Alleviation of cadmium toxicity in cucumber (Cucumis sativus) seedlings by the application of selenium

Hongyan Sun, Xiaoyun Wang, Yuna Wang, Yiying Wei, Guohui Wang

Abstract


In the present study, the role of selenium in cadmium toxicity was investigated in cucumber seedlings by hydroponic experiments. The application of Se for cucumber exposed to Cd significantly reduced Cd accumulation in all tissues, elevated Cd-depressed chlorophyll content, and improved photosynthetic performance. External Se significantly reduced ·OH, H2O2 and malondialdehyde content. Exogenous Se balanced Cd-depressed elements (e.g., Se enhanced Cd-induced decreases in root Zn, leaf/stem/root Mn concentrations) and carbohydrate contents. External Se also significantly decreased the Cd-induced increases in Na+K+-, Ca2+Mg2+- and total ATPase activities, which recovered almost to control level. Results indicate that application of Se can alleviate Cd toxicity in cucumber seedlings by reducing Cd uptake and reactive oxygen species (ROS) accumulation, moreover protecting photosynthetic machinery from damaging, balancing elements and carbohydrate contents, and improving ATPase activities in cucumber.


Keywords


alleviating effects; photosynthetic performance; ATPase

Full Text:

PDF HTML XML

References


Ahmed IM, Cao FB, Zhang M, Chen XH, Zhang GP, Wu FB, 2013. Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys. PLoS One 8: e77869. http://dx.doi.org/10.1371/journal.pone.0077869

Asgher M, Khan MIR, Anjum NA, Khan NA, 2015. Minimising toxicity of cadmium in plants—Role of plant growth regulators. Protoplasma 252: 399-413. http://dx.doi.org/10.1007/s00709-014-0710-4

Babani F, Lichtenthaler HK, 1996. Light-induced and age-dependent development of chloroplasts in etiolated barley leaves as visualized by determination of photosynthetic pigments, CO2 assimilation rates and different kinds of chlorophyll fluorescence ratios. J Plant Physiol 148: 555-566. http://dx.doi.org/10.1016/S0176-1617(96)80075-7

Bañuelos GS, Fakra SC, Walse SS, Marcus MA, Yang SI, Pickering IJ, Pilon-Smits EAH, Freeman JL, 2011. Selenium accumulation, distribution, and speciation in spineless prickly pear cactus: a drought- and salt-tolerant, selenium enriched nutraceutical fruit crop for biofortified foods. Plant Physiol 155: 315-327. http://dx.doi.org/10.1104/pp.110.162867

Breznik B, Germ M, Gaberscik A, Kreft I, 2005. Combined effect of elevated UV-B radiation and the addition of selenium on common (Fagopyrum esculenta Moench) and tartary [Fagopyrum tataricum (L.) Gaertn.] buckwheat. Photosynthetica 43: 583-589. http://dx.doi.org/10.1007/s11099-005-0091-1

Bur T, Probst A, Bianco A, Gandois L, Crouau Y, 2010. Cadmium critical concentrations in natural soils by assessing Collembola mortality, reproduction and growth. Ecotox Environ Safe 73: 415-422. http://dx.doi.org/10.1016/j.ecoenv.2009.10.010

Buysse J, Merckx R, 1993. An improved colorimetric method to quantify sugar content of plant tissue. J Exp Bot 44: 1627-1629. http://dx.doi.org/10.1093/jxb/44.10.1627

Cai Y, Cao F, Heng W, Zhang GP, Wu FB, 2011. Modulation of exogenous glutathione in phytochelatins and photosynthetic performance against Cd stress in the two rice genotypes differing in Cd tolerance. Biol Trace Elem Res 143: 1159-1173. http://dx.doi.org/10.1007/s12011-010-8929-1

Cao FB, Chen F, Sun HY, Zhang GP, Chen ZH, Wu FB, 2014a. Genome-wide transcriptome and functional analysis of two contrasting genotypes reveals key genes for cadmium tolerance in barley. BMC Genomics 15: 611. http://dx.doi.org/10.1186/1471-2164-15-611

Cao FB, Wang RF, Cheng WD, Zeng FR, Ahmed IM, Hu XN, Zhang GP, Wu FB, 2014b. Genotypic and environmental variation in cadmium, chromium, lead and copper in rice and approaches for reducing the accumulation. Sci Total Environ 496: 275-281. http://dx.doi.org/10.1016/j.scitotenv.2014.07.064

Chen F, Wang F, Wu FB, Mao WH, Zhang GP, Zhou MX, 2010. Modulation of exogenous glutathione in antioxidant defense system against Cd stress in the two barley genotypes differing in Cd tolerance. Plant Physiol Biochem 48: 663-672. http://dx.doi.org/10.1016/j.plaphy.2010.05.001

Ding F, Wang X, Shi Q, Wang M, Yang F, Gao Q, 2008. Exogenous nitric oxide alleviated the inhibition of photosynthesis and antioxidant enzyme activities in iron-deficient Chinese cabbage (Brassica chinesis L.). Agr Sci China 7: 168-179. http://dx.doi.org/10.1016/S1671-2927(08)60036-X

Duby G, Boutry M, 2009. The plant plasma membrane proton pump ATPase: A highly regulated P-type ATPase with multiple physiological roles. Pflueg Arch Eur J Physiol 457: 645-655. http://dx.doi.org/10.1007/s00424-008-0457-x

Ebbs S, Leonard W, 2001. Alteration of selenium transport and volatilization in barley (Hordeum vulgare) by arsenic. J. Plant Physiol 158: 1231-1233. http://dx.doi.org/10.1078/0176-1617-00440

Feng J, Shi Q, Wang X, Wei M, Yang F, Xu H, 2010. Silicon supplementation ameliorated the inhibition of photosynthesis and nitrate metabolism by cadmium (Cd) toxicity in Cucumis sativus L. Sci Hortic 123: 521-530. http://dx.doi.org/10.1016/j.scienta.2009.10.013

Feng R, Wei C, Tu S, 2013. The roles of selenium in protecting plants against abiotic stresses. Environ Exp Bot 87: 58-68. http://dx.doi.org/10.1016/j.envexpbot.2012.09.002

Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP, 2012. Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83: 33-46. http://dx.doi.org/10.1016/j.envexpbot.2012.04.006

Haghighi M, da Silva JAT, 2016. Influence of selenium on cadmium toxicity in cucumber (Cucumis sativus cv. 4200) at an early growth stage in a hydroponic system. Commun Soil Sci Plan 47: 142-155. http://dx.doi.org/10.1080/00103624.2015.1109650

Hartikainen H, 2005. Biogeochemistry of selenium and its impact on food chain quality and human health. J Trace Elem Med Biol 18: 309-318. http://dx.doi.org/10.1016/j.jtemb.2005.02.009

Hawrylak-Nowaka B, Dreslerb S, Wójcik M, 2014. Selenium affects physiological parameters and phytochelatins accumulation in cucumber (Cucumis sativus L.) plants grown under cadmium exposure. Sci Hortic 172: 10-18. http://dx.doi.org/10.1016/j.scienta.2014.03.040

He PP, Lv XZ, Wang GY, 2004. Effects of Se and Zn supplementation on the antagonism against Pb and Cd in vegetables. Environ Int 30: 167-172. http://dx.doi.org/10.1016/S0160-4120(03)00167-3

Hopper L, Parker DR, 1999. Plant availability of selenite and selenate as influenced by the competing ions phosphate and sulfate. Plant Soil 210: 199-207. http://dx.doi.org/10.1023/A:1004639906245

Janicka-Russak M, Kabała K, Burzynski M, 2012. Different effect of cadmium and copper on H+-ATPase activity in plasma membrane vesicles from Cucumis sativus roots. J Exp Bot 63: 4133-4142. http://dx.doi.org/10.1093/jxb/ers097

Kao WY, Tsai TT, Shin CN, 2003. Photosynthetic gas exchange and chlorophyll a fluorescence of three wild soybean species in response to NaCl treatments. Photosynthetica 41: 415-419. http://dx.doi.org/10.1023/B:PHOT.0000015466.22288.23

Kitajima M, Butler WL, 1975. Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376: 105-115. http://dx.doi.org/10.1016/0005-2728(75)90209-1

Kramer DM, Johnson G, Kiirats O, Edwards GE, 2004. New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79: 209-218. http://dx.doi.org/10.1023/B:PRES.0000015391.99477.0d

Li Mei, Wang Guirong, Li Junying, Cao Fangbin, 2016. Foliar application of betaine alleviates cadmium toxicity in maize seedlings. Acta Physiol Plant 38: 95. http://dx.doi.org/10.1007/s11738-016-2116-8

Lichtenthale H, Wellburn A, 1983. Determinations of total carotenoids and chlorophylls a and b of leaf extract in different solvents. Biochem Soc Trans 11: 591-592. http://dx.doi.org/10.1042/bst0110591

Lin L, Zhou WH, Dai HX, Cao FB, Zhang GP, Wu FB, 2012. Selenium reduces cadmium uptake and mitigates cadmium toxicity in rice. J Hazard Mater 235: 343-351. http://dx.doi.org/10.1016/j.jhazmat.2012.08.012

Liu WX, Shang SH, Feng X, Zhang GP, Wu FB, 2015. Modulation of exogenous selenium in cadmium-induced changes in antioxidative metabolism, cadmium uptake, and photosynthetic performance in the 2 tobacco genotypes differing in cadmium tolerance. Environ Toxicol Chem 34: 92-99. http://dx.doi.org/10.1002/etc.2760

Loganathan P, Hedley MJ, 1997. Downward movement of cadmium and phosphorus from phosphatic fertilisers in a pasture soil in New Zealand. Environ Pollut 95: 319-324. http://dx.doi.org/10.1016/S0269-7491(96)00142-X

Mateos-Naranjo E, Redondo-Gómez S, Cambrollé J, Figueroa ME, 2008. Growth and photosynthetic responses to copper stress of an invasive cordgrass, Spartina densiflora. Mar Environ Res 66: 459-466. http://dx.doi.org/10.1016/j.marenvres.2008.07.007

Muñoz AHS, Wrobel K, Corona JFG, Wrobel K, 2007. The protective effect of selenium inorganic forms against cadmium and silver toxicity in mycelia of Pleurotus ostreatus. Mycol Res 5: 626-632.

Pedrero Z, Madrid Y, Hartikainen H, Cámara C, 2008. Protective effect of selenium in broccoli (Brassica oleracea) plants subjected to cadmium exposure. J Agric Food Chem 56: 266-271. http://dx.doi.org/10.1021/jf072266w

Saidi I, Chtourou Y, Djebali W, 2014. Selenium alleviates cadmium toxicity by preventing oxidative stress in sunflower (Helianthus annuus) seedlings. J Plant Physiol 171: 85-91. http://dx.doi.org/10.1016/j.jplph.2013.09.024

Sun HY, Wang XY, Dai HX, Zhang GP, Wu FB, 2013. Effect of exogenous glutathione and selenium on cadmium-induced changes in cadmium and mineral concentrations and antioxidative metabolism in maize seedlings. Asian J Chem 25: 2970.

Terry N, Zayed AM, de Souza MP, Tarun AS, 2000. Selenium in higher plants. Annu Rev Plant Physiol Plant Mol Biol 51: 401-432. http://dx.doi.org/10.1146/annurev.arplant.51.1.401

Thangavel P, Sulthana AS, Subburam V, 1999. Interactive effect of selenium and mercury on the restoration potential of leaves of the medicinal plant, Portulaca oleracea Linn. Sci Total Environ 243-244: 1-8. http://dx.doi.org/10.1016/S0048-9697(98)00181-8

Thomson CD, 2004. Assesment of requirements for selenium and adequacy of selenium status: a review. Eur J Clin Nutr 58: 391-402. http://dx.doi.org/10.1038/sj.ejcn.1601800

Uraguchi S, Fujiwara T, 2012. Cadmium transport and tolerance in rice: perspectives for reducing grain cadmium accumulation. Rice 5: 5. http://dx.doi.org/10.1186/1939-8433-5-5

Wang F, Chen F, Cai Y, Zhang GP, Wu FB, 2011. Modulation of exogenous glutathione in ultrastructure and photosynthetic performance against Cd stress in the two barley genotypes differing in Cd tolerance. Biol Trace Elem Res 144: 1275-1288. http://dx.doi.org/10.1007/s12011-011-9121-y

Wu FB, Zhang GP, Dominy P, 2003. Four barley genotypes respond differently to cadmium: lipid peroxidation and activities of antioxidant capacity. Environ Exp Bot 50: 67-78. http://dx.doi.org/10.1016/S0098-8472(02)00113-2

Wu FB, Dong J, Qian QQ, Zhang GP, 2005. Subcellular distribution and chemical form of Cd and Cd-Zn interaction in different barley genotypes. Chemosphere 60: 1437-1446. http://dx.doi.org/10.1016/j.chemosphere.2005.01.071

Yathavakilla S, Caruso J, 2007. A study of Se-Hg antagonism in Glycine max (soybean) roots by size exclusion and reversed phase HPLC-ICPMS. Anal Bioanal Chem 389: 715-723. http://dx.doi.org/10.1007/s00216-007-1458-x

Yu J, Huang L, Hu W, Zhou Y, Mao W, Ye S, Nogues S, 2004. A role for brassinosteroids in the regulation of photosynthesis in Cucumis sativus. J Exp Bot 55: 1135-1143. http://dx.doi.org/10.1093/jxb/erh124

Zhang GP, Fukami M, Sekimoto H, 2002. Influence of cadmium on mineral concentrations and yield components in wheat genotypes differing in Cd tolerance at seedling stage. Field Crop Res 77: 93-98. http://dx.doi.org/10.1016/S0378-4290(02)00061-8

Zhang M, Tang S, Huang X, Zhang F, Pang Y, Huang Q, Yi Q, 2014. Selenium uptake, dynamic changes in selenium content and its influence on photosynthesis and chlorophyll fluorescence in rice (Oryza sativa L.). Environ Exp Bot 107: 39-45. http://dx.doi.org/10.1016/j.envexpbot.2014.05.005

Zhang M, Jin ZQ, Zhao J, Zhang GP, Wu FB, 2015. Physiological and biochemical responses to drought stress in cultivated and Tibetan wild barley. Plant Growth Regul 75: 567-574. http://dx.doi.org/10.1007/s10725-014-0022-x




DOI: 10.5424/sjar/2016144-10008