Abstract
The effect of sodium chloride (NaCl) on cadmium (Cd) tolerance, uptake, translocation, and compartmentation was investigated in 3 barley genotypes. Seedlings were cultivated hydroponically in the absence of NaCl and Cd (control), in the presence of 50 mM NaCl alone, in the presence of 10 µM Cd alone, and in the combined addition of NaCl (50 mM) and Cd (10 µM). Plants were cultivated during one month under 16 h light period at a minimal light intensity of 250 µmol m−2 s−1, a temperature of 25 ± 3 °C, and 70–80% of relative humidity. Results showed that NaCl alone did not significantly affect plant development and biomass production; however, Cd alone reduced plant development rate leading to a decline in biomass production in Raihane and Giza 127 but did not affect that in Amalou. NaCl addition in Cd-treated plants accentuated the Cd effect on plant growth. NaCl limited Cd accumulation in the roots and in the shoots in all tested barley varieties by reducing Cd-absorption efficiency and the translocation of Cd from the root to the shoot. In all Cd-treated plants, cell Cd compartmentalization showed the following gradient: organelles < cell wall < vacuole. NaCl in the medium increased Cd accumulation in the soluble fraction and reduced that in organelle and cell wall fractions. Globally our results showed that, although NaCl reduces Cd accumulation in barley, it accentuates the Cd toxic effects, hence limiting the plant yield. We advise farmers to avoid barley cultivation near mine sites and its irrigation with moderately salty water, although this plant is considered as salt tolerant.
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References
Adrees M, Ali S, Rizwan M et al (2015) The effect of excess copper on growth and physiology of important food crops: a review. Environ Sci Pollut Res 22:8148–8162. https://doi.org/10.1007/s11356-015-4496-5
Akhtar T, Zia-ur-rehman M, Naeem A et al (2016) Photosynthesis and growth response of maize (Zea mays L) hybrids exposed to cadmium stress. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-016-8246-0
Alexander J, Benford D, Cockburn A et al (2009) Marine biotoxins in shellfish – pectenotoxin group 1 scientific opinion of the panel on contaminants in the food chain Adopted on 27 May 2009. EFSA J 1019:1–76
Ali S, Bharwana SA, Rizwan M et al (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. https://doi.org/10.1007/s11356-015-4271-7
Arnon DI (1949) Copper enzymes in isolated chloroplasts Polyphenoloxidase in Beta Vulgaris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Aron D, Hoagland D (1940) Crop production in artificial solutions and in soils with special reference to factors affecting yields and absorption of inorganic nutrients. Soil Sci 50:463–485
Ayachi I, Ghabriche R, Kourouma Y et al (2021) Cd tolerance and accumulation in barley: screening of 36 North African cultivars on Cd-contaminated soil. Environ Sci Pollut Res 28:42722–42736. https://doi.org/10.1007/s11356-021-13768-y
Besbes M, Chahed J, Hamdane A (2022) Growth and element uptake by salt-sensitive crops under combined NaCl and Cd stresses. Ecotoxicol Environ Saf 241:59–64. https://doi.org/10.1016/j.ecoenv.2020.111295
Boussen S, Soubrand M, Bril H et al (2013) Transfer of lead, zinc and cadmium from mine tailings to wheat (Triticum aestivum) in carbonated Mediterranean (Northern Tunisia) soils. Geoderma 192:227–236. https://doi.org/10.1016/j.geoderma.2012.08.029
Chellaiah ER (2018) Cadmium (heavy metals) bioremediation by Pseudomonas aeruginosa: a minireview. Appl Water Sci 8:154. https://doi.org/10.1007/s13201-018-0796-5
Cheng M, Wang A, Liu Z et al (2018) Sodium chloride decreases cadmium accumulation and changes the response of metabolites to cadmium stress in the halophyte Carpobrotus rossii. Ann Botany 122:373–385. https://doi.org/10.1093/aob/mcy077
Chung SM (2022) Long-term sex-specific effects of cadmium exposure on osteoporosis and bone density: a 10-year community-based cohort study. J Clin Med 11:4–13. https://doi.org/10.3390/jcm11102899
Clemens S, Ma JF (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:489–512. https://doi.org/10.1146/annurev-arplant-043015-112301
Clemens S, Aarts MGM, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99. https://doi.org/10.1016/j.tplants.2012.08.003
Codex Alimentarius Commission (1995) Codex standard 193–1995: the general standard for contaminants and toxins in food and feed. International food standards of the FAO and WHO
Dawson IK, Russell J, Powell W et al (2015) Barley: a translational model for adaptation to climate change. New Phytol 206:913–931. https://doi.org/10.1111/nph.13266
Du Laing G, Rinklebe J, Vandecasteele B et al (2009) Trace metal behaviour in estuarine and riverine floodplain soils and sediments: a review. Sci Total Environ 407:3972–3985. https://doi.org/10.1016/j.scitotenv.2008.07.025
Fan Y, Chen X, Chen Z et al (2022) Pollution characteristics and source analysis of heavy metals in surface sediments of Luoyuan Bay, Fujian. Environ Res 203:111911. https://doi.org/10.1016/j.envres.2021.111911
European Food Safety Authority (2012) Cadmium dietary exposure in the European population. EFSA J 10:1–37. https://doi.org/10.2903/j.efsa.2012.2551
Ghallab A, Usman ARA (2007) Effect of sodium chloride-induced salinity on phyto-availability and speciation of Cd in soil solution. Water Air Soil Pollut 185:43–51. https://doi.org/10.1007/s11270-007-9424-y
Ghnaya T, Slama I, Messedi D et al (2007) Cd-induced growth reduction in the halophyte Sesuvium portulacastrum is significantly improved by NaCl. J Plant Res 120:309–316. https://doi.org/10.1007/s10265-006-0042-3
Guo J, Chen M, Huang Y et al (2022) Chloride application weakens cadmium immobilization by lime in paddy rice soil. Ecotoxicol Environ Saf 241:113761. https://doi.org/10.1016/j.ecoenv.2022.113761
Habiba U, Ali S, Farid M et al (2015) EDTA enhanced plant growth, antioxidant defense system, and phytoextraction of copper by Brassica napus L. Environ Sci Pollut Res 22:1534–1544. https://doi.org/10.1007/s11356-014-3431-5
Haider FU, Liqun C, Coulter JA et al (2021) Cadmium toxicity in plants: impacts and remediation strategies. Ecotoxicol Environ Saf 211:111887. https://doi.org/10.1016/j.ecoenv.2020.111887
Hassan MU, Chattha MU, Khan I et al (2019) Nickel toxicity in plants : reasons, toxic effects, tolerance mechanisms, and remediation possibilities — a review. Environ Sci Pollut Res 26:12673–12688
Huang Y, Wei K, Yang J et al (2007) Interaction of salinity and cadmium stresses on mineral nutrients, sodium, and cadmium accumulation in four barley genotypes. J Zhejiang Univ - Sci B 8(476):485. https://doi.org/10.1631/jzus.2007.B0476
Hussain B, Nadeem M, Abbas A et al (2021) Cadmium stress in paddy fields: effects of soil conditions and remediation strategies. Sci Total Environ 754:142188. https://doi.org/10.1016/j.scitotenv.2020.142188
Lefèvre I, Marchal G, Meerts P et al (2009) Chloride salinity reduces cadmium accumulation by the Mediterranean halophyte species Atriplex halimus L. Environ Exp Bot 65:142–152. https://doi.org/10.1016/j.envexpbot.2008.07.005
Li C, Zhou K, Qin W et al (2019) A review on heavy metals contamination in soil: effects, sources, and remediation techniques. Soil Sediment Contam 28:380–394. https://doi.org/10.1080/15320383.2019.1592108
Li X, Du J, Sun L et al (2022) Derivation of soil criteria of cadmium for safe rice production applying soil – plant transfer model and species sensitivity distribution. Int J Environ Res Public Health 19:8854. https://doi.org/10.3390/ijerph19148854
Lichtenthaler H, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592
Lin HC, Hao WM, Chu PH (2021) Cadmium and cardiovascular disease: an overview of pathophysiology, epidemiology, therapy, and predictive value. Rev Port Cardiol 40:611–617. https://doi.org/10.1016/j.repc.2021.01.009
Lopez-chuken UJ, Barceló-quintal ID, Ramirez-lara E et al (2021) Influence of chloride salinity on cadmium uptake by Nicotiana tabacum in a rhizofiltration system. Arch Environ Prot 47:35–40. https://doi.org/10.24425/aep.2021.136446
Lutts S, Lefèvre I (2015) How can we take advantage of halophyte properties to cope with heavy metal toxicity in salt-affected areas? Annals Bot 115:509–528. https://doi.org/10.1093/aob/mcu264
Manzoor H, Mehwish, Bukhat S et al (2022) Methyl jasmonate alleviated the adverse effects of cadmium stress in pea (Pisum sativum L.): a nexus of photosystem II activity and dynamics of redox balance. Front Plant Sci 13. https://doi.org/10.3389/fpls.2022.860664
Mariem W, Kilani BR, Benet G et al (2014) How does NaCl improve tolerance to cadmium in the halophyte Sesuvium portulacastrum? Chemosphere 117:243–250. https://doi.org/10.1016/j.chemosphere.2014.07.041
McLaughlin MJ, Palmer LT, Tiller KG et al (1994) Increased soil salinity causes elevated cadmium concentrations in field-grown potato tubers. J Environ Qual 23:1013–1018. https://doi.org/10.2134/jeq1994.00472425002300050023x
Mei XQ, Li SS, Li QS et al (2014) Sodium chloride salinity reduces Cd uptake by edible amaranth (Amaranthus mangostanus L.) via competition for Ca channels. Ecotoxicol Environ Saf 105:59–64. https://doi.org/10.1016/j.ecoenv.2014.04.005
Mühling KH, Andre L (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
Muñoz-Amatriaín M, Cuesta-Marcos A, Hayes PM, Muehlbauer GJ (2014) Barley genetic variation: implications for crop improvement. Brief Funct Genomic Proteomic 13:341–350. https://doi.org/10.1093/bfgp/elu006
Nefissi-Ouertani R, Arasappan D, Abid G, Ben Chikha M, Jardak R, Mahmoudi H, Mejri S, Ghorbel A, Ruhlman TA, Jansen RK (2021) Transcriptomic analysis of salt-stress-responsive genes in barley roots and leaves. Inter J Mol Sci. https://doi.org/10.3390/ijms22158155
Newton AC, Flavell AJ, George TS et al (2011) Crops that feed the world 4. Barley: a resilient crop? Strengths and weaknesses in the context of food security. Food Sec 3:141–178. https://doi.org/10.1007/s12571-011-0126-3
Ondrasek G, Rengel Z, Maurović N et al (2021) Growth and element uptake by salt-sensitive crops under combined nacl and cd stresses. Plants 10:1202. https://doi.org/10.3390/plants10061202
Othmani MA, Souissi F, da Silva EF, Coynel A (2015) Accumulation trends of metal contamination in sediments of the former Pb-Zn mining district of Touiref (NW Tunisia). J Afr Earth Sci 111:231–243. https://doi.org/10.1016/j.jafrearsci.2015.07.007
Qiu Q, Wang Y, Yang Z, Yuan J (2011) Effects of phosphorus supplied in soil on subcellular distribution and chemical forms of cadmium in two Chinese flowering cabbage (Brassica parachinensis L.) cultivars differing in cadmium accumulation. Food Chem Toxicol 49:2260–2267. https://doi.org/10.1016/j.fct.2011.06.024
Quadros IPS, Madeira NN, Loriato VAP et al (2022) Cadmium-mediated toxicity in plant cells is associated with the DCD/NRP-mediated cell death response. Plant Cell Environ 45:556–571. https://doi.org/10.1111/pce.14218
Rasafi T El, Oukarroum A, Haddioui A et al (2020) Cadmium stress in plants: a critical review of the effects, mechanisms, and tolerance strategies. Crit Rev Environ Sci Technol 52(5):675–726. https://doi.org/10.1080/10643389.2020.1835435
Rizwan M, Ali S, Adrees M et al (2016) Cadmium stress in rice: toxic effects, tolerance mechanisms, and management: a critical review. Environ Sci Pollut Res 23:17859–17879. https://doi.org/10.1007/s11356-016-6436-4
Ryan J, Sommer R (2012) Soil fertility and crop nutrition research at an international center in the Mediterranean region: achievements and future perspective. Arch Agron Soil Sci 58:37–41. https://doi.org/10.1080/03650340.2012.693601
Shi Z, Carey M, Meharg C et al (2020) Rice grain cadmium concentrations in the global supply-chain. Expo Health 12:869–876. https://doi.org/10.1007/s12403-020-00349-6
Smolders E, Lambregts RM (1998) Effect of soil solution chloride on cadmium availability to Swiss chard. J Environ Qual 27:426–431. https://doi.org/10.2134/jeq1998.00472425002700020025x
Smykalova I, Zamecnikova B (2003) The relationship between salinity and cadmium stress in barley. Biol Plant 46:269–273
Stephania G, Macpherson HG (2005) Food barley: importance, uses and local knowledge. Barley-based food in Southern Morocco in food barley: proceedings of the international workshop on food barley improvement, 14-17 January 2002, Hammamet, Tunisia. ICARDA, Aleppo, Syria, x+156 pp
Sterckeman T, Thomine S (2020) Mechanisms of cadmium accumulation in plants. Crit Rev Plant Sci 39:322–359. https://doi.org/10.1080/07352689.2020.1792179
Tai YT, Chou SH, Cheng CY et al (2022) The preferential accumulation of cadmium ions among various tissues in mice. Toxicol Rep 9:111–119. https://doi.org/10.1016/j.toxrep.2022.01.002
Tarhonska K, Lesicka M, Janasik B et al (2022) Cadmium and breast cancer – current state and research gaps in the underlying mechanisms. Toxicol Lett 361:29–42. https://doi.org/10.1016/j.toxlet.2022.03.003
Tellez-Plaza M, Guallar E, Fabsitz RR et al (2013) Cadmium exposure and incident peripheral arterial disease. Circ Cardiovasc Qual Outcomes 6:626–633. https://doi.org/10.1161/CIRCOUTCOMES.112.000663
Usman ARA, Kuzyakov Y, Stahr K (2005) Effect of immobilizing substances and salinity on heavy metals availability to wheat grown on sewage sludge-contaminated soil. Soil Sediment Contam 14:329–344. https://doi.org/10.1080/15320380590954051
Wali M, Fourati E, Hmaeid N et al (2015) NaCl alleviates Cd toxicity by changing its chemical forms of accumulation in the halophyte Sesuvium portulacastrum. Environ Sci Pollut Res 22:10769–10777. https://doi.org/10.1007/s11356-015-4298-9
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. https://doi.org/10.1071/SR99028
Yang JS, Dai Y, Liu Y et al (2020) Reduced cadmium accumulation in tobacco by sodium chloride priming. Environ Sci Pollut Res 27:37410–37418. https://doi.org/10.1007/s11356-020-09134-z
Yao P, Zhou H, Li X et al (2021) Effect of biochar on the accumulation and distribution of cadmium in tobacco (Yunyan 87) at different developmental stages. Ecotoxicol Environ Saf 207:111295. https://doi.org/10.1016/j.ecoenv.2020.111295
Zhao FJ, Jiang RF, Dunham SJ, McGrath SP (2006) Cadmium uptake, translocation and tolerance in the hyperaccumulator Arabidopsis halleri. New Phytol 172:646–654. https://doi.org/10.1111/j.1469-8137.2006.01867.x
Zhou M, Ghnaya T, Dailly H et al (2019) The cytokinin trans-zeatine riboside increased resistance to heavy metals in the halophyte plant species Kosteletzkya pentacarpos in the absence but not in the presence of NaCl l e. Chemosphere 233:954–965. https://doi.org/10.1016/j.chemosphere.2019.06.023
Zulfiqar U, Farooq M, Hussain S et al (2019) Lead toxicity in plants: impacts and remediation. J Environ Manag 250:109557. https://doi.org/10.1016/j.jenvman.2019.109557
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This work was conducted in the Laboratory of Extremophile Plants (LR10CBBC02) in the Biotechnology Center of Borj Cedria, Tunisia, and supported by the ARIMNET 2 project entitled “Exploring genotypic diversity to optimize barley grain and straw quality under marginal/stressful growth conditions, BEST.” The authors acknowledge the support of the National Gene Bank of Tunisia.
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I.A., R.G., and A.B. conducted the experimental work (culture, analysis). C.A. and M.H. are members of the project and participated in the experimental set-up. I.A. writo the MS. T.G. is the supervisor of the work and responsible for the conception and the writing – review and editing of the MS.
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Ayachi, I., Ghabriche, R., Zineb, A.b. et al. NaCl effect on Cd accumulation and cell compartmentalization in barley. Environ Sci Pollut Res 30, 49215–49225 (2023). https://doi.org/10.1007/s11356-023-25791-2
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DOI: https://doi.org/10.1007/s11356-023-25791-2