The Induction of Antioxidant Enzyme Activities in Cabbage Seedlings by Heavy Metal Stress
Cabbage seedlings grown in vitro were exposed to
excess levels of heavy metals, including Cd, Mo, and Zn. High metal
levels affected plant growth at cotyledonary stage. Seedlings under
Cd, Mo, and Zn treatments could not produce root hairs and true
leaves. Under stress conditions, seedlings accumulated a higher
amount of anthocyanins in their cotyledons than those in the control.
The pigments isolated from Cd and Zn stressed seedling cotyledons
appeared as pink, while under Mo stress, was dark pink or purple.
Moreover, excess Mo stress increased antioxidant enzyme activities
of APX, CAT, SOD. These results suggest that, under excess Mo
stress, the induced antioxidant enzyme activity of cabbage seedlings
may function as a protective mechanism to shield the plants from
toxicity and exacerbated growth.
[1] B. Passariello, V. Giuliano, S. Quaresima, M. Barbaro, S. Caroli, G.
Forte, G. Carelli, and I. Iavicoli, "Evaluation of the environmental
contamination at an abandoned mining site. Microchem. J., vol. 73, pp.
245-250. 2002.
[2] T. J. Bricker, J. Pichtel, H. J. Brown, and M. Simmons, "Phytoextraction
of Pb and Cd from superficial soil: effects of amendments and
croppings," J. Environ. Science. Health. Part A Toxic/Hazardous
Substances and Environmental Engineering, vol. 36, pp. 1597-1610,
2001.
[3] R. R. Mendel, "Molybdenum: biological activity and metabolism,"
Dalton Trans. vol. 21, pp. 3404-3409, Nov. 2005.
[4] K. S. Smith, L. S. Balistrieri, S. M. Smith and R. C. Severson,
"Distribution and Mobility of Molybdenum in the Terrestrial
Environment," in Molybdenum in Agriculture, U. C. Gupta, Ed.
Cambridge: Cambridge University Press, 1997, pp. 23-46.
[5] J. L. Stroud, F. J. Zhao, P. Buchner, F. Shinmachi, S. P. McGrath, J.
Abecassis, M. J. Hawkesford, and P. R. Shewry, "Impacts of sulphur
nutrition on selenium and molybdenum concentrations in wheat grain,"
J. Cereal Sci., vol. 52, pp. 111-113, 2010.
[6] M. S. Warne, D. Heemsbergen, D. Stevens, M. McLaughlin, G. Cozens,
M. Whatmuff, K. Broos, G. Barry, M. Bell, D. Nash, D. Pritchard, and
N. Penney, "Modeling the toxicity of copper and zinc salts to wheat in
14 soils," Environ. Toxicol. Chem., vol. 27, pp. 786-792, Apr. 2008.
[7] P. Mohanpuria, N. K. Rana, and S. K. Yadav, "Cadmium induced
oxidative stress influence on glutathione metabolic genes of Camellia
sinensis (L.) O. Kuntze," Environ. Toxicol., vol. 22, pp. 368-374, Aug.
2007.
[8] M. M. Posmyk, R. Kontek and K. M. Janas, "Antioxidant enzymes
activity and phenolic compounds content in red cabbage seedlings
exposed to copper stress," Ecotoxicol. Environ. Saf., vol. 72, pp. 596-
602, Feb. 2009.
[9] C. Bowler, M. Vanmontagu and D. Inze, "Superoxide dismutase and
stress tolerance," Ann. Rev. Plant Physiol. Mol. Biol., vol. 43, pp. 83-
116, June 1992.
[10] S. Srivastava. A. D. Pathak, P. S. Gupta, A. K. Shrivastava, and A. K.
Srivastava, "Hydrogen peroxide-scavenging enzymes impart tolerance to
high temperature induced oxidative stress in sugarcane," J. Environ.
Biol., vol. 33, pp. 657-661, May 2012.
[11] T. Murashige, and F. Skoog, "A revised medium for rapid growth and
bioassays with tobacco tissue cultures," Physiol. Plant, vol.15, pp. 473-
497, 1962.
[12] M. M. Giusti, and R. E. Wrolstad, "Anthocyanins Characterization and
Measurement of Anthocyanins by UV-Visible Spectroscopy," in Current
Protocols in Food Analytical Chemistry Hand Book of Food Analytical
Chemistry, vol. 12, R. E. Wrolstad, T. E. Acree, E. A. Decker, M. H.
Penner, D. S. Reid, S. J. Schwartz, C. F. Shoemker, D. Smith, and P.
Sporns, Ed. New York: John Wiley & Sons, 2001, pp.19-32,
[13] E. Gajewska, and M. Skłodowska, "Antioxidative responses and proline
level in leaves and roots of pea plants subjected to nickel stress," Acta
Physiol. Plant, vol. 27, pp. 329-339, 2005.
[14] M. M. Bradford, "A rapid and sensitive method for the quantification of
microgram quantities of protein utilizing the principle of protein-dye
binding," Anal. Biochem., vol. 72, pp. 248-254, May 1976.
[15] M. Minami, and H. Yoshikawa, "A simplified assay method of super
oxide dismutase," Clin. Chim. Acta, vol. 29, pp. 337-342, 1979.
[16] F. Paoletti, D. Aldinucci, A. Mocali, and A. Capparini, "A sensitive
spectrophotometric method for the determination of superoxide
dismutase activity in tissue extracts," Anal. Biochem., vol. 154, pp. 536-
541, May 1986.
[17] Y. Nakano, and K. Asada, "Hydrogen peroxide is scavenged by
ascorbate specific peroxidase in spinach chloroplasts," Plant Cell
Physiol., vol. 22, pp. 867-880, 1981.
[18] M. Kato, and S. Shimizu, "Chlorophyll metabolism in higher plants VI.
Involvement of peroxidase in chlorophyll degradation," Plant Cell
Physiol., vol. 26, pp. 1291-1301, 1985.
[19] S. P. McGrath, C. Mic├│, R. Curdy, and F. J. Zhao, "Predicting
molybdenum toxicity to higher plants: Influence of soil properties,"
Environ. Poll., vol.158, pp. 3095-3102, Oct. 2010.
[20] X. Bia, X. Fenga, Y. Yanga, G. Qiua, G. Lia, F. Lia, T. Liua, Z. Fua, and
Z. Jina, "Environmental contamination of heavy metals from zinc
smelting areas in Hezhang County, western Guizhou, China," Environ.
Inter., vol. 32, pp. 883-890, Sep. 2006.
[21] R. R. Mendel, "Biology of the molybdenum cofactor," J. Exp. Bot., vol.
58, pp. 2289-2296, Mar. 2007.
[22] S. S. Sharma, and K. J. Dietz, "The significance of amino acids and
amino acid derived molecules in plant responses and adaptation to heavy
metal stress," J. Exp. Bot., vol. 57, pp. 711-726, Mar. 2006.
[23] S. Chutipaijit, S. Cha-um, and K. Sompornpailin, "High contents of
proline and anthocyanin increase protective response to salinity in Oryza
sativa L. spp. indica," Aust. J. Crop Sci., vol. 5, pp. 1191-1198, 2011.
[24] S. L. di Toppi, and R. Gabrielli, "Response to cadmium in higher
plants," Environ. Exp. Bot., vol. 41, pp. 105-130, Apr. 1999.
[25] I. Sperdouli and M. Moustakas, "Interaction of proline, sugars, and
anthocyanins during photosynthetic acclimation of Arabidopsis thaliana
to drought stress," J. Plant Physiol., vol. 169, pp. 577-585, Apr. 2012.
[26] K. S. Gould, "Nature-s Swiss army knife: The diverse protective roles of
anthocyanins in leaves," J. Biomed. Biotechnol., vol. 2004, pp. 314-320,
Dec. 2004.
[27] V. V. Bolda, D. Botau1, R. Sz├┤ll├┤si, A. Pet├┤, A Gallé, and I. Tari,
"Studies on elemental composition and antioxidant capacity in callus
cultures and native plants of Vaccinium myrtillus L. local populations,"
Acta Biol. Szeged., vol. 55, pp. 255-259, 2011.
[28] L. P. Dai, X. J. Dong, and H. H. Ma, "Molecular mechanism for
cadmium-induced anthocyanin accumulation in Azolla imbricate,"
Chemosphere, vol. 87, pp. 319-325, Jan. 2012.
[29] V. Pasqualini, C. Robles, S. Garzino, S. Greff, A. Bousquet-Melou, and
G. Bonin, "Phenolic compounds content in Pinus halepensis Mill.
needles: a bioindicator of air pollution," Chemosphere, vol. 52, pp. 239-
248, Jul. 2003.
[30] M. Mobin, and N. A. Khan, "Photosynthetic activity, pigment
composition and antioxidative response of two mustard (Brassica
juncea) cultivars differing in photosynthetic capacity subjected to
cadmium stress," J. Plant Physiol., vol. 164, pp. 601-610, Apr. 2007.
[31] A. Sivaci, and E. Elmas, "The combined effects of cadmium and salinity
on some pigments and total phenolic compounds of Myriophyllum
heterophyllum Michx. and Potamogeton crispus L.," Afr. J. Agric. Res.,
vol. 7, pp. 3813-3818, Jul. 2012.
[32] R. K. Tewari, S. Y. Kim, E. J. Hahn, and K. Y. Paek, "Involvement of
nitric oxideinduced NADPH oxidase in adventitious root growth and
antioxidant defense in Panax ginseng," Plant Biotechnol. Rep., vol. 2,
pp. 113-122, June 2008.
[33] M. D. Groppa, M. L. Tomaro, and M. P. Benavides, "Polyamines as
protector against cadmium or copper-induced oxidative damage in
sunflower leaf discs," Plant Sci., vol. 161, pp. 481-488, Aug. 2001.
[34] E. Lombi, F. J. Zhao, S. J. Dunhan, and S. P. McGrath, "Cadmium
accumulation in populations of Thlaspi caerulescens and Thlaspi
goesingense," New Phytol., vol. 145, pp.11-20, Jan. 2000.
[35] M. C. Romero-Puertas, I. McCarthy, L. M. Sandalio, J. M. Palma, F. J.
Corpas, M. Gomez, and L. A. del Rio, "Cadmium toxicity and oxidative
metabolism of pea leaf peroxisomes," Fee Rad. Res., vol. 31, pp. 21-31,
Dec. 1999.
[36] P. Liu, Y. S. Yang, G.D. Xu, Y. H. Fang, and Y. A. Yang, "The
response of antioxidant enzymes of three soybean varieties to
molybdenum and boron in soil with a connection to plant quality," Plant
Soil Environ., vol. 51, pp. 351-359, 2005.
[1] B. Passariello, V. Giuliano, S. Quaresima, M. Barbaro, S. Caroli, G.
Forte, G. Carelli, and I. Iavicoli, "Evaluation of the environmental
contamination at an abandoned mining site. Microchem. J., vol. 73, pp.
245-250. 2002.
[2] T. J. Bricker, J. Pichtel, H. J. Brown, and M. Simmons, "Phytoextraction
of Pb and Cd from superficial soil: effects of amendments and
croppings," J. Environ. Science. Health. Part A Toxic/Hazardous
Substances and Environmental Engineering, vol. 36, pp. 1597-1610,
2001.
[3] R. R. Mendel, "Molybdenum: biological activity and metabolism,"
Dalton Trans. vol. 21, pp. 3404-3409, Nov. 2005.
[4] K. S. Smith, L. S. Balistrieri, S. M. Smith and R. C. Severson,
"Distribution and Mobility of Molybdenum in the Terrestrial
Environment," in Molybdenum in Agriculture, U. C. Gupta, Ed.
Cambridge: Cambridge University Press, 1997, pp. 23-46.
[5] J. L. Stroud, F. J. Zhao, P. Buchner, F. Shinmachi, S. P. McGrath, J.
Abecassis, M. J. Hawkesford, and P. R. Shewry, "Impacts of sulphur
nutrition on selenium and molybdenum concentrations in wheat grain,"
J. Cereal Sci., vol. 52, pp. 111-113, 2010.
[6] M. S. Warne, D. Heemsbergen, D. Stevens, M. McLaughlin, G. Cozens,
M. Whatmuff, K. Broos, G. Barry, M. Bell, D. Nash, D. Pritchard, and
N. Penney, "Modeling the toxicity of copper and zinc salts to wheat in
14 soils," Environ. Toxicol. Chem., vol. 27, pp. 786-792, Apr. 2008.
[7] P. Mohanpuria, N. K. Rana, and S. K. Yadav, "Cadmium induced
oxidative stress influence on glutathione metabolic genes of Camellia
sinensis (L.) O. Kuntze," Environ. Toxicol., vol. 22, pp. 368-374, Aug.
2007.
[8] M. M. Posmyk, R. Kontek and K. M. Janas, "Antioxidant enzymes
activity and phenolic compounds content in red cabbage seedlings
exposed to copper stress," Ecotoxicol. Environ. Saf., vol. 72, pp. 596-
602, Feb. 2009.
[9] C. Bowler, M. Vanmontagu and D. Inze, "Superoxide dismutase and
stress tolerance," Ann. Rev. Plant Physiol. Mol. Biol., vol. 43, pp. 83-
116, June 1992.
[10] S. Srivastava. A. D. Pathak, P. S. Gupta, A. K. Shrivastava, and A. K.
Srivastava, "Hydrogen peroxide-scavenging enzymes impart tolerance to
high temperature induced oxidative stress in sugarcane," J. Environ.
Biol., vol. 33, pp. 657-661, May 2012.
[11] T. Murashige, and F. Skoog, "A revised medium for rapid growth and
bioassays with tobacco tissue cultures," Physiol. Plant, vol.15, pp. 473-
497, 1962.
[12] M. M. Giusti, and R. E. Wrolstad, "Anthocyanins Characterization and
Measurement of Anthocyanins by UV-Visible Spectroscopy," in Current
Protocols in Food Analytical Chemistry Hand Book of Food Analytical
Chemistry, vol. 12, R. E. Wrolstad, T. E. Acree, E. A. Decker, M. H.
Penner, D. S. Reid, S. J. Schwartz, C. F. Shoemker, D. Smith, and P.
Sporns, Ed. New York: John Wiley & Sons, 2001, pp.19-32,
[13] E. Gajewska, and M. Skłodowska, "Antioxidative responses and proline
level in leaves and roots of pea plants subjected to nickel stress," Acta
Physiol. Plant, vol. 27, pp. 329-339, 2005.
[14] M. M. Bradford, "A rapid and sensitive method for the quantification of
microgram quantities of protein utilizing the principle of protein-dye
binding," Anal. Biochem., vol. 72, pp. 248-254, May 1976.
[15] M. Minami, and H. Yoshikawa, "A simplified assay method of super
oxide dismutase," Clin. Chim. Acta, vol. 29, pp. 337-342, 1979.
[16] F. Paoletti, D. Aldinucci, A. Mocali, and A. Capparini, "A sensitive
spectrophotometric method for the determination of superoxide
dismutase activity in tissue extracts," Anal. Biochem., vol. 154, pp. 536-
541, May 1986.
[17] Y. Nakano, and K. Asada, "Hydrogen peroxide is scavenged by
ascorbate specific peroxidase in spinach chloroplasts," Plant Cell
Physiol., vol. 22, pp. 867-880, 1981.
[18] M. Kato, and S. Shimizu, "Chlorophyll metabolism in higher plants VI.
Involvement of peroxidase in chlorophyll degradation," Plant Cell
Physiol., vol. 26, pp. 1291-1301, 1985.
[19] S. P. McGrath, C. Mic├│, R. Curdy, and F. J. Zhao, "Predicting
molybdenum toxicity to higher plants: Influence of soil properties,"
Environ. Poll., vol.158, pp. 3095-3102, Oct. 2010.
[20] X. Bia, X. Fenga, Y. Yanga, G. Qiua, G. Lia, F. Lia, T. Liua, Z. Fua, and
Z. Jina, "Environmental contamination of heavy metals from zinc
smelting areas in Hezhang County, western Guizhou, China," Environ.
Inter., vol. 32, pp. 883-890, Sep. 2006.
[21] R. R. Mendel, "Biology of the molybdenum cofactor," J. Exp. Bot., vol.
58, pp. 2289-2296, Mar. 2007.
[22] S. S. Sharma, and K. J. Dietz, "The significance of amino acids and
amino acid derived molecules in plant responses and adaptation to heavy
metal stress," J. Exp. Bot., vol. 57, pp. 711-726, Mar. 2006.
[23] S. Chutipaijit, S. Cha-um, and K. Sompornpailin, "High contents of
proline and anthocyanin increase protective response to salinity in Oryza
sativa L. spp. indica," Aust. J. Crop Sci., vol. 5, pp. 1191-1198, 2011.
[24] S. L. di Toppi, and R. Gabrielli, "Response to cadmium in higher
plants," Environ. Exp. Bot., vol. 41, pp. 105-130, Apr. 1999.
[25] I. Sperdouli and M. Moustakas, "Interaction of proline, sugars, and
anthocyanins during photosynthetic acclimation of Arabidopsis thaliana
to drought stress," J. Plant Physiol., vol. 169, pp. 577-585, Apr. 2012.
[26] K. S. Gould, "Nature-s Swiss army knife: The diverse protective roles of
anthocyanins in leaves," J. Biomed. Biotechnol., vol. 2004, pp. 314-320,
Dec. 2004.
[27] V. V. Bolda, D. Botau1, R. Sz├┤ll├┤si, A. Pet├┤, A Gallé, and I. Tari,
"Studies on elemental composition and antioxidant capacity in callus
cultures and native plants of Vaccinium myrtillus L. local populations,"
Acta Biol. Szeged., vol. 55, pp. 255-259, 2011.
[28] L. P. Dai, X. J. Dong, and H. H. Ma, "Molecular mechanism for
cadmium-induced anthocyanin accumulation in Azolla imbricate,"
Chemosphere, vol. 87, pp. 319-325, Jan. 2012.
[29] V. Pasqualini, C. Robles, S. Garzino, S. Greff, A. Bousquet-Melou, and
G. Bonin, "Phenolic compounds content in Pinus halepensis Mill.
needles: a bioindicator of air pollution," Chemosphere, vol. 52, pp. 239-
248, Jul. 2003.
[30] M. Mobin, and N. A. Khan, "Photosynthetic activity, pigment
composition and antioxidative response of two mustard (Brassica
juncea) cultivars differing in photosynthetic capacity subjected to
cadmium stress," J. Plant Physiol., vol. 164, pp. 601-610, Apr. 2007.
[31] A. Sivaci, and E. Elmas, "The combined effects of cadmium and salinity
on some pigments and total phenolic compounds of Myriophyllum
heterophyllum Michx. and Potamogeton crispus L.," Afr. J. Agric. Res.,
vol. 7, pp. 3813-3818, Jul. 2012.
[32] R. K. Tewari, S. Y. Kim, E. J. Hahn, and K. Y. Paek, "Involvement of
nitric oxideinduced NADPH oxidase in adventitious root growth and
antioxidant defense in Panax ginseng," Plant Biotechnol. Rep., vol. 2,
pp. 113-122, June 2008.
[33] M. D. Groppa, M. L. Tomaro, and M. P. Benavides, "Polyamines as
protector against cadmium or copper-induced oxidative damage in
sunflower leaf discs," Plant Sci., vol. 161, pp. 481-488, Aug. 2001.
[34] E. Lombi, F. J. Zhao, S. J. Dunhan, and S. P. McGrath, "Cadmium
accumulation in populations of Thlaspi caerulescens and Thlaspi
goesingense," New Phytol., vol. 145, pp.11-20, Jan. 2000.
[35] M. C. Romero-Puertas, I. McCarthy, L. M. Sandalio, J. M. Palma, F. J.
Corpas, M. Gomez, and L. A. del Rio, "Cadmium toxicity and oxidative
metabolism of pea leaf peroxisomes," Fee Rad. Res., vol. 31, pp. 21-31,
Dec. 1999.
[36] P. Liu, Y. S. Yang, G.D. Xu, Y. H. Fang, and Y. A. Yang, "The
response of antioxidant enzymes of three soybean varieties to
molybdenum and boron in soil with a connection to plant quality," Plant
Soil Environ., vol. 51, pp. 351-359, 2005.
@article{"International Journal of Biological, Life and Agricultural Sciences:63675", author = "J. Kumchai and J. Z. Huang and C. Y. Lee and F. C. Chen and S. W. Chin", title = "The Induction of Antioxidant Enzyme Activities in Cabbage Seedlings by Heavy Metal Stress", abstract = "Cabbage seedlings grown in vitro were exposed to
excess levels of heavy metals, including Cd, Mo, and Zn. High metal
levels affected plant growth at cotyledonary stage. Seedlings under
Cd, Mo, and Zn treatments could not produce root hairs and true
leaves. Under stress conditions, seedlings accumulated a higher
amount of anthocyanins in their cotyledons than those in the control.
The pigments isolated from Cd and Zn stressed seedling cotyledons
appeared as pink, while under Mo stress, was dark pink or purple.
Moreover, excess Mo stress increased antioxidant enzyme activities
of APX, CAT, SOD. These results suggest that, under excess Mo
stress, the induced antioxidant enzyme activity of cabbage seedlings
may function as a protective mechanism to shield the plants from
toxicity and exacerbated growth.", keywords = "Anthocyanin, antioxidant enzyme activity, heavy
metal, growth inhibition.", volume = "7", number = "1", pages = "78-6", }
