Summary
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.
Similar content being viewed by others
References
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.
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.
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.
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.
Christianson, M. L.; Warnick, D. A. Competence and determination in the process of in vitro shoot organogenesis. Dev. Biol. 95:288–293; 1983.
Croes, A. F.; Wullems, G. J. Hormonal induction of regeneration: how to open the black box? Adv. Hortic. Sci. 8:37–42; 1994.
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.
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.
De Klerk, G. J. Markers of adventitious root formation. Agronomie 16:563–571; 1996.
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.
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.
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.
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.
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).
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).
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.
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.
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.
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.
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.
Epstein, E.; Ludwig-Müller, J. Indole-3-butyric acid in plants: occurrence, synthesis, metabolism and transport. Physiol. Plant. 88:382–389; 1993.
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.
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.
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.
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.
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.
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.
Hartmann, H. T.; Kester, D. E.; Davies, F. T. Plant propagation: principles and practices. Englewood Cliffs, NJ: Prentice Hall; 1990.
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.
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.
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.
Jackson, M. B. Ethylene and responses of plants to soil waterlogging and submergence. Annu. Rev. Plant Physiol. 36:146–174; 1985.
Jacobs, T. W. Cell cycle control. Annu. Rev. Plant Physiol. 46:317–339; 1995.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Lyon, G. D.; Reglinski, T.; Newton, C. Novel disease control compounds: the potential to “immunize” plants against infection. Plant Pathol. 44:407–427; 1995.
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.
Milborrow, B. V. Inhibitors. In: Wilkins, M. B., ed. Advanced plant physiology. London: Pitman Publishing Ltd.; 1984:76–110.
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.
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.
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.
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.
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.
Rubery, P. H.; Sheldrake, A. R. Effect of pH and surface charge on cell uptake of auxin. Nat. New Biol. 244:285–288; 1973.
Smith, D. L.; Fedoroff, N. V. LRP1, a gene expressed in lateral and adventitious root primordia of Arabidopsis. Plant Cell 7:735–745; 1995.
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.
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.
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.
Thimann, K. V. Auxins and the growth of roots. Am. J. Bot. 23:561–569; 1936.
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.
Ueda, J. Promotive effect of capillarol and related compounds on root growth. Physiol. Plant. 76:42–46; 1989.
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.
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.
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.
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).
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.
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.
Went, F. W. The dual effect of auxin on root formation. Am. J. Bot. 26:24–29; 1939.
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.
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.
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.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
de Klerk, GJ., van der Krieken, W. & de Jong, J.C. Review the formation of adventitious roots: New concepts, new possibilities. In Vitro Cell.Dev.Biol.-Plant 35, 189–199 (1999). https://doi.org/10.1007/s11627-999-0076-z
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11627-999-0076-z