CY (2004) Effects of proline on copper transport in rice seedlings under excess of copper stress. Plant Sci 166:103–111
Clemens S, Palmgren MG, Kramer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315
Courbot M, Willems G, Motte P, Arvidsson S, Roosens N, Saumitou-Laprade P, Verbruggen N (2007) A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol 144:1052–1065
De Cnodder T, Vissenberg K, Van Der Straeten D, Verbelen JP (2005) Regulation of cell length in the Arabidopsis thaliana root by the ethylene precursor aminocyclopropane- 1-carboxylic acid: a matter of apoplastic reactions. New Phytol 168:541–550
Errabii T, Gandonou CB, Essalmani H, Abrini J, Idaomar M, Senhaji NS (2007) Effects of NaCl and mannitol induced stress on sugarcane (Saccharum sp.) callus cultures. Acta Physiol Plant 29:95–102
Faivre-Rampant O, Kevers C, Gaspar T (2000) IAA-oxidase activity and auxin protectors in nonrooting rac mutant shoots of tobacco in vitro. Plant Sci 153:73–80
Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jurgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153
Halliwell B, Gutteridge JMC (1986) Oxygen free radicals and iron in relation to biology and medicine:some problems and concept. Arch Biochem Biophys 246:501–514
Harrison-Murray RS, Clarkson DT (1973) Relationships between structural development and the absorption of ions by the root system of Cucurbita pepo. Planta 114:1–16
Helal HM, Upenov A, Issa GJ (1999) Growth and uptake of Cd and Zn by Leucaena leucocephala in reclaimed soils as affected by NaCl salinity. J Plant Nutr Soil Sci 162:589–592
Hernandez LE, Carpena-Ruiz R, Garate A (1996) Alterations in the mineral nutrition of pea seedlings exposed to cadmium. J Plant Nutr 19:1581–1598
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
Keltjens WG, Van Beusichem ML (1998) Phytochelatins as biomarker for heavy metal stress in maize (Zea mays L.) and wheat (Triticum aestivum L.): combined effects of copper and cadmium. Plant Soil 203:119–126
Krämer U, Talkea IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272
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
Lang ML, Zhang YX, Chai TY (2005) Identification of genes up-regulated in response to Cd exposure in Brassica juncea L. Gene 363:151–158
Li YM, Chaney RL, Schneiter AA (1994) Effect of soil chloride level on cadmium concentration in sunflower kernels. Plant Soil 167:275–280
Macek T, Mackova M, Pavlikova D, Szakova J, Truksa M, Singh Cundy A, Kotrba P, Yancey N, Scouten WH (2002) Accumulation of cadmium by transgenic tobacco. Acta Biotechnol 22:101–106
Maggio A, Miyazaki S, Veronese P, Fujita T, Ibeas JI, Damsz B, Narasimhan ML, Hasegawa PM, Joly RJ, Bressan RA (2002) Does proline accumulation play an active role in stress-induced growth reduction? Plant J 31:699–712
McLaughlin MJ, Tiller KG, Beech TA, Smart MK (1994) Soil salinity causes elevated cadmium concentrations in field-grown potato tubers. J Environ Qual 23:1013–1018
Mendoza-Cozatl DG, Moreno-Sanchez R (2006) Control of glutathione and phytochelatin synthesis under cadmium stress. J Theor Biol 238:919–936
Mühling KH, Läuchli A (2003) Interaction of NaCl and Cd stress on compartmentation pattern of cations, antioxidant enzymes and proteins in leaves of two wheat genotypes differing in salt tolerance. Plant Soil 253:219–231
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Parker DR, Norvell WA, Chaney RL (1995) Geochem-PC: a chemical speciation program for IBM compatibles. In: Loeppert RH, Schwab AP, Goldberg S (eds) Chemical equilibrium and reaction models. Soil Science Society of America, Madison, WI, pp 253–269
Rivetta A, Negrini N, Cocucci M (1997) Involvement of Ca2+-calmodulin in Cd2+ toxicity during the early phases of radish (Raphanus satious L.) seed germination. Plant Cell Environ 20:600–608
Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130
Sepehr MF, Ghorbanli M (2006) Physiological responses of Zea mays seedlings to interactions between cadmium and salinity. J Integr Plant Biol 48:807–813
Shao GS, Chen MX, Wang WX, Zhang GP (2008) The effect of salinity pretreatment on Cd accumulation and Cd-induced stress in BADH-Transgenic and nontransgenic rice seedlings. J Plant Growth Regul 27:205–210
Siripornadulsil S, Traina S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14:2837–2847
Smolders E, McLaughlin MJ (1996) Effect of Cl on Cd uptake by Swiss chard in nutrient solutions. Plant Soil 179:57–64
Smolders E, Lambrechts RM, McLaughlin MJ, Tiller KG (1997) Effect of soil solution chloride on Cd availability to Swiss chard. J Environ Qual 27:426–431
Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM (2005) A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 17:2230–2242
Sun RL, Zhou QX, Sun FH, Jin CX (2007) Antioxidative defense and proline/phytochelatin accumulation in a newly discovered Cd-hyperaccumulator, Solanum nigrum L. Environ Exp Bot 60:468–476
Ulmasov T, Murfett J, Hagen G, Guilfoyle T (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971
Van Assche F, Clijsters C (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206
van de Geijn SC, Petit CM (1978) In vivo measurement of cadmium (115mCd) transport and accumulation in the stems of intact tomato plants (Lycopersicon esculentum, Mill.). Planta 138:145–151
Verma DPS (1999) Osmotic stress tolerance in plants: role of proline and sulfur metabolisms. In: Shinozaki K, Yamaguchi-Shinozaki K (eds) Molecular responses to cold, drought, heat and salt stress in higher plants. Landes, Austin, pp 153–168
Weggler-Beaton K, McLaughlin MJ, Graham RD (2000) Salinity increases cadmium uptake by wheat and Swiss chard from soil amended with biosolids. Aust J Soil Res 38:37–45
Wellburn AR (1994) The special determinations of chlorophyll a and b as well as total carotenoides using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313
Williams LE, Pittman JK, Hall JL (2000) Emerging mechanisms for heavy metal transport in plants. Biochim Biophys Acta 1465:104–126
Xu J, Wang WY, Yin HX, Sun H, Mi Q (2009a) Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil. doi:10.1007/s11104-009-0011-4
Xu J, Yin HX, Li X (2009b) Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep 28:325–333
Xu J, Chai TY, Zhang YX, Lang ML, Han L (2009c) The cation-efflux transporter BjCET2 mediates zinc and cadmium accumulation in leaf of Brassica juncea L. Plant Cell Rep 28:1235–1242
Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445
Acknowledgments
The authors truly appreciate the time that the editor and two anonymous reviewers spent on helping to clarify the confusions and modify the paper. This research was supported by the Knowledge Innovation Program of the Chinese Academy of Sciences (Grant no. 0707013603) and the National Major Special Project on New Varieties Cultivation for Transgenic Organisms (Grant no. 2009ZX08009-130B).
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425_2009_1070_MOESM1_ESM.tif
Supplemental Fig. S1 Cadmium toxicity in Solanum nigrum seedlings is reduced by an appropriate concentration of salt. Seven-day-old seedlings were treated with different concentration of CdCl2 and 25 mM NaCl or their combination for 10 d. a Representative images showing seedling growth under different treatments as described above. b Primary root length. c Cd content. Vertical bars represent ±standard error. Different letters indicate significant differences, 5% level, Duncan’s mutiple range test. ck, untreated-control plants (TIFF 301 kb)
425_2009_1070_MOESM2_ESM.tif
Supplemental Fig. S2 NaCl reduced ROS accumulation and improved plasma membrane integrity (PI staining) under cadmium stress in roots of S. nigrum. ck, untreated-control plants (TIFF 205 kb)
425_2009_1070_MOESM3_ESM.tif
Supplemental Fig. S3 Effects of CdCl2, NaCl, and their combination on the accumulation of a proline, b glutathione and c phytochelatin in the leaves of S. nigrum seedlings. Vertical bars represent ±standard error. Different letters indicate significant differences, 5% level, Duncan’s mutiple range test. ck, untreated-control plants (TIFF 264 kb)
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Xu, J., Yin, H., Liu, X. et al. Salt affects plant Cd-stress responses by modulating growth and Cd accumulation. Planta 231, 449–459 (2010). https://doi.org/10.1007/s00425-009-1070-8
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DOI: https://doi.org/10.1007/s00425-009-1070-8