Effects of nickel on growth and the reproductive organs of Vicia faba plants

Sondes Helaoui , Iteb Boughattas , Sabrine Hattab , Marouane Mkhinini and Mohamed Banni

Abstract
High concentration of nickel (Ni) could provoke numerous toxic effects in plant tissues. The present study was undertaken to determine the effects of nickel (Ni) treatment on agronomic and production parameters of bean plants (Vicia faba). For that, plants were treated with four increasing concentrations of Ni: control: 0 mg/kg, C1: 150 mg/kg, C2: 250 mg/kg, and C3: 500 mg/kg. The effects of these Ni concentrations on growth, dry matter, pollen germination and viability, flower number and yield per plant were determined in bean plants. Our data demonstrated that Ni caused threats to plant growth and development. Also, our results showed a substantial reduction of pollen germination and viability in different concentrations of Ni loads. Furthermore, a clear negative effect of nickel was observed in fruit weight and seed set. Our study must be carefully considered in view of soil contamination and its subsequence effect on crop production.

Keywords
Nickel; Vicia faba; Pollen germination; Pollen viability; Production parameters.

DOI
10.21472/bjbs(2020)071706

Full text
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References
Adriano, D. C. Trace elements in terrestrial environments: Biochemistry, bioavailability and risks of metals. 2. ed. New York: Springer-Verlag, 2001. v. 4-12.

Atta-Aly, M. A. Effect of nickel addition on the yield and quality of parsley leaves. Scientia Horticulturae, v. 82, p. 9-24, 1999. https://doi.org/10.1016/S0304-4238(99)00032-1

Awasthi, K.; Sinha, P. Nickel stress induced antioxidant defence system in sponge gourd (Luffa cylindrica L.). Journal of Plant Physiology & Pathology, v. 1, p. 1, 2013. https://doi.org/10.4172/2329-955X.1000102

Bai, C.; Reilly, C. C.; Wood, B. W. Nickel deficiency disrupts metabolism of ureides, amino acids of young pecan foliage. Plant Physiology, v. 140, p. 433-443, 2006. https://doi.org/10.1104/pp.105.072983

Baligarx, V. C. Mechanisms of nickel uptake and hyperaccumulation by plants and implications for soil remediation. Advances in Agronomy, v. 117, p. 117-189, 2012. https://doi.org/10.1016/B978-0-12-394278-4.00003-9

Beda, H. Der Einfluss einer SO₂: Begasung auf Bildung und Keimkraft des Pollensvon Weisstanne, Abies alba (Mill.). Eidgenössische Anstalt für das Forstliche Versuchswesen, v. 58, p. 165-223, 1982.

Bishnoi, N. R.; Sheoran, I. S.; Singh, R. Effect of cadmium and nickel on mobilization of food reserves and activities of hydrolytic enzymes in germinating pigeon pea seeds. Biologia Plantarum, v. 35, p. 583-589, 1993. https://doi.org/10.1007/BF02928036

Bradl, H. Heavy metals in the environment: Origin, interaction and remediation. London: Elsevier, 2002.

Brown, P. H.; Welch, R. M.; Madison, J. T. Effect of nickel deficiency on soluble anion, amino acid and nitrogen levels in barley. Plant and Soil, v. 125, v. 19-27, 1990. https://doi.org/10.1007/BF00010740

Chen, C.; Huang, D.; Liu, J. Functions and toxicity of nickel in plants: Recent advances and future prospects. CLEAN - Soil, Air, Water, v. 37, p. 304-313, 2009. https://doi.org/10.1002/clen.200800199

Colas, F.; Mercier, S. Evaluation et maintien de la viabilité des pollens utilisés dans le programme d'amélioration des arbres. Mémoire de recherche forestière, 135. Projet de recherche n^o 3420-0205-212S. Biologie et conservation du pollen d'arbres forestiers, 2000.

DalCorso, G. Heavy metal toxicity in plants. In: Furini, A. (Eds). Plants and heavy metals. Dordrecht, Netherlands: Springer, 2012. (Springer Briefs in Molecular Science). p. 1-25. https://doi.org/10.1007/978-94-007-4441-7_1

Dalton, D.; Evans, H. J.; Hanus, F. J. Stimulation by nickel of soil microbial urease and hydrogenase activities in soybean grown in a low-nickel soil. Plant and Soil, v. 88, p. 245-258, 1985. https://doi.org/10.1007/BF02182451

DuBay, D. T.; Murdy, W. H. The impact of sulfur dioxide on plant sexual reproduction: In vivo and in vitro effects compared. Journal Environmental Quality, v. 12, p. 147-149, 1983. https://doi.org/10.2134/jeq1983.00472425001200010027x

Eskew, D. L.; Welch, R. M, Cary, E. E. Nickel: An essential micronutrient for legumes and possibly all higher plants. Science, v. 222, p. 621-623, 1983. https://doi.org/10.1126/science.222.4624.621

Fabiano, C.; Tezotto, T.; Favarin, J. L.; Polacco, J. C.; Mazzafera, P. Essentiality of nickel in plants: A role in plant stresses. Frontiers in Plant Science, 6:754, 2015. https://doi.org/10.3389/fpls.2015.00754

Feder, W. A. Bioassaying for ozone with pollen systems. Environmental Health Perspectives, v. 37, p. 117-123, 1981. https://doi.org/10.1289/ehp.8137117

Ferraz, P.; Fidalgo, F.; Almeida, A.; Teixeira, J. Phytostabilization of nickel by the zinc and cadmium hyper accumulator Solanum nigrum L. are metallothioneins involved. Plant Physiology and Biochemistry, v. 57, p. 254-260, 2012. https://doi.org/10.1016/j.plaphy.2012.05.025

Gajewska, E.; Sklodowska, M.; Slaba, M.; Mazur, J. Effect of nickel on antioxidative enzyme activities, proline and chlorophyll content in wheat shoots. Biologia Plantarum, v. 50, p. 653-659, 2006. https://doi.org/10.1007/s10535-006-0102-5

Gajewska, E.; Wielanek, M.; Bergier, K.; Skłodowska, M. Nickel-induced depression of nitrogen assimilation in wheat roots. Acta Physiologiae Plantarum, v. 31, p. 1291-1300, 2009. https://doi.org/10.1007/s11738-009-0370-8

Gill, R. A.; Zang, L.; Ali, B.; Farooq, M. A.; Cui, P.; Yang, S.; Ali, S.; Zhou, W. Chromium-induced physio-chemical and ultrastructural changes in four cultivars of Brassica napus L. Chemosphere, v. 120, p. 154-164, 2015. https://doi.org/10.1016/j.chemosphere.2014.06.029

Gonzàlez, M.; Baeza, E.; Lao, J. L.; Cuevas, J. Pollen load affects fruit set, size, and shape in cherimoya. Scientia Horticulturae, v. 110, p. 51-56, 2006. https://doi.org/10.1016/j.scienta.2006.06.015

Guderian, R. Air pollution: Phytotoxicity of active gases and its significance in air pollution control. Berlin: Springer-Vedag, 1977. (Ecological Studies, 22). https://doi.org/10.1007/978-3-642-66544-8

Guo, Y.; Marschner, H. Uptake, distribution, and binding of cadmium and nickel in different plant species. Journal of Plant Nutrition, v. 18, p. 2691-2706, 1995. https://doi.org/10.1080/01904169509365094

Hasanuzzaman, M.; Fujita, M. Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology, v. 22, p. 584-596, 2013. https://doi.org/10.1007/s10646-013-1050-4

Hasanuzzaman, M.; Nahar, K.; Anee, T. I.; Khan, M. I. R.; Fujita, M. Silicon-mediated regulation of antioxidant defense and glyoxalase systems confers drought stress tolerance in Brassica napus L. South African Journal of Botany, v. 115, p. 50-57, 2018. https://doi.org/10.1016/j.sajb.2017.12.006

INSG - International Nickel Study Group. Available from: <http://www.insg.org/stats.aspx>. Accessed on: Jun. 24, 2019.

Järup, L. Hazards of heavy metal contamination. British Medical Bulletin, v. 68, p. 167-182, 2003. https://doi.org/10.1093/bmb/ldg032

Jiang, Q. Y.; Zhuo, F.; Long, S. H.; Zhao, D. H.; Yang, D. J.; Ye, H. Z.; Li, S. S.; Jing, X. Y. Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd added soils. Scientific Reports, v. 6, 2016. https://doi.org/10.1038/srep21805

Kabata-Pendias, A.; Pendias, H. Trace elements in soils and plants. Boca Raton: CRC Press, 2001.

Kamran, M. A.; Eqani, S. A. M. A. S.; Bibi, S.; Xu, R-K.; Amna; Monis, M. F. H.; Katosoyiannis, A.; Bokhari, H.; Chaudhary, H. J. Bioaccumulation of nickel by E. sativa and role of plant growth promoting rhizobacteria (PGPRs) under nickel stress. Ecotoxicology and Environmental Safety, v. 126, p. 256-263, 2016. https://doi.org/10.1016/j.ecoenv.2016.01.002

Keller, T. Physiological bioindications of an effect of air pollution on plants. In: Steubing, L.; Jiger, H. J. (Eds.). Monitoring of air pollutants by plants: Methods and problems. Den Haag: Junk Publication, 2007. p. 85-95. (Task for Vegetation Science, 7).

Madhava Rao, K. V.; Sresty, T. V. S. Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Science, v. 157, p. 113-128, 2000. https://doi.org/10.1016/S0168-9452(00)00273-9

Maheshwari, R.; Dubey, R. Nickel toxicity inhibits ribonuclease and protease activities in rice seedlings: Protective effects of proline. Plant Growth Regulation, v. 51, p. 231-243, 2007. https://doi.org/10.1007/s10725-006-9163-x

Manning, W. J.; Feder, W. A. Effects of ozone on economic plants. In: Mansfield, T. A. (Ed.). Effects of air pollutants on plants. Cambridge: Cambridge University Press, 1976. p. 47-60.

Mohanty, S.; Das, A. B.; Das, P.; Mohanty, P. Effect of a low dose of aluminum on mitotic and meiotic activity, 4CDNA content, and pollen sterility in rice, Oryza sativa L. cv. Lalat. Ecotoxicology and Environmental Safety, v. 59, p. 70-75, 2004. https://doi.org/10.1016/j.ecoenv.2003.07.017

Moya, J. E.; Picazo, I. Influence of cadmium and nickel on growth, net photosynthesis and carbohydrate distribution in rice plants. Photosynthesis Research, v. 36, p. 75-80, 1993.

Nakazawa, R.; Kameda, Y.; Ito, T.; Ogita, Y.; Michihata, R.; Takenaga, H. Selection and characterization of nickel-tolerant tobacco cells. Biologia Plantarum, v. 48, p. 497-502, 2004.

Nmila, R. Absorption, transport et accumulation du cadmium chez la plante de tomate (Lycopersicon esculentum Mill.). Montpellier: USTL, 1992. (Thèse).

Nnorom, I. C.; Osibanjo, O. Heavy metal characterization of waste portable rechargeable batteries used in mobile phones. International Journal of Environmental Science & Technology, v. 6, no. 4, p. 641-650, 2009. https://doi.org/10.1007/BF03326105

Palacios, G.; Gomez, I.; Carbonell-Barrachina, A.; Pedreño, J. N.; Mataix, J. Effect of nickel concentration on tomato plant nutrition and dry matter yield. Journal of Plant Nutrition, v. 21, p. 2179-2191, 1998. https://doi.org/10.1080/01904169809365553

Parida, B. K.; Chhibba, I. M.; Nayyar, V. K. Influence of nickel-contaminated soils on fenugreek (Trigonella corniculata L.) growth and mineral composition. Scientia Horticulturae, p. 98, v. 113-119, 2003. https://doi.org/10.1016/S0304-4238(02)00208-X

Poonkothai, M.; Vijayavathi, B. S. Nickel as an essential element and a toxicant. International Journal of Environmental Sciences, v. 1, no. 4, p. 285-288, 2012.

Rizwan, M.; Mostofa, M. G.; Ahmad, M. Z.; Imtiaz, M.; Mehmood, S.; Adeel, M.; Dai, Z.; Li. Z.; Aziz, O.; Zhang, Y.; Tu, S. Nitric oxide induces rice tolerance to excessive nickel by regulating nickel uptake, reactive oxygen species detoxification and defense related gene expression. Chemosphere, v. 191, p. 23-35, 2018. https://doi.org/10.1016/j.chemosphere.2017.09.068

Ryser, P.; Sauder, R. Effects of heavy-metal-contaminated soil on growth, phenology and biomass turnover of Hieracium piloselloides. Environmental Pollution, v. 140, p. 52-61, 2006. https://doi.org/10.1016/j.envpol.2005.06.026

Salt, D. E.; Blaylock, M.; Kumar, N. P. B. A.; Dusenkov, V.; Ensley, B. D.; Chet, I.; Raskin, I.; Phytoremediation: A novel strategy for the removal of toxic metals from the environment using plants. Bio/Technology, v. 13, p. 468-474, 1995. https://doi.org/10.1038/nbt0595-468

Sawidis, T. H. D.; Reiss, H. D. Effects of heavy metals on pollen tube growth and ultrastructure. Protoplasma, v. 185, p. 113-122, 1995. https://doi.org/10.1007/BF01272851

Schmidt, R. R.; Michel, J. Facile synthesis of α-and β-O-glycosyl imidates; preparation of glycosides and disaccharides. Angewandte Chemie, v. 19, p. 731-732, 1980. https://doi.org/10.1002/anie.198007311

Seregin, I.; Ivanov, V. Physiological aspects of cadmium and lead toxic effects on higher plants. Russian Journal of Plant Physiology, v. 48, p. 523-544, 2001. https://doi.org/10.1023/A:1016719901147

Seregin, I.; Kozhevnikova, A.; Kazyumina, E.; Ivanov, V. Nickel toxicity and distribution in maize roots. Russian Journal of Plant Physiology, v. 50, p. 711-717, 2003. https://doi.org/10.1023/A:1025660712475

Shikazono, N.; Zakir, H. M.; Sudo, Y. Zinc contamination in river water and sediments at Taisyu Zn-Pb mine area, Tsushima Island, Japan. Journal of Geochemical Explorator, v. 98, p. 80-88, 2008. https://doi.org/10.1016/j.gexplo.2007.12.002

Shivanna, K. R. Pollen Biology and Biotechnology. Enfield: Science Publishers, 2003.

Siddiqui, M. H.; Al-Whaibi, M. H.; Basalah, M. O. Interactive effect of calcium and gibberellin on nickel tolerance in relation to antioxidant systems in Triticum aestivum L. Protoplasma, v. 248, p. 503-511, 2011. https://doi.org/10.1007/s00709-010-0197-6

Sirhindi, G.; Mir, M. A.; Abd-Allah, E. F.; Ahmad, P.; Gucel, S. Jasmonic acid modulates the physio-biochemical attributes, antioxidant enzyme activity, and gene expression in Glycine max under nickel toxicity. Frontiers in Plant Science, 2016. https://doi.org/10.3389/fpls.2016.00591

Tripathy, B. C.; Bhatia, B.; Mohanty, P. Inactivation of chloroplast photosynthetic electron-transport activity by Ni²⁺. Biochimica et Biophysica Acta (BBA) - Bioenergetics, v. 638, p. 217-224, 1981. https://doi.org/10.1016/0005-2728(81)90230-9

Varshney, S. R.; Varshney, C. K. Effects of sulfur dioxide on pollen germination and pollen tube growth. Environmental Pollution Series A, Ecological and Biological, v. 24, p. 87-92, 1980. https://doi.org/10.1016/0143-1471(81)90070-2

Visse, R. Germination and storage of pollen. Medelingen van de Landbouw School, v. 55, p. 1-68, 1955.

Wang, X.; Qu, R.; Huang, Q.; Wei, Z.; Wang, Z. Hepatic oxidative stress and catalyst metals accumulation in goldfish exposed to carbon nanotubes under different pH levels. Aquatic Toxicology, v. 160, p. 142-150, 2015. https://doi.org/10.1016/j.aquatox.2015.01.015

Wang, S.; Shi, X. Molecular mechanisms of metal toxicity and carcinogenesis. Molecular and Cellular Biochemistry, v. 222, p. 3-9, 2001. https://doi.org/10.1023/A:1017918013293

Weis, J. S.; Weis, P. Metal uptake, transport and release by wetland plants: Implications for phytoremediation and restoration. Environment International, v. 30, p. 685-700, 2004. https://doi.org/10.1016/j.envint.2003.11.002

Wuana, R. A.; Okieimen, F. E. Heavy metals in contaminated soils: A review of sources, chemistry, risks and best available strategies for remediation. International Scholarly Research Notices, v. 2011, Article ID 402647, 2011. https://doi.org/10.5402/2011/402647

Xiong, Z. T.; Peng, Y. H. Response of pollen germination and tube growth to cadmium with special reference to low concentration exposure. Ecotoxicology and Environmental Safety, v. 48, p. 51-55, 2011. https://doi.org/10.1006/eesa.2000.2002

Yousefi, N.; Chehregani, A.; Malayeri, B.; Lorestani, B.; Cheraghi, M. Effect of heavy metals on the developmental stages of ovule and seed proteins in Chenopodium botrys L. Chenopodiaceae. Biological Trace Element Research, v. 144, p. 1142-1149, 2011. https://doi.org/10.1007/s12011-009-8386-x


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