Betacyanin accumulation and guaiacol peroxidase activity in Beta vulgaris L. leaves following copper stress

Janet M. León Morales, Mario Rodríguez-Monroy, Gabriela Sepúlveda-Jiménez

Abstract


The effect of copper stress on betacyanin accumulation and guaiacol peroxidase (GPOD) activity in leaves of different age was evaluated in red beet (Beta vulgaris L. var. Crosby Egyptian) plants. In hydroponic culture, plants were treated with 0.3 μM (control), 50 μM, 100 μM, and 250 μM of CuSO4 for 6 days. Copper was taken up and accumulated in old roots but was not translocated to leaves. However in young leaves, the increase of lipid peroxidation and reduction of growth were evident from day 3 of copper exposure; whereas in old leaves, the lipid peroxidation and growth were the same from either copper-treated or control plants. In response to copper exposure, the betacyanin accumulation was evident in young leaves by day 3, and continued to increase until day 6. Betacyanin only were accumulated in old leaves until day 6, but the contents were from 4 to 5 times lower than those observed in young leaves at the same copper concentrations. GPOD activity increased 3.3- and 1.4-fold in young and old leaves from day 3 of copper treatment respectively, but only in the young leaves was sustained at the same level until day 6. Old roots shown betacyanin in the control plants, but the betacyanin level and growth were reduced with the copper exposure. In contrast, young roots emerged by copper effect also accumulated copper and showed the highest betacyanin content of all plant parts assayed. These results indicate that betacyanin accumulation and GPOD activity are defense responses to copper stress in actively growing organs.

Keywords


oxidative stress; betacyanin; abiotic stress; antioxidant compound; copper

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References


Nagajyoti PC, Lee KD, Sreekanth TVM. Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett. 2010;8(3):199-216. http://dx.doi.org/10.1007/s10311-010-0297-8

Salisbury FB, Ross CW. Plant physiology. Belmont CA: Wadsworth Pub. Co.; 1992. (vol 1).

Pasternak T, Rudas V, Potters G, Jansen M. Morphogenic effects of abiotic stress: reorientation of growth in seedlings. Environ Exp Bot. 2005;53(3):299-314. http://dx.doi.org/10.1016/j.envexpbot.2004.04.009

Jiang W, Liu D, Liu X. Effects of copper on root growth, cell division, and nucleolus of Zea mays. Biol Plant. 2001;44(1):105-109. http://dx.doi.org/10.1023/A:1017982607493

Liu D, Jiang W, Meng Q, Zou J, Gu J, Zeng M. Cytogenetical and ultrastructural effects of copper on root meristem cells of Allium sativum L. Biocell. 2009;33:25-32.

Lequeux H, Hermans C, Lutts S, Verbruggen N. Response to copper excess in Arabidopsis thaliana: impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiol Biochem. 2010;48(8):673-682. http://dx.doi.org/10.1016/j.plaphy.2010.05.005

Zhang H, Xia Y, Wang G, Shen Z. Excess copper induces accumulation of hydrogen peroxide and increases lipid peroxidation and total activity of copper-zinc superoxide dismutase in roots of Elsholtzia haichowensis. Planta. 2007;227(2):465-475. http://dx.doi.org/10.1007/s00425-007-0632-x

Maksymiec W. Signaling responses in plants to heavy metal stress. Acta Physiol Plant. 2007;29(3):177-187. http://dx.doi.org/10.1007/s11738-007-0036-3

Drażkiewicz M, Skórzyńska-Polit E, Krupa Z. Copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana. BioMetals. 2004;17(4):379-387. http://dx.doi.org/10.1023/B:BIOM.0000029417.18154.22

Mediouni C, Ammar WB, Houlné G, Chabouté ME, Jemal F. Cadmium and copper induction of oxidative stress and antioxidative response in tomato (Solanum lycopersicon) leaves. Plant Growth Regul. 2008;57(1):89-99. http://dx.doi.org/10.1007/s10725-008-9324-1

Khatun S, Ali MB, Hahn EJ, Paek KY. Copper toxicity in Withania somnifera: Growth and antioxidant enzymes responses of in vitro grown plants. Environ Exp Bot. 2008;64(3):279-285. http://dx.doi.org/10.1016/j.envexpbot.2008.02.004

Kováčik J, Grúz J, Bačkor M, Tomko J, Strnad M, Repčák M. Phenolic compounds composition and physiological attributes of Matricaria chamomilla grown in copper excess. Environ Exp Bot. 2008;62(2):145-152. http://dx.doi.org/10.1016/j.envexpbot.2007.07.012

Groppa MD, Tomaro ML, Benavides MP. Polyamines and heavy metal stress: the antioxidant behavior of spermine in cadmium- and copper-treated wheat leaves. BioMetals. 2006;20(2):185-195. http://dx.doi.org/10.1007/s10534-006-9026-y

Sgherri C, Cosi E, Navari-Izzo F. Phenols and antioxidative status of Raphanus sativus grown in copper excess. Physiol Plant. 2003;118(1):21-28. http://dx.doi.org/10.1034/j.1399-3054.2003.00068.x

Jouili H, Bouazizi H, El Ferjani E. Plant peroxidases: biomarkers of metallic stress. Acta Physiol Plant. 2011;33(6):2075-2082. http://dx.doi.org/10.1007/s11738-011-0780-2

Chaoui A, Jarrar B, EL Ferjani E. Effects of cadmium and copper on peroxidase, NADH oxidase and IAA oxidase activities in cell wall, soluble and microsomal membrane fractions of pea roots. J Plant Physiol. 2004;161(11):1225-1234. http://dx.doi.org/10.1016/j.jplph.2004.02.002

Zhang H, Zhang F, Xia Y, Wang G, Shen Z. Excess copper induces production of hydrogen peroxide in the leaf of Elsholtzia haichowensis through apoplastic and symplastic CuZn-superoxide dismutase. J Hazard Mater. 2010;178(1-3):834-843. http://dx.doi.org/10.1016/j.jhazmat.2010.02.014

Lin CC, Chen LM, Liu ZH. Rapid effect of copper on lignin biosynthesis in soybean roots. Plant Sci. 2005;168(3):855-861. http://dx.doi.org/10.1016/j.plantsci.2004.10.023

Maksymiec W, Russa R, Urbanik-Sypniewska T, Baszynski T. Effect of excess Cu on the photosynthetic apparatus of runner bean leaves treated at two different growth stages. Physiol Plant. 1994;91(4):715-721. http://dx.doi.org/10.1111/j.1399-3054.1994.tb03010.x

Vinit-Dunand F, Epron D, Alaoui-Sossé B, Badot PM. Effects of copper on growth and on photosynthesis of mature and expanding leaves in cucumber plants. Plant Sci. 2002;163(1):53-58. http://dx.doi.org/10.1016/S0168-9452(02)00060-2

Luna CM, González CA. Oxidative damage caused by an excess of copper in oat leaves. Plant Cell Physiol. 1993;35:11-15.

Tewari RK, Kumar P, Sharma PN. Antioxidant responses to enhanced generation of superoxide anion radical and hydrogen peroxide in the copper-stressed mulberry plants. Planta. 2005;223(6):1145-1153. http://dx.doi.org/10.1007/s00425-005-0160-5

Kováčik J, Bačkor M, Kaduková J. Physiological responses of Matricaria chamomilla to cadmium and copper excess. Environ Toxicol. 2008;23(1):123-130. http://dx.doi.org/10.1002/tox.20315

Skórzyńska-Polit E, Drażkiewicz M, Wianowska D, Maksymiec W, Dawidowicz AL, Tukiendorf A. The influence of heavy metal stress on the level of some flavonols in the primary leaves of Phaseolus coccineus. Acta Physiol Plant. 2004;26(3):247-254. http://dx.doi.org/10.1007/s11738-004-0014-y

Strack D, Steglich W, Wray V. Betalains. In: Waterman PG, editor. Methods in plant biochemistry. New York: Academic Press; 1993. p. 421-450. (vol 8).

Escribano J, Pedreño MA, García-Carmona F, Muñoz R. Characterization of the antiradical activity of betalains from Beta vulgaris L. roots. Phytochem Anal. 1998;9(3):124-127. http://dx.doi.org/10.1002/(SICI)1099-1565(199805/06)9:3<124::AID-PCA401>3.0.CO;2-0

Kanner J, Harel S, Granit R. Betalains: a new class of dietary cationized antioxidants. J Agric Food Chem. 2001;49(11):5178-5185. http://dx.doi.org/10.1021/jf010456f

Ibdah M, Krins A, Seidlitz HK, Heller W, Strack D, Vogt T. Spectral dependence of flavonol and betacyanin accumulation in Mesembryanthemum crystallinum under enhanced ultraviolet radiation. Plant Cell Environ. 2002;25(9):1145-1154. http://dx.doi.org/10.1046/j.1365-3040.2002.00895.x

Sepúlveda-Jiménez G, Rueda-Benítez P, Porta H, Rocha-Sosa M. Betacyanin synthesis in red beet (Beta vulgaris) leaves induced by wounding and bacterial infiltration is preceded by an oxidative burst. Physiol Mol Plant Pathol. 2004;64(3):125-133. http://dx.doi.org/10.1016/j.pmpp.2004.08.003

Wang CQ, Zhao JQ, Chen M, Wang BS. Identification of betacyanin and effects of environmental factors on its accumulation in halophyte Suaeda salsa. J Plant Physiol Mol Biol. 2006;32:195-201.

Wang CQ, Chen M, Wang BS. Betacyanin accumulation in the leaves of C3 halophyte Suaeda salsa L. is induced by watering roots with H2O2. Plant Sci. 2007;172(1):1-7. http://dx.doi.org/10.1016/j.plantsci.2006.06.015

Lichtenthaler HK. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol. 1987;148:350-382. http://dx.doi.org/10.1016/0076-6879(87)48036-1

Alia, Prasad KVSK, Pardha Saradhi P. Effect of zinc on free radicals and proline in Brassica and Cajanus. Phytochemistry. 1995;39(1):45-47. http://dx.doi.org/10.1016/0031-9422(94)00919-K

Schwartz SJ, Von Elbe JH. Quantitative determination of individual betacyanin pigments by high-performance liquid chromatography. J Agric Food Chem. 1980;28(3):540-543. http://dx.doi.org/10.1021/jf60229a032

Stasolla C, Yeung EC. Cellular ascorbic acid regulates the activity of major peroxidases in the apical poles of germinating white spruce (Picea glauca) somatic embryos. Plant Physiol Biochem. 2007;45(3-4):188-198. http://dx.doi.org/10.1016/j.plaphy.2007.02.007

Fernandes JC, Henriques FS. Biochemical, physiological, and structural effects of excess copper in plants. Bot Rev. 1991;57(3):246-273. http://dx.doi.org/10.1007/BF02858564

Russo M, Sgherri C, Izzo R, Navari-Izzo F. Brassica napus subjected to copper excess: phospholipases C and D and glutathione system in signalling. Environ Exp Bot. 2008;62(3):238-246. http://dx.doi.org/10.1016/j.envexpbot.2007.09.003

Chen CT, Chen TH, Lo KF, Chiu CY. Effects of proline on copper transport in rice seedlings under excess copper stress. Plant Sci. 2004;166(1):103-111. http://dx.doi.org/10.1016/j.plantsci.2003.08.015

Lim PO, Nam HG. Aging and senescence of the leaf organ. J Plant Biol. 2007;50(3):291-300. http://dx.doi.org/10.1007/BF03030657

Cuypers A, Vangronsveld J, Clijsters H. Biphasic effect of copper on the ascorbate-glutathione pathway in primary leaves of Phaseolus vulgaris seedlings during the early stages of metal assimilation. Physiol Plant. 2000;110(4):512-517. http://dx.doi.org/10.1111/j.1399-3054.2000.1100413.x

Remans T, Opdenakker K, Smeets K, Mathijsen D, Vangronsveld J, Cuypers A. Metal-specific and NADPH oxidase dependent changes in lipoxygenase and NADPH oxidase gene expression in Arabidopsis thaliana exposed to cadmium or excess copper. Funct Plant Biol. 2010;37(6):532. http://dx.doi.org/10.1071/FP09194

Cuypers A, Smeets K, Ruytinx J, Opdenakker K, Keunen E, Remans T, et al. The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thaliana seedlings. J Plant Physiol. 2011;168(4):309-316. http://dx.doi.org/10.1016/j.jplph.2010.07.010

Donahue JL, Okpodu CM, Cramer CL, Grabau EA, Alscher RG. Responses of antioxidants to paraquat in pea leaves (relationships to resistance). Plant Physiol. 1997;113(1):249-257. http://dx.doi.org/10.1104/pp.113.1.249

Ohe M, Rapolu M, Mieda T, Miyagawa Y, Yabuta Y, Yoshimura K, et al. Decline in leaf photooxidative-stress tolerance with age in tobacco. Plant Sci. 2005;168(6):1487-1493. http://dx.doi.org/10.1016/j.plantsci.2005.01.020

Jung S. Variation in antioxidant metabolism of young and mature leaves of Arabidopsis thaliana subjected to drought. Plant Sci. 2004;166(2):459-466. http://dx.doi.org/10.1016/j.plantsci.2003.10.012

Martínez-Parra J, Muñoz R. Characterization of betacyanin oxidation catalyzed by a peroxidase from Beta vulgaris L. roots. J Agric Food Chem. 2001;49(8):4064-4068. http://dx.doi.org/10.1021/jf0013555

Kasim WA. Changes induced by copper and cadmium stress in the anatomy and grain yield of Sorghum bicolor (L.) Moench. Int J Agri Biol. 2006;8:123-128.




DOI: https://doi.org/10.5586/asbp.2012.019

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