Shemin Pathway and Peroxidase Deficiency in a Fully Habituated and Fully Heterotrophic Non-Organogenic Sugarbeet Callus: An Adaptative Strategy or the Consequence of Modified Hormonal Balances and Sensitivities in These Cancerous Cells? A Review an
[en] There are many arguments for considering a specific fully habituated (auxin and cytokinin-independent) and fully heterotrophic non-organogenic (HNO) sugarbeet callus cell line as terminating a neoplastic progression, and thus to be made of cancerous cells. The similarities with animal tumour and cancer cells are recalled. All types of habituated tissues examined in the literature share at least three common biochemical characteristics: low apparent peroxidase activity, high content of polyamines (PAs) and low production of ethylene. However, results concerning their auxin and cytokinin levels are not consistent. Peroxidase synthesis in the achlorophyllous HNO callus appears to arise from aminolevulinic acid (ALA) synthesis through the Shemin pathway, commonly used by animals and fungi. This pathway is limited by disturbed nitrogen metabolism that diverts glutamate (directly used for ALA synthesis in green higher plants) from the Kreb's cycle into PA synthesis. There is no argument to suggest that the low ethylene production is caused by a competition with PAs for their common precursor, S-adenosylmethionine. The results we report here indicate modified anabolic and catabolic pathways of auxins and cytokinins but also the possibilities of unusual compounds playing similar roles (dehydrodiconiferyl alcohol glucosides, for instance). A higher turnover of PAs is shown in the HNO callus, which could suggest a role for H2O2 and gamma-aminobutyric acid, products or intermediates in the PA catabolic pathway, as secondary messengers. The habituated cells retain some sensitivity towards exogenous auxins and cytokinins. Their increased sensitivity to PAs and ethylene suggests modified hormonal balances for the control of these actively dividing cells.
Kevers, Claire ; Université de Liège - ULiège > Département des sciences de la vie > Biologie moléculaire et biotechnologie végétales
Bisbis, Badia; Université de Liège - ULiège > Hormonologie végétale
Penel, Claude; Université de Genève - UNIGE > Physiologie et Biochimie végétales
Greppin, Hubert; Université de Genève - UNIGE > Physiologie et Biochimie Végétales
Garnier, Frédérique; Université de Liège - ULiège > Hormonologie végétale
Rideau, Marc; Université de Tours > Pharmacie > Biologie Cellulaire
Huault, Claude; Université de Caen Basse-Normandie > Physiologie et Biochimie Végétales
Billard, Jean Pierre; Université de Caen Basse-Normandie > Physiologie et Biochimie Végétales
Foidart, Jean-Michel ; Université de Liège - ULiège > Département des sciences cliniques > Gynécologie - Obstétrique - Labo de biologie des tumeurs et du développement
Language :
English
Title :
Shemin Pathway and Peroxidase Deficiency in a Fully Habituated and Fully Heterotrophic Non-Organogenic Sugarbeet Callus: An Adaptative Strategy or the Consequence of Modified Hormonal Balances and Sensitivities in These Cancerous Cells? A Review an
ALBERTS B, BRAY D, LEWIS J, RASS M, ROBERTS K, WATSON J. (1989) Cancer. In: ALBERTS B. BRAY D, LEWIS J, RASS M, ROBERTS K, WATSON J, eds. Molecular Biology of the Cell. New York: Garland; 1187.
APELBAUM A, BURGOON AC, ANDERSON JD, LIEBERMAN M, BEN-ARIE R, MATTOO AK. (1981) Polyamines inhibit biosynthesis of ethylene in higher plant tissue and fruit protoplasts. Plant Physiol. 68, 453.
ATSUMI S, HAYASHI T (1978) The relationship between auxin concentration, auxin protection and auxin destruction in crown gall cells in vitro. Plant Cell Physiol. 19, 1391.
AUDISIO S, BAGNI N, SERAFINI-FRACASSINI D. (1976) Polyamines during the growth in vitro of Nicotiana glauca R. Graph habituated tissue. Z. Pflanzenphysiol. 77, 146.
AUVINEN M, PAASINEN A, ANDERSSON LC, HOLTTA E. (1992) Ornithine decarboxylase activity is critical for cell transformation. Nature 360, 355.
BAGNI N, SERAFINI-FRACASSINI D. (1973) The role of polyamines as growth factors in higher plants and their mechanism of action. In: Plant Growth Substances (Proceedings of the 8th International Conference, Tokyo). Tokyo: Hirokawa Publishers Co; 1205.
BAGNI N, SERAFINI-FRACASSINI D, CORSINI E. (1972) Tumors of Scorzonera hispanica: their content in polyamines. Z. Pflanzenphysiol. 67, 19.
BAJAJ S, RAJAM MV. (1996) Polyamine accumulation and near loss of morphogenesis in long-term callus cultures of rice. Plant Physiol. 112, 1343.
BAKRAN-PETRICIOLI T, KRSNIK-RASOL M. (1989) Protein pattern and peroxidase activity in normal and tumour pumpkin tissues. Biol. Vestn. 37, 3.
BALAGUE C, PECH C. (1985) Relationship between the level of intracellular 2,4-dichlorophenoxyacetic acid in pear cell cultures in vitro. J. Plant Growth Regul. 4, 81.
BAYER MH. (1982) Genetic tumors: physiological aspects of tumor formation in interspecies hybrids. In: KAHL G, SCHELL JS, eds. Molecular Biology of Plant Tumors. New York: Academic Press; 33.
BEDNAR TW, LINSMAIER-BEDNAR EM. (1989) Chemical carcinogenesis in plants and interaction with viruses and cancer causation. In: KAISER HE, ed. Comparative Aspects of Tumor Development. Dordrecht: Kluwer Acad. Publishers; 240.
BERGER RG, DRAWERT F, KINZFOLER A, KUNZ C, RADOLA BJ. (1985) Proteins and peroxidase in callus and suspension cultures of apple. Plant Physiol. 77, 211.
BERNAL MA, BISBIS B, PEDRENO MA, KEVERS C, PENEL C, GASPAR Th. (1997) Peroxidase isoenzymes in normal and habituated calli of sugar beet during their transfer from light to darkness. Biol. Plant. 39, 161.
BHATTACHARYA S, MUKHERJEE BB. (1983) IAA-oxidase activity in different conditions of growth and rooting in jute (Corchorus olitorius) callus. Indian J. Exp. Biol. 21, 347.
BINNS AN, CHEN RH, WOOD HN, LYNN DG. (1987) Cell division promoting activity of naturally occurring dehydrodiconiferyl glucosides: do cell wall components control cell division? Proc. Natl. Acad. Sci. USA 84, 980.
BIONDI S, HAGÈGE D, ROSSINI P, BAGNI N. (1993) Polyamine metabolism and ethylene biosynthesis in normal and habituated sugar beet callus. Physiol. Plant. 89, 699.
BISBIS B. (1998) Auxin, ethylene and polyamines interactions in a normal and habituated sugarbeet calli. Bull. Soc. Roy. Sc. Liege 67, 213.
BISBIS B, DUJARDIN E, KEVERS C, HAGÈGE D, GASPAR Th. (1994) Chlorophylls and carotenoids in a fully habituated nonorganogenic callus of Beta vulgaris. Biol. Plant. 36, 443.
BISBIS B, DE RIEK J, KEVERS C, GASPAR Th. (1995) Sucrose metabolism and CO2 uptake by chlorophyllous and non-chlorophyllous sugarbeet calli. Bull. Rech. Agron. Gembloux 30, 113.
BISBIS B, KEVERS C, CRÈCHE J, RIDEAU M, GASPAR Th. (1998a) Differential growth dependency of normal and habituated sugarbeet cell lines upon endogenous ethylene production and exogenous ethylene application. Physiol. Plant. 103, 201.
BISBIS B, KEVERS C, GASPAR, Th. (1997a) Atypical TCA cycle and replenishment in a non-photosynthetic fully habituated sugarbeet callus overproducing polyamines. Plant Physiol. Biochem. 35, 363.
BISBIS B, KEVERS C, HUAULT C, BILLARD JP, GASPAR Th. (1997b) Erythromycin as a tool to investigate the tetrapyrrole biosynthetic pathways in habituated and normal sugarbeet calli. Plant Growth Regul. 23, 147.
BISBIS B, KEVERS C, PENEL C, GREPPIN H, GASPAR Th. (1997c) Coexistence of the Beale and Shemin pathways for the biosynthesis of tetrapyrrole-containing compounds, including peroxidases, in a normal sugarbeet callus. Plant Peroxidase Newsletter 9, 13.
BISBIS B, KEVERS C, PENEL C, GREPPIN H, GASPAR Th. (1998b) Biosynthesis of tetrapyrrole-containing compounds, including peroxidases, in a non-chlorophyllous fully habituated sugarbeet callus via the unique shemin pathway. Plant Peroxidase Newsletter 11, 19.
BISHOP JM. (1987) The molecular genetics of cancer. Science 235, 305.
BLACK RC, BINNS AN, LYNN DG, CHANG CF. (1993) Cytokinin autonomous growth in tobacco tissues transformed by Agrobacterium tumefaciens lacking the cytokinin synthesizing gene. Plant Physiol. 102 (Suppl.), 61.
BLEECKER AB, SCHALLER GE. (1996) The mechanism of ethylene perception. Plant Physiol. 111, 653.
BOLTON WE, FREEBAIRN HT. (1975) Effect of naphthaleneacetic acid and ethylene on growth and physiology of habituated tobacco tissue cultures. Phyton (Buenos Aires) 33, 165.
BOUCHET M, GASPAR Th, THORPE TA. (1978) Soluble and cell-wall peroxidases and auxin destruction in normal and habituated tobacco callus. In Vitro 14, 819.
BOUILLENNE C, GASPAR Th. (1970) Auxin catabolism and inhibitors in normal and crown gall tissues of Impatiens balsamina. Canad. J. Bot. 48, 1159.
Bourgeade P, Boyer N, de Jaegher G, Gaspar Th. (1989) Carry-over of thigmomorphogenetic characteristics in calli derived from Bryonia dioica internodes. Plant Cell Tissue Organ Cult. 19, 199.
CAMPELL BR, SU LY, PENGELLY WL. (1992) Auxin autonomy in cultured tobacco teratoma tissues transformed by an auxin-mutant strain of Agrobacterium tumefaciens. Planta 188, 123.
CAMPELL BR, TOWN CD. (1991) physiology of hormone autonomous tissue lines derived from radiation-induced tumors of Arabidopsis thaliana. Plant Physiol. 97, 1166.
CARRIÉ B, HAGÈGE D, KEVERS C, GEUNS J., GASPAR Th. (1992) Auxin-induced growth enhancement of a sugarbeet callus while reducing ethylene production and polyamine content. Comptes Rendus Acad. Sci. Paris 315, 165.
CHAWLA HS. (1991) Regeneration potentiality and isozymic variations during morphogenesis of barley callus. Biol. Plant. 33, 175.
CHEN KH. (1987) Analysis of indole-3-acetic acid in tobacco genetic tumours and wheat GA3-insensitive mutant 'Tom Thumb'. Phd Thesis. College Park. MD, USA: University of of Maryland.
CHRISTOU P. (1987) Habituation in in vitro soybean cultures. Plant Physiol. 88, 809.
CRÈVECOEUR M, HAGÈGE D, CATESSON AM, GREPPIN H, GASPAR Th. (1992) Ultrastructural characteristics of cells from normal and habituated sugar beet calli. Plant Physiol. Biochem. 30, 87.
CRÈVECOEUR M, KEVERS C, GREPPIN H, GASPAR Th. (1987) A comparative biochemical and cytological characterization of normal and habituated sugarbeet calli. Biol. Plant. 29, 1.
DEL DUCA S, SERAFINI-FRACASSINI D. (1993) Polyamines and protein modification during the cell cycle. In: ORMROD JC, FRANCIS D, eds. Molecular and Cell Biology of the Plant Cell Cycle. Dordrecht: Kluwer Academic Publishers; 143.
DEL GROSO E, ALICCHIO R. (1981) Analysis in isozymatic patterns of Solanum melongena: differences between organized and unorganized tissues. Z. Pflanzenphysiol. 102, 467.
DOONAN J, HUNT T. (1996) Why don't plants get cancer? Nature 380, 481.
DU PLESSIS S, STIRK WA, CRESS WA, VAN STADEN J. (1996) Biochemical comparisons of habituated and non-habituated callus lines of Glycine max (L.) cv. Acne. Plant Growth Regul. 18, 223.
DYSON WH, HALL RH. (1972) N6-(Δ2-isopentenyl) adenine: its occurrence as a free nucleoside in an autonomous strain of tobacco tissue. Plant Physiol. 50, 616.
EINSET JW, SKOOG F. (1973) Biosynthesis of cytokinins in cytokinin-autotrophic tobacco callus. Proc. Natl. Acad. Sci. USA 70, 658.
EL-BAHR MK, KUTACEK M, OPATRNY Z. (1987) l-tryptophan aminotransferase and l-tryptophan dehydrogenase, enzymes of IAA synthesis, in normal and tumorous tobacco tissue cultures. Biochem. Physiol. Pflanzen, 182, 213.
ENGELMANN I, MACHEIX JJ, GASPAR Th. (1993) Phenolic compounds in hormone-dependent and independent sugarbeet callus lines compared to donor-plants. Saussurea 24, 15.
EVEN-CHEN Z, MATTOO AK, GOREN R. (1982) Inhibition of ethylene biosynthesis by aminoethoxyvinylglycine and polyamines shunts label from 3,4[14C]-methionine into spermidine in aged orange peel discs. Plant Physiol. 69, 385.
EVERETT NP. (1981) 2,4-D-independent cell cultures of sycamore (Acer pseudoplatanus L.): isolation, responses to 2,4-D and kinetin, and sensitivities to antimetabolites. J. Exp. Bot. 32, 171.
EVERSE J, EVERSE KE, GRISHAM MB. (1991) Peroxidases in Chemistry and Biology, Vol. II. Boca Raton: CRC Press.
FEUTRY S, PODER D, HAGÈGE D. (1995) Enhancement of diacylglycerol level and inositol phosphates turnover in a fully habituated sugar beet cell line. Plant Physiol. Biochem. 33, 115.
FLOH E, HANDRO W, MORGANTE JS. (1989) Isozymic patterns of peroxidase and IAA-oxidase in cultured tissues of tobacco plants of different ploidy. Rev. Bras. Biol. 49, 627.
GAAL I, KÖVES E. (1981) Biosynthesis indole-3-acetic acid tobacco callus cultures. Bot. Közlem. (Budapest) 86, 221.
GASPAR Th. (1995) The concept of cancer in in vitro plant cultures and the implication of habituation to hormones and hyperhydricity. Plant Tissue Culture Biotechnol. 1, 126.
GASPAR Th (1998) Plants can get cancer. Plant Physiol. Biochem. 36, 203.
GASPAR Th, KEVERS C, PENEL C, GREPPIN H. (1983) Auxin control of calcium-mediated peroxidase secretion by auxin-dependent and auxin-independent sugarbeet cells. Phytochemistry 22, 2657.
GASPAR Th, HAGÈGE D, KEVERS C et at. (1991) When plant teratomas turn into cancers in the absence of pathogens. Physiol. Plant. 83, 696.
GASPAR Th, HAGÈGE D, PENEL C, FOIDART JM, GREPPIN H. (1992a) Peroxidases and plant cancer in the absence of pathogens. In: PENEL C, GASPAR Th, GREPPIN H, ed. Plant Peroxidases 198090. Topics and Detailed Literature on Molecular, Biochemical, and Physiological Aspects. Switzerland: University of de Genève; 125.
GASPAR Th, KEVERS C, BOUILLENNE H, MAZIÈRE Y, BARBE JP. (1989) Ethylene production in relation to rose micropropagation. In: CLUSTERS H, DE PROFT M, MARCELLE R, VAN POUCKE M, eds. Biochemical and Physiological Aspects of Ethylene Production in Lower and Higher Plants. Dordrecht: Kluwer Acad. Publishers; 303.
GASPAR Th, KEVERS C, BISBIS B et al. (1995) Cancer végétal in vitro: aspects morphogénétiques et biochimiques. In: DUBOIS J, DEMARLY Y, eds. Quel Avenir Pour l'Amélioration Des Plantes. Paris: John Libbey Eurotext; 165.
GASPAR Th, KEVERS C, CRÈVECOEUR M, PENEL C, FOIDART JM, GREPPIN H. (1992b) Habituation and vitrification of plants cultured in vitro: a reciprocal relationship. Wiss. Zeitschr. Humboldt-University Berlin, Mathem./Naturwiss. 41, 35.
GASPAR Th, KEVERS C, HAUSMAN JF et al. (1996a) Peroxidase as an indissociable factor of auxin and polyamine metabolisms in the induction of rooting and flowering. In: OBINGER C, BURNER U, EBERMANN R, PENEL C, GREPPIN H, eds. Plant Peroxidases: Biochemistry and Physiology. Switzerland: University of de Genève; 226234.
GASPAR Th, KEVERS C, PENEL C, CRÈVECOEUR M, GREPPIN H. (1988) Biochemical characterization of normal and habituated sugarbeet calli. Relationship with anatomy, habituation and organogenesis. Potsdamer Forschungen B 57, 20.
GASPAR Th, KEVERS C, PENEL C, GREPPIN H, REID D, THORPE TA (1996b) Plant hormones and plant growth regulators in plant tissue cultures. In Vitro Cell. Dev. Biol. Plant 32, 272.
GASPAR Th, PENEL C, GREPPIN H. (1997) Do rooting induction and flowering evocation involve a similar interplay between indoleacetic acid, putrescine and peroxidases?. In: GREPPIN H, PENEL C, SIMON P, eds. Travelling Shot on Plant Development. Switzerland: University of de Genève; 111.
GASPAR Th, PENEL C, GREPPIN H, FOIDART JM. (1994) Plant cancer at the cell and organismic level, in the absence of pathogens, and the resulting loss of organogenic totipotency. Saussurea 25, 63.
GASPAR Th, PENEL C, THORPE T, GREPPIN H. (1982) Peroxidases 197080. A Survey of Their Biochemical and Physiological Roles in Higher Plants. Switzerland: University of de Genève.
GREPPIN H, PENEL C, GASPAR Th. (1986). Molecular and Physiological Aspects of Plant Peroxidases. Switzerland: University of de Genève; 468.
HAGÈGE D, KEVERS C, CRÈVECOEUR M, TOLLIER MT, MONTIES B, GASPAR Th. (1991a) Peroxidases, growth and differentiation of habituated sugarbeet cells. In: LOBARSZEWSKI J, GREPPIN H, PENEL C, GASPAR Th, eds. Molecular and Physiological Aspects of Plant Peroxidases. Switzerland: University of de Genève; 281.
HAGÈGE D, KEVERS C, GASPAR Th. (1991b) A comparison between ethylene production, ACC and mACC contents, and hydroperoxide level in normal and habituated sugarbeet calli. Physiol. Plant. 82, 397.
HAGÈGE D, KEVERS C, GASPAR T, THORPE TA. (1991c) Abnormal growth of habituated sugarbeet calli and cell suspensions. In Vitro Cell. Dev. Biol. 27, 112.
HAGÈGE D, KEVERS C, LE DILY F, GASPAR T, BOUCAUD J. (1990) NaCl dependent growth rate of normal and habituated calli, ethylene production and peroxidase activity. Comptes Rendus Acad. Sc. Paris. Sér. III 310, 259.
HAGÈGE D, PENEL C, CRÈVECOEUR M, KEVERS C, GASPAR Th, BOUCAUD J, GREPPIN H. (1991d) Plasmamembrane peroxidases from the auxin- and cytokinin-independent sugarbeet callus. Arch. Intern. Physiol. Biochim. Biophys. 99, 2.
HAGÈGE D, WERCK-REICHHART D, SCHMITT P, GASPAR Th. (1992) Deficiency in tetrapyrrole-containing compounds in a non-organogenic habituated sugarbeet cell line. Plant Physiol. Biochem. 30, 649.
HANSEN CE, MEINS FJ, MILANI A. (1985) Clonal and physiological variation in the cytokinin content of tobacco cell lines differing in cytokinin requirement and capacity for neoplastic growth. Differentiation 29, 1.
HERVAGAULT JF, ORTOLEVA PJ, ROSS J. (1991) A plausible model for reversal of neoplastic transformations in plants based on multiple steady states. Proc. Natl. Acad. Sci. USA 88, 10787.
HIRSCH AM, FORTUNE D. (1984) Peroxidase activity and isoperoxidase composition in cultured stem tissue, callus and cell suspensions of. Actinidia Chinensis, Z. Pflanzenphysiol. 113, 129.
HRIB J, VOOKOVA B, KORMUTAK A. (1997) Biochemical differences between normal callus and embryogenic suspensor mass of silver fir. Biol. Plant. 39, 507.
HUXTER TJ, REID DM, THORPE TA. (1979) Ethylene production by tobacco (Nicotiana tabacum) callus. Physiol. Plant. 46, 374.
HUXTER TJ, THORPE TA, REID DM. (1981) Shoot initiation in light and dark grown tobacco callus: the role of ethylene. Physiol. Plant. 53, 319.
JACKSON JA, LYNDON RF. (1990) Habituation: cultural curiosity or developmental determinant? Physiol. Plant. 79, 579.
KAISER HE. (1989) Neoplasic dissemination and spreading from the view point of comparative pathology: differences and similarities between animals and plants. In: Kaiser HE, ed. Comparative Aspects of Tumor Development. Dordrecht: Kluwer Academic Publishers; 1.
KAMINEK M, HADACKOVA V, LUSTINEC J. (1981) Plastids and the origin of cytokinin autonomy in tobacco tissue cultures. In: GUERN J. PÉAUD-LE NOËL C, eds. Metabolism and Molecular Activities of Cytokinins. Berlin: Springer-Verlag; 242.
KEPCZYNSKI J, MCKERSIE BD, BROWN DCW. (1992) Requirement of ethylene for growth of callus and embryogenesis in Medicago sativa L. J. Exp. Bot. 43, 1199.
KEVERS C, BISBIS B, FAIVRE-RAMPANT O, GASPAR Th. (1999) Putrescine metabolism in a fully habituated nonorganogenic sugarbeet callus and its relationship with growth. J. Plant Physiol. 154, 503.
KEVERS C, BISBIS B, FRANCK T, LE DILY F, HUAULT C. (1997a) On the possible causes of polyamine accumulation in in vitro plant tissues under neoplasic progression. In: Greppin H, Penel C, Simon P, eds. Travelling Shot on Plant Development. Switzerland: University of de Genève; 63.
Kevers C, Bisbis B, Le Dily F, Billard JP, Huault C, Gaspar Th. (1995) Darkness improves growth and delays necrosis in a non-chlorophyllous habituated sugarbeet callus. Biochemical changes. In Vitro Cell. Dev. Biol. 31, 122.
KEVERS G, BOYER N, COURDUROUX JC, GASPAR Th. (1992a) The influence of ethylene on proliferation and growth of rose shoot cultures. Plant Cell Tissue Organ Cult. 28, 175.
KEVERS C, COUMANS M, COUMANS-GILLès MF, GASPAR Th. (1984) Physiological and biochemical events leading to vitrification of plants cultured in vitro. Physiol. Plant. 61, 69.
KEVERS C, COUMANS M, DE GREEF W, HOFINGER M, GASPAR Th. (1981) Habituation in sugarbeet callus: auxin content, auxin protectors, peroxidase pattern and inhibitors. Physiol. Plant. 51, 281.
Kevers C, Filali M, Petit-Paly G, Hagège D, Rideau M, Gaspar Th. (1996) Habituation of plant cells does not mean insensitivity to plant growth regulators. In Vitro Cell. Dev. Biol. Plant 32, 204.
KEVERS C, GOLDBERG R, VANDEN DRIESSHE Th, GASPAR Th. (1992b) A relationship between ascorbate peroxidase activity and the conversion of 1-aminocyclopropane-1-carboxylic acid into ethylene. J. Plant Physiol. 139, 379.
KEVERS C, GREPPIN H, PENEL C, GASPAR Th. (1985) Short- and long-lerm effects of auxins on ethylene production by auxin-dependent and auxin-independent sugarbeet cell lines. Arch. Intern. Physiol. Bioch. 93, B39.
KEVERS C, MOTYKA V, KAMINEK M, GASPAR Th. (1997b) Cytokinin content and its relation to cytokinin oxidase in normal and habituated sugar beet tissues. Arch. Physiol. Bioch. 105, 9.
KEVERS C, STICHER L, PENEL C, GREPPIN H, GASPAR Th. (1982) Calcium-controlled peroxidase secretion by sugarbeet cell suspensions in relation to habituation. Plant Growth Regul. 1, 61.
KEVERS C, STICHER L, PENEL C, GREPPIN H, GASPAR Th. (1983) The effect of ergosterol, ergocalciferol and cholecalciferol on calcium-controlled peroxidase secretion by sugarbeet cells. Physiol. Plant. 57, 17.
KONSTANTINOVA TN, AKSENOVA NP, SERGEEVA LI. (1982) Study of peroxidase in photoperiodically neutral tobacco during the process of its generative development. Fiziol. Rast. 29, 639.
KÒVES E, SZABÒ M. (1987) Ethylene production in habituated and auxin requiring tobacco callus cultures. Does ethylene play a role in the habituation?. Physiol. Plant. 69, 351.
KOVACS EI, MALIGA P. (1973) Indoleacetic acid oxidase regulation in genetically tumorous and normal tobacco plants and in their tissue cultures. Acta Bot. Acad. Sci. Hung. 18, 315.
KRSNIK-RASOL M. (1991) Peroxidase as a developmental marker in plant tissue culture. Int. J. Dev. Biol. 35, 259-263.
KRSNIK-RASOL M, JELASKA S. (1991) Peroxidases in relation to differentiation and tumour transformation in plants. In: LOBARSZEWSKI J, GREPPIN H, PENEL C, GASPAR Th, eds. Molecular and Physiological Aspects of Plant Peroxidases. Switzerland: University of de Genève, 373.
KRSNIK-RASOL M, JELASKA S, SERMAN D. (1982) Isoperoxidases-early indicators of Somatic embryoid differentiation in pumpkin tissue. Acta Bot. Croat. 41, 33.
KULESCHA Z. (1952) Recherches sur l'élaboration de substances de croissance par les tissus végétaux. Rev. Gén. Bol. 59, 19.
KULESCHA Z, GAUTHERET R. (1948) Sur l'élaboration de substances de croissance par trois types de cultures de tissus de Scorsonère: cultures normales, cultures de crown-gall et cultures accoutumées à l'hétéro-auxine. Comptes Rendus Acad. Sci. Paris 227, 292.
KULPA GM, GALSKY AG, LIPETZ P, STEPHENS R. (1985) Polyamines and crown gall tumour growth. Plant Cell Report 4, 81.
KUTACEK M, EDER J, OPATRNY Z et al. (1981) Comparison of anthranilate synthase activity and IAA content in normal and auxin-habituated Dioscorea deltoidea. Biochem. Physiol. Pflanzen 176, 244.
LAGRIMINI LM, ROTHSTEIN S. (1987) Tissue-specificity of tobacco peroxidase isozymes and their induction by wounding and tobacco mosaic virus infection. Plant Physiol. 84, 438.
LAMBÉ P, NKUNG MUTAMBEL HS, FOUCHÉ JG, DELTOUR R, FOIDART JM, 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.
LE DILY F, HUAULT C, GASPAR Th, BILLARD JP. (1993a) 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.
LE DILY F, KEVERS C, HUAULT C, BILLARD JP, GASPAR Th. (1993b). Peroxidase deficiency in plant cancer cells as resulting from deviated nitrogen and sugar metabolisms? In: WELINDER KG, RASMUSSEN SK, PENEL C, GREPPIN H, eds. Proceedings Third International. Symposium: Plant Peroxidases: Biochemistry and Physiology. Switzerland: University of de Genève; 335.
LESCURE AM. (1970) Cinétique enzymatique des 3-indolylacétique oxydases de deux lignées de cellules d'Acer pseudoplatanus L. dépendante ou indépendante de l'auxine. Bull. Soc. Chim. Biol. 52, 953.
LIEBERMAN M, WANG SY, OWEN LD. (1979) Ethylene production by callus and suspension cells from cortex tissue of postclimacteric apples. Plant. Physiol. 63, 811.
LIPETZ J, GALSTON AW. (1959) Indole acetic acid oxidase and peroxidase in normal and crown-gall tissue cultures of Parthenocissus Tricuspidata. Am. J. Bot. 46, 193.
MAILLARD F, PILET PE, ZRYD JP. (1976) Auxin dependence and auxin oxidase of cultured sycamore cells. Experientia 32, 841.
MARTIN-LOUÇAO MA, RODRIGUEZ-BARRUECO C. (1983) Ethylene production by carob (Ceratonia siliqua) callus cultures on varing media. Physiol. Plant. 58, 204.
MCCANN PP, PEGG AE, SJOERDSMA A. (1987). Inhibition of Polyamine Metabolism: Biological Significance and Basis for New Therapies. San Diego: Academic Press; 371.
MEINS F. (1973) Evidence for the presence of a really transmissible oncogenic principle in crown-gall teratoma cells of tobacco. Differentiation 1, 21.
MEINS F. (1989) Habituation: heritable variation in the requirement of cultured plant cells for hormones. Annu. Rev. Genet. 23, 395.
MENSUALI SODI A, PANIZZA M, TOGNONI F. (1989) Studies on lavandin callus cultures: ethylene production in relation to growth. Biol. Plant. 31, 247.
MÉRILLON JM, FILALI M, DUPÉRON P, MONTAGU M, CHÈNIEUX JC, RIDEAU M. (1995) Effect of 2,4-dichlorophenoxyacetic acid and habituation on lipid and protein composition of microsomal membranes from periwinkle cell suspensions. Plant Physiol. Biochem. 33, 443.
MÉRILLON JM, OUELHAZI L, DOIREAU P, CHÉNIEUX JC, RIDEAU M. (1989) Metabolic changes and alkaloid production in habituated and non-habituated cells of Catharanthus roseus grown in hormone-free medium: comparing hormone-deprived non-habituated cells with habituated cells. J. Plant Physiol. 134, 54.
MIURA GA, MILLER CO. (1969) Cytokinins from a variant strain of cultured soybean cells. Plant Physiol. 44, 1035.
MOK MC, MOK DW, ARMSTRONG DJ, RABAKOARIHANTA A, KIM SG. (1980) Cytokinin autonomy in tissue cultures of Phaseolus: a genotype-specific and heritable trait. Genetics 94, 675.
MOUSDALE DMA, FIDGEON C, WILSON G. (1985) Auxin content and growth patterns in auxin-dependent and auxin-autotrophic plant cell and tissue cultures. Biol. Plant. 27, 257.
NAKAJIMA H, YOKOTA T, MATSUMOTOT, NOGUCHI M, TAKAHASHI N. (1979) Relationship between hormone content and autonomy in various autonomous tobacco cells cultured in suspension. Plant Cell Physiol. 29, 1489.
Nandi SK, Palni LMS, Parker CW. (1990) Dynamics of endogenous cytokinins during the growth cycle of a hormone-autotrophic genetic tumor line of tobacco. Plant Physiol. 94, 1084.
NEGRUTIU M, JACOBS M, GASPAR Th. (1979) Leaf formation and peroxidases from Arabidopsis callus. Z. Pflanzenphysiol. 91, 119.
NISHIOKA K. (1996). Polyamines in Cancer. Basic Mechanisms and Clinical Approaches. Houston: University of Texas.
NORDSTRÖM AC, ELIASSON L. (1991) Levels of endogenous indole-3-acetic acid and indole-acetylaspartic acid during adventitious root formation in pea cuttings. Physiol. Plant. 82, 599.
NORMANLY J, COHEN JD, FINK GR. (1993) Arabidopsis thaliana auxotrophs reveal a tryptophan-independent biosynthetic pathway for indole-3-acetic acid. Proc. Natl. Acad. Sci. USA 90, 10355.
OETIKER JH, AESCHBACHER G. (1997) Temperature-sensitive plant cells with shunted indole-3-acetic acid conjugation. Plant Physiol. 114, 1385.
PEDRENO M, FERRER MA, GASPAR Th, MUNOZ R, 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 Newsletter 5, 3.
PENEL C. (1997) Production and roles of hydrogen peroxide. In: Greppin H, Penel C, Simon P, eds. Travelling Shot on Plant Development. Switzerland: University of de Genève; 219-238.
PENEL C, STICHER L, KEVER C, GASPAR Th, GREPPIN H. (1984) Calcium-controlled peroxidase secretion by sugarbeet cells: effect of ionophores in relation to organogenesis. Biochem. Physiol. Pflanzen 179, 173.
PENEL C, GASPAR Th, GREPPIN H. (1992) Plant Peroxidases 198090. Topics and Detailed Literature on Molecular, Biochemical, and Physiological Aspects. Switzerland: University of de Genève; 481.
PENGELLY WL (1989) Neoplasic progression in plants. In: Kaiser HE, ed. Comparative Aspects of Tumor Development. Dordrecht: Kluwer Academic Publishers; 15.
PENGELLY WL, MEINS F. (1982) The relationship of indole-3-acetic acid content and growth of crown-gall tumour tissues of tobacco in culture. Differentiation 21, 27.
PENGELLY WL, MEINS F. (1983) Growth, auxin requirement, and indole-3-acetic acid content of cultured crown-gall and habituated tissues of tobacco. Differentiation 25, 101.
PENNEY GC, HAWKINS RA. (1981) Comparison between biochemical and histochemical assessments of peroxidase activity in rat mammary tumours. Histochem. J. 13, 983.
PETERS W, FÜCHTBAUER B, BECK E. (1995) Nitrate reductase activity is endogenously induced by zeatin riboside in habituated suspension cultured Chenopodium rubrum cells. J. Plant Physiol. 147, 401.
PHAN CT. (1983) Relation entre la structure anatomique et le métabolisme des tissus végétaux. III. Etude de l'activité et de la composition sous-unitaire de quelques enzymes dans les explants, les milieux et les cals de pommes, en culture. In Vitro, Rev. Can. Biol. Exp. 42, 19.
PHANG JM. (1985) The regulatory functions of proline and pyrroline-5-carboxylic acid. Curr. Top. Cell. Regul. 25, 91.
PLATT RS. (1954) The inactivation of auxin in normal and tumorous tissues. Ann. Biol. 30, 349.
PORCIANI S, BECCIOLINI A, LANINI A et al. (1993) Polyamines and proliferative activity in tumour tissues. Cell Prolifer. 26, 490.
RAMPUTH AI, BROWN AW. (1996) Rapid γ-aminobutyric acid synthesis and the inhibition of the growth and development of oblique-banded leaf-roller larvae. Plant Physiol. 111, 1349.
RUSSEL DH. (1973) Polyamines in Normal and Neoplastic Growth. New York: Raven Press.
SCOTT IM, HORGAN R. (1984) Mass-spectrometric quantification of cytokinin nucleotides and glycosides in tobacco crown gall tissue. Planta 161, 345.
SEILER N, MOULINOUX J. (1996) Les polyamines présentent-elles un intérêt dans le traitement du cancer?. Médecine/Sciences 12, 745.
SERAFINI-FRACASSINI D, BAGNI N, TORRIGIANI P. (1980) Nicotiana glauca Nicotiana langsdorffii tumor hybrid: growth, morphology, polyamines and nucleic acids in vitro. Canad. J. Bot. 58, 2285.
SLOVIN JP. (1997). Phytotoxic conjugates of indole-3-acetic acid: potential agents for biochemical selection of mutants in conjugate hydrolysis. Plant Growth Regul. 21, 215.
STONIER T. (1970) The role of auxin protectors in autonomous growth. In: Colloques Internationaux, les Cultures de Tissus de Plantes. Strasbourg: CNRS; 423.
SYONO K. (1979) Correlation between induction of auxin-nonrequiring tobacco calluses and increase in inhibitor(s) of IAA-destruction activity. Plant Cell Physiol. 20, 29.
SYONO K, FURUYA T. (1974) Induction of auxin-non-requiring tobacco calluses and its reversal by treatment with auxins. Plant Cell Physiol. 15, 7.
SZABÒ M, KÖVES E, SOMOGYI I. (1994) Development of auxin autotrophy in Nicotiana tabacum callus cultures. Physiol. Plant. 90, 348.
SZABÒ MS, TARI I, KÖVES E. (1981) Indole acetic acid oxidase activity in heterotrophic and autotrophic (habituated) tobacco callus tissues. Biochem. Physiol. Pflanzen. 176, 691.
TACCHINI R, FINK A, XUE GX, GASPAR Th, GREPPIN H. (1995) Analysis of proteins of a fully habituated nonorganogenic sugarbeet callus and a hormone-dependent one by high performance 2-D gel electrophoresis. Plant Physiol. Biochem. 33, 361.
TANDON P, ARYA HC. (1980) Auxin autotrophy and hyperauxinity of Eriophyes induced Zizyphus stem galls in culture. Biochem. Physiol. Pflanzen 175, 537.
TEUTONICO RA, DUDLEY MW, ORR JD, LYNN DG, BINNS AN. (1991) Activity and accumulation of cell division-promoting phenolics in tobacco tissue cultures. Plant Physiol. 97, 288.
TEYSSENDIER DE LA SERVE B, JOUANNEAU JP, PÉAUD-LENOëL C. (1982) Covalent link of the N6-(Δ2-isopentenyl) adenine nucleotide to the rRNA of cytokinin-requiring and of cytokinin-autonomous tobacco cells. J. Plant Growth Regul. 1, 25.
VAIN P, FLAMENT P, SOUDAIN P. (1989) Role of ethylene in embryogenic callus initiation and regeneration in Zea mays L. J. Plant Physiol. 135, 537.
WEISS JS. (1967) Auxin inactivation by normal and derived tobacco tissue cultures. Adv. Front. Plant Sci. 18, 155.
WEILER EW. (1981) Dynamics of endogenous growth regulators during the growth cycle of a hormone-autotrophic plant cell culture. Naturwiss. 67, 377.
WHITE PR, BRAUN AC. (1942) A cancerous neoplasm of plants. Cancer Res. 2, 597.
WOOD HN, BRAUN AC, Brandes H, Kende H. (1969) Studies on the distribution and properties of a new class of cell division-promoting substances from higher plant species. Proc. Natl. Acad. Sci. USA 62, 349.
WRIGHT AD, SAMPSON MB, NEUFFER MG, MICHALCZUK L, SLOVIN JP, COHEN JD. (1991) Indole-3-acetic acid biosynthesis in the mutant maize orange pericarp', a tryptophan auxotroph. Science 254, 998.
WYNDAELE R, CHRISTIAENSEN J, HOORSEELE R, RÜDELSHEIM P, VAN ONCKELEN H. (1988) Functional correlation between endogenous phytohormone levels and hormone autotrophy of transformed and habituated soybean cell lines. Plant Cell Physiol. 29, 1095.
YAHIA A, KEVERS C, GASPAR Th, CHÉNIEUX JC, RIDEAU M, CRÈCHE J. (1998) Cytokinins and ethylene stimulate indole alkaloid accumulation in cell suspension cultures of Catharanthus roseus by two distinct mechanisms. Plant Sci. 133, 9.
