Effect of plant growth regulators, calcium and citric acid on copper toxicity in pea seedlings

References

• Ahmad, P., G. Nabi, and M. Ashraf. 2011. Cadmium-induced oxidative damage in mustard [Brassica juncea (L.) Czern. & Coss.] plants can be alleviated by salicylic acid. South African Journal of Botany 77:36–44. doi: 10.1016/j.sajb.2010.05.003.
   Web of Science ®Google Scholar
• Ahmad, P., M. Sarwat, N. A. Bhat, M. R. Wani, A. G. Kazi, and L. S. P. Tran. 2015. Alleviation of cadmium toxicity in Brassica juncea L. (Czern. &Coss.) by calcium application involves various physiological and biochemical strategies. Plos One 10:e0114571. doi: 10.1371/journal.pone.0114571.
   PubMed Web of Science ®Google Scholar
• Airaki, M., M. Leterrier, R. M. Mateos, R. Valderrama, M. Chaki, J. B. Barroso, L. A. Del Río, J. M. Palma, and F. J. Corpas. 2012. Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant, Cell & Environment 35 (2):281–95. doi: 10.1111/j.1365-3040.2011.02310.x.
   PubMed Web of Science ®Google Scholar
• Alaoui-Sossé, B., P. Genet, F. Vinit-Dunand, M. L. Toussaint, D. Epron, and P. M. Badot. 2004. Effect of copper on growth in cucumber plants (Cucumis sativus) and its relationships with carbohydrate accumulation and changes in ion contents. Plant Science 166 (5):1213–8. doi: 10.1016/j.plantsci.2003.12.032.
   Web of Science ®Google Scholar
• Ali, M. A., H. N. Asghar, M. Y. Khan, M. Saleem, M. Naveed, and N. K. Niazi. 2015. Alleviation of nickel-induced stress in mung bean through application of gibberellic acid. International Journal of Agriculture and Biology 17 (5):990–4. doi: 10.17957/IJAB/15.0001.
   Web of Science ®Google Scholar
• Apel, K., and H. Hirt. 2004. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55 (1):373–99. doi: 10.1146/annurev.arplant.55.031903.141701.
   PubMed Web of Science ®Google Scholar
• Bergmeyer, H. U., and E. Bernt. 1974. Malate dehydrogenase in: Methods of enzymatic analysis. eds. H. U. Bergmeyer, pp. 1577–1580. New York: Academic Press Inc.
   Google Scholar
• Bouazizi, H., H. Jouili, and E. Ferjani. 2007. Copper-induced oxidative stress in maize shoots (Zea mays L.): H2O2 accumulation and peroxidases modulation. Acta Biologica Hungarica 58 (2):209–18. doi: 10.1556/ABiol.58.2007.2.7.
   PubMed Web of Science ®Google Scholar
• Borgmann, U., M. Nowierski, and D. G. Dixon. 2005. Effect of major ions on the toxicity of copper to Hyalella azteca and implications for the biotic ligand model. Aquatic Toxicology 73 (3):268–87. doi: 10.1016/j.aquatox.2005.03.017.
   PubMed Web of Science ®Google Scholar
• Bramm, J. 1992. Regulated expression of the calmodulin-related TCH genes in cultured Arabidopsis cells: induction by calcium and heat shock. Proceedings of the National Academy of Sciences of the United States of America 89:3213–3216.
   PubMed Web of Science ®Google Scholar
• Cha, J. Y., J. Y. Kim, I. J. Jung, M. R. Kim, A. Melencion, S. S. Alam, D. J. Yun, S. Y. Lee, M. G. Kim, W. Y. Kim. 2014. NADPH-dependent thioredoxin reductase A (NTRA) confers elevated tolerance to oxidative stress and drought. Plant Physiology and Biochemistry 80:184–91. doi: 10.1016/j.plaphy.2014.04.008.
   PubMed Web of Science ®Google Scholar
• Chaoui, A., and E. El Ferjani. 2013. β-Estradiol protects embryo growth from heavy metal toxicity in germinating lentil seeds. Journal of Plant Growth Regulation 32 (3):636–45. doi: 10.1007/s00344-013-9332-x.
   Web of Science ®Google Scholar
• Chaoui, A., and E. El Ferjani. 2014. Heavy metal-induced oxidative damage is reduced by β-Estradiol application in lentil seedlings. Plant Growth Regulation 74 (1):1–9. doi: 10.1007/s10725-014-9891-2.
   Web of Science ®Google Scholar
• Clemens, S. 2001. Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212 (4):475–86. doi: 10.1007/s004250000458.
   PubMed Web of Science ®Google Scholar
• Connan, S., and D. B. Stengel. 2011. Impacts of ambient salinity and copper on brown alga: 1. Interactive effects on photosynthesis, growth, and copper accumulation. Aquatic Toxicology 104 (1–2):94–107. doi: 10.1016/j.aquatox.2011.03.015.
   PubMed Web of Science ®Google Scholar
• Dghim, A. A., A. Mhamdi, M. V. Vaultier, M. P. Hasenfratz-Sauder, D. L. Thiec, P. Dizengremel, G. Noctor, and Y. Jolivet. 2013. Analysis of cytosolic isocitrate dehydrogenase and glutathione reductase 1 in photoperiod-influenced responses to ozone using Arabidopsis knockout mutants. Plant, Cell and Environment 36:1981–91. doi: 10.1111/pce.12104.
   PubMed Web of Science ®Google Scholar
• Falkowska, M., A. Poetryczuk, A. Piotrowska, A. Bajguz, A. Grygoruk, and R. Czerpal. 2011. The effect of gibberellic acid (GA3) growth, metal biosorption and metabolism of the green algae Chlorella vulgaris (Chlorophycear) beijerinck exposed to cadmium and lead stress. Polish Journal of Environmental Studies 20:53–9.
   Web of Science ®Google Scholar
• Farooq, H., H. N. Asghar, M. Y. Khan, M. Saleem, Z. A. Zahir. 2015. Auxin-mediated growth of rice in cadmium-contaminated soil. Turkish Journal of Agriculture and Forestry 39:272–6. doi: 10.3906/tar-1405-54.
   Web of Science ®Google Scholar
• Farzadfar, S., F. Zarinkamar, S. A. M. Modarres-Sanavy, and M. Hojati. 2013. Exogenously applied calcium alleviates cadmium toxicity in Matricaria chamomilla L. plants. Environmental Science and Pollution Research 20 (3):1413–22. doi: 10.1007/s11356-012-1181-9.
   PubMed Web of Science ®Google Scholar
• Feigl, G., D. Kumar, N. Lehotai, A. Pető, Á. Molnár, É. Rácz, A. Ördög, L. Erdei, Z. Kolbert, and G. Laskay. 2015. Comparing the effects of excess copper in the leaves of Brassica juncea (L. Czern) and Brassica napus (L.) seedlings: Growth inhibition, oxidative stress and photosynthetic damage. Acta Biologica Hungarica 66 (2):205–21. doi: 10.1556/018.66.2015.2.7.
   PubMed Web of Science ®Google Scholar
• Grappin, P., D. Bouinot, B. Sotta, E. Miginiac, and M. Jullien. 2000. Control of seed dormancy in Nicotiana plumbaginifolia: post-imbibition abscisic acid synthesis imposes dormancy maintenance. Planta 210 (2):279–85. doi: 10.1007/PL00008135.
   PubMed Web of Science ®Google Scholar
• Groot, S. P. C., and C. M. Karssen. 1987. Gibberellins regulate seed germination in tomato by endosperm weakening: a study with gibberellin-deficient mutants. Planta 171 (4):525–31. doi: 10.1007/BF00392302.
   PubMed Web of Science ®Google Scholar
• Habiba, U., S. Ali, M. Farid, M. B. Shakoor, M. Rizwan, M. Ibrahim, G. H. Abbasi, T. Hayat, and B. Ali. 2015. EDTA enhanced plant growth, antioxidant defense system, and phytoextraction of copper by Brassica napus L. Environmental Science and Pollution Research 22 (2):1534–44. doi: 10.1007/s11356-014-3431-5.
   PubMed Web of Science ®Google Scholar
• Hadi, F., N. Ali, and A. Ahmad. 2014. Enhanced phytoremediation of cadmium-contaminated Soil by Parthenium hysterophorus Plant: effect of gibberellic acid (GA3) and synthetic chelator, alone and in combinations. Bioremediation Journal 18 (1):46–55. doi: 10.1080/10889868.2013.834871.
   Web of Science ®Google Scholar
• He, S., Z. He, Q. Wu, L. Wang, and X. Zhang. 2015. Effects of GA3 on plant physiological properties, extraction, subcellular distribution and chemical forms of Pb in Lolium perenne. International Journal of Phytoremediation 17 (12):1153–9. doi: 10.1080/15226514.2015.1045124.
   PubMed Web of Science ®Google Scholar
• Iqbal, M., and M. Ashraf. 2013. Gibberellic acid mediated induction of salt tolerance in wheat plants: Growth, ionic partitioning, photosynthesis, yield and hormonal homeostasis. Environmental and Experimental Botany 86:76–85. doi: 10.1016/j.envexpbot.2010.06.002.
   Web of Science ®Google Scholar
• Ishida, A., K. Ookubo, and K. Ono. 1987. Formation of hydrogen peroxide by NAD(P)H oxidation with isolated cell wall-associated peroxidase from cultured liverwort cells, Marchantia polymorpha L. Plant and Cell Physiology 28:723–6. doi: 10.1093/oxfordjournals.pcp.a077349.
   Web of Science ®Google Scholar
• Islam, M. M., M. A. Hoque, E. Okuma, M. N. A. Banu, Y. Shimoishi, Y. Nakamura, and Y. Murata. 2009. Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. Journal of Plant Physiology 166 (15):1587–97. doi: 10.1016/j.jplph.2009.04.002.
   PubMed Web of Science ®Google Scholar
• Kapoor, D., R. Sharma, N. Handa, H. Kaur, A. Rattan, P. Yadav, V. Gautam, R. Kaur, and R. Bhardwaj. 2015. Redox homeostasis in plants under abiotic stress: role of electron carriers, energy metabolism mediators and proteinaceous thiols. Frontier in Environmental Science 3:13. doi: 10.3389/fenvs.2015.00013.
   Web of Science ®Google Scholar
• Karmous, I., K. Jaouani, A. Chaoui, and E. El Ferjani. 2012. Proteolytic activities in Phaseolus vulgaris cotyledons under copper stress. Physiology and Molecular Biology of Plants 18 (4):337–43. doi: 10.1007/s12298-012-0128-4.
   PubMedGoogle Scholar
• Kinraide, T. B., J. F. Pedler, and D. R. Parker. 2004. Relative effectiveness of calcium and magnesium in the alleviation of rhizotoxicity in wheat induced by copper, zinc, aluminum, sodium, and low pH. Plant and Soil 259 (1/2):201–8. doi: 10.1023/B:PLSO.0000020972.18777.99.
   Web of Science ®Google Scholar
• Kopittke, P. M., T. B. Kinraide, P. Wang, F. P. C. Blamey, S. M. Reichman, and N. W. Menzies. 2011. Alleviation of Cu and Pb rhizotoxicities in cowpea (Vigna unguiculata) as related to ion activities at root-cell plasma membrane surface. Environmental Science & Technology 45 (11):4966–73. doi: 10.1021/es1041404.
   PubMed Web of Science ®Google Scholar
• Lequeux, H., C. Hermans, S. Lutts, and N. Verbruggen. 2010. Response to copper excess in Arabidopsis thaliana: Impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiology and Biochemistry 48 (8):673–82. doi: 10.1016/j.plaphy.2010.05.005.
   PubMed Web of Science ®Google Scholar
• Leόn, A. M., J. M. Palma, F. J. Corpas, M. Gόmez, M. C. Romero-Puertas, D. Chatterjee, R. M. Mateos, L. A. Del Río, and L. M. Sandalio. 2002. Antioxidative enzymes in cultivars of pepper plants with different sensitivity to cadmium. Plant Physiology and Biochemistry 40:813–20. doi: 10.1016/S0981-9428(02)01444-4.
   Web of Science ®Google Scholar
• Lozano, R. M., J. H. Wong, B. C. Yee, A. Peters, K. Kobrehel, and B. B. Buchanan. 1996. New evidence for a role for thioredoxin h in germination and seedling development. Planta 200:100–6.
   Web of Science ®Google Scholar
• Luo, X. S., L. Z. Li, and D. M. Zhou. 2008. Effect of cations on copper toxicity to wheat root: implications for the biotic ligand model. Chemosphere 73 (3):401–6. doi: 10.1016/j.chemosphere.2008.05.031.
   PubMed Web of Science ®Google Scholar
• Matsumura, H., and S. Miyachi. 1980. Cycling assay for nicotinamide adenine dinucleotides. Methods in Enzymology 69:465–70.
   Google Scholar
• Meng, H., S. Hua, I. H. Shamsi, G. Jilani, Y. Li, and L. Jiang. 2009. Cadmium-induced stress on the seed germination and seedling growth of Brassica napus L., and its alleviation through exogenous plant growth regulators. Plant Growth Regulation 58 (1):47–59. doi: 10.1007/s10725-008-9351-y.
   Web of Science ®Google Scholar
• Mihoub, A., A. Chaoui, and E. El Ferjani. 2005. Biochemical changes associated with cadmium and copper stress in germinating pea seeds (Pisum sativum L.). Comptes Rendus Biologies 328 (1):33–41. doi: 10.1016/j.crvi.2004.10.003.
   PubMed Web of Science ®Google Scholar
• Najeeb, U., G. Jilani, S. Ali, M. Sarwar, L. Xu, and W. J. Zhou. 2011. Insight into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. Journal of Hazardous Materials 186 (1):565–74. doi: 10.1016/j.jhazmat.2010.11.037.
   PubMed Web of Science ®Google Scholar
• Noctor, G., G. Queval, and B. Gakière. 2006. NAD(P) synthesis and pyridine nucleotide cycling in plants and their potential importance in stress conditions. Journal of Experimental Botany 57 (8):1603–20. doi: 10.1093/jxb/erj202.
   PubMed Web of Science ®Google Scholar
• Petrov, V., J. Hille, B. Mueller-Roeber, and T. S. Gechev. 2015. ROS-mediated abiotic stress-induced programmed cell death in plants. Frontier in Plant Science 69:6. doi: 10.3389/fpls.2015.00069.
   PubMed Web of Science ®Google Scholar
• Potters, G., N. Horemans, and M. A. Jansen. 2010. The cellular redox state in plant stress biology: a charging concept. Plant Physiology and Biochemistry 48 (5):292–300. doi: 10.1016/j.plaphy.2009.12.007.
   PubMed Web of Science ®Google Scholar
• Rahoui, S., C. Ben, A. Chaoui, Y. Martinez, A. Yamchi, M. Rickauer, L. Gentzbittel, and E. El Ferjani. 2014. Oxidative injury and antioxidant genes regulation in cadmium-exposed radicles of six contrasted Medicago truncatula genotypes. Environmental Science and Pollution Research 21 (13):8070–83. doi: 10.1007/s11356-014-2718-x.
   PubMed Web of Science ®Google Scholar
• Rahoui, S., A. Chaoui, C. Ben, M. Rickauer, L. Gentzbittel, and E. El Ferjani. 2015. Effect of cadmium pollution on mobilization of embryo reserves in seedlings of six contrasted Medicago truncatula lines. Phytochemistry 111:98–106. doi: 10.1016/j.phytochem.2014.12.002.
   PubMed Web of Science ®Google Scholar
• Romero-Puertas, M. C., M. Rodríguez-Serrano, F. J. Corpas, M. Gómez, L. A. Del Río, and L. M. Sandalio. 2004. Cadmium-induced subcellular accumulation of O2·- and H2O2 in pea leaves. Plant, Cell and Environment 27 (9):1122–34. doi: 10.1111/j.1365-3040.2004.01217.x.
   Web of Science ®Google Scholar
• Rubio, M. I., I. Escrig, C. Mart⏧Nez-Cortina, F. J. L⏧Pez-Benet, and A. Sanz. 1994. Cadmium and nickel accumulation in rice plants. Effects on mineral nutrition and possible interactions of abscisic and gibberellic acids. Plant Growth Regulation 14 (2):151–7. doi: 10.1007/BF00025217.
   Web of Science ®Google Scholar
• Ryrie, I. J., and K. J. Scott. 1969. Nicotinate, quinolinate and nicotinamide as precursors in the biosynthesis of nicotinamide-adenine dinucleotide in barley. Biochemical Journal 115 (4):679–85. doi: 10.1042/bj1150679.
   PubMed Web of Science ®Google Scholar
• Sakouhi, L., S. Rahoui, M. Ben Massoud, S. Munemasa, E. El Ferjani, Y. Murata, and A. Chaoui. 2016. Calcium and EGTA alleviate cadmium toxicity in germinating chickpea seeds. Journal of Plant Growth Regulation 35 (4):1064–73. doi: 10.1007/s00344-016-9605-2.
   Web of Science ®Google Scholar
• Seo, M., E. Nambara, G. Choi, and S. Yamaguchi. 2009. Interaction of light and hormone signals in germinating seeds. Plant Molecular Biology 69 (4):463–72. doi: 10.1007/s11103-008-9429-y.
   PubMed Web of Science ®Google Scholar
• Sfaxi-Bousbih, A., A. Chaoui, and E. El Ferjani. 2010. Cadmium impairs mineral and carbohydrate mobilization during the germination of bean seeds. Ecotoxicology and Environmental Safety 73 (6):1123–9. doi: 10.1016/j.ecoenv.2010.01.005.
   PubMed Web of Science ®Google Scholar
• Sharaf, A. M., I. I. Farghal, and M. R. Sofy. 2009. Role of gibberellic acid in abolishing the detrimental effects of Cd and Pb on broad bean and lupin plants. Research Journal of Agriculture and Biological Sciences 5:668–73.
   Google Scholar
• Štolfa, I., T. Z. Feiffer, D. Špoljarić, T. Teklić, and Z. Lončarić. 2015. Heavy metal-induced oxidative stress in plants: Response of the antioxidative system. In Reactive oxygen species and oxidative damage in plants under stress. D. K. Gupta, J. M. Palma, and F. J. Corpas, eds. Switzerland: Springer International Publishing, pp. 127–163.
   Google Scholar
• Tian, S., L. Lu, J. Zhang, K. Wang, P. Brown, Z. He, J. Liang, and X. Yang. 2011. Calcium protects roots of Sedum alfredii H. against cadmium-induced oxidative stress. Chemosphere 84 (1):63–9. doi: 10.1016/j.chemosphere.2011.02.054.
   PubMed Web of Science ®Google Scholar
• Valderrama, R., F. J. Corpas, A. Carreras, M. V. Gómez-Rodríguez, M. Chaki, J. R. Pedrajas, A. Fernández-Ocaña, L. A. Del Río, and J. B. Barroso. 2006. The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants. Plant, Cell and Environment 29 (7):1449–59. doi: 10.1111/j.1365-3040.2006.01530.x.
   PubMed Web of Science ®Google Scholar
• Van Breusegem, F., and J. F. Dat. 2006. Reactive oxygen species in plant cell death. Plant Physiology 141 (2):384–90. doi: 10.1104/pp.106.078295.
   PubMed Web of Science ®Google Scholar
• Vulkan, R., U. Yermiyahu, U. Mingelgrin, G. Rytwo, and T. B. Kinraide. 2004. Sorption of copper and zinc to the plasma membrane of wheat root. The Journal of Membrane Biology 202 (2):97–104. doi: 10.1007/s00232-004-0722-7.
   PubMed Web of Science ®Google Scholar
• Xu, W., Y. Li, J. He, Q. Ma, X. Zhang, G. Chen, H. Wang, and H. Zhang, 2010. Cd uptake in rice cultivars treated with organic acids and EDTA. Journal of Environmental Sciences 22 (3):441–7. doi: 10.1016/S1001-0742(09)60127-3.
   Web of Science ®Google Scholar
• Zaheer, I. E., S. Ali, M. Rizwan, M. Farid, M. B. Shakoor, R. A. Gill, U. Najeeb, N. Iqbal, and R. Ahmad. 2015. Citric acid assisted phytoremediation of copper by Brassica napus L. Ecotoxicology and Environmental Safety 120:310–7. doi: 10.1016/j.ecoenv.2015.06.020.
   PubMed Web of Science ®Google Scholar
• Zawaski, C., and V. B. Busov. 2014. Roles of gibberellin catabolism and signaling in growth and physiological response to drought and short-day photoperiods in Populus trees. Plos One 9 (1):e86217. doi: 10.1371/journal.pone.0086217.
   PubMed Web of Science ®Google Scholar
• Zhao, Z., X. Hu, and C. W. Ross. 1987. Comparison of tissue preparation methods for assay of nicotinamide coenzymes. Plant Physiology 84 (4):987–8. doi: 10.1104/pp.84.4.987.
   PubMed Web of Science ®Google Scholar
• Zhu, X. F., T. Jiang, Z. W. Wang, G. J. Lei, Y. Z. Shi, G. X. Li, and S. J. Zheng. 2012. Gibberellic acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of IRT1 in Arabidopsis thaliana. Journal of Hazardous Materials 239–240:302–7. doi: 10.1016/j.jhazmat.2012.08.077.
   PubMed Web of Science ®Google Scholar