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Plant Physiol, July 2002, Vol. 129, pp. 1194-1206
The Physiology and Biophysics of an Aluminum Tolerance Mechanism
Based on Root Citrate Exudation in Maize1
Miguel A.
Piñeros,
Jurandir V.
Magalhaes,
Vera M.
Carvalho
Alves, and
Leon V.
Kochian*
United States Plant, Soil, and Nutrition Laboratory, United States
Department of Agriculture-Agricultural Research Service, Cornell
University, Ithaca, New York 14853 (M.A.P., J.V.M., L.V.K.); and
Brazilian Agricultural Research Maize and Sorghum Research Center, CP
151, 35701-970 Sete Lagoas, Brazil (V.M.C.A.)
Al-induced release of Al-chelating ligands (primarily
organic acids) into the rhizosphere from the root apex has been
identified as a major Al tolerance mechanism in a number of plant
species. In the present study, we conducted physiological
investigations to study the spatial and temporal characteristics of
Al-activated root organic acid exudation, as well as changes in root
organic acid content and Al accumulation, in an Al-tolerant maize
(Zea mays) single cross (SLP 181/71 × Cateto
Colombia 96/71). These investigations were integrated with biophysical
studies using the patch-clamp technique to examine Al-activated anion
channel activity in protoplasts isolated from different regions of the maize root. Exposure to Al nearly instantaneously activated a concentration-dependent citrate release, which saturated at rates close
to 0.5 nmol citrate h 1 root1, with the
half-maximal rates of citrate release occurring at about 20 µM Al3+ activity. Comparison of citrate
exudation rates between decapped and capped roots indicated the root
cap does not play a major role in perceiving the Al signal or in the
exudation process. Spatial analysis indicated that the predominant
citrate exudation is not confined to the root apex, but could be found
as far as 5 cm beyond the root cap, involving cortex and stelar cells.
Patch clamp recordings obtained in whole-cell and outside-out patches confirmed the presence of an Al-inducible plasma membrane anion channel
in protoplasts isolated from stelar or cortical tissues. The unitary
conductance of this channel was 23 to 55 pS. Our results suggest that
this transporter mediates the Al-induced citrate release observed in
the intact tissue. In addition to the rapid Al activation of citrate
release, a slower, Al-inducible increase in root citrate content was
also observed. These findings led us to speculate that in addition to
the Al exclusion mechanism based on root citrate exudation, a second
internal Al tolerance mechanism may be operating based on
Al-inducible changes in organic acid synthesis and compartmentation. We
discuss our findings in terms of recent genetic studies of Al tolerance
in maize, which suggest that Al tolerance in maize is a complex trait.
1
This work was supported by the U.S. Department
of Agriculture-National Research Initiative (grant no. 00-35100-9280
to M.A.P. and L.V.K.).
*
Corresponding author; e-mail Lvk1{at}cornell.edu; fax
607-255-2459.
© 2002 American Society of Plant Physiologists
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