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Stress and aberrant phenotypes in vitro culture

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Abstract

Stress responses are largely conserved in eukaryotic cells, but with plants having certain distinctive reactions to specific stresses, e.g. the induction of pathogenesis-related proteins. General responses to stress involve signaling stress detection via the redox system, checkpoints arresting the cell cycle and DNA repair processes stimulated in response to DNA damage. Specific responses to stress include the induction of protective metabolites, such as betaines, and protective proteins, for example, heat shock proteins. Chemical signals, e.g. reactive oxygen species, Ca2+ and plant hormones, acting through signal transduction cascades activate genomic re-programming. Genome plasticity in plants allows adaptation to environmental conditions and includes genomic or epigenetic changes (histone acetylation, methylation, chromatin remodeling etc.) and possibly directed mutation. In plants, recent research has indicated that intricate stress response mechanisms and `cross talk' between stress responses exist. Here, changes in the plant genome and in genomic expression in development and as a response to environmental stress are reviewed as background to a discussion of the basis of aberrant genomic expression in vitro. Markers are discussed which may be used to characterize the stress exposure of in vitro tissues.

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References

  • Araki T (2001) Transition from vegetative to reproductive phase. Curr. Opin. Plant Biol. 4: 63-68

    Google Scholar 

  • Bauschmann C, Langsdorf G & Lichtenthaler HK (2000) Imaging of the blue, green and red fluorescence emission of plants: an overview. Photosynthetica 38: 483-491

    Google Scholar 

  • Benson EE (2000) Do free radicals have a role in plant tissue culture recalcitrance? In Vitro Cell Dev. Biol. Plant 36: 163-170

    Google Scholar 

  • Bohr V, Anson RM, Mazur S & Dianov GL (1995) Oxidative DNA damage processing and changes with ageing. Toxicol. Lett. 102-103: 47-52

    Google Scholar 

  • Boyes J & Bird A (1991) DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein. Cell 64: 1123-1113

    Google Scholar 

  • Bowler C & Fluhr R (2000) The role of calcium and activated oxygen as signals for controlling cross-tolerance. Trends Plant Sci. 5: 241-246

    Google Scholar 

  • Bradshaw AD (1965) The evolutionary significance of phenotypic plasticity in plants. Adv. Genet. 13: 115-155

    Google Scholar 

  • Bray EA (1997) Plant responses to water deficit. Trends Plant Sci. 2: 48-54

    Google Scholar 

  • Bray EA, Bailey-Serres J & Weretilnyk E (2000) Responses to abiotic stresses. In: Buchanan B, Gruissem W & Jones R (eds.) Biochemistry and Molecular Biology of Plants (pp. 1158-1203). Amer. Soc. Plant Physiol., Rockville

  • Bruce A & Orr-Weaver TL (2001) Endoreplication cell cycles more for less. Cell 105: 297-306

    Google Scholar 

  • Cassells AC (2000) Aseptic microhydroponics: a strategy to advance microplant development and improve microplant physiology. Acta Hortic. 530: 187-194

    Google Scholar 

  • Cassells AC (2002) Tissue culture for ornamental breeding. In: Vainstein A (ed) Breeding for Ornamentals - Classical and Molecular Approaches (pp. 139-154). Kluwer, Dordrecht

  • Cassells AC & Roche T (1994) The influence of the gas permeability of the vessel lid and growth room light intensity on the characteristics of Dianthus microplants in vitro and ex vitrum. In: Lumsden PJ, Nicholas JR & Davies WJ (eds.) Physiology, Growth and Development of Plants in Culture (pp. 204-214). Kluwer, Dordrecht

  • Cassells AC & Walsh C (1994) The influence of the gas permeability of the culture lid on calcium uptake and stomatal function in Dianthus microplants. Plant Cell Tiss. Org. Cult 37: 171-178

    Google Scholar 

  • Cassells AC & Curry RF (2001) Oxidative stress and physiological, epigenetic and genetic variability in plant tissue culture: implications for micropropagators and genetic engineers. Plant Cell Tiss. Org. Cult. 64: 145-157

    Google Scholar 

  • Cassells AC, Doyle BM & Curry RF (2000) Proceedings of the International Symposium on Methods and Markers for Quality Assurance in Micropropagation. Acta Hortic 530

  • Cassells AC, Joyce SM, O'Herlihy EA, Perez-Sanz MJ & Walsh C (2003) Stress and quality in in vitro culture. Acta Hort (in press)

  • Christianson ML & Warnick DA (1983) Competence and determination in the process of in vitro shoot organogenesis. Dev. Biol. 95: 288-293

    Google Scholar 

  • Cullis CA (1990) DNA rearrangements in response to environmenttal stress. Adv. Genet. 28: 73-97

    Google Scholar 

  • Cullis CA (1999) The environment as an active generator of adaptive genomic variation. In: Lerner HR (ed) Plant Response to Environmental Stresses (pp. 149-160). Marcel Dekker Inc, New York,Basel

    Google Scholar 

  • D'Amato F (1985) Cytogenetics of plant cell and tissue cultures and their regenerants. CRC Crit. Rev. Plant Sci. 3: 73-112

    Google Scholar 

  • Danon A, Delorme V, Mailhac N & Gallois P (2000) Plant programmed cell death: a common way to die. Plant Physiol. Biochem. 38: 647-655

    Google Scholar 

  • Debergh P, Aitken-Christie J, Cohen D, Grout B, von Arnold S, Zimmerman R & Ziv M (1992) Reconsideration of the term ‘vitrification’ as used in micropropagation. Plant Cell Tiss. Org. Cult. 30: 135-140

    Google Scholar 

  • Dellaporta SL & Calderon-Urrea A (1994) Degree of DNA methylation in chicory (Cichorium intybus L.) influence of plant age and vernalization. Science 266: 1501-1505

    Google Scholar 

  • Diggle PK (1997) Architectural effects and interpretation of patterns of fruit and seed development. Annu. Rev. Ecol. Syst. 26: 531-552

    Google Scholar 

  • Duncan RR (1997) Tissue culture-induced variation and crop improvement. Adv. Agron. 58: 201-240

    Google Scholar 

  • Durzan DJ (1990) Adult vs. juvenile explants: directed totipotency. In: Rodriguez R, Sanchez Tame R & Durzan DJ (eds.) Molecular Basis of Plant Ageing (pp.19-25) Plenum Press, New York

    Google Scholar 

  • Evans MMS & Poethig RS (1995) Gibberellins promote vegetative phase change and reproductive maturity in maize. Plant Physiol. 108: 475-487

    Google Scholar 

  • Evans NH, McAinsh MR & Hetherington AM (2001) Calcium oscillations in higher plants. Curr. Opin. Plant Biol. 4: 415-420

    Google Scholar 

  • Farkas G, Leibovitch BA & Elgin SCR (2000) Chromatin organization and transcriptional control of gene expression in Drosophila. Gene 253: 117-136

    Google Scholar 

  • Finkelstein RR & Gibson SI (2001) ABA and sugar interactions regulating development: cross-talk or voices in a crowd? Curr. Opin. Plant Biol. 5: 26-32

    Google Scholar 

  • Finnegan EJ (2001a) Is plant gene expression regulated globally? Trends Genet. 17: 361-364

    Google Scholar 

  • Finnegan EJ (2001b) Epialleles - a source of random variation in times of stress. Curr. Opin. Plant Biol. 5: 101-106

    Google Scholar 

  • Fontes MA, Otoni WC, Carolino SMB, Brommonschenkel SH, Fontes EPB, Fari M & Luoro RP (1999) Hyperhydricity in pepper plants regeneration in vitro: involvement of BiP (Binding Protein) and ultrastructural aspects. Plant Cell Rep. 19: 81-87

    Google Scholar 

  • Franck T, Gaspar T, Kevers C, Penel C, Dommes J & Hausman JF (2001) Are hyperhydric shoots of Prunus avium L. energy deficient? Plant Sci. 160: 1145-1151

    Google Scholar 

  • Gaspar T (1991) Vitrification in micropropagation. In: Bajaj YPS (ed) Biotechnology in Agriculture and Forestry, High-tech and Micropropagation I Vol. 17 (pp. 117-114). Springer-Verlag, Berlin

    Google Scholar 

  • Gaspar pT, Bisbis B, Kevers C, Penel C, Greppin H, LeDily F, Billard JP, Huault C, Garnier F, Rideau M & Foidart JM (1998) Atypical metabolisms and biochemical cycles imposing the cancerous state on plant cells. Plant Growth Reg. 24: 135-144

    Google Scholar 

  • George EF (1993) Plant Propagation by Tissue Culture, Part 1. The Technology. Exegetics Ltd, Basingstoke, UK

    Google Scholar 

  • Grandbastien MA (1998) Activation of plant retrotransposons under stress conditions. Trends Plant Sci. 3: 181-187

    Google Scholar 

  • Guy C (1999) The influence of temperature extremes on gene expression, genomic structure, and the evolution of induced tolerance in plants. In: Lerner HR (ed) Plant Responses to Environmental Stresses (pp. 497-548). Marcel Dekker, New York

    Google Scholar 

  • Harding K, Benson EE & Roubelakis-Angelakis KA (1996) Methylated DNA changes associated with the initiation and maintenance of Vitis vinifera in vitro shoot and callus: a possible mechanism for age-related changes. Vitis 35: 79-85

    Google Scholar 

  • Hasenstein KH & Evans ML (1988) Effects of cations on hormone transport in primary roots of Zea mays. Plant Physiol. 86: 890-894

    Google Scholar 

  • Hirt H (2000) Results and Problems in Cell Differentiation.Vol. 27, Springer-Verlag, Berlin

    Google Scholar 

  • Howell SH (1998) The Molecular Genetics of Plant Development. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Huang H-J, Chen Y, Kuo J-L, Kuo T-T, Tzeng C-C, Huang B-L, Chen C-M & Huang L-C (1996) Rejuvenation of Sequoia sempervirens in vitro: changes in isoesterases and isoperoxidases. Plant Cell Physiol. 37: 77-80

    Google Scholar 

  • Ichimura K, Mizoguchi T, Yoshida R, Yuasa T & Shinozaki K (2000) Protein phosphorylation and dephosphorylation in environmental stress responses in plants. In: Kreis M & Walker JC (eds.) Advances in Botanical Research: Incorporating Advances in Plant Physiology 32 (pp. 355-377). Academic Press, New York

    Google Scholar 

  • Innes RW (2001) Mapping out the roles of MAP kinases in plant defense. Trend Plant Sci. 6: 392-394

    Google Scholar 

  • Inze D & Van Montagu M (2002) Oxidative Stress in Plants. Taylor and Francis, London

    Google Scholar 

  • Jabs T (1999) Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem. Pharmacol. 57: 231-245

    Google Scholar 

  • Jain SM (1997) Creation of variability by mutation and tissue culture for improving plants. Acta Hortic. 447: 69-77

    Google Scholar 

  • Jain SM (2001) Tissue culture-derived variation in crop improvement. Euphytica 118: 153-166

    Google Scholar 

  • Jain SM, Brar DS & Ahloowalia BS (eds.) (1998) Somaclonal Variation and Induced Mutations in Crop Improvement. Kluwer, Dordrecht

    Google Scholar 

  • Jones CS (1999) An essay on juvenility, phase change, and heteroblasty in seed plants. Int. J. Plant Sci. 160: s105-s111

    Google Scholar 

  • Joyce SM & Cassells AC (2002) Variation in potato microplant morphology in vitro and DNA methylation. Plant Cell Tiss. Org. Cult. 70: 125-137

    Google Scholar 

  • Kaeppler SM, Kaeppler HF & Rhee Y(2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol. Biol. 43: 179-188

    Google Scholar 

  • Kaeppler SM & Phillips RL (1993) Tissue culture-induced DNA methylation variation in maize. PNAS USA 90: 8773-8776

    Google Scholar 

  • Kasai H (1997) Analysis of a form of oxidative DNA damage, 8-hydroxy-2?-deoxyguanosine, as a marker of cellular oxidative stress during carcinogenesis. Mutation Res. 387: 147-163

    Google Scholar 

  • Kawata M, Ohmiya A, Shimamoto Y, Oona K & Takaiwa F (1995) Structural changes in the plastid genome of rice (Oryza sativa L.) During tissue culture. TAG 90: 364-371

    Google Scholar 

  • Kerbauy GB, Peters JA & Hell KG (1986) Cytokinin autotrophy and differentiation in tissue cultures of haploid Nicotiana tabacum L. Plant Sci. 45: 125-132

    Google Scholar 

  • Kerstetter RA & Poethig RS (1998) The specification of leaf identity during shoot development. Annu. Rev. Cell Dev. Biol. 14: 373-398

    Google Scholar 

  • Keshet I, Lieman-Hurwitz J & Cedar H (1986) DNA methylation affects the formation of active chromatin. Cell 44: 535-543

    Google Scholar 

  • Kilian A, Stiff C & Kleinhofs A (1995) Barley telomeres shorten during differentiation but grow in callus cultures. PNAS USA 92: 9555-9559

    Google Scholar 

  • Knight H & Knight MR (2001) Abiotic stress signaling pathways: specificity and cross-talk. Trends Plant Sci. 6: 262-267

    Google Scholar 

  • Kocsy G, Galiba G & Brunold C (2001) Role of glutathione in adaptation and signaling during chilling and cold acclimation in plants. Physiol. Plant 113: 158-164

    Google Scholar 

  • Kowalski B & Cassells AC (1999) Mutation breeding for yield and Phytophthora infestans (Mont.) de Bary foliar resistance in potato (Solanum tuberosum L. cv. Golden Wonder) using computerised image analysis in selection. Potato Res. 42: 121-130

    Google Scholar 

  • Krauss G (1999) Biochemistry of Signal Transduction and Regulation. Wiley-VCH, Weinheim

    Google Scholar 

  • Krishnamurthy KV, Krishnaraj R, Chozhavendan R & Samuel Christopher F (2000) The programme of cell death in plants and animals - a comparison. Curr. Sci. 79: 1169-1181

    Google Scholar 

  • Larkin PJ & Scowcroft WR (1981) Somaclonal variation - a novel source of variability from cell cultures for plant improvement. TAG 60: 197-214

    Google Scholar 

  • Larkins BA, Dilkes BP, Dante RA, Coelho CM, Woo YM & Liu Y (2001) Investigating the hows and whys of DNA endoreduplication. J Exp. Bot. 52: 183-192

    Google Scholar 

  • Laval J (1996) Role of DNA repair enzymes in the cellular resistance to oxidative stress. Pathol. Biol. 44: 14-24

    Google Scholar 

  • Lerner HR (ed) (1999) Plant Responses to Environmental Stresses. Marcel Dekker Inc, New York

    Google Scholar 

  • Lin C (2000) Plant blue-light receptors. Trends Plant Sci. 5: 337-342

    Google Scholar 

  • Locy DR, Wu S-J, Bisnette J, Barger TW, McNabb D, Zik M, Fromm H, Singh NK & Cherry JH (2000) The regulation of GABA accumulation by heat stress in Arabidopsis. In: Cherry JH, Locy DR & Rychter A (eds.) Plant Tolerance to Abiotic Stress in Agriculture: Role of Genetic Engineering (pp. 39-52). Kluwer, Dordrecht

    Google Scholar 

  • Lusso M & Kuc J (1999) Plant responses to pathogens. In: Lerner HR (ed) Plant Responses to Environmental Stresses (pp. 683-706). Marcel Dekker, New York

    Google Scholar 

  • Meins FJ & Foster R (1985) Reversible, cell-heritable changes during the development of tobacco pith tissues. Dev. Biol. 108: 1-5

    Google Scholar 

  • Molinete M, Vermeulen W, Burkle A, Menissier-deMurcia J, Kupper JH, Hoeijmakers JH & de Murcia G (1993) Overproduction of the poly(ADP-ribose) polymerase DNA-binding domain blocks alkylation-induced DNA repair synthesis in mammalian cells. EMBO J 12: 2109-2117

    Google Scholar 

  • Muller C & Leutz A (2001) Chromatin remodeling in development and differentiation. Curr. Opin. Genet. Dev. 11: 167-174

    Google Scholar 

  • Nagl W(1990) Gene amplification and related events. Biotechnol. Agric. For. 11: 153-201

    Google Scholar 

  • Nakao M (2001) Epigenetics: interaction of DNA methylation and chromatin. Gene 278: 25-31

    Google Scholar 

  • Ng H-H & Bird A (1999) DNA methylation and chromatin modification. Curr. Opin. Genet. Dev. 9: 158-163

    Google Scholar 

  • Ng H-H, Zhang Y, Hendrich B & Johnson CA et al. (1999) MBD2 and is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nature Genet. 23: 58-61

    Google Scholar 

  • Okamoto H & Hirochika H (2001) Silencing of transposable elements in plants. Trends Plant Sci. 6: 527-534

    Google Scholar 

  • Picoli EAT, Otoni WC, Figueira ML, Carolino SMB, Almeida RS, Silva EAM, Carvalho CR & Fontes EPB (2001) Hyperhydricity in in vitro eggplant regenerated plants; structural characteristics and involvement of BiP (binding protein). Plant Sci. 160: 857-868

    Google Scholar 

  • Pigliucci M (1998) Developmental phenotypic plasticity: where internal programming meets the external environment. Curr. Opin. Plant Biol. 1: 87-91

    Google Scholar 

  • Piqueras A, Cortina M, Serna MD & Casas JL (2002) Polyamines and hyperhydricity in micropropagated carnation plants. Plant Sci. 00: 1-8

    Google Scholar 

  • Pla M, Huguet G, Verdaguer D, Puigderrajols P, Llompart B, Nadal A & Molinas M (1998) Stress proteins co-expressed in suberized and lignified cells and in apical meristems. Plant Sci. 139: 49-57

    Google Scholar 

  • Posas F, Wurgler-Murphy SM, Maeda T, Witten EA, Thai TC & Saito H (1996)Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 ‘two component’ osmosensor. Cell 86: 865-875

    Google Scholar 

  • Pouteau S, Huttner E, Grandbastien MA & Caboche M (1991) Specific expression of the tobacco Tnt1 retrotransposon in protoplasts. EMBO J. 10: 1911-1918

    Google Scholar 

  • Preece JE & Sutter EG (1991) Acclimatization of microplants to the greenhouse. In: Debergh PC & Zimmerman RH (eds.) Micro-propagation: Technology and Application (pp. 71-91). Kluwer, Dordrecht

    Google Scholar 

  • Rathinasabapathi B (2000) Progress and prospects in genetic engineering for osmoprotectant synthesis. In: Cherry JH, Locy DR & Rychter A (eds.) Plant Tolerance to Abiotic Stress in Agriculture: Role of Genetic Engineering (pp. 139-156). Kluwer, Dordrecht

    Google Scholar 

  • Razin A & Cedar H (1993) DNA methylation and embryogenesis. In: Jost JP & Saluz HP (eds.) DNA Methylation: Molecular and Biological Significance (pp. 343-357). Birkhauser-Verlag, Basel

    Google Scholar 

  • Reddy ASN (2001) Calcium: silver bullet in signaling. Plant Sci.160: 381-404

    Google Scholar 

  • Richards EJ (1997) DNA methylation and plant development. TIG 13: 319-323

    Google Scholar 

  • Romeis T (2001) Protein kinases in the plant defence response. Curr. Opin. Plant Biol. 4: 407-414

    Google Scholar 

  • Roxas VP, Smith RK Jr., Allen ER & Allen RD (1997) Overexpression of glutathione S-transferase / glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nature Biotechnol. 15: 988-991

    Google Scholar 

  • Sharma R (2001) Phytochrome: aserine kinase illuminates the nucleus. Curr. Sci. 80: 178-188

    Google Scholar 

  • Shinozaki K & Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant Biol. 3: 217-223

    Google Scholar 

  • Smulders MJM, Rus-Kortekaas W & Vosman B (1995) Tissue culture induced DNA methylation polymorphisms in repetitive DNA of tomato calli and regenerated plants. TAG 91: 1257-1264

    Google Scholar 

  • Taiz L & Zeiger E (eds.) (2002) Plant Physiology. 3rd edn. Sinauer Associates, Sunderland

  • Telfer A & Poethig RS (1994) Leaf development in Arabidopsis. In: Meyerowitz EM & Somerville CR (eds.) Arabidopsis (pp. 379-401). Cold Spring Harbour Laboratory Press, New York

    Google Scholar 

  • Tena G, Asai T, Chiu W-L & Sheen J (2001) Plant mitogenactivated protein kinase signaling cascades. Curr. Opin. Plant Biol. 4: 392-400

    Google Scholar 

  • Thomashow M (2001) So what's new in the field of plant cold acclimation? Lots! Plant Physiol. 125: 89-93

    Google Scholar 

  • Trass J, Hulskamp, Gendreau E & Hofte H (1998) Endoreduplication and development: rule without dividing. Curr. Biol. 1: 498-503.

    Google Scholar 

  • Van Breusegem F, Vranova E, Dat JF & Inze D (2001) The role of active oxygen species in plant signal transduction. Plant Sci. 161: 405-414

    Google Scholar 

  • Van Camp W, Capiau K, Montagu M, Inze D & Stooten L (1996) Enhancement of oxidative stress tolerance in transgenic tobacco plants overproducing Fesuperoxide dismutase in chloroplasts. Plant Physiol. 112: 1703-1714

    Google Scholar 

  • Voesenek LACJ & Blom CWPM (1999) Stimulated shoot elonga tion: a mechanism of semiaquatic plants to avoid submergence stress. In: Lerner HR (ed) Plant Responses to Environmental Stresses (pp. 431-448). Marcel Dekker, New York

    Google Scholar 

  • Von Aderkas P & Bonga JM (2000) Influencing micropropagation and somatic embryogenesis in mature trees by manipulation of phase change, stress and culture environment. Tree Physiol. 20: 921-928

    Google Scholar 

  • Wade PA, Gegonne A, Jones PL & Ballestar E et al. (1999) Mi2-complex couples DNA methylation to chromatin remodeling and histone deacetylation. Nature Genet. 23: 62-66

    Google Scholar 

  • Walbot V & Cullis CA (1985) Rapid genomic changes in higher plants. Ann. Rev. Plant Physiol. 36: 367-96

    Google Scholar 

  • Wiseman H & Halliwell B (1996) Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem. J. 313: 17-29

    Google Scholar 

  • Wraczek M & Hirt H (2001)Plant MAP kinase pathways: how many and what for? Biol. Cell 93: 81-87

    Google Scholar 

  • Yoder JA & Bestor TH (1996) Genetic analysis of genomic methylation patterns in plants and mammals. Biol. Chem. 377: 605-610

    Google Scholar 

  • Zhu J-K (2001a) Cell signaling under salt, water and cold stresses. Curr. Opin. Plant Biol. 4: 401-406

    Google Scholar 

  • Zhu J-K (2001b) Plant salt tolerance. Trends Plant Sci. 6: 66-71

    Google Scholar 

  • Ziv M (1991) Vitrification: morphological and physiological dis orders of in vitro plants. In: Debergh PC & Zimmerman RH (eds.) Micropropagation: Technology and Application (pp. 47-70). Kluwer, Dordrecht

    Google Scholar 

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Joyce, S.M., Cassells, A.C. & Mohan Jain, S. Stress and aberrant phenotypes in vitro culture. Plant Cell, Tissue and Organ Culture 74, 103–121 (2003). https://doi.org/10.1023/A:1023911927116

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