Abstract
Because the term stress is used, most often subjectively, with variousmeanings, this paper first attempts to clarify the physiological definition,andthe appropriate terms as responses in different situations. The flexibility ofnormal metabolism allows the development of responses to environmental changeswhich fluctuate regularly and predictably over daily and seasonal cycles. Thusevery deviation of a factor from its optimum does not necessarily result instress. Stress begins with a constraint or with highly unpredictablefluctuations imposed on regular metabolic patterns that cause bodily injury,disease, or aberrant physiology. Stress is the altered physiological conditioncaused by factors that tend to alter an equilibrium. Strain is any physicaland/or chemical change produced by a stress, i.e. every established condition,which forces a system away from its thermodynamic optimal state. The papersecondly summarises the Strasser's state-change concept which is preciselythat suboptimality is the driving force for acclimation (genotype level) oradaptation (population level) to stress. The paper continues with the actualknowledge on the mechanisms of stress recognition and cell signalling. Briefly:plasma membranes are the sensors of environmental changes; phytohormones andsecond messengers are the transducers of information from membranes tometabolism; carbon balance is the master integrator of plant response; betwixtand between, some genes are expressed more strongly, whereas others arerepressed. Reactive oxygen species play key roles in up- and down-regulation ofmetabolism and structure. The paper shows finally that the above concepts canbeapplied to plant tissue cultures where the accumulating physiological andgenetical deviations (from a normal plant behaviour) are related to thestressing conditions of the in vitro culture media and ofthe confined environment. The hyperhydrated state of shoots and the cancerousstate of cells, both induced under conditions of stress in invitro cultures, are identified and detailed, because they perfectlyillustrate the stress-induced state-change concept. It is concluded that stressresponses include either pathologies or adaptive advantages. Stress may thuscontain both destructive and constructive elements : it is a selection factoraswell as a driving force for improved resistance and adaptive evolution.
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References
Alberts B., Bray D., Lewis J., Rass M., Roberts K. and Watson J. 1989. Cancer. In: Alberts B., Bray D., Lewis J., Rass M., Roberts K. and Watson J. (eds), Molecular Biology of the Cell. Garland, New York, pp. 1187–1216.
Altman A., Kaur-Sawhney R. and Galston W.A. 1977. Stabilization of oat leaf protoplasts through polyamine mediated inhibition of senescence. Plant Physiol. 60: 570–574.
Anonymous 1995. Habituation, hyperhydricity and plant cancer. Agricell Rep. 25: 29.
Arbillot J., Le Saos J., Billard J.P., Boucaud J. and Gaspar Th. 1991. Changes in fatty acid and lipid composition in normal and habituated sugar beet calli. Phytochemistry 30: 491–494.
Asard H., Berczi A. and Caubergs R.J. 1998. Plasma Membrane Redox Systems and their Role in Biological Stress and Disease. Kluwer Academic Publishers, Dordrecht, 332 pp.
Audisio S., Bagni N. and Serafini-Fracassini D. 1976. Polyamines during the growth in vitro of Nicotiana glauca R. Graph. habituated tissue. Z. Pflanzenphysiol. 77: 146–151.
Badiani M., Paolacci A.R., D'annibale A. and Sermanni G.G. 1993. Antioxidants and photosynthesis in the leaves of Triticum durum L. seedlings acclimated to low, non-chilling temperature. J. Plant Physiol. 142: 18–24.
Basra A.S. 1994. Stress-Induced Gene Expression in Plants. Harwood Academic Publishers, Chur, Switzerland, 287 pp.
Basu A.K. and Marnett L. 1984. Molecular requirements for the mutagenicity of malondialdehyde and related acroleins. Cancer Res. 44: 2848–2854.
Berczi A. and Moller I.M. 1998. NADH — monodehydroascorbate oxidoreductase is one of the redox enzymes in spinach leaf plasma membranes. Plant Physiol. 116: 1029–1036.
Bisbis B., Dommes J., Kevers C., Foidart J.M., Penel C., Greppin H. et al. 2000a. Unusual pathway for the biosynthesis of aminolevulinic acid and tetrapyrolic compounds, including peroxidases, and its relationship with the overproduction of polyamines and underemission of ethylene, in higher plant cancerous cells. Plant Peroxidase Newslett. 14: 55–68.
Bisbis B., Le Dily F., Kevers C., Billard J.P., Huault C. and Gaspar Th. 1993. Disturbed sugar metabolism in a fully habituated monorganogenic callus of Beta vulgaris (L.). Plant Growth Regul. 13: 257–261.
Bisbis B., Wagner A.M., Kevers C. and Gaspar Th. 2000b. A comparison of respiratory pathways in fully habituated and normal non-organogenic sugarbeet callus. J. Plant Physiol. 156: 312–318.
Bisbis B., Kevers C. and Gaspar Th. 1997. Atypical TCA cycle and replenishment in a non-photosynthetic fully habituated sugarbeet callus overproducing polyamines. Plant Physiol. Biochem. 35: 363–368.
Björkman O. and Demming B. 1987. Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170: 489–504.
Bray E.A., Baily-Serres J. and Weretilnyk E. 2000. Responses to abiotic stresses. In: Buchanan B., Gruissem W. and Jones R. (eds), Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, MD, pp. 1158–1203.
Böttcher I. and Göring H. 1987. Die Vitrifikation der Pflanzen ber der in vitro-Kultur as Infiltration Problem. Biol. Rundsch. 25: 191–193.
Brownleader M.D., Harborne J.B. and Dey P.M. 1997. Carbohydrate metabolism: primary metabolism of monosaccharides. In: Plant Biochemistry. Academic Press, London, pp. 111–140.
Burdon R.H. 1996. Control of cell proliferation by reactive oxygen species. Biochem. Soc. Transact. 24: 1028–1032.
Cajelli E., Ferraris A. and Brambilla G. 1987. Mutagenicity of 4-hydroxynonenal in V19 Chinese hamster cells. Mutat. Res. 190: 169–171.
Carrie B., Bisbis B., Penel C., Gaspar Th. and Greppin H. 1994. Disturbed sugar metabolism in a fully habituated nonorganogenic callus of Beta vulgaris. Additional data. Saussurea 25: 143–151.
Cassells A.C., Croke J.T. and Doyle B.M. 1997. Evaluation of image analysis, flow cytometry and RAPD analysis for the assessment of somaclonal variation and induced mutation in tissueculture derived Pelargonium plants. Angew. Bot. 7: 119–124.
Cassells A.C. and Curry R.F. 2001. Oxidative stress and physiological, epigenetic and genetic variability in plant tissue culture: implications for micropropagators and genetic engineers. Plant Cell Tissue Organ. Cult. 64: 145–167.
Cassells A.C., Doyle B.M. and Curry R.F. 2000. Methods and Markers for Quality Assurance in Micropropagation. Acta Hortic. 530.
Cassells A.C., Joyce S.M., Curry R.F. and McCarthy T.F. 1999b. Detection of economically important variability in micropropagation. In: Altman A., Izhar S. and Ziv M. (eds), Plant Biotechnology and In Vitro Biology in the 21st Century. Kluwer Academic Publishers, Dordrecht, pp. 241–244.
Cassells A.C., Kowalski B., Fitzgerald D.M. and Murphy G.A. 1999a. The use of image analysis to study developmental variation in micropropagated potatoes (Solanum tuberosum L.). Potato Res. 4: 541–548.
Cerutti P., Larsson R. and Krupitza G. 1990. Mechanisms of oxidant carcinogenesis. In: Harris C.C. and Liotta L.A. (eds), Genetic Mechanisms in Carcinogenesis and Tumor Progression. Wiley-Liss, Inc, pp. 69–82.
Chaerle L. and Van Der Straeten D. 2000. Imaging techniques and the early detection of plant stress. Trends Plant Sci. 5: 495–501.
Crèvecoeur M., Kevers C., Greppin H. and Gaspar Th. 1987. A comparative biochemical and cytological characterization of normal and habituated sugarbeet calli. Biol. Plant 29: 1–6.
Dang C.V. and Semenza G.L. 1999. Oncogenic alterations of metabolism. Trends Biochem. Sci. 24: 68–72.
Danneberger K.T. 2000. Effects of humidity on plant growth. In: Wilkinson R.E. (ed.), Plant–Environment Interactions. 2nd edn. Marcel Dekker, New York, pp. 343–360.
Debergh P., Aitken-Christie J., Cohen D., Grout B., Von Arnold S., Zimmerman R. et al. 1992. Reconsideration of the term vitrification as used in micropropagation. Plant Cell Tissue Organ Cult. 30: 140–165.
De Klerk G.J. 1990. How to measure somaclonal variation. Acta Bot. Neerl. 3: 129–144.
Dianzani M.V. 1989. Lipid peroxidation and cancer. A critical reconsideration. Tumori 75: 351–357.
Doonan J. and Hunt T. 1996. Why don't plants get cancer? Nature 380: 481–482.
Drolet G., Dumbroff E.B., Legge R.L. and Thompson J.E. 1986. Radical scavenging properties of polyamines. Phytochemistry 25: 367–371.
Druart P. 1998. Regulation of axillary branching in micropropagation of woody fruit species. Acta Hort. 227: 369–380.
Duncan R.R. 2000. Plant tolerance to acid soil constraints: genetic resources, breeding methodology, and plant improvement. In: Wilkinson R.E. (ed.), Plant—Environment Interactions. 2nd edn. Marcel Dekker, New York, pp. 1–38.
Foyer C.H., Lopez-Delgado H., Dat J.F. and Scott I.M. 1997. Hydrogen peroxide-and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol. Plant 100: 241–254.
Franck T., Crèvecoeur M., Wuest J., Greppin H. and Gaspar Th. 1998a. Cytological comparison of leaves and stems of Prunus avium L. shoots cultured on a solid medium with agar or gelrite. Biotechn. Histochem. 73: 32–43.
Franck T., Gaspar Th., Kevers C., Penel C., Dommes J. and Hausman J.F. 2001. Are hyperhydric shoots of Prunus avium L. energy deficient? Plant Sci. 160: 1145–1151.
Franck T., Kevers C. and Gaspar Th. 1995. 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.
Franck T., Kevers C., Hausman J.F., Dommes J., Penel C., Greppin H. et al. 2000. Redox capacities of in vitro cultured plant tissues: the case of hyperhydricity. In: Van den Driessche Th., Guisset J.L. and Petiau-de Vries G.M. (eds), The Redox State and Circadian Rhythms. Kluwer Academic Publishers, Dordrecht, pp. 235–255.
Franck T., Kevers C., Penel C., Gaspar Th., Hausman J.F. and Greppin H. 1998b. Reducing properties and markers of lipid peroxidation in normal and hyperhydrating shoots of Prunus avium L. J. Plant Physiol. 153: 339–346.
Gaspar Th. 1995. The concept of cancer in in vitro plant cultures and the implication of habituation to hormones and hyperhydricity. Plant Tissue Cult. Biotechnol. 1: 126–136.
Gaspar Th. 1998. Plants can get cancer. Plant Physiol. Biochem. 36: 203–204.
Gaspar Th. 1999. Tumours, neoplastic progressions and cancers in plants. In: Strnad M., Pec P. and Beck E. (eds), Advances in Regulation of Plant Growth and Development. Peres Cy Publishers, Prague, pp. 183–192.
Gaspar Th., Bisbis B., Kevers C., Penel C., Greppin H., Le Dily F. et al. 1998. Atypical metabolisms and biochemical cycles imposing the cancerous state on plant cells. Plant Growth Regul. 24: 135–144.
Gaspar Th., Hagege D., Kevers C., Penel C., Crèvecoeur M., Engelmann I. et al. 1991. When plant teratomas turn into cancers in the absence of pathogens. Physiol. Plant 83: 696–701.
Gaspar Th., Hagege D., Penel C., Foidart J.M. and Greppin H. 1992. Peroxidases and plant cancer in the absence of pathogens. In: Penel C., Gaspar Th. and Greppin H. (eds), Plant Peroxidases 1980–1990. Topics and Detailed Literature on Molecular, Biochemical and Physiological Aspects. University of Geneva, Switzerland, pp. 125–137.
Gaspar Th., Kevers C., Bisbis B., Franck T., Crevecoeur M., Greppin H. et al. 2000. Loss of plant organogenic tolipotency in the course of in vitro neoplastic progression. Vitro Cell Dev. Biol. — Plant 36: 171–181.
Gaspar Th., Kevers C., Franck T., Bisbis B., Billard J.P., Huault C. et al. 1995. Paradoxical results in the analysis of hyperhydric tissues considered as being under stress: questions for a debate. Bulg. J. Plant Physiol. 21: 80–97.
Gautheret R.J. 1942. Hétéro-auxines et cultures de tissus végétaux. Bull. Soc. Chim. Biol. 24: 13–41.
Genkov T., Tsoneva P. and Ivanova I. 1997. Effect of cytokinins on photosynthetic pigments and chlorophyllase activity in in vitro culture of axillary buds of Dianthus caryophyllus L. J. Plant Growth Regul. 16: 169–172.
Gogorcena Y., Iturbe-Ormaetxe I., Escuredo P.R. and Becana M. 1995. Antioxidant defences against activated oxygen in pea nodules subjected to water stress. Plant Physiol. 108: 753–759.
Gonzalez J.A., Hidalgo A., Caler J.A., Palos R. and Navas P. 1994. Nutrient uptake changes in ascorbate free radical-stimulated onion roots. Plant Physiol. 104: 271–276.
Greenberg J.T. 1996. Programmed cell death: a way of life for plants. Proc. Natl. Acad. Sci. USA 93: 12034–12097.
Hagege D., Catania R., Micalef H. and Gaspar Th. 1992a. Nuclear shape and DNA content of fully habituated nonorganogenic sugarbeet cells. Protoplasma 166: 49–54.
Hagege D., Deby C., Kevers C., Foidart J.M. and Gaspar Th. 1993. Anti-lipoperoxidant potential of the fully habituated nonorganogenic sugarbeet callus. Arch. Int. Physiol. Biochim. Biophys. 101: P9.
Hagege D., Kevers C., Crevecoeur M., Tollier M., Monties B. and Gaspar Th. 1991. Peroxidases, growth and differentiation of habituated sugarbeet cells. In: Lobarzewski J., Greppin H., Penel C. and Gaspar Th. (eds), Biochemical, Molecular, and Physiological Aspects of Plant Peroxidases. University of Geneva, Switzerland, pp. 281–290.
Hagege D., Kevers C., Geuns J. and Gaspar Th. 1994. Ethylene production and polyamine content of fully habituated sugarbeet calli. J. Plant Physiol. 143: 722–725.
Hagege D., Kevers C., Salabert P.h. and Gaspar Th. 1992b. Protective systems against activated oxygen species compared in normal and fully habituated nonorganogenic sugarbeet calluses. In Vitro Cell Dev. Biol. 28: 143–147.
Hagege D., Nouvelot A., Boucaud J. and Gaspar Th. 1990. Malondialdehyde titration with thiobarbiturate in plant extracts: Avoidance of pigment interference. Phytochem. Anal. 1: 86–89.
Halliwell B. 1996. Free radicals proteins and DNA: oxidative damage versus regulation. Biochem. Soc. Transact. 24: 1023–1027.
Hartwell L. 1992. Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells. Cell 71: 543–546.
Hasegawa P.M., Bressan R.H., Zhu J.K. and Bohnert H.J. 2000. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51: 463–499.
Hildrum K.I., Scanlan R.A. and Libbey L.M. 1976. In: Walker E.A., Bogovski P. and Gricinte L. (eds), Environmental n-Nitroso Compounds Analysis and Formation. International Agency for Research on Cancer (IARC), Lyon, France, pp. 205–214.
Horemans N., Asard H. and Caubergs R.J. 1998. Carrier-mediated uptake of dehydroascorbate into higher plant plasma membranes vesicles shows trans-stimulation. FEBS Lett. 421: 41–44.
Iturbe-Ormaetxe I., Escuredo P.R., Arrese-Igor C. and Becana M. 1998. Oxidative damage in pea plants exposed to water deficit or paraquat. Plant Physiol. 116: 173–181.
Jemmali A., Boxus P.h., Kevers C. and Gaspar Th. 1995. Carryover of morphological and biochemical characteristics associated with hyperflowering of micropropagated strawberries. J. Plant Physiol. 147: 435–440.
Jouve L., Franck T., Gaspar Th., Cattivelli L. and Hausman J.F. 2000. Poplar acclimation to cold during in vitro conservation at low non-freezing temperature: metabolic and proteic changes. J. Plant Physiol. 157: 117–123.
Karp A. 1993. Are your plants normal? Genetic instability in regenerated and transgenic plants. Agro-Food-Industry Hitech May–June 7–12.
Kevers C., Bisbis B., Franck Th., Le Dily F., Huault C., Billard J.P. et al. 1997. On the possible causes of polyamine accumulation in in vitro plant tissues under neoplasic progression. In: Greppin H., Penel C. and Simon P. (eds), Traveling Shot on Plant Development. University of Geneva, Switzerland, pp. 63– 71.
Kevers C., Bisbis B., Le Dily F., Huault C., Billard J.P. and Gaspar Th. 1995. Darkness improves growth and delays necrosis in a non chlorophyllous habituated sugarbeet callus. Biochemical changes. In Vitro Cell Biol. 31: 122–126.
Kevers C., Bisbis B., Penel C., Greppin H., Dommes J. and Gaspar Th. 1999a. Changes in the levels of hormones and related enzyme activities in the course of a neoplasic progression in a sugarbeet cell in culture. A critical appraisal. Curr. Top. Phytochem. 2: 35–49.
Kevers C., Coumans M., Coumans-Gilles M.F. and Gaspar Th. 1984. Physiological and biochemical events leading to vitrification of plants cultured in vitro. Physiol. Plant. 61: 69–74.
Kevers C. and Gaspar Th. 1986. Vitrification of carnation in vitro: changes in water content, extracellular space, air volume, and ion level. Physiol. Vég. 24: 647–653.
Kevers C., Greimers R., Franck Th., Bisbis B., Dommes J. and Gaspar Th. 1999b. Flow cytometry estimation of nuclear size and ploidy level of habituated calli of sugarbeet. Biol. Plant 42: 321–332.
Kozai T., Iwabuchi K., Watanabe K. and Watanabe I. 1991. Photoautotrophic and photomixotrophic growth of strawberry plantlets in vitro and changes in nutrient composition of the medium. Plant Cell Tissue Organ. Cult. 25: 107–115.
Krause G.H. and Weis E. 1991. Chlorophyll fluorescence and photosynthesis. The basic. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 313–349.
Lambe P., Nkung Mutambel H.S., Fouche J.G., Deltour R., Foidart J.M. and Gaspar Th. 1997. DNA methylation as a key process in regulation of organogenic totipotency and plant neoplastic progression? In Vitro Cell Dev. Biol. — Plant 33: 155–162.
Larcher W. 1980. Physiological Plant Ecology. Springer Verlag, New York.
Le Dily F., Billard J.P. and Boucaud J. 1991. Polyamine levels in relation to growth and NaCl concentration in normal and habituated sugarbeet callus. Plant Cell Environ. 14: 327–332.
Le Dily F., Billard J.P., Huault C., Kevers C. and Gaspar Th. 1993a. Fully habituated sugarbeet callus: Under permanent stress? In Vitro Cell Dev. Biol. 29: 149–154.
Le Dily F., Huault C., Gaspar Th. and Billard J.P. 1993b. Does altered nitrogen metabolism and H2O2 accumulation explain the vitrified status of the fully habituated callus of Beta vulgaris (L)? Plant Cell Tissue Organ Cult. 35: 69–74.
Leon J., Rojo E. and Sanchez-Serrano J.J. 2001. Wound signalling in plants. J. Exp. Bot. 52: 1–9.
Levitt J. 1980. Responses of Plant to Environmental Stresses. Vol. I. Academic Press, New York.
Levitt J. 1982. Stress terminology. In: Turner N.C. and Kramer P.J. (eds), Adaptation of Plants to Water and High Temperature Stress. Wiley-Interscience, New York, pp. 437–439.
Lichtenthaler H.K. 1996. Vegetation stress: an introduction to the stress concepts in plants. J. Plant Physiol. 148: 4–14.
Liners F., Gaspar Th. and Van Cutsem P. 1994. Acetyl-and methyl-esterification of pectins of friable and compact sugarbeet calli: consequences for intercellular adhesion. Planta 192: 545– 556.
Luthe D.S., Kraus J.V., Wang D. and Park S.Y. 2000. In: Wilkinson R.E. (ed.), Plant Environment — Interactions. 5th edn. Marcel Dekker Inc, New York, pp. 283–319.
Lutts S. and Kinet J.M. 1998. Les effets des stress sur la croissance et le développement: vue synoptique. Bull. Soc. Roy. Sci. Liège 67: 117–136.
Murphy T.M., Asard H. and Cross A.R. 1998. Possible sources of reactive oxygen during the oxidative burst in plants. In: Asard H. and Berczi A. (eds), Plasma Membrane Redox Systems and their Role in Biological Stress and Disease. Kluwer Academic Publishers, Dordrecht, pp. 215–246.
Nilsen E. and Orcutt D.M. 1996. The Physiology of Plants Under Stress — Abiotic factors. John Wiley and Sons, Inc, New York, 689.
Osmond C.B., Austin M.P., Berry J.A., Billings W.D., Boyer J.S., Dacey J.W.H. et al. 1987. Stress physiology and the distribution of plants. Bioscience 37: 38–48.
Phillips R.L., Kaeppler S.M. and Olhoft P. 1994. Genetic instability of plant tissue cultures: breakdown of normal controls. Proc. Natl. Acad. Sci. USA 91: 5222–5226.
Pedreno M.A., Ferrer M.A., Gaspar Th., Munoz R. and Ros Barcelo A. 1995. The polyfunctionality of cell wall peroxidases avoids the necessity of an independent H2O2-generating system for phenolic coupling in the cell wall. Plant Peroxidase Newslett. 5: 3–8.
Polle A., Chakrabarti K., Chakrabarti S., Seifert F., Schram P. and Rennenberg H. 1992. Antioxidants and manganese deficiency in needles of Norway spruce (Picea abies L.) trees. Plant Physiol. 99: 1084–1089.
Porciani S., Becciolani A., Lanini A., Balzi M., Boanini P., Mauri P. et al. 1993. Polyamines and proliferative activity in tumor tissues. Cell Prolif. 26: 490.
Rani V. and Raina S.N. 2000. Genetic fidelity or organized meristem-derived micropropagated plants. A critical reappraisal. In Vitro Cell Dev. Biol. — Plant 36: 319–330.
Rubinstein B. and Luster D.G. 1993. Plasma membrane redox activity: components and roles in plant processes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44: 131–155.
Rugini E., Tarini P. and Rossodivata M.E. 1987. Control of shoot vitrification of almond and olive grown in vitro. Acta Hort. 212: 177–183.
Smirnoff N. 1995. Environment and Plant Metabolism. Flexibility and Acclimation. Bios Scientific Publishers Ltd, Oxford, 270.
Smith T.A. 1985. Polyamines. Annu. Rev. Plant Physiol. 36: 117–143.
Strasser R.J. 1988. A concept for stress and its application in remote sensing. In: Lichtenthaler H.K. (ed.), Applications of Chlorophyll Fluorescence. Kluwer Academic Publishers, Dordrecht, pp. 333–337.
Strasser R.J., Srivastava A. and Govindjee S. 1995. Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem. Photobiol. 61: 32–42.
Swartz H.J. 1991. Post culture behaviour: genetic and epigenetic effects and related problems. In: Debergh P.C. and Zimmerman R.H. (eds), Micropropagation: Technology and Applications. Kluwer Academic Publishers, Dordrecht, pp. 95–121.
Tomos A.D. 1990. Growth — A role for plant growth regulators? In: Davies W.J. and Jeffcoat B. (eds), Importance of Root to Shoot Communication in the Responses to Environmental Stress. British Society of Plant Growth Regulation Monograph., pp. 53–69.
Tsimilli-Michael M., Krüger H.J. and Strasser R.J. 1996. About the perpetual state changes in plants approaching harmony with their environment. Arch. Sci. Geneva 49: 173–203.
Vaca C.E., Wilhelm J. and Harms-Ringahl M. 1988. Interaction of lipid peroxidation products with DNA. A review. Mutat. Res. 195: 137–149.
Van Huylenbroeck J.M. and Debergh P.C. 1996. Impact of sugar concentration in vitro on photosynthesis and carbon metabolism during ex vitro acclimatization of Spatiphyllum plantlets. Physiol. Plant. 96: 298–304.
Wilkinson R.E. 2000. Plant — Environment Interactions. 2nd edn. Marcel Dekker, Inc, New York, 456 pp.
Winston G.W. 1990. Physiochemical basis for free radical formation in cells: production and defenses. In: Alscher R.G. and Cumming J.R. (eds), Stress Responses in Plants; Adaptation and Acclimation Mechanisms. Wiley-Liss Inc, New York, pp. 57–86.
Zhu J.K. 2001. Plant salt tolerance. Trends Plant Sci. 6: 66–71.
Ziv M. 1991. Vitrification: morphological and physiological disorders of in vitro plants. In: Debergh P.C. and Zimmerman R.H. (eds), Micropropagation: Technology and Applications. Kluwer Academic Publishers, Dordrecht, pp. 45–70.
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Gaspar, T., Franck, T., Bisbis, B. et al. Concepts in plant stress physiology. Application to plant tissue cultures. Plant Growth Regulation 37, 263–285 (2002). https://doi.org/10.1023/A:1020835304842
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DOI: https://doi.org/10.1023/A:1020835304842