Effect of NaCl, copper and cadmium ions on halophytes with different types of salt resistance: accumulation, physiological and biochemical reactions
Viktor Nesterov
A D , Elena Bogdanova A , Olga Makurina B , Svetlana Rozina C and Olga Rozentsvet A
+ Author Affiliations
- Author Affiliations
A Samara Federal Research Scientific Center RAS, Institute of Ecology of Volga River Basin RAS, 10 Komzin St., Togliatti, 445003, Russia.
B Samara National Research University, 34 Moskovskoye shosse, Samara, 443086, Russia.
C Medical University Reaviz, 227 Chapaevskaya St., Samara, 443001, Russia.
D Corresponding author. Email: nesvik1@mail.ru
Functional Plant Biology 48(10) 1053-1061 https://doi.org/10.1071/FP21083
Submitted: 19 March 2021 Accepted: 23 June 2021 Published: 23 July 2021
Abstract
The capacities of the euhalophyte SaLi-Cornia perennans Willd. and glycohalophyte Artemisia santonica L. to accumulate NaCl, Cu, and Cd, as well as their physiological and biochemical responses to these compounds, was investigated. Seeds were germinated in distilled water for 1–3 days and then sown in containers with sand. Plants were watered with Robinson’s nutrient solution. After 3 months, plants were divided into two groups: experimental and control. In the experimental group, soil was treated with 1M NaCl, 10 mM Cu(NO3)2, and 10 mM Cd(NO3)2 for 24 h. The exposure to high concentration of NaCl in the experiment did not affect the baseline level of Na, which was twice as high in S. perennans as in A. santonica. Plant exposure to Cu and Cd caused their accumulation in the aboveground parts of both species. The accumulation capacity of the euhalophyte was many times higher than that of the glycohalophyte. We analysed functional parameters of leaves by measuring photosynthetic pigments, structural parameters of membranes by assessing the lipid profile, and the balance of pro/antioxidant processes. Using data on changes in several biochemical parameters, the sensitivity of the two different halophytes to metal ions was as follows: for S. perennans – Cu > Na > Cd; for A. santonica – Na > Cu > Cd. Our findings suggest that S. perennans can be used for heavy metal extraction from soil in phytoremediation, whereas A. santonica will be more effective for greening of polluted territories.
Keywords: salt accumulation, copper, cadmium, euhalophytes, glycohalophytes, phytoremediation, heavy metals.
References
Ahmed HAI, Shabala L, Shabala S (2021) Understanding the mechanistic basis of adaptation of perennial Sarcocornia quinqueflora species to soil salinity. Physiologia Plantarum| Understanding the mechanistic basis of adaptation of perennial Sarcocornia quinqueflora species to soil salinity.Crossref | GoogleScholarGoogle Scholar | 33826749PubMed |
Amari T, Ghnaya T, Abdelly C (2017) Nickel, cadmium and lead phytotoxicity and potential of halophytic plants in heavy metal extraction. South African Journal of Botany 111, 99–110.
| Nickel, cadmium and lead phytotoxicity and potential of halophytic plants in heavy metal extraction.Crossref | GoogleScholarGoogle Scholar |
Aravind P, Prasad MNV (2003) Zinc alleviates cadmium-induced oxidative stress in Ceratophyllum demersum L: a free-floating freshwater macrophyte. Plant Physiology and Biochemistry 41, 391–397.
| Zinc alleviates cadmium-induced oxidative stress in Ceratophyllum demersum L: a free-floating freshwater macrophyte.Crossref | GoogleScholarGoogle Scholar |
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911–917.
| A rapid method of total lipid extraction and purification.Crossref | GoogleScholarGoogle Scholar | 13671378PubMed |
Boyarkin AN (1951) Rapid method for determining peroxidase activity. Biochemistry 16, 352–355. [In Russian]
Cambrollé J, Redondo-Gymez S, Mateos-Naranjo E, Figueroa ME (2008) Comparison of the role of two Spartina species in terms of phytostabilization and bioaccumulation of metals in the estuarine sediment. Marine Pollution Bulletin 56, 2037–2042.
| Comparison of the role of two Spartina species in terms of phytostabilization and bioaccumulation of metals in the estuarine sediment.Crossref | GoogleScholarGoogle Scholar | 18805558PubMed |
Cambrollé J, Mancilla-Leyton JM, Munoz-Valles S, Luque T, Figueroa ME (2012) Zinc tolerance and accumulation in the salt-marsh shrub Halimione portulacoides. Chemosphere 86, 867–874.
| Zinc tolerance and accumulation in the salt-marsh shrub Halimione portulacoides.Crossref | GoogleScholarGoogle Scholar | 22099539PubMed |
Clemente R, Walker DJ, Pardo T, Martinez-Fernandez D, Bernal MP (2012) The use of a halophytic plant species and organic amendments for the remediation of a trace elements-contaminated soil under semiarid conditions. Journal of Hazardous Materials 223–224, 63–71.
| The use of a halophytic plant species and organic amendments for the remediation of a trace elements-contaminated soil under semiarid conditions.Crossref | GoogleScholarGoogle Scholar | 22595543PubMed |
De Souza MM, Mendes CR, Doncato KB, Badiale-Furlong E, Costa CS (2018) Growth, phenolics, photosynthetic pigments, and antioxidant response of two new genotypes of sea asparagus (Salicornia neei Lag.) to salinity under greenhouse and field conditions. Agriculture 8, 115
| Growth, phenolics, photosynthetic pigments, and antioxidant response of two new genotypes of sea asparagus (Salicornia neei Lag.) to salinity under greenhouse and field conditions.Crossref | GoogleScholarGoogle Scholar |
Devi S, Nandwal AS, Angrish R, Arya SS, Kumar N, Sharma SK (2016) Phytoremediation potential of some halophytic species for soil salinity. International Journal of Phytoremediation 18, 693–696.
| Phytoremediation potential of some halophytic species for soil salinity.Crossref | GoogleScholarGoogle Scholar | 26684673PubMed |
Eid MA (2011) Halophytic plants for phytoremediation of heavy metals contaminated. Soil Science Society of America Journal 7, 377–382.
Ermakov AI, Arasimovich VV, Smirnova-Ikonnikova MI, Yarosh NP, Lukovnikova GA (1972) Biochemical research methods of plants. Kolos, Leningrad (in Russian).
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
| Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar |
Gajewska E, Sklodowska M (2007) Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves. Biometals 20, 27–36.
| Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves.Crossref | GoogleScholarGoogle Scholar | 16752220PubMed |
Gopal R, Rizvi AH (2008) Excess lead alters growth, metabolism and translocation of certain nutrients in radish. Chemosphere 70, 1539–1544.
| Excess lead alters growth, metabolism and translocation of certain nutrients in radish.Crossref | GoogleScholarGoogle Scholar | 17923149PubMed |
Guarino F, Ruiz KB, Castiglione S, Cicatelli A, Biondi S (2020) The combined effect of Cr(III) and NaCl determines changes in metal uptake, nutrient content, and gene expression in quinoa (Chenopodium quinoa Willd.). Ecotoxicology and Environmental Safety 193, 110345
| The combined effect of Cr(III) and NaCl determines changes in metal uptake, nutrient content, and gene expression in quinoa (Chenopodium quinoa Willd.).Crossref | GoogleScholarGoogle Scholar | 32092578PubMed |
Hameed A, Khan MA (2011) Halophytes: biology and economic potentials. Karachi University Journal of Science 39, 40–44.
Han R-M, Lefevre I, Ruan C-J, Qin P, Lutts S (2012) NaCl differently interferes with Cd and Zn toxicities in the wetland halophyte species Kosteletzkya virginica (L.) Presl. Plant Growth Regulation 68, 97–109.
| NaCl differently interferes with Cd and Zn toxicities in the wetland halophyte species Kosteletzkya virginica (L.) Presl.Crossref | GoogleScholarGoogle Scholar |
Hasegawa H, Abdullah Al Mamun M, Tsukagoshi Y, Ishii K, Sawai H, Begume ZA, Asami MS, Maki T, Rahman IMM (2019) Chelator-assisted washing for the extraction of lead, copper, and zinc from contaminated soils: a remediation approach. Applied Geochemistry 109, 104397
| Chelator-assisted washing for the extraction of lead, copper, and zinc from contaminated soils: a remediation approach.Crossref | GoogleScholarGoogle Scholar |
Huang G-T, Ma S-L, Bai L-P, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo ZF (2012) Signal transduction during cold, salt, and drought stresses in plants. Molecular Biology Reports 39, 969–987.
| Signal transduction during cold, salt, and drought stresses in plants.Crossref | GoogleScholarGoogle Scholar | 21573796PubMed |
Hussain B, Ashraf MN, Rahman S-U, Abbas A, Lia J, Farooq M (2021) Cadmium stress in paddy elds: effects of soil conditions and remediation strategies. The Science of the Total Environment 754, 142188
| Cadmium stress in paddy elds: effects of soil conditions and remediation strategies.Crossref | GoogleScholarGoogle Scholar | 33254942PubMed |
Kachout SS, Mansoura AB, Mechergui R, Leclerc JC, Rejeb MN, Ouerghi Z (2012) Accumulation of Cu, Pb, Ni and Zn in the halophyte plant Atriplex grown on polluted soil. Journal of the Science of Food and Agriculture 92, 336–342.
| Accumulation of Cu, Pb, Ni and Zn in the halophyte plant Atriplex grown on polluted soil.Crossref | GoogleScholarGoogle Scholar | 21935956PubMed |
Kadukova J, Manousaki E, Kalogerakis N (2008) Pb and Cd accumulation and phyto-excretion by salt cedar (Tamarix smyrnensis Bunge). International Journal of Phytoremediation 10, 31–46.
| Pb and Cd accumulation and phyto-excretion by salt cedar (Tamarix smyrnensis Bunge).Crossref | GoogleScholarGoogle Scholar | 18709930PubMed |
Kates M (1975) Techniques of lipidology: isolation, analysis and identification of lipids. (Elsevier: Amsterdam, New York)
Korolyuk MA, Ivanova LI, Mayorova IG, Tokarev VE (1988) Method for determination of catalase activity. (Laboratory work) [in Russian]
Labudda M (2013) Lipid peroxidation as a biochemical marker for oxidative stress during drought. An effective tool for plant breeding, Warsaw, Poland, e-wydawnictwo.eu.
Lichtenthaler HK (1987) Chlorophylls and carotenoids pigments of photosynthetic biomembranes. ‘Methods in Enzymology’ (Eds R Dous, L Packer) (Academic Press Inc.:New York)
Lin AJ, Zhang XH, Chen MM, Qing C (2007) Oxidative stress and DNA damage induced by cadmium accumulation. Journal of Environmental Sciences (China) 19, 596–602.
| Oxidative stress and DNA damage induced by cadmium accumulation.Crossref | GoogleScholarGoogle Scholar |
Liu X, Yang C, Zhang L, Li L, Liu S, Yu J, You L, Zhou D, Xia C, Zhao J, Wu H (2011) Metabolic profiling of cadmium-induced effects in one pioneer intertidal halophyte Suaeda salsa by NMR-based metabolomics. Ecotoxicology (London, England) 20, 1422–1431.
| Metabolic profiling of cadmium-induced effects in one pioneer intertidal halophyte Suaeda salsa by NMR-based metabolomics.Crossref | GoogleScholarGoogle Scholar |
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry 193, 265–275.
| Protein measurement with the Folin phenol reagent.Crossref | GoogleScholarGoogle Scholar | 14907713PubMed |
Manousaki E, Kalogerakis N (2011) Halophytes-an emerging trend in phytoremediation. International Journal of Phytoremediation 13, 959–969.
| Halophytes-an emerging trend in phytoremediation.Crossref | GoogleScholarGoogle Scholar | 21972564PubMed |
Manousaki E, Kadukova J, Papadantonakis N, Kalogerakis N (2008) Phytoextraction and phytoexcretion of Cd by the leaves of Tamarix smyrnensis growing on contaminated non-saline and saline soils. Environmental Research 106, 326–332.
| Phytoextraction and phytoexcretion of Cd by the leaves of Tamarix smyrnensis growing on contaminated non-saline and saline soils.Crossref | GoogleScholarGoogle Scholar | 17543928PubMed |
Mishra S, Srivastava S, Tripathi RD, Kumar R, Seth CS, Gupta DK (2006) Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 65, 1027–1039.
| Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation.Crossref | GoogleScholarGoogle Scholar | 16682069PubMed |
Mittler R (2017) ROS Are Good. Trends in Plant Science 22, 11–19.
| ROS Are Good.Crossref | GoogleScholarGoogle Scholar | 27666517PubMed |
Mueller MJ (2004) Archetype signals in plants: the phytoprostanes. Current Opinion in Plant Biology 7, 441–448.
| Archetype signals in plants: the phytoprostanes.Crossref | GoogleScholarGoogle Scholar | 15231268PubMed |
Nanjo Y, Nouri MZ, Komatsu S (2011) Quantitative proteomic analyses of crop seedlings subjected to stress conditions; a commentary. Phytochemistry 72, 1263–1272.
| Quantitative proteomic analyses of crop seedlings subjected to stress conditions; a commentary.Crossref | GoogleScholarGoogle Scholar | 21084103PubMed |
Noctor G, Foyer CH (1998) A re-evaluation of the ATP: NADPH budget during C3 photosynthesis. A contribution from nitrate assimilation and its associated respiratory activity? Journal of Experimental Botany 49, 1895–1908.
| A re-evaluation of the ATP: NADPH budget during C3 photosynthesis. A contribution from nitrate assimilation and its associated respiratory activity?Crossref | GoogleScholarGoogle Scholar |
Pandey N, Sharma CP (2002) Effect of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage. Plant Science 163, 753–758.
| Effect of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage.Crossref | GoogleScholarGoogle Scholar |
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants. Ecotoxicology and Environmental Safety 60, 324–349.
| Salt tolerance and salinity effects on plants.Crossref | GoogleScholarGoogle Scholar | 15590011PubMed |
Robinson SP, Downton WJS (1984) Potassium, sodium, and chloride content of isolated intact chloroplasts in relation to ionic compartmentation in leaves. Archives of Biochemistry and Biophysics 228, 197–206.
| Potassium, sodium, and chloride content of isolated intact chloroplasts in relation to ionic compartmentation in leaves.Crossref | GoogleScholarGoogle Scholar | 6696431PubMed |
Rozentsvet OA, Nesterov VN, Sinyutina NF (2012) The effect of copper ions on the lipid composition of subcellular membranes in Hydrilla verticillata. Chemosphere 89, 108–113.
| The effect of copper ions on the lipid composition of subcellular membranes in Hydrilla verticillata.Crossref | GoogleScholarGoogle Scholar | 22608709PubMed |
Rozentsvet OA, Bogdanova ES, Ivanova LA, Ivanov LA, Tabalenkova GN, Zakhozhiy IG, Nesterov VN (2016) Structural and functional organization of the photosynthetic apparatus in halophytes with different strategies of salt tolerance. Photosynthetica 54, 405–413.
| Structural and functional organization of the photosynthetic apparatus in halophytes with different strategies of salt tolerance.Crossref | GoogleScholarGoogle Scholar |
Rozentsvet OA, Nesterov VN, Bogdanova ES (2017) Structural, physiological and biochemical aspects of salinity tolerance of halophytes. Russian Journal of Plant Physiology 64, 464–477.
| Structural, physiological and biochemical aspects of salinity tolerance of halophytes.Crossref | GoogleScholarGoogle Scholar |
Sghaier DB, Duarte B, Bankaji I, Cacador I, Sleimi N (2015) Growth, chlorophyll fluorescence and mineral nutrition in the halophyte Tamarix gallica cultivated in combined stress conditions: Arsenic and NaCl. Journal of Photochemistry and Photobiology. B, Biology 149, 204–214.
| Growth, chlorophyll fluorescence and mineral nutrition in the halophyte Tamarix gallica cultivated in combined stress conditions: Arsenic and NaCl.Crossref | GoogleScholarGoogle Scholar | 26093232PubMed |
Shabala S, Bose J, Hedrich R (2014) Salt bladders: do they matter? Trends in Plant Science 19, 687–691.
| Salt bladders: do they matter?Crossref | GoogleScholarGoogle Scholar | 25361704PubMed |
Sharma A, Gontia I, Agarwal PK, Jha B (2010) Accumulation of heavy metals and its biochemical responses in Salicornia brachiata, an extreme halophyte. Marine Biology Research 6, 511–518.
| Accumulation of heavy metals and its biochemical responses in Salicornia brachiata, an extreme halophyte.Crossref | GoogleScholarGoogle Scholar |
Shevyakova NI, Netronina IA, Aronova EE, Kuznetsov VV (2003) Compartmentation of cadmium and iron in Mesembryanthemum crystallinum plants during the adaptation to cadmium stress. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 50, 678–685.
| Compartmentation of cadmium and iron in Mesembryanthemum crystallinum plants during the adaptation to cadmium stress.Crossref | GoogleScholarGoogle Scholar |
Song J, Wang B (2015) Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Annals of Botany 115, 541–553.
| Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model.Crossref | GoogleScholarGoogle Scholar | 25288631PubMed |
Srivastava AK, Bhargava P, Rai LC (2005) Salinity and copper-induced oxidative damage and changes in antioxidative defense system of Anabaena doliolum. World Journal of Microbiology & Biotechnology 21, 1291–1298.
| Salinity and copper-induced oxidative damage and changes in antioxidative defense system of Anabaena doliolum.Crossref | GoogleScholarGoogle Scholar |
Taranto F, Pasqualone A, Mangini G, Tripodi P, Miazzi MM, Pavan S, Montemurro C (2017) Polyphenol oxidases in crops: biochemical, physiological and genetic aspects. International Journal of Molecular Sciences 18, 377
| Polyphenol oxidases in crops: biochemical, physiological and genetic aspects.Crossref | GoogleScholarGoogle Scholar |
Titov AF, Talanova VV, Kaznina NM, Laidinen GF (2007) Plant resistance to heavy metals. (Karelian Scientific Center of the Russian Academy of Sciences: Petrozavodsk) [In Russian]
Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Science 164, 645–655.
| Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants.Crossref | GoogleScholarGoogle Scholar |
Zhu MH, Ding YS, Zheng DC, Tao P, Ji YX, Cui Y, Gong WM, Ding DW (2005) Accumulation and tolerance of Cu, Zn, Pb and Cd in plant Suaeda heteroptera Kitag. in tideland. Haiyang Huanjiang Kexue 24, 13–16.
Zulfiqar U, Farooq M, Hussain S, Maqsood M, Hussain M, Ishfaq M, Ahmad M, Anjum MZ (2019) Lead toxicity in plants: impacts and remediation. Journal of Environmental Management 250, 109557
| Lead toxicity in plants: impacts and remediation.Crossref | GoogleScholarGoogle Scholar | 31545179PubMed |
