Skip to main content
SpringerLink
Log in

A rapid increase in cytokinin levels and enhanced ethylene evolution precede Al3+-induced inhibition of root growth in bean seedlings (Phaseolus vulgaris L.)

  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The role of plant hormones in aluminium (Al3+)-inducedinhibition of root growth was investigated in roots of Phaseolusvulgaris L. cv. Strike. Changes in ethylene evolution and changes inthe content and composition of cytokinins (CKs), at intervals up to 150min after treatment with Al3+, were determined by gaschromatography (GC) and combined gas chromatography-mass spectrometry (GC-MS),respectively. Seedlings were cultivated in a continuously aerated nutrientsolution at pH 4.5 with and without Al3+. The growth rate ofAl3+-treated roots was significantly decreased after 360min. Ethylene evolution from excised root tips doubled after 15min of Al3+ treatment and reached a maximum 30min after treatment. Levels of CK nucleotides declined 60 to 80%after only 5 min of Al3+ treatment whereas the zeatin(Z) content increased six-fold. The increase in Z continued over the entire 150min-sampling period and reached a level 80 times higher than thatin roots not exposed to Al3+. These results show thatAl3+-induced inhibition of root growth is preceded by significantchanges in CK content and composition and enhanced ethylene evolution. Since CKcan induce ethylene production, the rapid increase in CK, particularly Z anddihydrozeatin (dZ), may contribute to inhibition of root-growth either directlyor indirectly by affecting plant hormone homeostasis.

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

  • Abeles F.B., Morgan P.W. and Saltveit M.E. Jr 1992. Regulation by ethylene production by internal, environmental, and stress factors. In: Ethylene in Plant Biology. 2nd edn. Academic Press, San Diego, pp. 56–82.

    Google Scholar 

  • Åstot C., Dolezal K., Nordström A., Wang Q., Kunkel T. and Moritzt T. 2000. An alternative cytokinin biosynthesis pathway. Proc. Natl. Acad. Sci. USA 97: 14778–14783.

    Google Scholar 

  • Baluska F., Volkmann D. and Barlow P.W. 1999. Hormone-cytoskeleton interactions in plant cells. In: Hooykaas P.J.J., Hall M.A. and Libbenga K.R. (eds), Biochemistry and Molecular Biology of Plant Hormones. Elsevier, Amsterdam, pp. 363–390.

    Google Scholar 

  • Bennet R.J. and Breen C.M. 1993. Aluminium toxicity towards an understanding of how plant roots react to the physical environment. In: Randall P.J., Delhaize E., Richards R.A. and Munns R. (eds), Genetic Aspects of Plant Mineral Nutrition. Kluwer Acad Publ., Dordrecht, pp. 103–116.

    Google Scholar 

  • Bertell G. and Eliasson L. 1992. Cytokinin effects on root growth and possible interactions with ethylene and indole-3-acetic acid. Physiol. Plant. 84: 255–261.

    Google Scholar 

  • Bieleski R.L. 1964. The problem of halting enzyme action when extracting plant tissues. Anal. Biochem. 9: 431–442.

    Google Scholar 

  • Binns A.N. 1994. Cytokinin accumulation and action: Biochemical, genetic, and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45: 173–196.

    Google Scholar 

  • Blevins D.G. and Lukaszewski K.M. 1997. Boron in plant architecture and function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 481–500.

    Google Scholar 

  • Burström H.G. and Svensson S.-B. 1972. Hormonal regulation of root growth and development. In: Kaldewey H. and Vardar Y. (eds), Hormonal Regulation in Plant Growth and Development. Verlag Chemie, Weinheim, pp. 125–136.

    Google Scholar 

  • Calba H. and Jaillard B. 1997. Effect of aluminium on ion uptake and H+ release by maize. New Phytologist 137: 607–615.

    Google Scholar 

  • Cary A.J., Liu W. and Howell S.H. 1995. Cytokinin action is coupled to ethylene in its effects on the inhibition of root and hypocotyl elongation in Arabidopsis thaliana seedlings. Plant Physiol. 107: 1075–1082.

    Google Scholar 

  • Clarkson D.T. 1965. The effect of aluminium and some trivalent metal cations on cell division in the root apices of Allium cepa. Ann. Bot. 29: 309–315.

    Google Scholar 

  • Eliasson L., Bertell G. and Bolander E. 1989. Inhibitory action of auxin on root elongation not mediated by ethylene. Plant Physiol. 91: 310–314.

    Google Scholar 

  • Faure J.-D. and Howell S.H. 1999. Cytokinin perception and signal Transduction. In: Hooykaas P.J.J., Hall M.A. and Libbenga K.R. (eds), Biochemistry and Molecular Biology of Plant Hormones. Elsevier, Amsterdam, pp. 461–474.

    Google Scholar 

  • Foy C.D. 1984. Physiological effects of hydrogen, aluminium and manganese toxicities in acid soils. In: Adams F. (ed.), Soil Acidity and Liming. Agronomy Monograph. 2nd edn. Vol. 12. ASA-CSSA-SSSA, Madison, WI, pp. 57–97.

    Google Scholar 

  • Gunsé B., Poschenrieder Ch. and Barcelö J. 1997. Water transport properties of roots and root cortical cells in proton-and Alstressed maize varieties. Plant Physiol. 11: 595–602.

    Google Scholar 

  • Gunsé B., Poschenrieder Ch. and Barceló J. 2000. The role of ethylene metabolism in the short-term responses to aluminium by roots of two maize cultivars different in Al-resistance. Envir. Exp. Bot. 43: 73–81.

    Google Scholar 

  • Hammerton R.D., Nicander B. and Tillberg E. 1996. Identification of some major cytokinins in Phaseolus vulgaris and their distribution. Physiol. Plant. 96: 77–84.

    Google Scholar 

  • Hare P.D., Cress W.A. and van Staden J. 1997. The involvement of cytokinins in plant responses to environmental stress. Plant Growth Regul. 23: 79–103.

    Google Scholar 

  • Imaseki H. 1999. Control of ethylene synthesis and metabolism. In: Hooykaas P.J.J., Hall M.A. and Libbenga K.R. (eds), Biochemistry and Molecular Biology of Plant Hormones. Elsevier, Amsterdam, pp. 209–245.

    Google Scholar 

  • Jones D.L., Shaff J.E. and Kochian L.V. 1995. Role of calcium and other ions in directing root hair tip growth in Linnobium stoloniferum. I. Inhibition of tip growth by aluminium. Planta. 197: 672–680.

    Google Scholar 

  • Kasai M., Sasaki M., Yamamoto Y., Maeshima M. and Matsumoto H. 1994. Possible involvement of abscisic acid induction of two vacuolar H+-pumps activities in barley roots under aluminum stress. In: 5th Int. Symp Genetics and Molecular Biology of Plant Nutrition., Davis, California.

  • Kende H. and Zeevaart J.A.D. 1997. The five “classical” plant hormones. Plant Cell 9: 1197–1210.

    Google Scholar 

  • Kochian L.V. 1995. Cellular mechanisms of aluminum toxicity and resistance in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 46: 237–260.

    Google Scholar 

  • Kollmeier M., Felle H.H. and Horst W.J. 2000. Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum? Plant Physiol. 122: 945–956.

    Google Scholar 

  • Kovác P. 1993. Alkylation. In: Blau K. and Halket J.M. (eds), Handbook of Derivatives for Chromatography. J Wiley and Sons, New York, p. 116.

    Google Scholar 

  • Letham D.S. 1994. Cytokinins as phytohormones–Sites of biosynthesis, translocation and function of translocated cytokinin. In: Mok D.W.S. and Mok M.C. (eds), Cytokinins, Chemistry, Activity and Function. CRC Press, London, pp. 75–80.

    Google Scholar 

  • Llugany M. 1994. Respuestas diferenciales de cultivares de Zea mays L a la toxicidad por aluminio. PhD Diss., Universidad Autónoma de Barcelona, Spain.

    Google Scholar 

  • Llugany M., Poschenrieder Ch. and Barceló J. 1995. Monitoring of aluminium induced inhibition of root elongation in four maize cultivars differing in tolerance to aluminium and proton toxicity. Physiol. Plant. 93: 265–271.

    Google Scholar 

  • Lynch J. and Brown K.M. 1997. Ethylene and plant responses to nutritional stress. Physiol. Plant. 100: 613–619.

    Google Scholar 

  • Massot N., Poschenrieder Ch. and Barceló J. 1994. Aluminium-induced increase of zeatin riboside and dihydrozeatin riboside in Phaseolus vulgaris L. cultivars. J. Plant. Nutr. 17: 225–265.

    Google Scholar 

  • Morgan P.W. and Drew M.C. 1997. Ethylene and plant responses to stress. Physiol. Plant. 100: 620–630.

    Google Scholar 

  • Morris R.O. 1986. Genes specifying auxin and cytokinin biosynthesis in phytopathogens. Annu. Rev. Plant Physiol. Plant Mol. Biol. 37: 509–538.

    Google Scholar 

  • Motyka V., Faiss M., Strnad M., Kaminek M. and Schmülling T. 1996. Changes in cytokinin content and cytokinin oxidase activity in response to derepression of ipt gene transcription in transgenic tobacco calli and plants. Plant Physiol. 112: 1035– 1043.

    Google Scholar 

  • Nicander B., Ståhl U., Bjürkman P.O. and Tillberg E. 1993. Immunoaffinity co-purification of cytokinins and analysis by highperformance liquid chromatography with ultraviolet-spectrum detection. Planta. 189: 312–320.

    Google Scholar 

  • Palmer M.V. and Wong O.C. 1985. Identification of cytokinins from xylem exudate of Phaseolus vulgaris L. Plant Physiol. 79: 296–298.

    Google Scholar 

  • Pan W.L., Hopkins A.G. and Jackson W.A. 1989. Aluminium inhibition of shoot lateral branches of Glycine max and reversal by exogenous cytokinin. Plant Soil 120: 1–9.

    Google Scholar 

  • Rengel Z. 1992. Disturbance of cell Ca2+ homeostasis as a primary trigger of Al toxicity syndrome. Plant Cell Environ. 15: 931– 938.

    Google Scholar 

  • Ryan P.R., DiTomaso J.M. and Kochian L.V. 1993. Aluminium toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. J. Exp. Bot. 44: 437–446.

    Google Scholar 

  • Short K. and Torrey J.G. 1971. Cytokinins in seedling roots of pea. Plant Physiol. 49: 155–160.

    Google Scholar 

  • Sivaguru M., Baluska F., Volkmann D., Felle H.H. and Horst W.J. 1999. Impacts of aluminium on the maize skeleton: short-term effects on the distal part of the transition zone. Plant Physiol. 119: 1073–1082.

    Google Scholar 

  • Stenlid G. 1982. Cytokinins as inhibitors of root growth. Physiol. Plant. 56: 500–506.

    Google Scholar 

  • Su W. and Howell S.H. 1992. A single genetic locus, Ckr1, defines Arabidopsis mutants in which root growth is resistant to low concentrations of cytokinin. Plant Physiol. 99: 1569–1574.

    Google Scholar 

  • Vázquez M.D., Poschenrieder Ch., Corrales I. and Barceló J. 1999. Change in apoplastic aluminium during the initial growth response to aluminium by roots of a tolerant maize variety. Plant Physiol. 119: 435–444.

    Google Scholar 

  • Vogel J.P., Woeste K.E., Theologis A. and Kieber J.J. 1998. Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc. Natl. Acad. Sci. USA 95: 4766–4771.

    Google Scholar 

  • Wissemeier A.H. and Horst W.J. 1995. Effect of calcium supply on aluminium-induced callose formation, its distribution and persistence in roots of soybean (Glycine max (L.) Merr.). J. Plant. Physiol. 145: 470–476.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratorio Fisiología Vegetal, Facultad de Ciencias, Universidad Autónoma de Barcelona, Bellaterra, E-08 193, Spain

    N. Massot, J. Barceló & Ch. Poschenrieder

  2. Department of Plant Biology, Swedish University of Agricultural Sciences, Uppsala, SE-750 07, Sweden

    B. Nicander & E. Tillberg

Authors
  1. N. Massot
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. Nicander
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Barceló
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ch. Poschenrieder
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. Tillberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Tillberg.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Massot, N., Nicander, B., Barceló, J. et al. A rapid increase in cytokinin levels and enhanced ethylene evolution precede Al3+-induced inhibition of root growth in bean seedlings (Phaseolus vulgaris L.). Plant Growth Regulation 37, 105–112 (2002). https://doi.org/10.1023/A:1020511007138

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020511007138

Search

Navigation