Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-25T04:50:04.243Z Has data issue: false hasContentIssue false
  • English
  • Français

Cathodic amelioration of the adverse effects of oxidative stress accompanying procedures necessary for cryopreservation of embryonic axes of recalcitrant-seeded species

Published online by Cambridge University Press:  11 May 2011

Patricia Berjak ,
Sershen ,
Boby Varghese  and
N.W. Pammenter
Patricia Berjak*
Affiliation:
Plant Germplasm Conservation Research, School of Biological and Conservation Sciences, University of KwaZulu-Natal, South Ring Road, Westville Campus, Durban4001, South Africa
Sershen
Affiliation:
Plant Germplasm Conservation Research, School of Biological and Conservation Sciences, University of KwaZulu-Natal, South Ring Road, Westville Campus, Durban4001, South Africa
Boby Varghese
Affiliation:
Plant Germplasm Conservation Research, School of Biological and Conservation Sciences, University of KwaZulu-Natal, South Ring Road, Westville Campus, Durban4001, South Africa
N.W. Pammenter
Affiliation:
Plant Germplasm Conservation Research, School of Biological and Conservation Sciences, University of KwaZulu-Natal, South Ring Road, Westville Campus, Durban4001, South Africa
*
*Correspondence Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Several of the procedures necessary for cryopreservation of excised zygotic embryonic axes are known to be accompanied by emission of damaging levels of reactive oxygen species (ROS). These have been shown to be associated with shoot apical meristem necrosis, curtailing subsequent axis development to root production only, particularly for tropical/subtropical recalcitrant-seeded species. Here we report on the application of the principles of electrochemistry in the generation of strongly reducing, high pH cathodic water, by electrolysis of a solution containing calcium and magnesium chloride. The cathodic water in which Strychnos gerrardii axes were immersed for 30 min following dehydration, and importantly, after dehydration followed by cryopreservation, was shown to have strongly antioxidative properties in counteracting the damaging effects of ROS bursts and promoting shoot development. In a parallel experiment, axes of Boophane disticha exhibited enhanced total antioxidant activity when exposed to cathodic water both immediately following excision, and after flash-drying. For both species, the efficacious effects of cathodic treatment were manifest after the axes had been in culture for 4 h, suggesting that ROS were not quenched at source, but probably counteracted by enhancement of activity of endogenous antioxidants. Cathodic water therefore affords a non-toxic means of amelioration of oxidative, stress-related damage, which, coupled with the strongly fungicidal activity of the acidic, anionic water fraction, offers significant, and apparently non-injurious, advances towards successful cryopreservation of germplasm – and probably generally improved success of in-vitro-based procedures for plant tissues.

Keywords

Boophane distichacathodic watercryopreservationembryonic axesprotectionreactive oxygen speciesStrychnos gerrardiisuperoxide
Type
Research Article
Information
Seed Science Research , Volume 21 , Issue 3 , September 2011 , pp. 187 - 203
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Antunes, F. and Cadenas, E. (2000) Estimation of H2O2 gradients across biomembranes. FEBS Letters 475, 121–126.CrossRefGoogle ScholarPubMed
Bailey-Serres, J. and Mittler, R.(Guest and Monitoring Editors) (2006) The roles of reactive oxygen species in plants. Plant Physiology 141, 311.CrossRefGoogle Scholar
Bailly, C. (2004) Active oxygen species and antioxidants in seed biology. Seed Science Research 14, 93–107.CrossRefGoogle Scholar
Benson, E.E. and Bremner, D. (2004) Oxidative stress in the frozen plant: a free radical point of view. pp. 205–241in Fuller, B.J.; Lane, N.; Benson, E.E. (Eds) Life in the frozen state. Boca Raton, CRC Press.CrossRefGoogle Scholar
Benson, E.E. and Noronha-Dutra, A.A. (1988) Chemiluminescence in cryopreserved plant tissue cultures: the possible role of singlet oxygen in cryo injury. CryoLetters 9, 120–131.Google Scholar
Benson, E.E., Lynch, P.T. and Jones, J. (1995) The use of the iron chelating agent desferrioxamine in rice cell cryopreservation: a novel approach for improving recovery. Plant Science 110, 249–258.CrossRefGoogle Scholar
Benson, E.E., Harding, K. and Johnston, J. (2007) Cryopreservation of shoot-tips and meristems. pp. 163–184in Day, J.G.; Stacey, G. (Eds) Methods in molecular biology, Vol. 368, Cryopreservation and freeze drying protocols. Totowa, NJ, Humana Press.CrossRefGoogle Scholar
Berjak, P. (1978) Viability extension and improvement of stored seeds. South African Journal of Science 74, 365–368.Google Scholar
Berjak, P. and Pammenter, N.W. (2008) From Avicennia to Zizania: seed recalcitrance in perspective. Annals of Botany 101, 213–228.CrossRefGoogle Scholar
Berjak, P., Farrant, J.M., Mycock, D.J. and Pammenter, N.W. (1990) Recalcitrant (homoiohydrous) seeds: the enigma of their desiccation sensitivity. Seed Science and Technology 18, 297–310.Google Scholar
Bhattacharjee, S. (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plants. Current Science 89, 1113–1121.Google Scholar
Bolwell, G.P., Bindschedler, L.V., Blee, K.A., Butt, V.S., Davies, D.R., Gardner, S.L., Gerrish, C. and Minibayeva, F. (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. Journal of Experimental Botany 53, 1367–1376.Google ScholarPubMed
Cassandra, , Benson, E.E., Berjak, P., Goveia, M. and Pammenter, N.W. (2011) Exploring the use of DMSO and ascorbic acid to promote shoot development by excised embryonic axes of recalcitrant seeds. CryoLetters (in press).Google Scholar
Cheng, H.-Y. and Song, S.-Q. (2008) Possible involvement of reactive oxygen species scavenging enzymes in desiccation sensitivity of Antiaris toxicaria seeds and axes. Journal of Integrative Plant Biology 50, 1549–1556.CrossRefGoogle ScholarPubMed
Côme, D. and Corbineau, F. (1996) Metabolic damage related to desiccation sensitivity. pp. 83–97in Ouédraogo, A.-S.; Poulsen, K.; Stubsgaard, F. (Eds) Intermediate/recalcitrant tropical forest tree seeds. Rome, IPGRI.Google Scholar
Dickie, J.B. and Pritchard, H.W. (2002) Systematic and evolutionary aspects of desiccation tolerance in seeds. pp. 239–259in Black, M.; Pritchard, H.W. (Eds) Desiccation and survival in plants. Drying without dying. Wallingford, Oxon, CABI Publishing.CrossRefGoogle Scholar
Foyer, C.H. and Noctor, G. (2005) Redox homeostasis and antioxidant signalling: a metabolic interface between stress perception and physiological responses. Plant Cell 17, 1866–1875.CrossRefGoogle ScholarPubMed
Gill, S.S. and Tuteja, N. (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48, 909–930.CrossRefGoogle ScholarPubMed
Goveia, M.J.T. (2007) The effect of developmental status and excision injury on the success of cryopreservation of germplasm from non-orthodox seeds. MSc thesis, University of KwaZulu-Natal (Westville Campus), Durban, South Africa. Available at websitehttp://researchspace.ukzn.ac.za/xmlui/handle/10413/1052 (accessed March 2011).Google Scholar
Goveia, M., Kioko, J.I. and Berjak, P. (2004) Developmental status is a critical factor in the selection of excised recalcitrant axes as explants for cryopreservation. Seed Science Research 14, 241–248.CrossRefGoogle Scholar
Gutiérrez, R., Alvarado, J.L., Presno, M., Pérez-Veyna, O., Serrano, C.J. and Yahuaca, P. (2010) Oxidative stress modulation by Rosmarinus officinalis in CCl4-induced liver cirrhosis. Phytotherapy Research 24, 595–601.CrossRefGoogle ScholarPubMed
Hajari, E., Berjak, P., Pammenter, N.W. and Watt, M.P. (2009) Micropropagation of Ekebergia capensis Sparrm. using in vitro nodal segments and roots. Journal of Horticultural Science and Biotechnology 84, 87–91.CrossRefGoogle Scholar
Halliwell, B. (2006) Reactive oxygen species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiology 141, 312–322.CrossRefGoogle ScholarPubMed
Halliwell, B. and Gutteridge, J.M.C. (1999) Free radicals in biology and medicine (3rd edition). Oxford, UK, Oxford University Press.Google Scholar
Hanaoka, K. (2001) Antioxidant effects of reduced water produced by electrolysis of sodium chloride solutions. Journal of Applied Electrochemistry 31, 1307–1313.CrossRefGoogle Scholar
Hanaoka, K., Sun, D., Lawrence, R., Kamitani, Y. and Fernandes, G. (2004) The mechanism of enhanced antioxidant effects against superoxide anion radicals of reduced water produced by electrolysis. Biophysical Chemistry 107, 71–82.CrossRefGoogle ScholarPubMed
Hazra, B., Sarkar, R., Mandal, S., Biswas, S. and Mandal, N. (2009) Studies on antioxidant and antiradical activities of Dolichus biflorus seed extract. African Journal of Biotechnology 8, 3927–3933.Google Scholar
Hendry, G.A.F. (1993) Oxygen, free radical processes and seed longevity. Seed Science Research 3, 141–153.CrossRefGoogle Scholar
Hiraoka, A., Takemoto, M., Suzuki, T., Shinohara, A., Chiba, M., Shirao, M. and Yoshimura, Y. (2004) Studies on the properties and real existence of aqueous solution systems that are assumed to have antioxidant activities by the action of ‘active hydrogen’. Journal of Health Science 50, 456–465.CrossRefGoogle Scholar
Huang, Y.-R., Hung, Y.-C., Hsu, S.-Y., Huang, Y.-W. and Hwang, D.-F. (2008) Application of electrolyzed water in the food industry. Food Control 19, 329–345.CrossRefGoogle Scholar
Johnston, J.W., Dussert, S., Gale, S., Nadarajan, J., Harding, K. and Benson, E.E. (2006) Optimisation of the azinobis-3-ethyl-benzothiazoline-6-sulphonic acid radical scavenging assay for physiological studies of total antioxidant activity in woody plant germplasm. Plant Physiology and Biochemistry 44, 193–201.CrossRefGoogle ScholarPubMed
Kioko, J.I., Berjak, P., Pammenter, N.W., Watt, P. and Wesley-Smith, J. (1998) Desiccation and cryopreservation of embryonic axes of Trichilia dregeana Sond. CryoLetters 19, 5–11.Google Scholar
Kranner, I. and Birtić, S. (2005) A modulating role for antioxidants in desiccation tolerance. Integrative and Comparative Biology 45, 734–740.CrossRefGoogle ScholarPubMed
Kranner, I., Minibayeva, F., Beckett, R.P.andSeal, C.E. (2010a) What is stress? Concepts, definitions and applications in seed science. New Phytologist 188, 655–673.CrossRefGoogle Scholar
Kranner, I., Roach, T., Beckett, R.P., Whitaker, C. and Minibayeva, F. (2010b) Early production of reactive oxygen species during seed germination and early seedling growth in Pisum sativum. Journal of Plant Physiology 167, 805–811.CrossRefGoogle ScholarPubMed
Lee, M.Y., Kim, Y.K., Ryoo, K.K., Lee, Y.B. and Park, E.J. (2006) Electrolyzed-reduced water protects against oxidative damage to DNA, RNA and protein. Applied Biochemistry and Biotechnology 135, 273–289.CrossRefGoogle ScholarPubMed
Liszkay, A., van der Zalm, E. and Schopfer, P. (2004) Production of reactive oxygen intermediates (O2∙− , H2O2 and ∙OH) by maize roots and their role in wall loosening and elongation. Plant Physiology 136, 3114–3123.CrossRefGoogle Scholar
Masella, R., Di Benedetto, R., Varì, R., Filesi, C. and Giovannini, C. (2005) Novel mechanisms of natural antioxidant compounds in biological systems: involvement of glutathione and glutathione-related enzymes. Journal of Nutritional Biochemistry 16, 577–586.CrossRefGoogle ScholarPubMed
Minibayeva, F., Kolesnikov, O., Chasov, A., Beckett, R.P., Lüthje, S., Vylegzhanina, N., Buck, F. and Böttger, M. (2009) Wound-induced apoplastic peroxidase activities: their roles in the production and detoxification of reactive oxygen species. Plant, Cell and Environment 32, 497–508.CrossRefGoogle ScholarPubMed
Misra, H.R. and Fridovich, I. (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Journal of Biological Chemistry 247, 3170–3175.CrossRefGoogle Scholar
Müller, K., Linkies, A., Vreeburg, R.A., Fry, S.C., Krieger-Liszkay, A. and Leubner-Metzger, G. (2009) In vivo wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiology 150, 1855–1865.CrossRefGoogle ScholarPubMed
Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.CrossRefGoogle Scholar
Mycock, D.J. (1999) Addition of calcium and magnesium to a glycerol and sucrose cryoprotectant solution improves the quality of plant embryo recovery from cryostorage. CryoLetters 20, 77–82.Google Scholar
Ngobese, N.Z., Berjak, P. and Pammenter, N.W. (2011) The effects of the steps of cryopreservation on the viability of zygotic embryos of selected amaryllid species. 10th Conference of the International Society for Seed Science. Informativo ABRATES 21, 105.Google Scholar
Obert, B., Benson, E.E., Millam, S., Pret'ová, A. and Bremner, D.H. (2005) Moderation of morphogenetic and oxidative stress responses in flax in vitro cultures by hydroxynonenal and desferrioxamine. Journal of Plant Physiology 162, 537–547.CrossRefGoogle ScholarPubMed
Pammenter, N.W., Adamson, J.H. and Berjak, P. (1974) Viability of stored seeds: extension by cathodic protection. Science 186, 1123–1124.CrossRefGoogle ScholarPubMed
Pammenter, N.W., Greggains, V., Kioko, J.I., Wesley-Smith, J., Berjak, P. and Finch-Savage, W.E. (1998) The time factor during dehydration of non-orthodox (recalcitrant) seeds: effects of differential drying rates on viability retention in Ekebergia capensis. Seed Science Research 8, 463–471.CrossRefGoogle Scholar
Pammenter, N.W., Berjak, P., Wesley-Smith, J. and Vander Willigen, C. (2002) Experimental aspects of drying and recovery. pp. 263–291in Black, M.; Pritchard, H.W. (Eds) Desiccation and survival in plants. Drying without dying. Wallingford, Oxon, CABI Publishing.Google Scholar
Pammenter, N.W., Berjak, P., Goveia, M., Sershen, Kioko, J.I., Whitaker, C. and Beckett, R.P. (2011) Topography determines the impact of reactive oxygen species on shoot apical meristems of recalcitrant embryos of tropical species during processing for cryopreservation. Acta Horticulturae (in press).CrossRefGoogle Scholar
Perán, R., Berjak, P., Pammenter, N.W. and Kioko, J.I. (2006) Cryopreservation, encapsulation and promotion of shoot production of embryonic axes of a recalcitrant species, Ekebergia capensis Sparrm. CryoLetters 27, 1–12.Google ScholarPubMed
Pitzschke, A., Forzani, C. and Hirt, H. (2006) Reactive oxygen species signaling in plants. Antioxidants and Redox Signaling 8, 1757–1764.CrossRefGoogle ScholarPubMed
Pukacka, S. and Ratajczak, E. (2006) Antioxidative response of ascorbate–glutathione pathway enzymes and metabolites to desiccation of recalcitrant Acer saccharinum seeds. Journal of Plant Physiology 163, 1259–1266.CrossRefGoogle ScholarPubMed
Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M. and Rice-Evans, C. (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine 26, 1231–1237.CrossRefGoogle ScholarPubMed
Roach, T., Ivanova, M., Beckett, R.P., Minibayeva, F.V., Green, I., Pritchard, H.W. and Kranner, I. (2008) An oxidative burst of superoxide in embryonic axes of recalcitrant sweet chestnut seeds as induced by excision and desiccation. Physiologia Plantarum 133, 131–139.CrossRefGoogle ScholarPubMed
Roach, T., Beckett, R.P., Minibayeva, F.V., Colville, L., Whitaker, C., Chen, H., Bailly, C. and Kranner, I. (2010) Extracellular superoxide production, viability and redox poise in response to desiccation in recalcitrant Castanea sativa seeds. Plant, Cell and Environment 33, 59–75.Google ScholarPubMed
Sacandé, M., Jøker, D., Dulloo, M.E. and Thomsen, K.A. (Eds) (2004) Comparative storage behaviour of tropical tree seeds. Rome, IPGRI.Google Scholar
Samarth, R.M., Panwar, M., Kumar, M., Soni, A., Kumar, M. and Kumar, A. (2008) Evaluation of antioxidant and radical-scavenging activities of certain radio-protective plant extracts. Journal of Food Chemistry 106, 868–873.CrossRefGoogle Scholar
Scandalios, J.G. (1993) Oxygen stress and superoxide dismutase. Plant Physiology 101, 7–12.CrossRefGoogle Scholar
Schopfer, P. and Liszkay, A. (2006) Plasma membrane-generated reactive oxygen intermediates and their role in cell growth of plants. Biofactors 28, 73–81.CrossRefGoogle ScholarPubMed
Sershen, , Pammenter, N.W., Berjak, P. and Wesley-Smith, J. (2007) Cryopreservation of embryonic axes of selected amaryllid species. CryoLetters 28, 387–399.Google ScholarPubMed
Shao, H.-B., Chu, L.-Y., Lu, Z.-H. and Kang, C.-M. (2008) Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. International Journal of Biological Sciences 4, 8–14.CrossRefGoogle Scholar
Shirahata, S., Kabayama, S., Nakano, M., Miura, T., Kusumoto, K., Gotoh, M., Hayashi, H., Otsubo, K., Morisawa, S. and Katakura, Y. (1997) Electrolyzed-reduced water scavenges active oxygen species and protects DNA from oxidative damage. Biochemical and Biophysical Research Communications 234, 269–274.CrossRefGoogle ScholarPubMed
Sirdaarta, J. and Cock, I.E. (2008) Vitamin E and Trolox™ reduce toxicity of Aloe barbadensis Miller juice in Artemia franciscana nauplii but individually are toxic at high concentrations. The Internet Journal of Toxicology™ 5, ISSN: 1559–3916. Available at http://www.ispub.com/journal/the_internet_journal_of_toxicology/(accessed March 2011).Google Scholar
Smirnoff, N. (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytologist 125, 27–58.CrossRefGoogle ScholarPubMed
Sutherland, J.R., Diekmann, M. and Berjak, P. (2002) Forest tree seed health for germplasm conservation. Rome, IPGRI.Google Scholar
Touchell, D. and Walters, C. (2000) Recovery of embryos of Zizania palustris following exposure to liquid nitrogen. CryoLetters 21, 261–270.Google ScholarPubMed
Tripathi, R., Mohan, H. and Kamat, J.P. (2007) Modulation of oxidative damage by natural products. Journal of Food Chemistry 100, 81–90.CrossRefGoogle Scholar
Van Breusegem, F., Bailey-Serres, J. and Mittler, R. (2008) Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiology 147, 978–984.CrossRefGoogle ScholarPubMed
Varghese, B. and Naithani, S.C. (2002) Desiccation-induced changes in lipid peroxidation, superoxide level and antioxidant enzymes activity in neem (Azadirachta indica A. Juss) seeds. Acta Physiologiae Plantarum 24, 79–87.CrossRefGoogle Scholar
Varghese, B., Sershen, , Berjak, P., Varghese, D. and Pammenter, N.W. (2011) Differential drying rates of recalcitrant Trichilia dregeana embryonic axes: a study of survival and oxidative stress metabolism. Physiologia Plantarum DOI: 10.1111/j.1399-3054.2011.01469.CrossRefGoogle ScholarPubMed
Walters, C., Pammenter, N.W., Berjak, P. and Crane, J. (2001) Desiccation damage accelerated ageing and respiration in desiccation tolerant and sensitive seeds. Seed Science Research 11, 135–148.Google Scholar
Whitaker, C., Beckett, R.P., Minibayeva, F.V. and Kranner, I. (2010) Production of reactive oxygen species in excised and cryopreserved explants of Trichilia dregeana Sond. South African Journal of Botany 76, 112–118.CrossRefGoogle Scholar
Yin, J.-J., Lao, F., Fu, P.P., Warner, W.G., Zhao, Y., Wang, P.C., Qiu, Y., Sun, B., Xing, G., Dong, J., Liang, X.-J. and Chen, C. (2009) The scavenging of reactive oxygen species and the potential for cell protection by functionalized fullerene materials. Biomaterials 30, 611–621.CrossRefGoogle ScholarPubMed