Skip to main content
SpringerLink
Log in

Hormonal regulation of growth in cultured plant cells

  • Symposia Proceeding
  • Mechanisms of Cellular Control
  • Published:
In Vitro Aims and scope Submit manuscript

Summary

The group of naturally occurring plant hormones known as the cytokinins are defined by their ability to stimulate cell division in mature, differentiated, mitotically inactive cells in tissue culture. Evidence from the literature suggests that cytokinins play a specific role in regulating the progress of a plant cell through its division cycle;. the hormone appears to trigger the transition from G2 to mitosis. However the cytokinins are capable of evoking an array of physiological and developmental responses (many of which do not involve cell division) from different plant tissues and organs. One biochemical effect of the cytokinins is a dramatic and rapid stimulation of polyribosome formation in cultured soybean, cells which require these hormones for growth. Stationary-phase soybean cells, transferred to a medium containing a cytokinin, double in cell number within 36 hr, but when transferred to a medium of the same composition lacking a cytokinin, they do not grow., In vivo labeling with [35S] methionine and slab-gel electrophoresis demonstrated that cytokinin brings about qualitative changes in the spectrum of proteins synthesized by soybean cells which precede hormone-induced cell division. We have shown that cytokinin-induced polyribosome formation is the result of an effect of the hormone on protein synthesis at the translational level. We propose that, in the absence of the hormone, certain genes are transcribed but their messengers are not translated. These include mRNA's for specific cell division proteins. Cytokinins act as permissive factors, allowing cells to complete a genetically programmed sequence of events which was initiated by other factors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. van Overbeek, J., M. E. Conklin, and A. F. Blakeslee. 1941. Factors in coconut milk essential for growth and development ofDatura embryos. Science 94: 350–351.

    Article  Google Scholar 

  2. Caplin, S. M., and F. C. Steward. 1948. Effect of coconut milk on the growth of explants from carrot root. Science 108: 655–657.

    Article  PubMed  Google Scholar 

  3. Henderson, J. H. M., M. E. Durrell, and J. Bonner. 1952. The culture of normal sunflower stem callus. Am. J. Bot. 39: 467–473.

    Article  CAS  Google Scholar 

  4. Steward, F. C., and S. M. Caplin. 1951. A tissue culture from potato tuber: the synergistic action of 2,4-D and coconut milk. Science 113: 518–520.

    Article  PubMed  CAS  Google Scholar 

  5. Shantz, E. M., and F. C. Steward. 1952. Coconut milk factor: the growth promoting substances in coconut milk. J. Am. Chem. Soc. 74: 6133–6135.

    Article  CAS  Google Scholar 

  6. Shantz, E. M., and F. C. Steward. 1955. The identification of compound A from coconut milk as 1,3-diphenylurea. J. Am. Chem. Soc. 77: 6351–6353.

    Article  CAS  Google Scholar 

  7. Miller, C. O., F. Skoog, H. H. von Saltza, F. S. Okumura, and F. H. Strong. 1956. Isolation, structure, and synthesis of kinetin, a substance promoting cell division. J. Am. Chem. Soc. 78: 1175.

    Google Scholar 

  8. Miller, C. O. 1965. Evidence for the natural occurrence of zeatin and derivatives: compounds from maize which promote cell division. Proc. Natl. Acad. Sci. U.S.A. 54: 1052–1058.

    Article  PubMed  CAS  Google Scholar 

  9. Letham, D. S. 1963. Purification of factors inducing cell division extracted from plum fruitlets. Life Sci. 2: 152–157.

    Article  CAS  Google Scholar 

  10. Letham, D. S. 1974. Regulators of cell division in plant tissues. XX. The cytokinins of coconut milk. Physiol. Plant. 32: 66–70.

    Article  CAS  Google Scholar 

  11. Van Staden, J., and S. E. Drewes. 1975. Identification of zeatin and zeatinriboside in coconut milk. Physiol. Plant. 34: 104–109.

    Article  Google Scholar 

  12. Dyson, W. H., and R. H. Hall. 1972. N6-(Δ2-isopentenyl) adenosine: its occurrence as a free nucleoside in an autonomous strain of tobacco tissue. Plant Physiol. 50: 616–621.

    PubMed  CAS  Google Scholar 

  13. Skoog, F., F. M. Strong, and C. O. Miller. 1965. Cytokinins. Science 148: 532.

    Article  PubMed  Google Scholar 

  14. Hall, R. H., L. Csonka, and H. David, and B. McLennon. 1967. Cytokinins in the soluble RNA of plant tissues. Science 156: 69–71.

    Article  PubMed  CAS  Google Scholar 

  15. Kende, H. 1971. The cytokinins Int. Rev. Cytol. 31: 301–338.

    Article  PubMed  CAS  Google Scholar 

  16. Skoog, F., and D. J. Armstrong. 1970. Cytokinins. Annu. Rev. Plant Physiol. 21: 359–384.

    Article  CAS  Google Scholar 

  17. Hall, R. A., 1973. Cytokinins as a probe of developmental processes. Annu. Rev. Plant Physiol. 24: 415–444.

    Article  CAS  Google Scholar 

  18. Short, K. C., and J. G. Torrey. 1972. Cytokinins in seedling roots of pea. Plant Physiol. 49: 155–160.

    PubMed  CAS  Google Scholar 

  19. Phillips, H. L., Jr., and J. G. Torrey. 1971. The quiescent center in cultured roots ofConvolvulus arvensis L. Am. J. Bot. 58: 665–671.

    Article  Google Scholar 

  20. Philips, H. L., Jr., and J. G. Torrey. 1972. Duration of cell cycles in cultured roots of Convolvulus. Am. J. Bot. 59: 183–188.

    Article  Google Scholar 

  21. Kende, H. 1965. Kinetin-like factors in the root exudate of sunflowers. Proc. Natl. Acad. Sci. U.S.A. 53: 1302–1307.

    Article  PubMed  CAS  Google Scholar 

  22. Sitton, D., C. Itai, and H. Kende. 1967. Decreased cytokinin production in the roots as a factor in shoot senescence. Planta 73: 296–300.

    Article  CAS  Google Scholar 

  23. Jordan, W. R., and F. Skoog. 1971. Effects of cytokinin on growth and auxin in coleoptiles of derootedAvena seedlings. Plant Physiol. 48: 97–99.

    PubMed  CAS  Google Scholar 

  24. Nitsch, J. P., and A. Lance-Nougaréde. 1967. L'action conjugee des auxins et des cytokinines sur les cellules de moelle de Tabac: Etude physiologique et microscopic électronique. Bull. Soc. Fr. Physiol. Vég. 13: 81–118.

    CAS  Google Scholar 

  25. Gifford, E. M., Jr., and J. P. Nitsch. 1969. Responses of tobacco pith nuclei to growth substances. Planta 85: 1–10.

    Article  Google Scholar 

  26. Matthysse, A. G., and J. G. Torrey. 1967. DNA synthesis in relation to polyploid mitoses in excised pea root segments culturedin vitro. Exp. Cell Res. 48: 484–498.

    Article  PubMed  CAS  Google Scholar 

  27. Libbenga, K. R., and J. G. Torrey. 1973. Hormone-induced endoreduplication prior to mitosis in cultured pea pod root cortex cells. Am. J. Bot. 60: 293–299.

    Article  CAS  Google Scholar 

  28. Miller, C. O. 1961. A kinetin-like compound in maize. Proc. Natl. Acad. Sci. U.S.A. 47: 170–174.

    Article  PubMed  CAS  Google Scholar 

  29. Fosket, D. E., and J. G. Torrey. 1969. Hormonal control of cell proliferation and xylem differentiation in cultured tissuesGlycine max var. Biloxi. Plant Physiol. 44: 871–880.

    CAS  Google Scholar 

  30. Jouanneau, J. P., and C. Péaud-Lenöel. 1967. Croissance et synthèse des proteines de suspensions cellulaires de Tabac sensibles à la kinetine. Physiol. Plant. 20: 834–850.

    Article  CAS  Google Scholar 

  31. Tandeau de Marsac, N., and J. P. Jouanneau. 1972. Variation de l'exigence en cytokinine de lignées clonales de cellules de Tabac. Physiol. Vég. 10: 369–380.

    CAS  Google Scholar 

  32. Braun, A. C., and H. N. Wood. 1962. On the activation of certain essential biosynthetic systems in the cells ofVinca rosea. Proc. Natl. Acad. Sci. U.S.A. 48: 1776–1782.

    Article  PubMed  CAS  Google Scholar 

  33. Miller, C. O. 1975. Revised methods for purification of ribosyl-trans-zeatin fromVinca rosea L. crown gall tumor tissue. Plant Physiol. 55: 448–449.

    PubMed  CAS  Google Scholar 

  34. Miller, C. O. 1975. Cell-division factors fromVinca rosea L. crown gall tumor tissue. Proc. Natl. Acad. Sci. U.S.A. 72: 1883–1886.

    Article  PubMed  CAS  Google Scholar 

  35. Short, K. C., and J. G. Torrey. 1972. Cytokinin production in relation to the growth of pea-root callus tissue. J. Exp. Bot. 23: 1099–1105.

    Article  CAS  Google Scholar 

  36. Sargent, P. A., and J. King. 1974. Investigations of growth-promoting factors in conditioned soybean root cells in the liquid medium in which they growth: cytokinin-like compounds. Can. J. Bot. 52: 2459–2463.

    CAS  Google Scholar 

  37. Einset, J. W., and F. Skoog. 1973. Biosynthesis of cytokinins in cytokinin-autotrophic tobacco callus. Proc. Natl. Acad. Sci. U.S.A. 70: 658–660.

    Article  PubMed  CAS  Google Scholar 

  38. Das, N. K., K. Patau, and F. Skoog. 1958. Autoradiographic and microspectrophotometric studies of DNA synthesis in excised tobacco pith tissue. Chromosoma 9: 606–617.

    Article  PubMed  CAS  Google Scholar 

  39. Patau, K., and N. K. Das. 1961. The relationship of DNA synthesis and mitosis in tobacco pith tissue culturedin vitro. Chromosoma 11: 553–572.

    Article  PubMed  CAS  Google Scholar 

  40. Simard, A. 1971. Initiation of DNA synthesis by kinetin and experimental factors in tobacco pith tissuein vitro. Can. J. Bot. 49: 1541–1549.

    CAS  Google Scholar 

  41. Fosket, D. E., and K. C. Short. 1973. The role of cytokinin in the regulation of growth, DNA synthesis and cell proliferation in cultured soybean tissues (Glycine max var. Biloxi). Physiol. Plant. 28: 14–23.

    Article  CAS  Google Scholar 

  42. Jouanneau, J. P. 1971. Contrôle par les cytokinines de la synchronisation des mitoses dans les cellules de tabac. Exp. Cell Res. 67: 329–337.

    Article  PubMed  CAS  Google Scholar 

  43. Jouanneau, J. P., and N. Taudeau de Marsac. 1973. Stepwise effects of cytokinin activity and DNA synthesis upon mitotic cycle events in partially synchronized tobacco cells. Exp. Cell Res. 77: 167–174.

    Article  PubMed  CAS  Google Scholar 

  44. Rose, R. J. 1970. The effects of cycloheximide on cell division in partially synchronized plant cells. Aust. J. Biol. Sci. 23: 573–583.

    CAS  Google Scholar 

  45. Webster, P. L., 1973. Effects of cycloheximide on mitosis inVinca faba root-meristem cells. J. Exp. Bot. 24: 239–244.

    Article  CAS  Google Scholar 

  46. Zetterberg, A. 1966. Synthesis and accumulation of nuclear and cytoplasmic proteins during interphase in mouse fibroblastsin vitro. Exp. Cell Res. 42: 500–511.

    Article  PubMed  CAS  Google Scholar 

  47. Stanners, C. P., and H. Becker. 1971. Control of macromolecular synthesis in proliferating and resting Syrian hamster cells in monolayer culture. I. Ribosome function. J. Cell. Physiol. 77: 31–42.

    Article  PubMed  CAS  Google Scholar 

  48. Verma, D. P. S., and A. Marcus. 1974. Activation of protein synthesis upon dilution of anArachis cell culture from stationary phase. Plant Physiol. 53: 83–87.

    PubMed  CAS  Google Scholar 

  49. Rudland, P. S. 1974. Control of translation in cultured cells: continued synthesis and accumulation of messenger RNA in nondividing cultures. Proc. Natl. Acad. Sci. U.S.A. 71: 750–754.

    Article  PubMed  CAS  Google Scholar 

  50. Cella, R., F. Sala, and H. E. Street. 1976. Studies on the growth in culture of plant cells. XIX. Changes in the levels of free and membrane-bound polyribosomes during the growthAcer pseudoplatanus cells in batch suspension culture. J. Exp. Bot. 27: 263–276.

    Article  CAS  Google Scholar 

  51. Jouanneau, J. P. 1970. Renouvellement des proteines et effet specifique de la kinetine sur des cultures de cellules de Tabac. Physiol. Plant. 23: 232–244.

    Article  CAS  Google Scholar 

  52. Trewavas, A., 1972. Control of the protein turnover rates inLemna minor. Plant Physiol. 49: 47–51.

    PubMed  CAS  Google Scholar 

  53. Klambt, D. 1974. Einfluss von auxin und cytokinin auf die RNA-synthese in sterilem tabakgewebe. Planta 118: 7–16.

    Article  Google Scholar 

  54. Klambt, D. 1976. Cytokinin effects on protein synthesis ofin vitro systems of higher plants. Plant Cell Physiol. 17: 73–76.

    Google Scholar 

  55. Hirschberg, K., G. Hubner, and H. Borriss. 1972. Cytokinin-induziertde novo synthese der nitratreductase in embryonen vonAgrostemma githago. Planta 108: 333–337.

    Article  CAS  Google Scholar 

  56. Jouanneau, J. P. 1975. Protein synthesis requirement for the cytokinin effect upon tobacco cell division. Exp. Cell Res. 91: 184–190.

    Article  PubMed  CAS  Google Scholar 

  57. Fosket, D. 1977. Regulation of the plant cell cycle by cytokinin. In: T. R. Rost, and E. L. Gifford (Eds.),Mechanism and Control of Cell Division. Dowden, Hutchinson Ross, New York.

    Google Scholar 

  58. Short, K. C., D. A. Tepfer, and D. E. Fosket. 1974. Regulation of polyribosome formation and cell division in cultured soybean cells by cytokinin. J. Cell Sci. 15: 75–87.

    PubMed  CAS  Google Scholar 

  59. Fosket, D. E., M. J. Volk, and M. Goldsmith. 1977. Polyribosome formation in relation to cytokinin-induced cell division in suspension cultures ofGlycine max. Plant Physiol., in press.

  60. Verma, D. P. S., and A. Marcus. 1974. Oxygen availability as a control factor in the density-dependent regulation of protein synthesis in cell culture. J. Cell Sci. 15: 331–337.

    Google Scholar 

  61. Wollgiehn, R., and B. Parthier. 1964. Der einfluss des kinetins auf den RNS-und protein-stoffwechsel in abgeschnittenen, mit hemmstoffen behandelten tabakblattern. Phytochemistry 3: 241–248.

    Article  CAS  Google Scholar 

  62. Paranjothy, K., and P. F. Wareing 1971. The effects of abscisic acid, kinetin and 5-fluorouracil on ribonucleic acid and protein synthesis in senescing radish leaf discs. Plant. 99: 112–119.

    Article  CAS  Google Scholar 

  63. Zwar, J. A. 1973. Effects of cytokinins on the nucleic acids of tobacco pith. J. Exp. Bot. 24: 701–710.

    Article  CAS  Google Scholar 

  64. Sussex, I., M. Clutter, and V. Walbot. 1975. Benzyladenine reversal of abscisic acid inhibition of growth and RNA synthesis in germinating bean axes. Plant Physiol. 56: 575–578.

    PubMed  CAS  Google Scholar 

  65. Gordon, M. E., D. S. Letham, and J. E. Beever. 1975. Regulation of cell division in plant tissues. XXIV. The effects of cytokinin on ribosome yield from radish cotyledons. Physiol. Plant. 35: 27–35.

    Article  CAS  Google Scholar 

  66. Muren, R. C., and D. E. Fosket. 1977. Cytokinin-mediated translational control of protein synthesis in cultured cells ofGlycine max. J. Exp. Bot., in press.

  67. Payne, E. S., A. Brownrigg, A. Yarwood, and D. Boulter. 1971. Changing protein synthetic machinery during development of seeds ofVicia faba. Phytochemistry 10: 2299–2303.

    Article  CAS  Google Scholar 

  68. Travis, R. L., and J. L. Key. 1971. Correlation between polyribosome level and the ability to induce nitrate reductase in dark-grown corn seedlings. Plant Physiol. 48: 617–620.

    Article  PubMed  CAS  Google Scholar 

  69. Beevers, L., and R. Poulson. 1972. Protein synthesis in cotyledons ofPisum sativum L. I. Changes in cell-free amino acid incorporation capacity during seed development and maturation. Plant Physiol. 49: 476–481.

    PubMed  CAS  Google Scholar 

  70. Tepfer, D. A., and D. E. Fosket. 1977. Hormone-mediated translational control of protein synthesis in cultured cells ofGlycine max. Dev. Biol., in press.

  71. Stanners, C. P. 1966. The effect of cycloheximide on polyribosomes from hamster cells. Biochem. Biophys. Res. Commun. 24: 758–764.

    Article  CAS  Google Scholar 

  72. Fan, H., and S. Penman. 1970. Regulation of protein synthesis in mammalian cells. II. Inhibition of protein synthesis at the level of initiation during mitosis. J. Mol. Biol. 50: 655–670.

    Article  PubMed  CAS  Google Scholar 

  73. Palmiter, R. D. 1972. Regulation of protien synthesis in chick oviduct. II. Modulation of polypeptide elongation and initiation rates by estrogen and progesterone. J. Biol. Chem. 247: 6770.

    PubMed  CAS  Google Scholar 

  74. Crippa, M., and P. R. Gross. 1969. Maternal and embryonic contributions to the functional messenger RNA of early development. Proc. Natl. Acad. Sci. U.S.A. 62: 120–127.

    Article  PubMed  CAS  Google Scholar 

  75. Chen, D., S. Sarid, and E. Katchalski. 1968. Studies on the nature of messenger RNA in germinating wheat embryos. Proc. Natl. Acad. Sci. U.S.A. 60: 902–909.

    Article  PubMed  CAS  Google Scholar 

  76. Weeks, D. P., and A. Marcus. 1971. Preformed messenger of quiescent wheat embryos. Biochim. Biophys. Acta 232: 671–684.

    PubMed  CAS  Google Scholar 

  77. Schultz, G. A., D. Chen, and E. Katchalski. 1972. Localization of a messenger RNA in a ribosomal fraction from ungerminated wheat embryos. J. Mol. Biol. 66: 379–390.

    Article  PubMed  CAS  Google Scholar 

  78. Spiegel, S., and A. Marcus. 1975. Polyribosome formation in early wheat embryo germination independent of either transcription or polyadenylation. Nature 256: 228–230.

    Article  CAS  Google Scholar 

  79. Gordon, M. E., and P. I. Payne. 1976.In vitro translation of the long-lived messenger ribonucleic acid of dry seeds. Planta 130: 269–273.

    Article  CAS  Google Scholar 

  80. Williams, J. G., and S. Penman. 1975. The messenger RNA sequences in growing and resting mouse fibroblasts. Cell 6: 197–206.

    Article  PubMed  CAS  Google Scholar 

  81. Rudland, P. S., S. Weil, and A. R. Hunter. 1975. Changes in RNA metabolism and accumulation of presumptive messenger RNA during transition from the growing to the quiescent state of cultured mouse fibroblasts. J. Mol. Biol. 96: 745–766.

    Article  PubMed  CAS  Google Scholar 

  82. Bandman, E., and T. Gurney, Jr. 1975. Differences in cytoplasmic distribution of newly synthesized poly(A) in serum-stimulated and resting cultures of 3T3 cells. Exp. Cell Res. 90: 159–168.

    Article  PubMed  CAS  Google Scholar 

  83. Lodish, H. F. 1971. Alpha and beta globin messenger ribonucleic acid. Different amounts and rates of initiation of translation. J. Biol. Chem. 246: 7131–7138.

    PubMed  CAS  Google Scholar 

  84. Lodish, H. F. 1974. Model for the regulation of mRNA translation applied to haemoglobin synthesis. Nature 251: 385–388.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Author notes

  1. D. A. Tepfer

    Present address: Molecular Biology Institute, University of California, 90024, Los Angeles, California

Authors and Affiliations

  1. Department of Developmental and Cell Biology, University of California, Irvine, 92717, Irvine, California

    D. E. Fosket & D. A. Tepfer

Authors
  1. D. E. Fosket
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. A. Tepfer
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Research conducted at the University of California, Irvine, was supported by N.S.F. Grant BMS 75-02599 to D.E.F.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fosket, D.E., Tepfer, D.A. Hormonal regulation of growth in cultured plant cells. In Vitro 14, 63–75 (1978). https://doi.org/10.1007/BF02618175

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02618175

Key words

Search

Navigation