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Title: ORGANIC ACID SECRETION AS A MECHANISM OF ALUMINUM TOLERANCE. A MODEL INCORPORATING THE ROOT CORTEX, EPIDERMIS, AND THE EXTERNAL UNSTIRRED LAYER

Author
item Kinraide, Thomas
item PARKER, DAVID - UNIVERSITY OF CALIFORNIA
item Zobel, Richard

Submitted to: Journal of Experimental Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/29/2005
Publication Date: 5/31/2005
Citation: Kinraide, T.B., Parker, D.R., Zobel, R.W. 2005. Organic acid secretion as a mechanism of aluminum tolerance. A model incorporating the root cortex, epidermis, and the external unstirred layer. Journal of Experimental Botany, 56:1853-1865.

Interpretive Summary: Some plants are resistant to the aluminum present in the acidic soils that covers a large portion of the earth. This tolerance is commonly attributed to the secretion of organic acids that bind aluminum. However, the measured amount of organic acid that is secreted appears to be inadequate; so the mechanism of aluminum resistance is not understood as it must be in order to mount a rational program of breeding or bioengineering to improve plant performance in acidic soils. We have proposed an alternative mechanism of resistance that we test by modeling and experimentation. In the new mechanism the root-interior tissue, but not the external root surface, need be protected from Al. The mechanism accounts for the small amount of organic acid secreted by root tips and accounts for the low cost to the plant. The mechanism also indicates the root anatomical and physiological features that must be incorporated into resistant plants.

Technical Abstract: The resistance of some plants to Al has been attributed to the secretion of Al3+-binding organic acid (OA) anions from the Al-sensitive root tips. Evidence for the OA secretion hypothesis of resistance is substantial, but the mode of action remains unknown because the OA secretion appears to be too small to reduce adequately the activity of Al3+ at the root surface. In our study we consider a mechanism for the reduction of Al3+ at the root surface and just beneath the epidermis by complexation with secreted OA2–. According to our computations, Al3+ activity is insufficiently reduced at the surface of the root tips to account for the Al resistance of Triticum aestivum L. cv. Atlas 66, a malate-secreting wheat. Experimental treatments to decrease the thickness of the unstirred layer (increased aeration and removal of root-tip mucilage) failed to enhance sensitivity to Al3+. On the basis of additional modeling, the observed spatial distribution of Al in roots, and the anatomical responses to Al, we propose that the epidermis is an essential component of the diffusion pathway for both OA and Al. We suggest that Al3+ in the cortex must be reduced to small concentrations to substantially alleviate the inhibition of root elongation and that the outer surface of the epidermis can tolerate relatively large concentrations of Al3+. If OA secretion is required for reducing Al3+ mainly beneath the root surface, rather than in the rhizosphere, then the metabolic cost to plants will be greatly reduced.