Habituation of plant cells does not mean insensitivity to plant growth regulators

  • C. Kevers
  • M. Filali
  • G. Petit-Paly
  • D. Hagège
  • M. Rideau
  • Th. Gaspar
Physiology
Received:
Accepted:

Summary

Fully habituated organogenic and nonorganogenic sugarbeet calluses reacted to application of the synthetic auxin [3-benzo(b) selenienyl] acetic acid by changes in growth and ethylene production. Treatment of fully habituated cells of periwinkle with 2,4-dichlorophenoxyacetic acid led to the decrease of free cytokinin contents (isopentenyl adenine, zeatin riboside, and zeatin) during the late exponential phase of growth. The polyamine contents were also modified and the capacity to biotransform secologanin into ajmalicine was decreased. Treatment of the habituated periwinkle cells with zeatin greatly increased the amount of a polypeptide of 16 kDa; this response was more marked than that displayed by the auxin-dependent line. These data show that hormone-independent calluses and cell suspensions can retain some sensitivity to growth hormones. However, differences of responses were observed between the auxin-dependent lines and the habituated lines.

Key words

Beta vulgaris Catharanthus roseus ethylene habituation periwinkle plant growth regulators polyamines proteins sugarbeet 2D-PAGE 
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References

  1. Binns, A. N.; Roman, G.; Teutonico, R. A. Accumulation of dehydrodiconiferyl alcohol glucoside in cytokinin habituated cell lines. In: Kaminek, M.; Mok, D. W. S.; Zazimalova, E., eds. Physiology and biochemistry of cytokinins in plants. The Hague: SPB Academic Publishing; 1992:59–64.Google Scholar
  2. Bishop, J. M. The molecular genetics of cancer. Science 235:305–311; 1987.PubMedCrossRefGoogle Scholar
  3. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254; 1976.PubMedCrossRefGoogle Scholar
  4. Braun, A. C.; Morel, G. A comparison of normal, habituated and crown-gall tumor tissue implants in the European grape. Am. J. Bot. 37:499–505; 1950.CrossRefGoogle Scholar
  5. Butcher, D. N. Plant tumour cells. In: Street, H. E., ed. Plant tissue and cell culture. Oxford, England: Blackwell Scientific Publications; 19977 429–461.Google Scholar
  6. Butcher, D. N. Plant tumour cells. In: Street, H. E., ed. Plant tissue and cell culture. Oxford, England: Blackwell Scientific Publications; 1977: 429–461.Google Scholar
  7. Campell, B. R.; Town, C. D. Physiology of hormone autonomous tissue lines derived from radiation-induced tumours ofArabidopsis thaliana. Plant Physiol. 97:1166–1173; 1991.PubMedCrossRefGoogle Scholar
  8. Carrié, B.; Hagège, D.; Kevers, C., et al. Auxin-induced growth enhancement of a sugarbeet callus while reducing ethylene production and polyamine. Paris, France: C. R. Acad. Sci. 315:165–170; 1992.Google Scholar
  9. Chen, K. H. Analysis of indole-3-acetic acid in tobacco genetic tumours and wheat GA3-insensitive mutant “Toru Thumb.” 1987. PhD Thesis, Univ. of Maryland, College Park, MD.Google Scholar
  10. Christou, P. Habituation inin vitro soybean cultures. Plant Physiol. 88:809–812; 1987.Google Scholar
  11. Crèvecoeur, M.; Hagège, D.; Catesson, A. M., et al. Ultrastructural characteristics of cells from normal and habituated sugar beet calli. Plant Physiol. Biochem. 30:87–95; 1992.Google Scholar
  12. Décendit, A.; Liu, D.; Ouelhazi, L., et al. Cytokinin-enhanced accumulation of indole alkaloids inCatharanthus roseus cell cultures. The factors affecting the cytokinin response. Plant Cell Rep. 11:400–403; 1992.CrossRefGoogle Scholar
  13. Everett, N. P. 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. 32:171–182; 1981.CrossRefGoogle Scholar
  14. Gamborg, O. L.; Miller, R. A.; Ojima, K. Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell Res. 50:151–158; 1968.PubMedCrossRefGoogle Scholar
  15. Gaspar, Th. Seleniated forms of indolylacetic acid: new powerful synthetic auxins. Acros Organics Acta. 1:65–66; 1995.Google Scholar
  16. Gaspar, Th.; Hagège, D.; Kevers, et al. When plant teratomas turn into cancers in the absence of pathogens. Physiol. Plant. 83:696–701; 1991.CrossRefGoogle Scholar
  17. Gaspar, Th.; Kevers, C.; Bisbis, B., et al. Cancer végétalin vitro: aspects morphogénétiques et biochimiques. In: Dubois, J.; Demarly, Y., eds. Quel avenir pour l'amélioration des plantes. Paris, France: John Libbey Eurotext; 1995:165–171.Google Scholar
  18. Gaspar, Th.; Kevers, C.; Penel, C., et al. Auxin control of calcium-mediated peroxidase secretion by auxin-dependent and auxin-independent sugarbeet cells. Phytochemistry 22:2657–2660; 1983.CrossRefGoogle Scholar
  19. Gaspar, Th.; Kevers, C.; Penel, C., et al. Biochemical characterization of normal and habituated sugarbeet calli: relationship with anatomy, habituation and organogenesis. Potsdamer Forschungen B57:20–30; 1988.Google Scholar
  20. Gautheret, R. J. Hétéro-auxines et cultures de tissus végétaux. Bull. Soc. Chim. Biol. 24:13–41; 1942.Google Scholar
  21. Gautheret, R. J. Sur la variabilité de propriétés physiologiques des cultures de tissus végétaux. Rev. Gén. Bot. 62:1–106; 1955.Google Scholar
  22. Hagège, D. Etude comparative du cal normal et du cal habitué deBeta vulgaris L.altissima: aspects cytologiques, ultrastructuraux et biochimiques. Relations avec l'état tumoral. 1990. Thèse Doct. Univ. of Caen. Caen, France.Google Scholar
  23. Hagège, D. Proto-oncogenes in plants: widespread conserved genes for which roles? Plant Physiol. Biochem. 31:621–629; 1993.Google Scholar
  24. Hagège, D.; Catania, R.; Micalef, H., et al. Nuclear shape and DNA content of fully habituated nonorganogenic sugarbeet cells. Protoplasma 166:49–54; 1992a.CrossRefGoogle Scholar
  25. Hagège, D.; Kevers, C.; Boucaud, J., et al. Polyamines, phospholipids, and peroxides in normal and habituated sugarbeet calli. J. Plant Physiol. 136:641–645; 1990a.Google Scholar
  26. Hagège, D.; Kevers, C.; Gaspar, Th., et al. A comparison between ethylene production, ACC and mACC contents, and hydroperoxyde level in normal and habituated sugarbeet calli. Physiol. Plant. 82:397–400; 1991.CrossRefGoogle Scholar
  27. Hagège, D.; Kevers, C.; Le Dily, et al. NaCl dependent growth rate of normal and habituated calli, ethylene production and peroxidase activity. Paris, France: C. R. Acad. Sci. 310:259–264; 1990b.Google Scholar
  28. Hagège, D.; Werck-Reichart, D.; Schmitt, P., et al. Deficiency in tetrapyrrole-containing compounds in a non-organogenic habituated sugarbeet cell line. Plant Physiol. Biochem. 30:649–654; 1992b.Google Scholar
  29. Hansen, C. E.; Meins, F., Jr.; Aebi, R. Hormonal regulation of zeatin riboside accumulation by cultured tobacco cells. Planta 172:520–525; 1987.CrossRefGoogle Scholar
  30. Hervagault, J. F.; Ortoleva, P. J.; Ross, J., et al. Reversal of the crown-gall tumor: an interpretation based on multiple steady state. Proc. Natl. Acad. Sci. USA 88:10797–10800; 1991.PubMedCrossRefGoogle Scholar
  31. Ikeda, M.; Ojima, M.; Oshira, K., et al. Habituation in suspension-cultured soybean cells to thiamine and its precursors. Plant Cell Physiol. 20:733–739; 1979.Google Scholar
  32. Jackson, J. A.; Lyndon, R. F. Habituation: cultural curiosity or developmental determinant? Physiol. Plant. 79:579–583; 1990.CrossRefGoogle Scholar
  33. Jemmali, A.; Boxus, P.; Kevers, C., et al. Carry over of morphological and biochemical characteristics associated to hyperflowering of micropropagated strawberries. J. Plant Physiol. 147:435–440; 1995.Google Scholar
  34. Kevers, C. Control by 2,4-D of auxin protectors in sugar-beet callus. Arch. Intern. Physiol. 20:733–739; 1981.Google Scholar
  35. Kevers, C.; Coumans, M.; De Greef, W., et al. Habituation in sugarbeet callus: auxin content, auxin protectors, peroxidase pattern and inhibitors. Physiol. Plant. 51:281–286; 1981.CrossRefGoogle Scholar
  36. Kevers, C.; Greppin, H.; Penel, C., et al. Short- and long-term effects of auxins on ethylene production by auxin-dependent and auxin-independent sugarbeet cell lines. Arch. Intern. Physiol. Biochem. 93: B39-B40; 1985.Google Scholar
  37. Kevers, C.; Sticher, L.; Penel, C., et al. Calcium-controlled peroxidase secretion by sugarbeet cell suspensions in relation to habituation. Plant Growth Regul. 1:61–66; 1982.CrossRefGoogle Scholar
  38. Kulescha, Z. Recherches sur l'élaboration de substances de croissance par les tissus végétaux. Rev. Gén. Bot. 59:19–41; 1952.Google Scholar
  39. Kulescha, Z.; Gautheret, R. Sur l'élaboration de substances de croissance par 3 types de cultures de tissus de Scorzonère: cultures normales, cultures de crowngall et cultures accountumées à l'hétéro-auxine. Paris, France: C. R. Acad. Sci. 227:292–294; 1948.Google Scholar
  40. Kutacek, M.; Eeder, J.; Opatrny, Z., et al. Comparison of anthranilate synthase activity and IAA content in normal and auxin-habituatedDioscorea deltoida tissue cultures. Biochem. Physiol. Pflanz. 176:244–250; 1981.Google Scholar
  41. Le Dily, F.; Billard, J. P.; Gaspar, Th., et al. Disturbed nitrogen metabolism associated with the hyperhydric status of sugarbeet. Physiol. Plant. 88:129–134; 1993.CrossRefGoogle Scholar
  42. Mayer, J. E.; Hahne, G.; Palme, K., et al. A simple and general plant tissue extraction procedure for two-dimensional gel electrophoresis. Plant Cell Rep. 6:77–81; 1987.CrossRefGoogle Scholar
  43. Meins, F., Jr. Habituation of cultured plant cells. In: Kahl, G.; Schell, J. S., eds. Molecular biology of plant tumors. London: Academic Press; 1982:3–31.Google Scholar
  44. Meins, F., Jr. Habituation: heritable variation in the requirement of cultured plant cells for hormones. Annu. Rev. Genet. 23:395–408; 1989.PubMedCrossRefGoogle Scholar
  45. Mérillon, J. M.; Dupéron, P.; Montagu, M., et al. Modulation by cytokinin of membrane lipids inCatharanthus roseus cells. Plant Physiol. Biochem. 1:749–755; 1993.Google Scholar
  46. Mérillon, J. M.; Filali, M.; Dupéron, P., et al. Effect of 2,4-dichlorophenoxyacetic acid and habituation on lipid and protein composition of microsomal membranes from periwinkle cell suspensions. Plant Physiol. Biochem. 33:443–451; 1995a.Google Scholar
  47. Mérillon, J. M.; Huguet, F.; Fauconneau, B., et al. Specific binding of verapamil to microsomal membranes ofCatharanthus roseus cell suspensions. J. Plant Physiol. 146:279–282; 1995b.Google Scholar
  48. Mérillon, J. M.; Ouelhazi, L.; Doireau, P., et al. Metabolic changes and alkaloid production in habituated and non-habituated cells ofCatharanthur roseus grown in hormone-free medium: comparing hormone-deprived non-habituated cells with habituated cells. J. Plant Physiol. 134:54–60; 1989.Google Scholar
  49. Mérillon, J. M.; Ramawat, K.; Andreu, F., et al. Accumulation alcaloïdique dans des lignées cellulaires deCatharanthus roseus entretenues en présence ou en l'absence de phytohormones. Paris, France: C. R. Acad. Sci. 303:689–692; 1986.Google Scholar
  50. Mousdale, D. M. A.; Fidgeon, C.; Wilson, G., et al. Auxin content and growth patterns in auxin-dependent and auxin-autotrophic plant cell and tissue cultures. Biol. Plant. 27:257–264; 1985.Google Scholar
  51. Nakajima, H.; Yokota, T.; Matsumoto, T., et al. Relationship between hormone content and autonomy in various autonomous tobacco cells cultured in suspension. Plant Cell Physiol. 29:1489–1499; 1979.Google Scholar
  52. Nanney, D. L. Epigenetic control systems. Proc. Natl. Acad. Sci. USA 44:712–717; 1958.PubMedCrossRefGoogle Scholar
  53. Oakley, B. R.; Kirsch, D. R.; Norris, N. R., et al. A simplified ultra-sensitive silver stain for detecting proteins in polyacrylamide gel. Anal. Biochem. 105:361–363; 1980.PubMedCrossRefGoogle Scholar
  54. Ouelhazi, L.; Filali, M.; Décendit, A., et al. Differential protein accumulation in zeatin-and 2,4-D-treated cells ofCatharanthus roseus. Correlation with indole alkaloid biosynthesis. Plant Physiol. Biochem. 31:421–431; 1993.Google Scholar
  55. Pengelly, W. L.; Meins, F., Jr. The relationship of indole-3-acetic content and growth of crown-gall tumour tissues of tobacco in culture. Differentiation 21:27–31; 1982.PubMedCrossRefGoogle Scholar
  56. Persinger, S. M.; Town, C. D. Isolation and characterization of hormone-autonomous tumours ofArabidopsis thaliana. J. Exp. Bot. 42:1363–1370; 1991.CrossRefGoogle Scholar
  57. Ramagli, L.; Rodriguez, L. V. Quantitation of microgram amounts of proteins in two-dimensional polyacrylamide gel electrophoresis sample buffer. Electrophoresis 6:559–563; 1985.CrossRefGoogle Scholar
  58. Ramawat, K. G.; Viel, C.; Chénieux, J. C., et al. Quaternary alkaloid production inRuta graveolens: suspension culture and habituation of some strains. Indian J. Exp. Biol. 25:471–475; 1987.Google Scholar
  59. Saunders, J. W.; Daub, M. E. Shoot regeneration from hormone-autonomous callus from shoot cultures of several sugarbeet (Beta vulgaris L.) genotypes. Plant Sci. Lett. 34:219–233; 1984.CrossRefGoogle Scholar
  60. Smith, H. H. Plant genetic tumours. Prog. Exp. Tumor Res. 15:138–164; 1972.PubMedGoogle Scholar
  61. Street, H. E. Growth in organized and unorganized systems: knowledge gained by culture of organs and tissue explants. In: Steward, F. C., ed. Plant physiology. Vol. 5B. New York: Academic Press; 1969:223–224.Google Scholar
  62. Syono, K.; Fujita, T., Habituation as a tumorous state that is interchangeable with a normal state in plant cells. Int. Rev. Cytol. 152:265–299; 1994.Google Scholar
  63. Syono, K.; Furuya, T. Introduction of auxin-nonrequiring tobacco calluses and its reversal by treatments with auxins. Plant Cell Physiol. 15:7–17; 1974.Google Scholar
  64. Szabò, M.; Köves, E.; Somogyi, I., et al. Development of auxin autotrophy inNicotiana tabacum callus cultures. Physiol. Plant. 90:348–352; 1994.CrossRefGoogle Scholar
  65. Vankova, R.; Gaudinova, A.; Kamineck, M., et al. The effect of interaction of synthetic cytokinin and auxin on production of natural cytokinins by immobilized tobacco cells. In: Kaminek, M.; Mok, D. W. S.; Zazimalova, E., eds. Physiology and biochemistry of cytokinins in plants. The Hague: SPB Academic Publishing; 1992:395–400.Google Scholar
  66. Walters, H. J. P.; Geuns, J. M. C. High speed HPLC analysis of polyamines in plant tissues. Plant Physiol. 83:232–234; 1987.Google Scholar
  67. White, P. R. Neoplastic growth in plants. Q. Rev. Biol. 26:1–16; 1951.PubMedCrossRefGoogle Scholar

Copyright information

© Society for In Vitro Biology 1996

Authors and Affiliations

  • C. Kevers
    • 1
  • M. Filali
    • 2
  • G. Petit-Paly
    • 2
  • D. Hagège
    • 3
  • M. Rideau
    • 2
  • Th. Gaspar
    • 1
  1. 1.Hormonologie fondamentale et appliquée, Institut de Botanique B-22Université de LiègeLiègeBelgium
  2. 2.Laboratoire de Biologie Cellulaire et Biochimie Végétale EA 1370Université de Tours, Faculté de PharmacieToursFrance
  3. 3.Laboratoire de Biochimie et Physiologie VégétaleUniversité de Bretagne OccidentaleBrestFrance

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