THE PLANT CELL, Vol 7, Issue 11 1913-1922, Copyright © 1995 by American Society of Plant Biologists

RESEARCH ARTICLES

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

D. L. Jones and L. V. Kochian
U.S. Plant, Soil, and Nutrition Laboratory, U.S. Department of Agriculture-Agricultural Research Service, Cornell University, Tower Road, Ithaca, New York 14853-2901

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.

This article has been cited by other articles:

				P. R. Ryan, Q. Liu, P. Sperling, B. Dong, S. Franke, and E. Delhaize A Higher Plant {Delta}8 Sphingolipid Desaturase with a Preference for (Z)-Isomer Formation Confers Aluminum Tolerance to Yeast and Plants Plant Physiology, August 1, 2007; 144(4): 1968 - 1977. [Abstract] [Full Text] [PDF]

				J. Zhang, Z. He, H. Tian, G. Zhu, and X. Peng Identification of aluminium-responsive genes in rice cultivars with different aluminium sensitivities J. Exp. Bot., June 1, 2007; 58(8): 2269 - 2278. [Abstract] [Full Text] [PDF]

				O. Krinke, Z. Novotna, O. Valentova, and J. Martinec Inositol trisphosphate receptor in higher plants: is it real? J. Exp. Bot., February 1, 2007; 58(3): 361 - 376. [Abstract] [Full Text] [PDF]

				K. M. Gabrielson, J. D. Cancel, L. F. Morua, and P. B. Larsen Identification of dominant mutations that confer increased aluminium tolerance through mutagenesis of the Al-sensitive Arabidopsis mutant, als3-1 J. Exp. Bot., March 1, 2006; 57(4): 943 - 951. [Abstract] [Full Text] [PDF]

				J. F. Ma, R. Shen, S. Nagao, and E. Tanimoto Aluminum Targets Elongating Cells by Reducing Cell Wall Extensibility in Wheat Roots Plant Cell Physiol., May 1, 2004; 45(5): 583 - 589. [Abstract] [Full Text] [PDF]

				M. Sivaguru, B. Ezaki, Z.-H. He, H. Tong, H. Osawa, F. Baluska, D. Volkmann, and H. Matsumoto Aluminum-Induced Gene Expression and Protein Localization of a Cell Wall-Associated Receptor Kinase in Arabidopsis Plant Physiology, August 1, 2003; 132(4): 2256 - 2266. [Abstract] [Full Text] [PDF]

				M. Sivaguru, S. Pike, W. Gassmann, and T. I. Baskin Aluminum Rapidly Depolymerizes Cortical Microtubules and Depolarizes the Plasma Membrane: Evidence that these Responses are Mediated by a Glutamate Receptor Plant Cell Physiol., July 15, 2003; 44(7): 667 - 675. [Abstract] [Full Text] [PDF]

				M. A. R. Milla, E. Butler, A. R. Huete, C. F. Wilson, O. Anderson, and J. P. Gustafson Expressed Sequence Tag-Based Gene Expression Analysis under Aluminum Stress in Rye Plant Physiology, December 1, 2002; 130(4): 1706 - 1716. [Abstract] [Full Text] [PDF]

				A. R. Facanha and A. L. Okorokova-Facanha Inhibition of Phosphate Uptake in Corn Roots by Aluminum-Fluoride Complexes Plant Physiology, August 1, 2002; 129(4): 1763 - 1772. [Abstract] [Full Text] [PDF]

				K. Liu and S. Luan Internal Aluminum Block of Plant Inward K+ Channels PLANT CELL, June 1, 2001; 13(6): 1453 - 1466. [Abstract] [Full Text] [PDF]

				M. Kollmeier, P. Dietrich, C. S. Bauer, W. J. Horst, and R. Hedrich Aluminum Activates a Citrate-Permeable Anion Channel in the Aluminum-Sensitive Zone of the Maize Root Apex. A Comparison Between an Aluminum- Sensitive and an Aluminum-Resistant Cultivar Plant Physiology, May 1, 2001; 126(1): 397 - 410. [Abstract] [Full Text]

				H. Osawa and H. Matsumoto Possible Involvement of Protein Phosphorylation in Aluminum-Responsive Malate Efflux from Wheat Root Apex Plant Physiology, May 1, 2001; 126(1): 411 - 420. [Abstract] [Full Text]

				W.-H. Zhang, P. R. Ryan, and S. D. Tyerman Malate-Permeable Channels and Cation Channels Activated by Aluminum in the Apical Cells of Wheat Roots Plant Physiology, March 1, 2001; 125(3): 1459 - 1472. [Abstract] [Full Text]

				Y. Yamamoto, Y. Kobayashi, and H. Matsumoto Lipid Peroxidation Is an Early Symptom Triggered by Aluminum, But Not the Primary Cause of Elongation Inhibition in Pea Roots Plant Physiology, January 1, 2001; 125(1): 199 - 208. [Abstract] [Full Text]

				I. R. Silva, T. J. Smyth, D. F. Moxley, T. E. Carter, N. S. Allen, and T. W. Rufty Aluminum Accumulation at Nuclei of Cells in the Root Tip. Fluorescence Detection Using Lumogallion and Confocal Laser Scanning Microscopy Plant Physiology, June 1, 2000; 123(2): 543 - 552. [Abstract] [Full Text]

				L. J. Allen, K. B. MacGregor, R. S. Koop, D. H. Bruce, J. Karner, and A. W. Bown The Relationship between Photosynthesis and a Mastoparan-Induced Hypersensitive Response in Isolated Mesophyll Cells Plant Physiology, April 1, 1999; 119(4): 1233 - 1242. [Abstract] [Full Text]

				M. Sivaguru, D. Volkmann, H. H. Felle, and W. J. Horst Impacts of Aluminum on the Cytoskeleton of the Maize Root Apex. Short-Term Effects on the Distal Part of the Transition Zone Plant Physiology, March 1, 1999; 119(3): 1073 - 1082. [Abstract] [Full Text]

				E. B. Blancaflor, D. L. Jones, and S. Gilroy Alterations in the Cytoskeleton Accompany Aluminum-Induced Growth Inhibition and Morphological Changes in Primary Roots of Maize Plant Physiology, September 1, 1998; 118(1): 159 - 172. [Abstract] [Full Text]

				J. Degenhardt, P. B. Larsen, S. H. Howell, and L. V. Kochian Aluminum Resistance in the Arabidopsis Mutant alr-104 Is Caused by an Aluminum-Induced Increase in Rhizosphere pH Plant Physiology, May 1, 1998; 117(1): 19 - 27. [Abstract] [Full Text]

				D. L. Jones, L. V. Kochian, and S. Gilroy Aluminum Induces a Decrease in Cytosolic Calcium Concentration in BY-2 Tobacco Cell Cultures Plant Physiology, January 1, 1998; 116(1): 81 - 89. [Abstract] [Full Text]

				J. Kopka, C. Pical, J. E. Gray, and B. Müller-Röber Molecular and Enzymatic Characterization of Three Phosphoinositide-Specific Phospholipase C Isoforms from Potato Plant Physiology, January 1, 1998; 116(1): 239 - 250. [Abstract] [Full Text]

				K. D. Richards, E. J. Schott, Y. K. Sharma, K. R. Davis, and R. C. Gardner Aluminum Induces Oxidative Stress Genes in Arabidopsis thaliana Plant Physiology, January 1, 1998; 116(1): 409 - 418. [Abstract] [Full Text]