Review the formation of adventitious roots: New concepts, new possibilities

  • Geert-Jan de Klerk
  • Wim van der Krieken
  • Joke C. de Jong
Developmental Biology/Morphogenesis


Considerable progress has recently been made in understanding adventitious root formation using physiological studies. It is recognized that rooting is a process consisting of distinct phases, each with its own requirements. In this review, the successive phases in the rooting process are described and the possible roles of wounding-related compounds, auxin, ethylene and phenolic compounds during these specific phases are discussed. Recent results are assisting the development of advanced rooting treatments. Molecular studies on rooting are underway and will be essential in revealing the mechanisms underlying adventitious root formation.

Key words

adventitious rooting auxin cell cycle activation ethylene non-auxin factors phenolics rooting phases wounding-related compounds 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Attfield, E. M.; Evans, P. K. Stages in the initiation of root and shoot organogenesis in cultured leaf explants of Nicotiana tabacum cv. Xanthi nc. J. Exp. Bot. 42:59–63; 1991.CrossRefGoogle Scholar
  2. Blazkova, A.; Sotta, B.; Tranvan, H.; Maldiney, R.; Bonnet, M.; Einhorn, J.; Kerhoas, L.; Miginiac, E. Auxin metabolism and rooting in young and mature clones of Sequoia sempervirens. Physiol. Plant. 99:73–80; 1997.CrossRefGoogle Scholar
  3. Bollmark, M.; Kubat, B.; Eliasson, L. Variation in endogenous cytokinin content during adventitious root formation in pea cuttings. J. Plant Physiol. 132:262–265; 1988.Google Scholar
  4. Burritt, D. J.; Leung, D. W. M. Organogenesis in cultured petiole explants of Begonia x erythrophylla: the timing and specificity of the inductive stimuli. J. Exp. Bot. 47:557–567; 1996.CrossRefGoogle Scholar
  5. Christianson, M. L.; Warnick, D. A. Competence and determination in the process of in vitro shoot organogenesis. Dev. Biol. 95:288–293; 1983.PubMedCrossRefGoogle Scholar
  6. Croes, A. F.; Wullems, G. J. Hormonal induction of regeneration: how to open the black box? Adv. Hortic. Sci. 8:37–42; 1994.Google Scholar
  7. Curir, P.; Van Sumere, C. F.; Termini, A.; Barthe, P.; Marchesini, A.; Dolci, M. Flavonoid accumulation is correlated with adventitious root formation in Eucalyptus gunnii Hook micropropagated through axillary bud stimulation. Plant Physiol. 92:1148–1153; 1990.PubMedGoogle Scholar
  8. De Klerk, G. J. Hormone requirements during the successive phases of rooting of Malus microcuttings. In: Terzi, M.; Cella, R.; Falavigna, A., ed. Current issues in plant cellular and molecular biology. Dordrecht, The Netherlands: Kluwer Academic Publishers; 1995:111–116.Google Scholar
  9. De Klerk, G. J. Markers of adventitious root formation. Agronomie 16:563–571; 1996.Google Scholar
  10. De Klerk, G. J.; Ter Brugge, J.; Smulders, R.; Benschop, M. Basic peroxidases and rooting in microcuttings of Malus. Acta Hortic. 280:29–36; 1990.Google Scholar
  11. De Klerk, G. J.; Keppel, M.; Ter Brugge, J.; Meekes, H. Timing of the phases in adventitious root formation in apple microcuttings. J. Exp. Bot. 46:965–972; 1995.CrossRefGoogle Scholar
  12. De Klerk, G. J.; Ter Brugge, J.; Marinova, S. Effectiveness of indoleacetic acid, indolebutyric acid and naphthaleneacetic acid during adventitious root formation in vitro in Malus ‘Jork 9’. Plant Cell Tissue Organ Cult. 49:39–44; 1997a.CrossRefGoogle Scholar
  13. De Klerk, G. J.; Arnholdt-Schmitt, B.; Lieberei, R.; Neumann, K. H. Regeneration of roots, shoots and embryos: physiological, biochemical and molecular aspects. Biol. Plant. 39:53–66; 1997b.CrossRefGoogle Scholar
  14. De Klerk, G. J.; Marinova, S.; Rouf, S.; Ter Brugge, J. Salicylic acid affects rooting of apple microcuttings by enhancement of oxidation of auxin. Acta Hortic.; 1998. (in press).Google Scholar
  15. De Klerk, G. J.; Paffen, A.; Jasik, J.; Haralampieva, V. A dual effect of ethylene during rooting of apple microcuttings. In: Altman, A.; Ziv, M., ed. Proceedings of the Congress on Plant Biotechnology and In Vitro Biology in the 21st Century. Dordrecht, The Netherlands: Kluwer Academic Publishers. (In press).Google Scholar
  16. Delbarre, A.; Muller, P.; Imhoff, V.; Guern, J. Comparison of mechanisms controlling uptake and accumulation of 2,4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta 198:532–541; 1996.CrossRefGoogle Scholar
  17. De Wit, L.; Liu, J.-H.; Reid, D. M. Production of ethylene by gravistimulation; a potential problem with the interpretation of data from some experimental techniques. Plant Cell Environ. 13:237–242; 1990.CrossRefGoogle Scholar
  18. Diaz-Sala, C.; Hutchison, K. W.; Goldfarb, W.; Greenwood, M. S. Maturation-related loss in rooting competence by loblolly pine stem cuttings: the role of auxin transport, metabolism and tissue sensitivity. Physiol. Plant. 97:481–490; 1996.CrossRefGoogle Scholar
  19. Doerner, P.; Jørgensen, J.-E.; You, R.; Steppuhn, J.; Lamb, C. Control of root growth and development by cyclin expression. Nature (Lond.) 380:520–523; 1996.CrossRefGoogle Scholar
  20. Dominov, J. A.; Stenzler, L.; Lee, S.; Schwarz, J. J.; Leisner, S.; Howell, S. H. Cytokinins and auxins control the expression of a gene in Nicotiana plumbagnifolia cells by feedback regulation. Plant Cell 4:451–461; 1992.PubMedCrossRefGoogle Scholar
  21. Epstein, E.; Ludwig-Müller, J. Indole-3-butyric acid in plants: occurrence, synthesis, metabolism and transport. Physiol. Plant. 88:382–389; 1993.CrossRefGoogle Scholar
  22. Finstad, K.; Brown, D. W.; Joy, K. Characterization of competence during induction of somatic embryogenesis in alfalfa tissue culture. Plant Cell Tissue Organ Cult. 34:125–132; 1993.CrossRefGoogle Scholar
  23. Gorst, J. R.; Slaytor, M.; De Fossard, R. A. The effect of indole-3-butyric acid and riboflavin on the morphogenesis of adventitious roots of Eucalyptus ficifolia F. Muell. grown in vitro. J. Exp. Bot. 34:1503–1515; 1983.CrossRefGoogle Scholar
  24. Grace, N. H. Physiologic curve of response to phytohormones by seeds, growing plants, cuttings and lower plant forms. Can. J. Res. C 15:538–546; 1937.Google Scholar
  25. Guan, H.; Huisman, P.; De Klerk, G. J. Rooting of apple stem slices in vitro is affected by rapid decline of indoleacetic acid in the medium. J. Appl. Bot. 71:80–84; 1997.Google Scholar
  26. Hackett, W. P.; Lund, S. T.; Smith, A. G. The use of mutants to understand competence for shoot-borne root initiation. In: Altman, A.; Waisel, Y., ed. Biology of root formation and development. New York and London: Plenum Publishing Corp.; 1997:169–174.Google Scholar
  27. Haissig, B. E.; Davis, T. D. A historical evaluation of adventitious rooting research to 1993. In: Davis, T. D.; Haissig, B. E., ed. Biology of adventitious root formation. New York and London: Plenum Publishing Corp.; 1994:275–331.Google Scholar
  28. Hartmann, H. T.; Kester, D. E.; Davies, F. T. Plant propagation: principles and practices. Englewood Cliffs, NJ: Prentice Hall; 1990.Google Scholar
  29. Hemerly, A. S.; Ferreira, P.; De Almeira Engler, J.; Van Montagu, M.; Engler, G.; Inzé, D. cdc2a expression in Arabidopsis thaliana is linked with competence for cell division. Plant Cell 5:1711–1723; 1993.PubMedCrossRefGoogle Scholar
  30. Hitchcock, A. E.; Zimmerman, P. W. Effect of the use of growth substances on the rooting response of cuttings. Contrib. Boyce Thompson Inst. 8:63–79; 1936.Google Scholar
  31. Howard, A.; Pelc, S. R. Synthesis of deoxyribonucleic acid in normal and irradiated cells and its relation to chromosome breakage. Heredity (Suppl.) 6:216–273; 1953.Google Scholar
  32. Jackson, M. B. Ethylene and responses of plants to soil waterlogging and submergence. Annu. Rev. Plant Physiol. 36:146–174; 1985.CrossRefGoogle Scholar
  33. Jacobs, T. W. Cell cycle control. Annu. Rev. Plant Physiol. 46:317–339; 1995.CrossRefGoogle Scholar
  34. James, D. J.; Thurbon, I. J. Phenolic compounds and other factors controlling rhizogenesis in vitro in the apple rootstocks M.9 and M.26. Z. Pflanzenphysiol. 105:11–20; 1981.Google Scholar
  35. Jasik, J.; De Klerk, G. J. Anatomical and ultrastructural examination of adventitious root formation in stem slices of apple. Biol. Plant. 39:79–90; 1997.CrossRefGoogle Scholar
  36. Jönsson, Å. Chemical structure and growth activity of auxins and antiauxins. In: Ruhland, W., ed. Encyclopedia of plant physiology. Vol. IVX. Berlin, Gottingen, Heidelberg: Springer-Verlag; 1961:959–1006.Google Scholar
  37. Kenney, G.; Sudi, J.; Blackman, G. E. The uptake of growth substances XIII. Differential uptake of indole-3yl-acetic acid through the epidermal and cut surfaces of etiolated stem segments. J. Exp. Bot. 20:820–840; 1969.CrossRefGoogle Scholar
  38. Kevers, C.; Hausman, J. F.; Faivre-Rampant, O.; Evers, D.; Gaspar, T. Hormonal control of adventitious rooting: progress and questions. J. Appl. Bot. 71:71–79; 1997.Google Scholar
  39. Kling, G. J.; Meyer, M. M. Effects of phenolic compounds and indoleacetic acid on adventitious root initiation in cuttings of Phaseolus aureus, Acer saccharinum, and Acer griseum. HortScience 18:352–354; 1983.Google Scholar
  40. Libbenga, K. R.; Mennes, A. M. Hormone binding and signal transduction, In: Davies, P. J., ed. Plant hormones. Dordrecht, The Netherlands: Kluwer Academic Publishers; 1995:272–297.Google Scholar
  41. Liu, J. H.; Reid, D. M. Adventitious rooting in hypocotyls of sunflower (Helianthus annuus) seedlings. IV. The role of changes in endogenous free and conjugated indole-3-acetic acid. Physiol. Plant. 86:285–292; 1992a.CrossRefGoogle Scholar
  42. Liu, J. H.; Reid, D. M. Auxin and ethylene-stimulated adventitious rooting in relation to tissue sensitivity to auxin and ethylene production in sunflower hypocotyls. J. Exp. Bot. 43:1191–1198; 1992b.CrossRefGoogle Scholar
  43. Lyon, G. D.; Reglinski, T.; Newton, C. Novel disease control compounds: the potential to “immunize” plants against infection. Plant Pathol. 44:407–427; 1995.CrossRefGoogle Scholar
  44. Meyer, E. M.; Morgan, P. W.; Yang, S. F. Ethylene. In: Wilkins, M. B., ed. Advanced plant physiology. London: Pitman Publishing Ltd.; 1984:111–126.Google Scholar
  45. Milborrow, B. V. Inhibitors. In: Wilkins, M. B., ed. Advanced plant physiology. London: Pitman Publishing Ltd.; 1984:76–110.Google Scholar
  46. Mitsuhashi, M.; Shibaoka, H.; Shimokoriyama, M. Morphological and physiological characterization of IAA-less-sensitive and IAA-sensitive phases in rooting of Azukia cuttings. Plant Cell Physiol. 10:867–874; 1969.Google Scholar
  47. Mudge, K. W. Effect of ethylene on rooting. In: Davis, T. D.; Haissig, B. E.; Sankhla, N., ed. Adventitious root formation by cuttings. Portland: Dioscorides Press; 1988:150–161.Google Scholar
  48. Nordström, A. C.; Eliasson, L. Levels of endogenous indole-3-acetic acid and indole-3-acetylaspartic acid during adventitious root formation in pea cuttings. Physiol. Plant 82:599–605; 1991.CrossRefGoogle Scholar
  49. Nordström, A. C.; Jacobs, A. C.; Eliasson, L. Effect of exogenous indole-3-acetic acid and indole-3-butyric acid on the internal levels of the respective auxins and their conjugation with aspartic acid during adventitious root formation in pea cuttings. Plant Physiol. 96:856–861; 1991.PubMedCrossRefGoogle Scholar
  50. Quinto, C.; Wijfjes, A. H. M.; Bloemberg, G. V.; Blok-Tip, L.; LoApez-Lara, I. M.; Lugtenberg, B. J. J.; Thomas-Oates, J. E.; Spaink, H. P. Bacterial nodulation protein NodZ is a chitin oligosaccharide fucosyltransferase which can also recognize related substrates of animal origin. Proc. Natl. Acad. Sci. USA 94:4336–4341; 1997.PubMedCrossRefGoogle Scholar
  51. Rubery, P. H.; Sheldrake, A. R. Effect of pH and surface charge on cell uptake of auxin. Nat. New Biol. 244:285–288; 1973.PubMedGoogle Scholar
  52. Smith, D. L.; Fedoroff, N. V. LRP1, a gene expressed in lateral and adventitious root primordia of Arabidopsis. Plant Cell 7:735–745; 1995.PubMedCrossRefGoogle Scholar
  53. Smith, D. R.; Thorpe, T. A. Root initiation in cuttings of Pinus radiata seedlings. II. Growth regulator interactions. J. Exp. Bot. 26:193–202; 1975.CrossRefGoogle Scholar
  54. Smulders, M. J. M.; Van de Ven, E. T. W. M.; Croes, A. F.; Wullems, G. J. Metabolism of 1-naphthaleneacetic acid in explants of tobacco: evidence for release of free hormone from conjugates. J. Plant Growth Regul. 9:27–34; 1990.CrossRefGoogle Scholar
  55. Suttle, J. Effect of ethylene treatment on polar IAA transport, net IAA uptake and specific binding of N-1-naphthylphthalamic acid in tissues and microsomes isolated from etioated pea epicotyls. Plant Physiol. 88:795–799; 1988.PubMedGoogle Scholar
  56. Thimann, K. V. Auxins and the growth of roots. Am. J. Bot. 23:561–569; 1936.CrossRefGoogle Scholar
  57. Thimann, K. V.; Went, F. W. On the chemical nature of the rootforming hormone. Proc. K. Ned. Akad. Wet. Ser. C Biol. Med. Sci. 37:456–459; 1934.Google Scholar
  58. Ueda, J. Promotive effect of capillarol and related compounds on root growth. Physiol. Plant. 76:42–46; 1989.CrossRefGoogle Scholar
  59. Van der Krieken, W. M.; Breteler, H.; Visser, M. H. M. Uptake and metabolism of indolebutyric acid during root formation of Malus microcuttings. Acta Bot. Neerl. 41:435–442; 1992.Google Scholar
  60. Van der Krieken, W. M.; Breteler, H.; Visser, M. H. M.; Mavridou, D. The role of the conversion of IBA into IAA on root regeneration in apple: introduction of a test system. Plant Cell Rep. 12:203–206; 1993.CrossRefGoogle Scholar
  61. Van der Krieken, W. M.; Kodde, J.; Visser, M. H. M.; Tsardakas, D.; Blaakmeer, A.; De Groot, K.; Leegstra, L. Increased induction of adventitious rooting by slow release auxins and elicitors. In: Altman, A.; Waisel, Y., ed. Biology of root formation and development. New York and London: Plenum Publishing Corp.; 1997:95–105.Google Scholar
  62. Van der Lek, H. A. A. Over eenige toepasingen van ‘groeistoffen’ in de practijk van de plantenteelt. Vakbl. Biol. 22:29–35; 1941 (in Dutch).Google Scholar
  63. Visser, E. J. W.; Cohen, J. D.; Barendse, G. W. M.; Blom, C. W. P. M.; Voesenek, L. A. C. J. An ethylene-mediated increase in sensitivity to auxin induces adventitious root formation in flooded Rumex palustris Sm. Plant Physiol. 112:1687–1692; 1996.Google Scholar
  64. Vieitez, A. M.; Sánchez, C.; San-José, S. Prevention of shoot-tip necrosis in shoot cultures of chestnut and oak. Soi. Hortic. (Canterb.) 41:151–159; 1989.CrossRefGoogle Scholar
  65. Went, F. W. The dual effect of auxin on root formation. Am. J. Bot. 26:24–29; 1939.CrossRefGoogle Scholar
  66. Zhou, J.; Wu, H.; Collet, G. F. Histological study of initiation and development in vitro of adventitious roots in minicuttings of apple rootstocks of M26 and EMLA9. Physiol. Plant. 84:433–440; 1992.CrossRefGoogle Scholar
  67. Zimmerman, W.; Crocker, W.; Hitchcock, A. E. Initiation and stimulation of roots from exposure of plants to carbon monoxide gas. Contrib. Boyce Thompson Inst. 5:1–17; 1933.Google Scholar
  68. Zimmerman, W.; Wilcoxon, F. Several chemical growth substances which cause initiation of roots and other responses in plants. Contrib. Boyce Thompson Inst. 7:209–217; 1935.Google Scholar

Copyright information

© Society for In Vitro Biology 1999

Authors and Affiliations

  • Geert-Jan de Klerk
    • 1
  • Wim van der Krieken
    • 2
  • Joke C. de Jong
    • 2
  1. 1.Centre for Plant Tissue Culture ResearchLisseThe Netherlands
  2. 2.Research Institute for Agrobiology and Soil Fertility (AB-DLO)WageningenThe Netherlands

Personalised recommendations