Biologia plantarum 52:413-422, 2008 | DOI: 10.1007/s10535-008-0085-5

Production of reactive oxygen species and development of antioxidative systems during in vitro growth and ex vitro transfer

P. Baťková1,2, J. Pospíšilová1,*, H. Synková1
1 Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Prague, Czech Republic
2 Faculty of Science, Charles University Prague, Prague, Czech Republic

Ex vitro transfer is often stressful for in vitro grown plantlets. Water stress and photoinhibition, often accompanying the acclimatization of in vitro grown plantlets to ex vitro conditions, are probably the main factors promoting production of reactive oxygen species (ROS) and in consequence oxidative stress. The extent of the damaging effects of ROS depends on the effectiveness of the antioxidative systems which include low molecular mass antioxidants (ascorbate, glutathione, tocopherols, carotenoids, phenols) and antioxidative enzymes (superoxide dismutase, ascorbate peroxidase, catalase, glutathione reductase, monodehydroascorbate reductase, dehydroascorbate reductase). This review is focused on ROS production and development of antioxidative system during in vitro growth and their further changes during ex vitro transfer.

Keywords: ascorbate; ascorbate peroxidase; carotenoids; catalase; dehydroascorbate reductase; glutathione; glutathione reductase; malondialdehyde; peroxidase; superoxide dismutase
Subjects: antioxidants, antioxidant enzymes; ascorbate peroxidase; carotenoids; catalase; dehydroascorbate reductase; ex vitro transfer; glutathione reductase; in vitro culture, growth control; malondialdehyde; peroxidase; photoinhibition; superoxide dismutase (SOD); water stress

Received: December 7, 2007; Accepted: January 31, 2008; Published: September 1, 2008Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Baťková, P., Pospíšilová, J., & Synková, H. (2008). Production of reactive oxygen species and development of antioxidative systems during in vitro growth and ex vitro transfer. Biologia plantarum52(3), 413-422. doi: 10.1007/s10535-008-0085-5.
Download citation

References

  1. Adams, L.K., Benson, E.E., Staines, H.J., Bremmer, D.H., Millan, S., Deighton, N.: Effect of the lipid peroxidation products 4-hydroxy-2-nonenal and malondialdehyde on the proliferation and morphogenetic development of in vitro plant cells.-J. Plant Physiol. 155: 376-386, 1999. Go to original source...
  2. Agarwal, S., Pandey, V.: Antioxidant enzyme responses to NaCl stress in Cassia angustifolia.-Biol. Plant. 48: 555-560, 2004. Go to original source...
  3. Agarwal, S., Sairam, R.K., Srivastava, G.C., Meena, R.C.: Changes in antioxidant enzymes activity and oxidative stress by abscisic acid and salicylic acid in wheat genotypes.-Biol. Plant. 49: 541-550, 2005. Go to original source...
  4. Ali, B.M., Hahn, E.-J., Paek, K.-Y.: Effect of temperature on oxidative stress defence systems, lipid peroxidation and lipoxygenase activity in Phalaenopsis.-Plant Physiol. Biochem. 43: 213-223, 2005a. Go to original source...
  5. Ali, B.M., Hahn, E.-J., Paek, K.-Y.: Effects of light intensities on antioxidant enzymes and malondialdehyde content during short-term acclimatization on micropropagated Phalaenopsis plantlet.-Environ. exp. Bot. 54: 109-120, 2005b. Go to original source...
  6. Ali, B.M., Hahn, E.-J., Paek, K.-Y.: Antioxidative responses of Echinacea angustifolia cultured roots to different levels of CO2 in bioreactor liquid cultures.-Enzyme microb. Technol. 39: 982-990, 2006a. Go to original source...
  7. Ali, B.M., Hahn, E.-J., Paek, K.-Y.: Copper-induced changes in the growth, oxidative metabolism, and saponin production in suspension culture roots of Panax ginseng in bioreactors.-Plant Cell Rep. 25: 1122-1132, 2006b. Go to original source...
  8. Arruda, S.C.C., Souza, G.M., Almeida, M., Gonçalves, A.N.: Anatomical and biochemical characterization of the calcium effect on Eucalyptus urophylla callus morphogenesis in vitro.-Plant Cell Tissue Organ Cult. 63: 143-154, 2000. Go to original source...
  9. Azevedo, H., Pinto, C.G.G., Santos, C.: Cadmium effects in sunflower: membrane permeability and changes in catalase and peroxidase activity in leaves and calluses.-J. Plant. Nutr. 28: 2233-2241, 2005. Go to original source...
  10. Badawi, G.H., Yamauchi, Y., Shimada, E., Sasaki, R., Kawano, N., Tanaka, K., Tanaka, K.: Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts.-Plant Sci. 166: 919-928, 2004. Go to original source...
  11. Bellaire, B.A., Carmody, J., Braud, J., Gossett, D.R., Banks, S.W., Cran Lucas, M., Fowler, T.E.: Involvement of abscisic acid-dependent and-independent pathways in the upregulation of antioxidant enzyme activity during NaCl stress in cotton callus tissue.-Free Rad. Res. 33: 531-545, 2000. Go to original source...
  12. Benson, E.E.: Do free radicals have a role in plant tissue culture recalcitrance?-In Vitro cell. dev. Biol. Plant. 36: 163-170, 2000.
  13. Buddendorf-Joosten, J.M.C., Woltering, E.J.: Components of the gaseous environment and their effects on plant growth and development in vitro.-Plant Growth Regul. 15: 1-16, 1994. Go to original source...
  14. Bueno, P., Piqueras, A., Kurepa, J., Savouré, A., Verbruggen, N., Van Montagu, M., Inzé, D.: Expression of antioxidant enzymes in response to abscisic acid and high osmoticum in tobacco BY-2 cell cultures.-Plant Sci. 138: 27-34, 1998. Go to original source...
  15. Carvalho, L.C., Amâncio, S.: Antioxidant defence system in plantlets transferred from in vitro to ex vitro: effects of increasing light intensity and CO2 concentration.-Plant Sci. 162: 33-40, 2002. Go to original source...
  16. Carvalho, L.C., Vilela, B.J., Vidigal, P., Mullineaux, P.M., Amâncio, S.: Activation of the ascorbate-glutathione cycle is an early response of micropropagated Vitis vinifera L. explants transferred to ex vitro.-Int. J. Plant Sci. 167: 759-770, 2006. Go to original source...
  17. Chakrabarty, D., Park, S.Y., Ali, M.B., Shin, K.S., Paek, K.Y.: Hyperhydricity in apple: ultrastructural and physiological aspects.-Tree Physiol. 26: 377-388, 2006. Go to original source...
  18. Chandrasekhara Reddy, P., Halesh, G.K., Najranabhaiah, S.N.: Effect of PEG stress on growth and associated physiological and biohemical changes in selected and non selected upland rice.-Indian J. Plant Physiol. 9: 413-418, 2004.
  19. Chen, J., Ziv, M.: The effect of ancymidol on hyperhydricity, regeneration, starch and antioxidant enzymatic activities in liquid-cultured Narcissus.-Plant Cell Rep. 20: 22-27, 2001. Go to original source...
  20. Dertinger, U., Schaz, U., Schulze, E.-D.: Age-dependence of the antioxidative system in tobacco with enhanced glutathione reductase activity or senescence-induced production of cytokinins.-Physiol. Plant. 119: 19-29, 2003. Go to original source...
  21. Deryabin, A.N., Sin'kevich, M.S., Dubinina, I.M., Burakhanova, E.A., Trunova, T.I.: Effect of sugars on the development of oxidative stress induced by hypothermia in potato plants overexpressing yeast invertase gene.-Russ. J. Plant Physiol. 54: 32-38, 2007.
  22. Desjardins, Y.: Photosynthesis in vitro-on the factors regulating CO2 assimilation in micropropagation systems.-Acta Hort. 393: 45-61, 1995. Go to original source...
  23. Dewir, Y.H., Chakrabarty, D., Ali, M.B., Hahn, E.J., Paek, K.Y.: Effects of hydroponic solution EC, substrates, PPF and nutrient scheduling on growth and photosynthetic competence during acclimatization of micropropagated Spathiphyllum plantlets.-Plant growth Regul. 46: 241-251, 2005. Go to original source...
  24. Dewir, Y.H., Chakrabarty, D., Ali, M.B., Hahn, E.J., Paek, K.Y.: Lipid peroxidation and antioxidant enzyme activities of Euphorbia millii hyperhydric shoots.-Environ. exp. Bot. 58: 93-99, 2006. Go to original source...
  25. Dewir, Y.H., Chakrabarty, D., Ali, M.B., Sing, N., Hahn, E.-J., Paek, K.-Y.: Influence of GA3, sucrose and solid medium/bioreactor culture on in vitro flowering of Spathiphyllum and association of glutathione metabolism.-Plant Cell Tissue Organ Cult. 90: 225-235, 2007. Go to original source...
  26. Dutta Gupta, S., Datta, S.: Antioxidant enzyme activities during in vitro morphogenesis of gladiolus and the effect of application of antioxidants on plant regeneration.-Biol. Plant. 47: 179-183, 2003/4.
  27. Erice, G., Aranjuelo, I., Irigoyen, J.J., Sánchez-Díaz, M.: Effect of elevated CO2, temperature and limited water supply on antioxidant status during regrowth of nodulated alfalfa.-Physiol. Plant. 130: 33-45, 2007. Go to original source...
  28. Erturk, U., Sivritepe, N., Yerlikaya, C., Bor, M., Ozdemir, F., Turkan, I.: Response of the cherry rootstock to salinity in vitro.-Biol. Plant. 51: 597-600, 2007. Go to original source...
  29. Fazeli, F., Ghorbanli, M., Niknam, V.: Effect of drought on biomass, protein content, lipid peroxidation and antioxidant enzymes in two sesame cultivars.-Biol. Plant. 51: 98-103, 2007. Go to original source...
  30. Fornazier, R.F., Ferreira, R.R., Pereira, G.J.G., Molina, S.M.G., Smith, R.J., Lea, P.J., Azevedo, R.A.: Cadmium stress in sugar cane callus cultures: Effect on antioxidant enzymes.-Plant cell tissue Organ cult. 71: 125-131, 2002. Go to original source...
  31. Franck, T., Kevers, C., Gaspar, T.: Protective enzymatic systems against activated oxygen species compared in normal and vitrified shoots of Prunus avium L. raised in vitro.-Plant Growth Regul. 16: 253-256, 1995. Go to original source...
  32. Gajewska, E., Skłodowska, M., Słaba, M., Mazur, J.: Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots.-Biol. Plant. 50: 653-659, 2006. Go to original source...
  33. Gechev, T., Gadjev, I., Dukiandjiev, S., Minkov, I.: Reactive oxygen species as signalin molecules controlling stress adaptation in plants.-In: Pessarakli, M. (ed.): Handbook of Photosynthesis, Second Edition, Revised and Expanded. Pp. 209-218. Marcel Dekker, New York 2005. Go to original source...
  34. Gomes, R.A., Jr., Gratão, P.L., Gaziola, S.A., Mazzafera, P., Lea, P.J., Azevedo, R.A.: Selenium-induced oxidative stress in cofee cell suspension cultures.-Funct. Plant Biol. 34: 449-456, 2007.
  35. Gomes, R.A., Moldes, C.S., Delite, F.S., Gratão, P.L., Mazzafera, P., Lea, P.J., Azevedo, R.A.: Nickel elicits a fast antioxidant response in Coffea arabica calls.-Plant Physiol. Biochem. 44: 420-429, 2006. Go to original source...
  36. Gomes, R.A., Jr., Moldes, C.S., Delite, F.S., Pompeu, G.B., Gratão, P.L., Mazzafera, P., Lea, P.J., Azevedo, R.A.: Antioxidant metabolism of coffee cell suspension cultures in response to cadmium.-Chemosphere 65: 1330-1337, 2006. Go to original source...
  37. Gossett, D.R., Millhollon, E.P., Cran Lucas, M., Banks, S.W., Marney, M.-M.: The effect of NaCl on antioxidant enzyme activities in callus tissue of salt-tolerant and salt-sensitive cotton cultivars (Gossypium hirsutum L.).-Plant Cell Rep. 13: 498-503, 1994. Go to original source...
  38. Hatzilazarou, S.P., Syros, T.D., Yupsanis, T.A., Bosabalidis, A.M., Economou, A.S.: Peroxidases, lignin and anatomy during in vitro and ex vitro rooting gardenia (Gardenia jasminoides Ellis) microshoots.-J. Plant Physiol. 163: 827-836, 2006. Go to original source...
  39. Hadži-Tašković Šukalović, V., Vuletić, M.: The relationship between respiration rate and peroxidase activities in maize root mitochondria.-Biol. Plant. 51: 297-302, 2007. Go to original source...
  40. Hernández, J.A., Escobar, C., Creissen, G., Mullineaux, P.M.: Antioxidant enzyme induction in pea plants under high irradiance.-Biol. Plant. 50: 395-399, 2006. Go to original source...
  41. Hoque, M.A., Banu, M.N.A., Okuma, E., Murata, Y.: Exogenous proline and glycinebetaine increase NaCl-induced ascorbate glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco bright Yellow-2 suspension-cultured cells.-J. Plant Physiol. 164: 1457-1468, 2007. Go to original source...
  42. Hossain, Z., Mandal, A.K.A., Datta, K.S., Biswas, A.K.: Development of NaCl-tolerant strain in Chrysanthemum morifolium Ramat. through in vitro mutagenesis.-Plant Biol. 8: 450-461, 2006. Go to original source...
  43. Hossain, Z., Mandal, A.K.A., Datta, K.S., Biswas, A.K.: Development of NaCl-tolerant line in Chrysanthemum morifolium Ramat. through shoot organogenesis of selected callus line.-J. Biotechnol. 129: 658-667, 2007. Go to original source...
  44. Israr, M., Sahi, S.V.: Antioxidative responses to mercury in the cell cultures of Sesbania drummondii.-Plant Physiol. Biochem. 44: 590-595, 2006. Go to original source...
  45. Jain, M., Nandwal, A.S., Kundu, B.S., Kumar, B., Sheoran, I.S., Kumar, N., Mann, A., Kukreja, S.: Water relations, activities of antioxidants, ethylene evolution and membrane integrity of pigeonpea roots as affected by soil moisture.-Biol. Plant. 50: 303-306, 2006. Go to original source...
  46. Jeon, M.-W., Ali, M.B., Hahn, E.-J., Paek, K.-Y.: Photosynthetic pigments, morphology and leaf gas exchange during ex vitro acclimatization of micropropagated CAM Doritaenopsis plantlets under relative humidity and air temperature.-Environ. exp. Bot. 55: 183-194, 2006. Go to original source...
  47. Jiang, M., Zhang, J.: Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves.-J. exp. Bot. 53: 2401-2410, 2002. Go to original source...
  48. Jiang, M.-Y., Zhang, J.-H.: Abscisic acid and antioxidative defense in plant cells.-Acta bot. sin. 46: 1-9, 2004.
  49. Johnston, J.W., Harding, K., Benson, E.E.: Antioxidant status and genotypic tolerance of Ribes in vitro cultures to cryopreservation.-Plant Sci. 172: 524-534, 2007. Go to original source...
  50. Khanna-Chopra, R., Selote, D.S.: Acclimation to drought stress generates oxidative stress tolerance in drought-resistant than-susceptible wheat cultivars under field conditions.-Environ. exp. Bot. 60: 276-283, 2007. Go to original source...
  51. Koca, H., Ozdemir, F., Turkan, I.: Effect of salt stress on lipid peroxidation and superoxide dismutase and peroxidase activities of Lycopersicon esculentum and L. pennellii.-Biol. Plant. 50: 745-748, 2006. Go to original source...
  52. Kozai, T., Smith, M.A.L.: Environmental control in plant tissue culture-general introduction and overview.-In: Aitken-Christie, J., Kozai, T., Smith, M.L. (ed.): Automation and Environmental Control in Plant Tissue Culture. Pp. 301-318. Kluwer Academic Publishers, Dordrecht 1995. Go to original source...
  53. Kubota, C., Fujiwara, K., Kitaya, Y., Kozai, T.: Recent advances in environment control in micropropagation.-In: Goto, E., Kurata, K., Hayashi, M., Sasa, S. (ed.): Plant Production in Closed Ecosystems. Pp. 153-169. Kluwer Academic Publishers, Dordrecht 1997. Go to original source...
  54. Kwak, J.M., Nguyen, V., Schroeder, J.I.: The role of reactive oxygen species in hormonal responses.-Plant Physiol. 141: 323-329, 2006. Go to original source...
  55. Lai, Q.-X., Bao, Z.-Y., Zhu, Z.-J., Qian, Q.-Q., Mao, B.-Z.: Effect of osmotic stress on antioxidant enzymes activities in leaf discs of PSAG12-IPT modified gerbera.-J. Zhejiang Univ. Sci. B 8: 458-464, 2007. Go to original source...
  56. Lambreva, M., Christov, K., Tsonev, T.: Short-term effect of elevated CO2 concentration and high irradiance on the antioxidant enzymes in bean plants.-Biol. Plant. 50: 617-623, 2006. Go to original source...
  57. Lee, B.-R., Kim, K.-Y., Jung, W.-J., Avice, J.-C., Ourry, A., Kim, T.-H.: Peroxidases and lignification in relation to the intensity of water-deficit stress in white clover (Trifolium repens L.).-J. exp. Bot. 58: 1271-1279, 2007. Go to original source...
  58. Levine, A.: Oxidative stresses as a regulator of environmental responses in plants.-In: Lerner, H.R. (ed.): Plant Responses to Environmental Stresses. From Phytohormones to Genome Reoganization. Pp. 247-264. Marcel Dekker, New York-Basel 1999. Go to original source...
  59. Liu, Q., Yang, J.L., He, L.S., Li, Y.Y., Zheng, S.J.: Effect of aluminum on cell wall, plasma membrane, antioxidants and root elongation in triticale.-Biol. Plant. 52: 87-92, 2008. Go to original source...
  60. Lombardi, L., Sebastiani, L.: Copper toxicity in Prunus cerasifera: growth and antioxidant enzyme responses of in vitro grown plants.-Plant Sci. 168: 797-802, 2005. Go to original source...
  61. Lombardi, L., Sebastiani, L., Vitagliano, C.: Physiological, biochemical, and molecular effects of in vitro induced iron deficiency in peach rootstock Mr.S2/5.-J. Plant Nutr. 26: 2149-2163, 2003. Go to original source...
  62. Lu, S., Peng, X., Guo, Z., Zhang, G., Wang, Z., Wang, C., Pang, C., Fan, Z., Wang, J.: In vitro selection of salinity tolerant variants from triploid bermudagrass (Cynodon transvaalensis × C. dactylon) and their physiological responses to salt and drought stress.-Plant cell Rep. 26: 1413-1420, 2007. Go to original source...
  63. Ludwig-Muller, J.: Peroxidase isoenzymes as markers for the rooting ability of easy-to-root and difficult-to-root Grevillea species and cultivars of Protea obtusifolia (Proteaceae).-In vitro cell. dev. Biol. Plant. 39: 377-383, 2003. Go to original source...
  64. Mandhania, S., Madan, S., Sawhney, V.: Antioxidant defense mechanism under salt stress in wheat seedlings.-Biol. Plant. 50: 227-231, 2006. Go to original source...
  65. Miszalski, Z., Kornas, A., Gawronska, K., Ślesak, I., Niewiadomska, E., Kruk, J., Christian, A.L., Fischer-Schliebs, E., Krisch, R., Lüttge, U.: Superoxide dismutase activity in C3 and C3/CAM intermediate species.-Biol. Plant. 51: 86-92, 2007. Go to original source...
  66. Molina, A., Bueno, P., Marín, M.C., Rodríguez-Rosales, M.P., Belver, A., Venema, K., Donaire, J.P.: Involvement of endogenous salicylic acid content, lipoxygenase and antioxidant enzyme activities in the response of tomato cell suspension cultures to NaCl.-New Phytol. 156: 409-415, 2002. Go to original source...
  67. Molassiotis, A.N., Sotiropoulos, T., Tanou, G., Diamantidis, G., Therios, I.: Boron-induced oxidative damage and antioxidant and nucleolytic responses in shoot tip culture of the apple rootstock EM 9 (Malus domestica Borkh).-Environ. exp. Bot. 56: 54-62, 2006. Go to original source...
  68. Molassiotis, A.N., Sotiropoulos, T., Tanou, G., Kofidis, G., Diamantidis, G., Therios, I.: Antioxidant and anatomical responses in shoot culture of the apple rootstock MM 106 treated with NaCl, KCl, mannitol or sorbitol.-Biol. Plant. 50: 61-68, 2006. Go to original source...
  69. Morkunas, I., Garnczarska, M., Bednarski, W., Ratajczak, E., Waplak, S.: Metabolic and ultrastructural responses of lupine embryos axes to sugar starvation.-J. Plant Physiol. 160: 311-319, 2003. Go to original source...
  70. Niknam, V., Razavi, N., Ebrahimzadeh, H., Sharifizadeh, B.: Effect of NaCl on biomass, protein and proline contents, and antioxidant enzymes in seedlings and calli of two Trigonella species.-Biol. Plant. 50: 591-596, 2006. Go to original source...
  71. Obert, B., Benson, E.E., Millam, S., Preťvá, A., Bremner, D.H.: Moderation of morphogenetic and oxidative stress responses in flax in vitro cultures by hydroxynonenal and desferrioxamine.-J. Plant Physiol. 162: 537-547, 2005. Go to original source...
  72. Olmos, E., Piqueras, A., Martínez-Solano, J.R., Hellín, E.: The subcellular localization of peroxidase and the implication of oxidative stress in hyperhydrated leaves of regenerated carnation plants.-Plant Sci. 130: 97-105, 1997. Go to original source...
  73. Papadakis, A.K., Roubelakis-Angelakis, K.A.: Oxidative stress could be responsible for the recalcitrance of plant protoplasts.-Plant Physiol. Biochem. 40: 549-559, 2002. Go to original source...
  74. Piqueras, A., Han, B.H., Van Huylenbroeck, J.M., Debergh, P.C.: Effect of different environmental conditions in vitro on sucrose metabolism and antioxidant enzymatic activities in cultured shoots of Nicotiana.-Plant Growth Regul. 25: 5-10, 1998. Go to original source...
  75. Pospíšilová, J., Čatský, J., Šesták, Z.: Photosynthesis in plants cultivated in vitro.-In: Pessarakli, M. (ed.): Handbook of Photosynthesis. Pp. 525-540. Marcel Dekker, New York 1997.
  76. Pospíšilová, J., Dodd, I.C.: Role of plant growth regulators in stomatal limitation to photosynthesis during water stress.-In: Pessarakli, M. (ed.): Handbook of Photosynthesis, Second Edition, Revised and Expanded. Pp. 811-825. Marcel Dekker, New York 2005.
  77. Pospíšilová, J., Solárová, J., Čatský, J.: Photosynthetic responses to stresses during in vitro cultivation.-a review.-Photosynthetica 26: 3-18, 1992.
  78. Pospíšilová, J., Synková, H., Haisel, D., Semorádová, Š.: Acclimation of plantlets to ex vitro conditions: effects of air humidity, irradiance, CO2 concentration and abscisic acid.-Acta Hort. 748: 29-38, 2007. Go to original source...
  79. Procházková, D., Wilhelmová, N.: Leaf senescence and activities of the antioxidant enzymes.-Biol. Plant. 51: 401-406, 2007. Go to original source...
  80. Qin, Y.H., Zhang, S.L., Zhang, L.X., Zhu, D.Y., Syed, A.: Response of in vitro strawberry to silver nitrate (AgNO3).-HortScience 40: 747-751, 2005. Go to original source...
  81. Queirós, F., Fidalgo, F., Santos, I., Salema, R.: In vitro selection of salt tolerant cell lines in Solanum tuberosum L.-Biol. Plant. 51: 728-734, 2007. Go to original source...
  82. Qureshi, M.I., Abdin, M.Z., Qadir, S., Iqbal, M.: Lead-induced oxidative stress and metabolic alterations.-Biol. Plant. 51: 121-128, 2007. Go to original source...
  83. Racchi, M.L., Bagnoli, F., Balla, I., Danti, S.: Differential activity of catalase and superoxide dismutase in seedlings and in vitro micropropagated oak (Quercus robur L.)-Plant Cell Rep. 20: 169-174, 2001.
  84. Ray, T., Saha, P., Roy, S.C.: Commercial production of Cordyline terminalis (L) Kunth. from shoot apex meristem and assessment for genetic stability of somaclones by isozyme markers.-Scientia Hort. 108: 289-294, 2006. Go to original source...
  85. Rodríguez-Rosales, M.P., Kerkeb, L., Bueno, P., Donaire, J.P.: Changes induced by NaCl in lipid content and composition, lipogenase, plasma membrane H+-ATPase and antioxidant enzyme activities of tomato (Lycopersicon esculentum Mill.) calli.-Plant Sci. 143: 143-150, 1999. Go to original source...
  86. Romanowska, E., Wróblewska, B., Drożak, A., Zienkiewicz, M., Siedlecka, M.: Effect of Pb ions on superoxide dismutase and catalase activities in leaves of pea plants griown in high and low irradiance.-Biol. Plant. 52: 80-86, 2008. Go to original source...
  87. Saher, S., Fernández-García, N., Piqueras, A., Hellín, E., Olmos, E.: Reducing properties, energy efficiency and carbohydrate metabolism in hyperhydric and normal carnation shoots cultured in vitro: a hypoxia stress?-Plant Physiol. Biochem. 43: 573-582, 2005a. Go to original source...
  88. Saher, S., Piqueras, A., Hellin, E., Olmos, E.: Hyperhydricity in micropropagated carnation shoots: the role of oxidative stress.-Physiol. Plant. 120: 1152-161, 2004. Go to original source...
  89. Saher, S., Piqueras, A., Hellin, E., Olmos, E.: Prevention of hyperhydricity in micropropagated carnation shoots by bottom cooling: implications of oxidative stress.-Plant Cell Tissue Organ Cult. 81: 149-158, 2005b. Go to original source...
  90. Scebba, F., Arduini, I., Ercoli, L., Sebastiani, L.: Cadmium effects on growth and antioxidant enzymes activities in Miscanthus sinensis.-Biol. Plant. 50: 688-692, 2006. Go to original source...
  91. Semorádová, Š., Synková, H., Pospíšilová, J.: Responses of tobacco plantlets to changes of irradiance during transfer from in vitro to ex vitro conditions.-Photosynthetica 40: 605-614, 2002. Go to original source...
  92. Shamsi, I.H., Wei, K., Zhang, G.P., Jilani, G.H., Hassan, M.J.: Interactive effects of cadmium and aluminum on growth and antioxidative enzymes in soybean.-Biol. Plant. 52: 165-169, 2008. Go to original source...
  93. Shao, H.-B., Chu, L.-Y., Lu, Z.-H., Kang, C.-M.: Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells.-Int. J. biol. Sci. 4: 8-14, 2008.
  94. Sharma, P., Dubey, R.S.: Ascorbate peroxidase from rice seedlings: properties of enzyme isoforms, effects of stresses and protective role of osmolytes.-Plant Sci. 167: 541-550, 2004. Go to original source...
  95. Sharma, P., Dubey, R.S.: Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings.-Plant Growth Regul. 46: 209-221, 2005. Go to original source...
  96. Sharma, P., Dubey, R.S.: Involvement of oxidative stress and role of antioxidative defence system in growing rice seedlings exposed to toxic concentrations of aluminum.-Plant Cell Rep. 26: 2027-2038, 2007. Go to original source...
  97. Shohael, A.M., Ali, M.B., Yu, K.-W., Hahn, E.-J., Paek, K.-Y.: Effect of light on oxidative stress, secondary metabolites and induction of antioxidant enzymes in Eleutherococcus senticosus somatic embryos in bioreactor.-Process Biochem. 41: 1179-1185, 2006a Go to original source...
  98. Shohael, A.M., Ali, M.B., Yu, K.-W., Hahn, E.-J., Paek, K.-Y.: Effect of temperature on secondary metabolites production and antioxidant enzyme activities in Eleutherococcus senticosus somatic embryos.-Plant cell Tissue Organ Cult. 85: 219-228, 2006b. Go to original source...
  99. Sivritepe, N., Erturk, U., Yerlikaya, C., Turkan, I., Bor, M., Ozdemir, F.: Response of the cherry rootstock to water stress induced in vitro.-Biol. Plant. 52: 573-576, 2008. Go to original source...
  100. Ślesak, I., Hałdaś, W., Ślesak, H.: Influence of exogenous carbohydrates on superoxide dismutase activity in Trifolium repens L. explants cultured in vitro.-Acta biol. cracov. 48: 93-98, 2006.
  101. Ślesak, I., Libik, M., Karpinska B., Karpinski, S., Miszalski, Z.: The role of hydrogen peroxide in regulation of plant metabolism and cellular signalling in response to environmental stresses.-Acta. biochim. polon. 54: 39-50, 2007. Go to original source...
  102. Ślesak, I., Libik, M., Miszalski, Z.: Superoxide dismutase activity in callus from C3-CAM intermediate plant Mesembryanthemum crystallinum.-Plant Cell Tissue Organ Cult. 75: 49-55, 2003. Go to original source...
  103. Ślesak, I., Miszalski, Z.: Superoxide dismutase-like protein from roots of the intermediate C3-CAM plant Mesembryanthemum crystallinum L. in in vitro culture.-Plant Sci. 164: 497-505, 2003.
  104. Sriskandarajah, S., Prinsen, E., Motyka, V., Dobrev, P.I., Serek, M.: Regenerative capacity of cacti Schlumbergera and Rhipsalidopsis in relation to endogenous phytohormones, cytokinin oxidase/dehydrogenase, and peroxidase activities.-J. Plant Growth Regul. 25: 79-88, 2006. Go to original source...
  105. Synková, H., Pospíšilová, J.: In vitro precultivation of tobacco affects the response of antioxidative enzymes to ex vitro acclimation.-J. Plant Physiol. 159: 781-789, 2002. Go to original source...
  106. Synková, H., Semorádová, Š., Schnáblová, R., Witters, E., Hušák, M., Valcky, R.: Cytokinin-induced activity of antioxidant enzymes in transgenic Pssu-ipt tobacco during plant ontogeny.-Biol. Plant. 50: 31-41, 2006. Go to original source...
  107. Syros, T., Yupsanis, T., Zafiriadis, H., Economou, A.: Activity and isoforms of peroxidases, lignin and anatomy, during adventitious rooting in cuttings of Ebenus cretica L.-J. Plant Physiol. 161: 69-77, 2004. Go to original source...
  108. Tang, W., Harris, L.C., Outhavong, V., Newton, R.J.: Antioxidants enhance in vitro plant regeneration by inhibiting the accumulation of peroxidase in Virginia pine (Pinus virginiana Mill.)-Plant Cell Rep. 22: 871-877, 2004a. Go to original source...
  109. Tang, W., Newton, R.J.: Peroxidase and catalase activities are involved in direct adventitious shoot formation induced by thidiazuron in eastern white pine (Pinus strobus L.) zygotic embryos.-Plant physiol. Biochem. 43: 760-769, 2005. Go to original source...
  110. Tang, W., Newton, R.J., Outhavong, V.: Exogenously added polyamines recover browning tissues into normal callus cultures and improve plant regeneration in pine.-Physiol. Plant. 122: 386-395, 2004b. Go to original source...
  111. Van Huylenbroeck, J.M., Piqueras, A., Debergh, P.C.: Effect of light intensity on photosynthesis and toxic 02 scavenging enzymes during acclimatization of micropropagated Calathea.-Phyton 37: 283-290, 1997.
  112. Van Huylenbroeck, J.M., Piqueras, A., Debergh, P.C.: The evolution of photosynthetic capacity and the antioxidant enzymatic system during acclimatization of micropropagated Calathea plants.-Plant Sci. 155: 59-66, 2000. Go to original source...
  113. Van Huylenbroeck, J.M., Van Laare, I.M.B., Piqueras, A., Debergh, P.C., Bueno, P.: Time course of catalase and superoxide dismutase during acclimatization and growth of micropropagated Calathea and Spathiphyllum plants.-Plant Growth Regul. 26: 7-14, 1998. Go to original source...
  114. Vilela, B.J., Carvalho, L.C., Ferreira, J., Amâcio, S.: Gain of function of stomatal movements in rooting Vitis vinifera L. plants: regulation by H2O2 is independent of ABA before the protruding of roots.-Plant Cell Rep. 26: 2149-2157, 2007 Go to original source...
  115. Vital, S.A., Fowler, R.W., Virgen, A., Gossett, D.R., Banks, S.W., Rodriguez, J.: Opposite roles for superoxide and nitric oxide in the NaCl stress-induced upregulation of antioxidant enzyme activity in cotton callus tissue.-Environ. exp. Bot. 62: 60-68, 2008. Go to original source...
  116. Wang, Y.-L., Wang, X.-D., Zhao, B., Wang, Y.-C.: Reduction of hyperhydricity in the culture of Lepidium meyenii shoots by the addition of rare earth elements.-Plant Growth Regul. 52: 151-159, 2007. Go to original source...
  117. Xiong, Y.-C., Xing, G.-M., Gong, C.-M., Li, F.-M., Wang, S.-M., Li, Z.-X., Wang, Y.-F.: Dual role of abscisic acid on antioxidative defense in grass pea seedlings (Lathyrus sativus L.).-Pakistan J. Bot. 38: 999-1014, 2006.
  118. Xu, C.-M., Zhao, B., Wang, X.-D., Wang, Y.-C.: Lanthanum relieves salinity-induced oxidative stress in Saussurea involucrata.-Biol. Plant. 51: 567-570, 2007. Go to original source...
  119. Zhang, A., Jiang, M., Zhang, J., Tan, M., Hu, X.: Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants.-Plant Physiol. 141: 475-487, 2006. Go to original source...
  120. Zhang, F., Guo, J.-K., Yang, Y.-L., He, W.-L., Zhang, L.-X.: Changes in the pattern of antioxidant enzymes in wheat exposed to water deficit and rewatering.-Acta Physiol. Plant. 26: 345-352, 2004.
  121. Zhang, F., Wang, Y., Yang, Y., Wu, H., Wang, D., Liu, J.: Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica.-Plant Cell Environ. 30: 775-785, 2007. Go to original source...
  122. Zlatev, Z.S., Lidon, F.C., Ramalho, J.C., Yordanov, I.T.: Comparison of resistance to drought of three bean cultivars.-Biol. Plant. 50: 389-394, 2006. Go to original source...