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. 1995 Nov;7(11):1913–1922. doi: 10.1105/tpc.7.11.1913

Aluminum Inhibition of the Inositol 1,4,5-Trisphosphate Signal Transduction Pathway in Wheat Roots: A Role in Aluminum Toxicity?

D L Jones 1, L V Kochian 1
PMCID: PMC161049  PMID: 12242363

Abstract

In crop plants, aluminum (Al) rhizotoxicity is a major problem worldwide; however, the cause of Al toxicity remains elusive. The effects of Al on the inositol 1,4,5-trisphosphate (Ins[1,4,5]P3)-mediated signal transduction pathway were investigated in wheat roots. Exogenously applied Al (50 [mu]M) rapidly inhibited root growth (<2 hr) but did not affect general root metabolism. An Ins(1,4,5)P3 transient was generated in root tips, either before or after exposure to Al for 1 hr, by treating the roots with H2O2 (10 mM). Background (unstimulated) levels of Ins(1,4,5)P3 were similar in both Al-treated and Al-untreated root apices. However, H2O2-stimulated levels of Ins(1,4,5)P3 in root apices showed a significant (>50%) reduction after Al exposure in comparison with untreated controls, indicating that Al may be interfering with the phosphoinositide signaling pathway. When phospholipase C (PLC) was assayed directly in the presence of Al or other metal cations in microsomal membranes, AlCl3 and Al-citrate specifically inhibited PLC action in a dose-dependent manner and at physiologically relevant Al levels. Al exposure had no effect on inositol trisphosphate dephosphorylation or on a range of enzymes isolated from wheat roots, suggesting that Al exposure may specifically target PLC. Possible mechanisms of PLC inhibition by Al and the role of Ins(1,4,5)P3 in Al toxicity and growth are discussed. This study provides compelling evidence that the phytotoxic metal cation Al has an intracellular target site that may be integrally involved in root growth.

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Selected References

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  1. Aducci P., Marra M. IP3 levels and their modulation FY fusicoccin measured by a novel [3H] IP3 binding assay. Biochem Biophys Res Commun. 1990 May 16;168(3):1041–1046. doi: 10.1016/0006-291x(90)91134-e. [DOI] [PubMed] [Google Scholar]
  2. Anderson R. A., Marchesi V. T. Regulation of the association of membrane skeletal protein 4.1 with glycophorin by a polyphosphoinositide. Nature. 1985 Nov 21;318(6043):295–298. doi: 10.1038/318295a0. [DOI] [PubMed] [Google Scholar]
  3. Balke N. E., Hodges T. K. Plasma membrane adenosine triphosphatase of oat roots: activation and inhibition by mg and ATP. Plant Physiol. 1975 Jan;55(1):83–86. doi: 10.1104/pp.55.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
  5. Birchall J. D., Chappell J. S. Aluminum, chemical physiology, and Alzheimer's disease. Lancet. 1988 Oct 29;2(8618):1008–1010. doi: 10.1016/s0140-6736(88)90754-4. [DOI] [PubMed] [Google Scholar]
  6. 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. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  7. Claro E., Sarri E., Picatoste F. Measurement of phospholipase C activity in brain membranes. Methods Mol Biol. 1995;41:177–188. doi: 10.1385/0-89603-298-1:177. [DOI] [PubMed] [Google Scholar]
  8. Europe-Finner G. N., Newell P. C. Inositol 1,4,5-trisphosphate and calcium stimulate actin polymerization in Dictyostelium discoideum. J Cell Sci. 1986 Jun;82:41–51. doi: 10.1242/jcs.82.1.41. [DOI] [PubMed] [Google Scholar]
  9. Hirayama T., Ohto C., Mizoguchi T., Shinozaki K. A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3903–3907. doi: 10.1073/pnas.92.9.3903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lazof D. B., Goldsmith J. G., Rufty T. W., Linton R. W. Rapid Uptake of Aluminum into Cells of Intact Soybean Root Tips (A Microanalytical Study Using Secondary Ion Mass Spectrometry). Plant Physiol. 1994 Nov;106(3):1107–1114. doi: 10.1104/pp.106.3.1107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Long D. M., Oaks A. Stabilization of nitrate reductase in maize roots by chymostatin. Plant Physiol. 1990 Jul;93(3):846–850. doi: 10.1104/pp.93.3.846. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Martin R. B. Aluminium speciation in biology. Ciba Found Symp. 1992;169:5–25. doi: 10.1002/9780470514306.ch2. [DOI] [PubMed] [Google Scholar]
  13. McDonald L. J., Mamrack M. D. Aluminum affects phosphoinositide hydrolysis by phosphoinositidase C. Biochem Biophys Res Commun. 1988 Aug 30;155(1):203–208. doi: 10.1016/s0006-291x(88)81069-6. [DOI] [PubMed] [Google Scholar]
  14. McDonald L. J., Mamrack M. D. Phosphoinositide hydrolysis by phospholipase C modulated by multivalent cations La(3+), Al(3+), neomycin, polyamines, and melittin. J Lipid Mediat Cell Signal. 1995 Jan;11(1):81–91. doi: 10.1016/0929-7855(94)00029-c. [DOI] [PubMed] [Google Scholar]
  15. Memon A. R., Rincon M., Boss W. F. Inositol Trisphosphate Metabolism in Carrot (Daucus carota L.) Cells. Plant Physiol. 1989 Oct;91(2):477–480. doi: 10.1104/pp.91.2.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nishimura M., Kaku K., Azuno Y., Okafuji K., Inoue Y., Kaneko T. Stimulation of phosphoinositol turnover and protein kinase C activation by granulocyte-macrophage colony-stimulating factor in HL-60 cells. Blood. 1992 Aug 15;80(4):1045–1051. [PubMed] [Google Scholar]
  17. Nixon R. A., Clarke J. F., Logvinenko K. B., Tan M. K., Hoult M., Grynspan F. Aluminum inhibits calpain-mediated proteolysis and induces human neurofilament proteins to form protease-resistant high molecular weight complexes. J Neurochem. 1990 Dec;55(6):1950–1959. doi: 10.1111/j.1471-4159.1990.tb05781.x. [DOI] [PubMed] [Google Scholar]
  18. Ohman L. O., Martin R. B. Citrate as the main small molecule binding Al3+ in serum. Clin Chem. 1994 Apr;40(4):598–601. [PubMed] [Google Scholar]
  19. Pical C., Sandelius A. S., Melin P. M., Sommarin M. Polyphosphoinositide Phospholipase C in Plasma Membranes of Wheat (Triticum aestivum L.) : Orientation of Active Site and Activation by Ca and Mg. Plant Physiol. 1992 Nov;100(3):1296–1303. doi: 10.1104/pp.100.3.1296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Price A. H., Taylor A., Ripley S. J., Griffiths A., Trewavas A. J., Knight M. R. Oxidative Signals in Tobacco Increase Cytosolic Calcium. Plant Cell. 1994 Sep;6(9):1301–1310. doi: 10.1105/tpc.6.9.1301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ryan P. R., Kochian L. V. Interaction between Aluminum Toxicity and Calcium Uptake at the Root Apex in Near-Isogenic Lines of Wheat (Triticum aestivum L.) Differing in Aluminum Tolerance. Plant Physiol. 1993 Jul;102(3):975–982. doi: 10.1104/pp.102.3.975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schomerus C., Küntzel H. CDC25-dependent induction of inositol 1,4,5-trisphosphate and diacylglycerol in Saccharomyces cerevisiae by nitrogen. FEBS Lett. 1992 Aug 3;307(3):249–252. doi: 10.1016/0014-5793(92)80688-d. [DOI] [PubMed] [Google Scholar]
  23. Uno I., Fukami K., Kato H., Takenawa T., Ishikawa T. Essential role for phosphatidylinositol 4,5-bisphosphate in yeast cell proliferation. Nature. 1988 May 12;333(6169):188–190. doi: 10.1038/333188a0. [DOI] [PubMed] [Google Scholar]
  24. Yamamoto Y. T., Conkling M. A., Sussex I. M., Irish V. F. An Arabidopsis cDNA related to animal phosphoinositide-specific phospholipase C genes. Plant Physiol. 1995 Mar;107(3):1029–1030. doi: 10.1104/pp.107.3.1029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. You G. F., Nelson D. J. Al3+ versus Ca2+ ion binding to methionine and tyrosine spin-labeled bovine brain calmodulin. J Inorg Biochem. 1991 Mar;41(4):283–291. doi: 10.1016/0162-0134(91)80021-9. [DOI] [PubMed] [Google Scholar]

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