Abstract
The study investigates the effect of cadmium (Cd), salinity (NaCl), and combined stress on rhizosphere pH, growth parameters, membrane leakage, and genotoxicity in Vicia faba. Germinated seeds were exposed for 48 h to 0.01 mM Cd(NO3)2 (Cd), 50 mM NaCl (S50), 150 mM NaCl (S150), and Cd-NaCl (CdS50 and CdS150). An accumulation of Cd and Na was found essentially in Vicia roots under each single stress factor associated with variations in rhizosphere pH. Additional NaCl in metallic solution significantly dropped the rhizosphere pH and decreased Cd concentrations in roots by 2.3 and 3.8 times for CdS50 and CdS150, respectively. Growth parameters (root length and fresh and dry matters), mitotic activity, and micronucleus formation were not influenced by Cd and low concentration of NaCl when applied separately or together, while 150 mM of NaCl, alone or combined with Cd, affected negatively all the studied parameters, as well as chromosome and nucleus stability. V. faba seems to reduce the transport of Cd in saline conditions and therefore salinity (50 mM) may act as a protection against Cd accumulation.
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References
Abbas G, Saqib M, Akhtar J, Murtaza G, Shahid M (2015) Effect of salinity on rhizosphere acidification and antioxidant activity of two acacia species. Can J For Res 45:124–129. https://doi.org/10.1139/cjfr-2014-0354
Acosta JA, Jansen B, Kalbitz K, Faz A, Martínez-Martínez S (2011) Salinity increases mobility of heavy metals in soils. Chemosphere 85:1318–1324. https://doi.org/10.1016/j.chemosphere.2011.07.046
Ahmad A, Hadi F, Ahmad H, Jan AU, Rahman K, Ahmad S (2017) Salinity in soil increased cadmium uptake and accumulation potential of two terrestrial plants. Int J Biosci 10(3):132–142. https://doi.org/10.12692/ijb/10.3.132-142
Åkesson A, Bjellerup P, Lundh T, Lidfeldt J, Nerbrand C, Samsioe G, Skerfving S, Vahter M (2006) Cadmium-induced effects on bone in a population-based study of women. Environ Health Perspect 114(6):830–834. https://doi.org/10.1289/ehp.8763
Bäckström M, Karlsson S, Bäckman L, Folkeson L, Lind B (2004) Mobilisation of heavy metals by deicing salts in a roadside environment. Water Res 38:720–732. https://doi.org/10.1016/j.watres.2003.11.006
Ben Ahmed C, Magdich S, Ben Rouin B, Boukhris M, Ben Abdullah F (2012) Saline water irrigation effects on soil salinity distribution and some physiological responses of field grown Chemlali olive. J Environ Manag 113:538–544. https://doi.org/10.1016/j.jenvman.2012.03.016
Boulbaba A, Marzouk L, Ben Rabah R, Najet S (2012) Variations of natural soil salinity in an arid environment using underground watertable effects on salinization of soils in irrigated perimeters in South Tunisia. Int J Geosci 3:1040–1047. https://doi.org/10.4236/ijg.2012.35105
Bravin MN, Garnier C, Lenoble V, Gérard F, Dudal Y, Hinsinger P (2012) Root-induced changes in pH and dissolved organic matter binding capacity affect copper dynamic speciation in the rhizosphere. Geochim Cosmochim Acta 84:256–268. https://doi.org/10.1016/j.gca.2012.01.031
Bulut F, Akicni S (2010) The effect of salinity on growth and nutrient composition in broad bean (Vicia faba L.) seedlings. Fresenius Environ Bull 19:2901–2910
Charef, A, Ayed L, Azzouzi R (2011) Irrigation water qualities-soil pollution (heavy metals and salinity) in Mornag irrigated perimeter (SW Tunis, North Tunisia). In: Proceedings of the 15th International Water Technology Conference, Alexandria, Egypt
Cheng M, Wang A, Liu Z, Gendall AR, Rochfort S, Tang C (2018) Sodium chloride decreases cadmium accumulation and changes the response of metabolites to cadmium stress in the halophyte Carpobrotus rossii. Ann Bot 122:373–385. https://doi.org/10.1093/aob/mcy077
Council Directive 86/278/EEC of 12 June 1986 on the protection of the environment, and in particular of the soil, when sewage sludge is used in agriculture. OJ No L181 :6-12
Dahmouni M, Hörmann G, Jouzdan O, Hachicha M (2018) Export of salt and heavy metals in an area irrigated with treated wastewater: a case study from Cebala-Borj Touil (Tunisia). Desalin Water Treat 102:61–70. https://doi.org/10.5004/dwt.2018.21825
De Vos CHR, Schat H, Vooijs R, Ernst WHO (1991) Increased resistance to copper-induced damage of the root cell plasmalemma in copper tolerant in Silene cucubalus. Physiol Plant 82:523–528. https://doi.org/10.1111/j.1399-3054.1991.tb02942.x
El-Bastawisy ZM, El-Katony TM, Abd El-Fatah SN (2018) Genotypic variability in salt tolerance of Vicia faba during germination and early seedling growth. J King Saud Univ Sci 30:270–277. https://doi.org/10.1016/j.jksus.2017.04.004
Farooqui A, Suhail S, Zeeshan M (2017) Cadmium induced oxidative stress and biochemical responses in cyanobacterium Nostoc muscorum. Russ J Plant Physiol 64(1):124–132. https://doi.org/10.1134/S102144371701006X
Franzisky BL, Geilfus CM, Kränzlein M, Zhang X, Zörb C (2019) Shoot chloride translocation as a determinant for NaCl tolerance in Vicia faba L. J Plant Physiol 236:23–33. https://doi.org/10.1016/j.jplph.2019.02.012
Hachicha M, Ben Aissa I (2014) Managing salinity in Tunisian oases. J Life Sci 8(9):775–782. https://doi.org/10.17265/1934-7391/2014.09.007
Hachicha M, Kanzari S, Mansour M, Jouzdan O, Arselan A (2013) Salinity risk and management in Tunisian semi-arid area. J. Life Sci 7:196–201. https://doi.org/10.17265/1934-7391/2013.02.013
Hardiman RT, Jacoby B (2006) Absorption and translocation of Cd in bush beans (Phaseolus Vulgaris). Physiol Plant 61:670–674. https://doi.org/10.1111/j.1399-3054.1984.tb05189.x
Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59. https://doi.org/10.1023/A:1022371130939
Hyder O, Chung M, Cosgrove D, Herman JM, Li Z, Firoozmand A, Gurakar A, Koteish A, Pawlik TM (2013) Cadmium exposure and liver disease among US adults. J Gastrointest Surg 17:1265–1273. https://doi.org/10.1007/s11605-013-2210-9
Iqbal M (2016) Vicia faba bioassay for environmental toxicity monitoring: a review. Chemosphere 144:785–802. https://doi.org/10.1016/j.chemosphere.2015.09.048
Isayenkov SV, Maathuis FJ (2019) Plant salinity stress: many unanswered questions remain. Front Plant Sci 10:1–11. https://doi.org/10.3389/fpls.2019.00080
Johri N, Jacquillet G, Unwin R (2010) Heavy metal poisoning: the effects of cadmium on the kidney. Biometals 23(5):783–792. https://doi.org/10.1007/s10534-010-9328-y
Jones DL (1998) Organic acids in the rhizosphere-a critical review. Plant Soil 205:25–44. https://doi.org/10.1023/A:1004356007312
Jones DL, Darrah PR (1994) Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166:247–257. https://doi.org/10.1007/BF00008338
Kanzari S, Hachicha M, Bouhlila R, Battle J (2012) Simulation of water and salts dynamics in Bouhajla (Central Tunisia): exceptional rainfall effect. J Soil Water Res 7:36–44. https://doi.org/10.17221/17/2011-SWR
Katerji N, Mastrorilli M, Lahmer FZ, Maalouf F, Oweis T (2011) Faba bean productivity in saline drought conditions. Eur J Agron 35:2–12. https://doi.org/10.1016/j.eja.2011.03.001
Kharrat M, Ouchari H (2011) Faba bean status and prospects in Tunisia. Grain Legume 56:11–12
Klay S, Charef A, Ayed L, Houman B, Rezgui F (2010) Effect of irrigation with treated wastewater on geochemical properties (saltiness, C, N and heavy metals) of isohumic soils (Zaouit Sousse perimeter, Oriental Tunisia). Desalination 253:180–187. https://doi.org/10.1016/j.desal.2009.10.019
Louati D, Majdoub R, Rigane H, Abida H (2018) Effects of irrigating with saline water on soil salinization (Eastern Tunisia). Arab J Sci Eng 43:3793–3805. https://doi.org/10.1007/s13369-018-3215-1
Mahdi AHA (2016) Improvement of salt tolerance in Vicia faba (L.) plants by exogenous application of polyamines. Egypt J Agron 38:1–21
Marschner H (1995) Mineral nutrition of higher plants. Academic, London
Matijević L, Romić D, ROmić M, Maurović N, Kondres N (2014) Faba bean (Vicia faba L.) salt stress response under different soil organic matter content. Agric Conspec Sci 7:13–18
McLaughlin MJ, Palmer LT, Tiller KG, Beech TA, Smart MK (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
Metwali EMR, Abdelmoneim TS, Bakheit MA, Kadasa NMS (2015) Alleviation of salinity stress in faba bean (Vicia faba L.) plants by inoculation with plant growth promoting rhizobacteria (PGPR). Plant Omics J 8:449–460
Muofhe ML, Dakora FD (2000) Modification of rhizosphere pH by the symbiotic legume Aspalathus linearis growing in a sandy acidic soil Aust. J Plant Physiol 27:1169–1173. https://doi.org/10.1071/PP99198
Nouairi I, Methanni K, Mhadhbi H, Jebara M (2012) Effects of CaCl2 pretreatment on antioxidant enzyme and leaf lipid content of faba bean (Vicia faba L.) seedlings under cadmium stress. Plant Growth Regul 68(1):37–47. https://doi.org/10.1007/s10725-012-9691-5
Nye PH (1981) Changes of pH across the rhizosphere induced by roots. Plant Soil 61:7–26
Nyquist J, Greger M (2009) Response of two wetland plant species to Cd exposure at low and neutral pH. Environ Exp Bot 65:417–424. https://doi.org/10.1016/j.envexpbot.2008.11.011
Ozkutlu F, Turan M, Öztürkmen AL (2013) Soil salinity increase Cd uptake of lettuce (Lattuca Sativa L.). ProEnvironment 6:389–395
Paalman MAA, van der Weijden CH, Loch JPG (1994) Sorption of cadmium on suspended matter under estuarine conditions: competition and complexation with major seawater ions. Water Air Soil Pollut 73:49–60. https://doi.org/10.1007/BF00477975
Parvez S, Abbas G, Shahid M, Amjad M, Hussain M, Asad SA, Imran M, Naeem MA (2020) Effect of salinity on physiological, biochemical and photostabilizing attributes of two genotypes of quinoa (Chenopodium quinoa Willd.) exposed to arsenic stress. Ecotoxicol Environ Saf 187:109814. https://doi.org/10.1016/j.ecoenv.2019.109814
Pinto AP, Simões I, Mota AM (2008) Cadmium impact on root exudates of sorghum and maize plants: a speciation study. J Plant Nutr 31:1746–1755. https://doi.org/10.1080/01904160802324829
Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, Del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52(364):2115–2126. https://doi.org/10.1093/jexbot/52.364.2115
Sauvé S, Hendershot W, Allen HE (2000) Solid-solution partitioning of metals in contaminated soils: dependence on pH, total metal burden, and organic matter. Environ Sci Technol 34:1125–1131. https://doi.org/10.1021/es9907764
Smolders E, McLaughlin MJ (1996) Chloride increases Cd uptake in Swiss chard in a resin-buffered nutrient solution. Soil Sci Soc Am J 60:1443–1447. https://doi.org/10.2136/sssaj1996.03615995006000050022x
Souguir D, EL Ferjani E, Ledoigt G, Goupil P (2011) Sequential effects of cadmium on genotoxicity and lipoperoxidation in Vicia faba roots. Ecotoxicology 20:329–336. https://doi.org/10.1007/s10646-010-0582-0
Souguir D, EL Ferjani E, Ledoigt G, Goupil P (2013) Transcript accumulation of stress related genes in Vicia faba roots under a short exposure to cadmium. Plant Biosyst 149:280–288. https://doi.org/10.1080/11263504.2013.822432
Souguir D, Abd-Alla HI, Hörmann G, Hachicha M (2018) Chromosomal and nuclear alterations in the root-tip cells of Vicia faba induced by sodium chloride. Water Environ Res 90:164–171. https://doi.org/10.2175/106143017X14902968254827
Tavakkoli E, Rengasamy P, McDonald GK (2010) High concentrations of Na+ and Cl− ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress. J Exp Bot 61:4449–4459. https://doi.org/10.1093/jxb/erq251
Zeng F, Chen S, Miao Y, Wu F, Zhang G (2008) Changes of organic acid exudation and rhizosphere pH in rice plants under chromium stress. Environ Pollut 155:284–289. https://doi.org/10.1016/j.envpol.2007.11.019
Zhang ZH, Tang C, Rengel Z (2005) Salt dynamics in rhizosphere of Puccinellia ciliata Bor. In a loamy soil. Pedosphere 15:784–791
Zhang S, Zhang H, Qin R, Jiang W, Liu D (2009) Cadmium induction of lipid peroxidation and effects on root tip cells and antioxidant enzyme activities in Vicia faba L. Ecotoxicology 18:814–823. https://doi.org/10.1007/s10646-009-0324-3
Zhou LL, Cao J, Zhang FS, Li L (2009) Rhizosphere acidification of faba bean, soybean and maize. Sci Total Environ 407:4356–4362. https://doi.org/10.1016/j.scitotenv.2009.02.006
Zhou Q, Liu ZD, Liu Y, Jiang J, Xu RK (2016) Relative abundance of chemical forms of Cu(II) and Cd(II) on soybean roots as influenced by pH, cations and organic acids. Sci Rep 6:36373. https://doi.org/10.1038/srep36373
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The authors are grateful to “The Ministry of Higher Education and Scientific Research” (MESRS, Tunisia) and to “The German Ministry of Research and Education” (BMBF, Germany) for supporting this work.
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Souguir, D., Hörmann, G. & Hachicha, M. Salinity decreases cadmium accumulation in Vicia faba. Environ Sci Pollut Res 27, 18893–18901 (2020). https://doi.org/10.1007/s11356-020-08396-x
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DOI: https://doi.org/10.1007/s11356-020-08396-x