Concepts in plant stress physiology. Application to plant tissue cultures

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.

[1]  B. Halliwell Free radicals, proteins and DNA: oxidative damage versus redox regulation. , 1996, Biochemical Society transactions.

[2]  T. Genkov,et al.  Effect of Cytokinins on Photosynthetic Pigments and Chlorophyllase Activity in in Vitro Cultures of Axillary Buds of Dianthus caryophyllus L. , 1997, Journal of Plant Growth Regulation.

[3]  P. Debergh,et al.  Impact of sugar concentration in vitro on photosynthesis and carbon metabolism during ex vitro acclimatization of Spathiphyllum plantlets , 1996 .

[4]  A. Wagner,et al.  A comparison of respiratory pathways in fully habituated and normal non-organogenic sugarbeet callus , 2000 .

[5]  R. F. Curry,et al.  Oxidative stress and physiological, epigenetic and genetic variability in plant tissue culture: implications for micropropagators and genetic engineers , 2001, Plant Cell, Tissue and Organ Culture.

[6]  C. Kevers,et al.  Physiological and biochemical events leading to vitrification of plants cultured in vitro , 1984 .

[7]  T. Gaspar,et al.  Nuclear shape and DNA content of fully habituated nonorganogenic sugarbeet cells , 1992, Protoplasma.

[8]  D. Orcutt,et al.  The Physiology of Plants Under Stress, Abiotic Factors , 1996 .

[9]  J. Billard,et al.  Changes in fatty acid and lipid composition in normal and habituated sugar beet calli , 1991 .

[10]  J. Billard,et al.  Atypical metabolisms and biochemical cycles imposing the cancerous state on plant cells , 1998, Plant Growth Regulation.

[11]  A. Paolacci,et al.  Antioxidants and Photosynthesis in the Leaves of Triticum durum L. Seedlings Acclimated to Low, Non-Chilling Temperature , 1993 .

[12]  J. Etherington,et al.  Physiological Plant Ecology. , 1977 .

[13]  P. Navas,et al.  Nutrient Uptake Changes in Ascorbate Free Radical-Stimulated Onion Roots , 1994, Plant physiology.

[14]  H. Greppin,et al.  Special symposium: In vitro plant recalcitrance loss of plant organogenic totipotency in the course of In vitro neoplastic progression , 2000, In Vitro Cellular & Developmental Biology - Plant.

[15]  H. Asard,et al.  Possible sources of reactive oxygen during the oxidative burst in plants , 1998 .

[16]  Wilhelm Gruissem,et al.  Biochemistry & Molecular Biology of Plants , 2002 .

[17]  T. K. Danneberger Effects of Humidity on Plant Growth , 2000 .

[18]  E C WASSINK,et al.  Chlorophyll fluorescence and photosynthesis. , 1951, Advances in enzymology and related subjects of biochemistry.

[19]  N. Bagni,et al.  Polyamines during the Growth in vitro of Nicotiana glauca R. Grah. habituated Tissue , 1976 .

[20]  L. Marnett,et al.  Molecular requirements for the mutagenicity of malondialdehyde and related acroleins. , 1984, Cancer research.

[21]  J. Foidart,et al.  When plant teratomas turn into cancers in the absence of pathogens , 1991 .

[22]  J. Harborne,et al.  3 – Carbohydrate Metabolism: Primary Metabolism of Monosaccharides , 1997 .

[23]  C. Penel,et al.  Are hyperhydric shoots of Prunus avium L. energy deficient? , 2001, Plant science : an international journal of experimental plant biology.

[24]  A. Cassells,et al.  The use of image analysis to study developmental variation in micropropagated potato (Solanum tuberosum L.) plants , 1999, Potato Research.

[25]  J. Greenberg,et al.  Programmed cell death: a way of life for plants. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[26]  M. Dianzani,et al.  Lipid Peroxidation and Cancer: A Critical Reconsideration , 1989, Tumori.

[27]  V. Rani,et al.  Genetic fidelity of organized meristem-derived micropropagated plants: A critical reappraisal , 2000, In Vitro Cellular & Developmental Biology - Plant.

[28]  C. Kevers,et al.  Vitrification of carnation in vitro: changes in water content, extracellular space, air volume, and ion levels , 1986 .

[29]  H. Bohnert,et al.  PLANT CELLULAR AND MOLECULAR RESPONSES TO HIGH SALINITY. , 2000, Annual review of plant physiology and plant molecular biology.

[30]  M. Ziv Vitrification: morphological and physiological disorders of in vitro plants , 1991 .

[31]  M. Dianzani,et al.  Lipid peroxidation and cancer. , 1993, Critical reviews in oncology/hematology.

[32]  B. Monties,et al.  Peroxidases, growth and differentiation of habituated sugarbeet cells , 1991 .

[33]  M. Harms-Ringdahl,et al.  Interaction of lipid peroxidation products with DNA. A review. , 1988, Mutation research.

[34]  H. Lichtenthaler Vegetation stress : an introduction to the stress concept in plants , 1996 .

[35]  Brczi,et al.  NADH-Monodehydroascorbate oxidoreductase is one of the redox enzymes in spinach leaf plasma membranes , 1998, Plant physiology.

[36]  Y. Gogorcena,et al.  Antioxidant Defenses against Activated Oxygen in Pea Nodules Subjected to Water Stress , 1995, Plant physiology.

[37]  M. Crèvecoeur,et al.  Cytological comparison of leaves and stems of Prunus avium L. shoots cultured on a solid medium with agar or gelrite. , 1998, Biotechnic & histochemistry : official publication of the Biological Stain Commission.

[38]  J. Boucaud,et al.  Malondialdehyde titration with thiobarbiturate in plant extracts: Avoidance of pigment interference , 1990 .

[39]  J. Foidart,et al.  DNA methylation as a key process in regulation of organogenic totipotency and plant neoplastic progression? , 1997, In Vitro Cellular & Developmental Biology - Plant.

[40]  R. Greimers,et al.  Flow Cytometry Estimation of Nuclear Size and Ploidy Level of Habituated Calli of Sugar Beet , 1999, Biologia Plantarum.

[41]  J. Billard,et al.  Disturbed sugar metabolism in a fully habituated nonorganogenic callus of Beta vulgaris (L.) , 1993, Plant Growth Regulation.

[42]  D. Luster,et al.  Plasma Membrane Redox Activity: Components and Role in Plant Processes , 1993 .

[43]  J. Geuns,et al.  Ethylene Production and Polyamine Content of Fully Habituated Sugarbeet Calli , 1994 .

[44]  S. Kaeppler,et al.  Genetic instability of plant tissue cultures: breakdown of normal controls. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[45]  T. Franck,et al.  Protective enzymatic systems against activated oxygen species compared in normal and vitrified shoots of Prunus avium L. L. raised in vitro , 1995, Plant Growth Regulation.

[46]  S. Costanzo,et al.  CONTROL OF SHOOT "VITRIFICATION" OF ALMOND AND OLIVE GROWN IN VITRO , 1987 .

[47]  J. Hausman,et al.  Reducing properties, and markers of lipid peroxidation in normal and hyperhydrating shoots of Prunus avium L. , 1998 .

[48]  T. Kozai,et al.  Photoautotrophic and photomixotrophic growth of strawberry plantlets in vitro and changes in nutrient composition of the medium , 1991, Plant Cell, Tissue and Organ Culture.

[49]  R. Alscher,et al.  Stress responses in plants: Adaptation and acclimation mechanisms. , 1990 .

[50]  Z. Hall Cancer , 1906, The Hospital.

[51]  J. Palta,et al.  Responses to abiotic stresses. , 1998 .

[52]  P. V. Cutsem,et al.  Acetyl- and methyl-esterification of pectins of friable and compact sugar-beet calli: consequences for intercellular adhesion , 1994, Planta.

[53]  A. Srivastava,et al.  POLYPHASIC CHLOROPHYLL a FLUORESCENCE TRANSIENT IN PLANTS AND CYANOBACTERIA * , 1995 .

[54]  C. Kevers,et al.  Carry-over of Morphological and Biochemical Characteristics Aßociated with Hyperflowering of Micropropagated Strawberries , 1995 .

[55]  G. Semenza,et al.  Oncogenic alterations of metabolism. , 1999, Trends in biochemical sciences.

[56]  R. F. Curry,et al.  Detection of Economically Important Variability in Micropropagation , 1999 .

[57]  C. Kevers,et al.  Atypical TCA cycle and replenishment in a non-photosynthetic fully habituated sugarbeet callus overproducing polyamines , 1997 .

[58]  J. Doonan,et al.  Why don't plants get cancer? , 1996, Nature.

[59]  J. Hausman,et al.  Redox capacities of in vitro cultured plant tissues: the case of hyperhydricity , 2000 .

[60]  E. B. Dumbroff,et al.  Radical scavenging properties of polyamines , 1986 .

[61]  J. Billard,et al.  Does altered nitrogen metabolism and H2O2 accumulation explain the vitrified status of the fully habituated callus of Beta vulgaris (L.)? , 1993, Plant Cell, Tissue and Organ Culture.

[62]  H. Rennenberg,et al.  Antioxidants and Manganese Deficiency in Needles of Norway Spruce (Picea abies L.) Trees. , 1992, Plant physiology.

[63]  Leland Hartwell,et al.  Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells , 1992, Cell.

[64]  J. Berry,et al.  Stress physiology and the distribution of plants , 1987 .

[65]  L. Cattivelli,et al.  Poplar acclimation to cold during in vitro conservation at low non-freezing temperature: metabolic and proteic changes , 2000 .

[66]  P. Debergh,et al.  Reconsideration of the term ‘vitrification’ as used in micropropagation , 1992, Plant Cell, Tissue and Organ Culture.

[67]  G. Klerk How to measure somaclonal variation , 1990 .

[68]  H. Asard,et al.  Carrier mediated uptake of dehydroascorbate into higher plant plasma membrane vesicles shows trans‐stimulation , 1998, FEBS letters.

[69]  Neil C. Turner,et al.  Adaptation of plants to water and high temperature stress , 1980 .

[70]  A. Ferraris,et al.  Mutagenicity of 4-hydroxynonenal in V79 Chinese hamster cells. , 1987, Mutation research.

[71]  G. Krause,et al.  Chlorophyll Fluorescence and Photosynthesis: The Basics , 1991 .

[72]  K Dave,et al.  A CRITICAL APPRAISAL , 2002 .

[73]  H. Greppin,et al.  Molecular and physiological aspects of plant peroxidases , 1986 .

[74]  B. M. Doyle,et al.  Evaluation of image analysis, flow cytometry, and RAPD analysis for the assessment of somaclonal variation and induced mutation in tissue culture-derived Pelargonium plants , 1997 .

[75]  O. Björkman,et al.  Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins , 1987, Planta.

[76]  A. Altman,et al.  Stabilization of Oat Leaf Protoplasts through Polyamine-mediated Inhibition of Senescence. , 1977, Plant physiology.

[77]  J. Sánchez-Serrano,et al.  Wound signalling in plants. , 2001, Journal of experimental botany.

[78]  J. Billard,et al.  Polyamine levels in relation to growth and NaCl concentration in normal and habituated sugarbeet callus cultures , 1991 .

[79]  Mary E. S. Loomis,et al.  The Basics: , 1990, Is That True?.

[80]  P. R. Escuredo,et al.  Oxidative Damage in Pea Plants Exposed to Water Deficit or Paraquat , 1998 .

[81]  R. Burdon Control of cell proliferation by reactive oxygen species. , 1996, Biochemical Society transactions.

[82]  P. Cerutti,et al.  Mechanisms of oxidant carcinogenesis. , 1990, Progress in clinical and biological research.

[83]  N. Smirnoff,et al.  Environment and plant metabolism: flexibility and acclimation. , 1995 .

[84]  D. Straeten,et al.  Imaging techniques and the early detection of plant stress. , 2000, Trends in plant science.

[85]  Shu Fuka Plant-Environment Interactions, 2nd ed , 2001 .

[86]  H. Asard,et al.  Plasma Membrane Redox Systems and their Role in Biological Stress and Disease , 1998, Springer Netherlands.

[87]  J. Dat,et al.  Hydrogen peroxide‐ and glutathione‐associated mechanisms of acclimatory stress tolerance and signalling , 1997 .

[88]  R. Duncan Plant Tolerance to Acid Soil Constraints: Genetic Resources, Breeding Methodology, and Plant Improvement , 2000 .

[89]  J. Billard,et al.  Paradoxical results in the analysis of hyperhydric tissues considered as being under stress: questions for a debate , 1995 .