Please wait a minute...
Journal of Integrative Agriculture  2013, Vol. 12 Issue (10): 1783-1790    DOI: 10.1016/S2095-3119(13)60367-6
Physiology & Biochentry · Tillage · Cultivation Advanced Online Publication | Current Issue | Archive | Adv Search |
Exogenous Nitric Oxide Involved in Subcellular Distribution and Chemical Forms of Cu2+ Under Copper Stress in Tomato Seedlings
 DONG Yu-xiu, WANG Xiu-feng , CUI Xiu-min
1 Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an 271018, P.R.China
2 College of Resources and Environment, Shandong Agricultural University, Tai’an 271018, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  Nitric oxide (NO), a bioactive signaling molecule, serves as an antioxidant and anti-stress agent under abiotic stress. A hydroponics experiment was conducted to investigate the effects of sodium nitroprusside (SNP), a NO donor, on tomato seedlings exposed to 50 μmol L-1 CuCl2. The results show that copper is primarily stored in the soluble cell sap fraction in the roots, especially after treatment with Cu+SNP treatment, which accounted for 66.2% of the total copper content. The copper concentration gradually decreased from the roots to the leaves. In the leaves, exogenous NO induces the storage of excess copper in the cell walls. Copper stress decreases the proportion of copper integrated with pectates and proteins, but exogenous NO remarkably reverses this trend. The alleviating effect of NO is blocked by hemoglobin. Thus, exogenous NO is likely involved in the regulation of the subcellular copper concentrations and its chemical forms under copper stress. Although exogenous NO inhibited the absorption and transport of excess copper to some extent, the copper accumulation in tomato seedlings significantly increased under copper stress. The use of exogenous NO to enhance copper tolerance in some plants is a promising method for copper remediation.

Abstract  Nitric oxide (NO), a bioactive signaling molecule, serves as an antioxidant and anti-stress agent under abiotic stress. A hydroponics experiment was conducted to investigate the effects of sodium nitroprusside (SNP), a NO donor, on tomato seedlings exposed to 50 μmol L-1 CuCl2. The results show that copper is primarily stored in the soluble cell sap fraction in the roots, especially after treatment with Cu+SNP treatment, which accounted for 66.2% of the total copper content. The copper concentration gradually decreased from the roots to the leaves. In the leaves, exogenous NO induces the storage of excess copper in the cell walls. Copper stress decreases the proportion of copper integrated with pectates and proteins, but exogenous NO remarkably reverses this trend. The alleviating effect of NO is blocked by hemoglobin. Thus, exogenous NO is likely involved in the regulation of the subcellular copper concentrations and its chemical forms under copper stress. Although exogenous NO inhibited the absorption and transport of excess copper to some extent, the copper accumulation in tomato seedlings significantly increased under copper stress. The use of exogenous NO to enhance copper tolerance in some plants is a promising method for copper remediation.
Keywords:  tomato seedlings       nitric oxide       copper stress       subcellular distribution       chemical form  
Received: 20 September 2012   Accepted:
Fund: 

This work was supported partially by the National Natural Science Foundation of China (31201619), Profession Expert Group of Facility Cultivation and Engineering (CARS- 25-D-03) and the Sci-Tech Development Project of Tai’an City, China (32606).

Corresponding Authors:  Correspondence CUI Xiu-min, Tel: +86-538-8241546, Mobile: 13905489073, Fax: +86-538-8242250, E-mail: xiumincui@sdau.edu.cn     E-mail:  xiumincui@sdau.edu.cn
About author:  DONG Yu-xiu, E-mail: zwfy1@sdau.edu.cn;

Cite this article: 

DONG Yu-xiu, WANG Xiu-feng , CUI Xiu-min. 2013. Exogenous Nitric Oxide Involved in Subcellular Distribution and Chemical Forms of Cu2+ Under Copper Stress in Tomato Seedlings. Journal of Integrative Agriculture, 12(10): 1783-1790.

[1]Andrea P, Nora L, Jorge L J, Jose L, Irma T, Laszlo E. 2011. Involemant of nitric oxide and auxin in signal transduction of copper-induced morphological responses in Arabidopsis seedlings. Annals of Botany, 108, 449- 457.

[2]Arasimowicz M, Floryszak Wieczorek J. 2007. Nitric oxide as a bioactive signaling molecule in plant stress responses. Plant Science, 172, 876-887

[3]Baker A J M. 1981. Accumulators and excluders strategies in the response of plants to heavy metals. Journal of Plant Nutrition, 3, 643-654

[4]Burkhead J L, Gogolin Reynolds K A, Abdel-Ghany S E, Cohu C M, Pilon M. 2009. Copper homeostasis. New Phytologist, 182, 799-816

[5]Chen Y X. 2008. Plant Contaminated Chemistry of Heavy Metal in Soil. Science Press, China. pp. 41-54

[6](in Chinese) Clemens S. 2001. Molecular mechanisms of plant metal tolerance and homeostasis. Planta, 212, 475-486

[7]Ernst W H O, Nelissen H J M, Ten Bookum W M. 2000. Combination toxicology of metal-enriched soils: physiological responses of a Zn- and Cu-resistant population of Silene vulgaris on polymetallic soils. Environmental & Experimental Botany, 43, 55-71

[8]Fu X P, Dou C M, Chen Y X, Chen X C, Shi J Y, Yu M G, Xu J. 2011. Subcellular distribution and chemical forms of cadmium in Phytolacca americana L. Journal of Hazardous Materials, 186, 103-107

[9]Hall J L. 2002. Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany, 53, 1-11

[10]Hardiman R T, Jacoby B. 1984. Absorption and translocation of Cd in bush beans (Phaseolus vulgaris). Physiologia Plantarum, 61, 670-674

[11]Hayens R J. 1980. Ion exchange properties of roots and ionic interactions within the root POPLsn: their role in ion accumu1ation by plants. The Botanical Review, 46, 75-99

[12]Isaure M P, Fayard B, Sarret G, Pairis S, Bourguignon J. 2006. Localization and chemical forms of cadmium in plant samples by combining analytical electron microscopy and X-ray spectro microscopy. Spectrochim Acta, 61, 1242-1252

[13]Liu J, Xiong Z, Li T, Huang H. 2004. Bioaccumulation and ecophysiological responses to copper stress in two populations of Rumex dentatus L. from Cu contaminated and non-contaminated sites. Environmental & Experimental Botany, 52, 43-51

[14]Lou L, Shen Z, Li X. 2004. The copper tolerance mechanisms of Elsholtzia haichowensis, a plant from copper-enriched soils. Environmental & Experimental Botany, 51, 111-120

[15]Lozano-Rodríguez E, Hernandez L E, Bonay P, Carpena- Ruiz R O. 1997. Distribution of cadmium in shoot and root tissues of maize and pea plants: physiological disturbances. Journal of Experimental Botany, 48, 123- 128. Lugany M, Lombini A, Poschenrieder C, Dinelli E, Barcelo J. 2003. Different mechanisms account for enhanced copper resistance in Silene armeria populations from mine spoil and serpentine sites. Plant Soil, 251, 55-63

[16]MacFarlane G R, Burchett M D. 2000. Cellular distribution of copper, lead and zinc in Grey mangrove, Avicennia marina Vierh. Aquatic Botany, 68, 45-49

[17]Miyasaka, Hawes. 2001. Possible role of root border cells in detection and avoidance of aluminium toxicity. Plant Physiology, 125, 1978-1987

[18]Nishizono H, Ichikawa H, Suziki S, Ishii F. 1987. The role of root cell wall in the heavy metal tolerance of Athyium yoloscese. Plant Soil, 101, 15-20

[19]Neill S J, Desikan R, Clarke A, Hurst R D, Hancocontrol J T. 2002. Hydrogen peroxide and nitric oxide as signalling molecules in plants. Journal of Experimental Botany, 53, 1237-1247

[20]Ouariti O, Boussama N, Zarrouk M, Cherif A, Ghorbal M H. 1997. Cadmium and copper induced changes in tomato membrane lipids. Phytochemistry, 45, 1343-1350

[21]Pittman J K. 2005. Managing the manganese, molecular mechanisms of manganese transport and homeostasis. New Phytologist, 167, 733-742

[22]Qiu R L, Thangavel P, Hu P J, Senthikumar P, Ying R R, Tang Y T. 2011. Interaction of cadmium and zinc on accumulation and sub-celluar distribution in leaves of hyperaccumulator Potentilla griffithii. Journal of Hazardous Materials, 186, 1425-1430

[23]Salt D E, Prince R C, Picontrolering I J. 2002. Chemical speciation of accumulated metals in plants, evidence from X-ray absorption spectroscopy. Microchemical Journal, 71, 255-259

[24]Sanità di Toppi L, Gabbrielli R. 1999. Response to cadmium in higher plants. Environmental & Experimental Botany, 41, 105-130

[25]Tanyolac D, Ekmekc Y, Unalan S. 2007. Changes in photochemical and antioxidant enzyme activities in maize (Zea mays L.) leaves exposed to excess copper. Chemosphere, 67, 89-98

[26]Tewari R K, Hahn E J, Paek K Y. 2008. Modulation of copper toxicity-induced oxidative damage by nitric oxide supply in the adventitious roots of Panax ginseng. Plant Cell Report, 27, 171-181

[27]Tong Y P , Kneer R , Zhu Y G . 2 0 0 4 . Vacu o lar compartmentalization, a second-generation approach to engineering plants for phytoremediation. Trends in Plant Science, 9, 7-9

[28]Wójcik M, Vangronsveld J, Haen J D, Tukiendorf A. 2005. Cadmium tolerancein Thlaspi caerulescens II. Localization of cadmiumin Thlaspicae rule scens. Environmental & Experimental Botany, 53, 163-171

[29]Wu F B, Dong J, Qian Q Q, Zhang G P. 2005. Subcellular distribution and chemical form of Cd and Cd-Zn interaction in different barley genotypes. Chemosphere, 60, 1437-1446

[30]Xiong J, Fu G, Tao L, Zhu C. 2010. Roles of nitric oxide in alleviating heavy metal toxicity in plants. Archives of Biochemistry and Biophysics, 497, 13-20

[31]Xu J L, Bao Z P, Yang J R, Liu H, Song W C. 1991. Chemical forms of Pb, Cd and Cu in crops. Chinese Journal of Applied Ecology, 2, 244-248

[32](in Chinese) Zhang Y K, Han X J, Chen X L, Jin H, Cui X M. 2009. Exogenous nitric oxide on antioxidative system and ATPase activities from tomato seedlings under copper stress. Scientia Horticulturae, 123, 217-223. (in Chinese)
[1] HU Mei-mei, DOU Qiao-hui, CUI Xiu-min, LOU Yan-hong, ZHUGE Yu-ping. Polyaspartic acid mediates the absorption and translocation of mineral elements in tomato seedlings under combined copper and cadmium stress[J]. >Journal of Integrative Agriculture, 2019, 18(5): 1130-1137.
[2] WEI Kang, WANG Li-yuan, RUAN Li, ZHANG Cheng-cai, WU Li-yun, LI Hai-lin, CHENG Hao. Endogenous nitric oxide and hydrogen peroxide detection in indole- 3-butyric acid-induced adventitious root formation in Camellia sinensis[J]. >Journal of Integrative Agriculture, 2018, 17(10): 2273-2280.
[3] LIU Bin, CHEN Li, CHEN Shi-bao, LI Ning, ZHENG Han, JIN Ke, PANG Huan-cheng, MA Yi-bing. Subcellular Cd accumulation characteristic in root cell wall of rice cultivars with different sensitivities to Cd stress in soil[J]. >Journal of Integrative Agriculture, 2016, 15(9): 2114-2122.
[4] LIU Yu-chen, WANG Juan, SU Pei-ying, MA Chun-mei , ZHU Shu-hua. Effect of Nitric Oxide on the Interaction Between Mitochondrial Malate Dehydrogenase and Citrate Synthase[J]. >Journal of Integrative Agriculture, 2014, 13(12): 2616-2624.
[5] ZHAO Xiu-feng, CHEN Lin, Muhammad I A Rehmani, WANG Qiang-sheng, WANG Shao-hua, HOU Pengfu, LI Gang-hua , DING Yan-feng. Effect of Nitric Oxide on Alleviating Cadmium Toxicity in Rice (Oryza sativa L.)[J]. >Journal of Integrative Agriculture, 2013, 12(9): 1540-1550.
[6] ZHANG Zi-kun, LI Hua, HE Hong-jun , LIU Shi-qi. Grafting Raises the Cu Tolerance of Cucumber Through Protecting Roots Against Oxidative Stress Induced by Cu Stress[J]. >Journal of Integrative Agriculture, 2013, 12(5): 815-824.
[7] GUO Jun-xiang, CHEN Er-ying, YIN Yan-ping, WANG Ping, LI Yong, CHEN Xiao-guang, WU Guanglei. Nitric Oxide Content in Wheat Leaves and Its Relation to Programmed Cell Death of Main Stem and Tillers Under Different Nitrogen Levels[J]. >Journal of Integrative Agriculture, 2013, 12(2): 239-250.
[8] Mahesh S Kulye, LIU Hua, QIU De-wen. The Role of Radical Burst in Plant Defense Responses to Necrotrophic Fungi[J]. >Journal of Integrative Agriculture, 2012, 12(8): 1305-1312.
[9] LIU Jing, HOU Zhi-hui, LIU Guo-hua, HOU Li-xia, LIU Xin. Hydrogen Sulfide May Function Downstream of Nitric Oxide in Ethylene- Induced Stomatal Closure in Vicia faba L.[J]. >Journal of Integrative Agriculture, 2012, 12(10): 1644-1653.
[10] LIU Li-qin, DONG Yu, GUAN Jun-feng. Effects of Nitric Oxide on the Quality and Pectin Metabolism of Yali Pears During Cold Storage[J]. >Journal of Integrative Agriculture, 2011, 10(7): 1125-1133.
No Suggested Reading articles found!