The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation in maize

被引:153
作者
Piñeros, MA
Magalhaes, JV
Alves, VMC
Kochian, LV [1 ]
机构
[1] Cornell Univ, USDA ARS, US Plant Soil & Nutr Lab, Ithaca, NY 14853 USA
[2] Brazilian Agr Res Maize & Sorghum Res Ctr, BR-35701970 Sete Lagoas, Brazil
关键词
D O I
10.1104/pp.002295
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
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 AI-activated root organic acid exudation, as well as changes in root organic acid content and Al accumulation, in an AI-tolerant maize (Zea mays) single cross (SLP 181/71 x 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) root(-1), with the half-maximal rates of citrate release occurring at about 20 mum 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 AI-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.
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页码:1194 / 1206
页数:13
相关论文
共 34 条
[1]   A MALACHITE GREEN PROCEDURE FOR ORTHO-PHOSPHATE DETERMINATION AND ITS USE IN ALKALINE PHOSPHATASE-BASED ENZYME-IMMUNOASSAY [J].
BAYKOV, AA ;
EVTUSHENKO, OA ;
AVAEVA, SM .
ANALYTICAL BIOCHEMISTRY, 1988, 171 (02) :266-270
[2]  
BENNET R J, 1991, Plant and Soil, V134, P153
[3]   THE EFFECTS OF ALUMINUM ON ROOT CAP FUNCTION AND ROOT DEVELOPMENT IN ZEA-MAYS-L [J].
BENNET, RJ ;
BREEN, CM ;
FEY, MV .
ENVIRONMENTAL AND EXPERIMENTAL BOTANY, 1987, 27 (01) :91-+
[4]   Hematoxylin staining as a phenotypic index for aluminum tolerance selection in tropical maize (Zea mays L.) [J].
Cançado, GMA ;
Loguercio, LL ;
Martins, PR ;
Parentoni, SN ;
Paiva, E ;
Borém, A ;
Lopes, MA .
THEORETICAL AND APPLIED GENETICS, 1999, 99 (05) :747-754
[5]   ALUMINUM TOLERANCE IN WHEAT (TRITICUM-AESTIVUM L) .2. ALUMINUM-STIMULATED EXCRETION OF MALIC-ACID FROM ROOT APICES [J].
DELHAIZE, E ;
RYAN, PR ;
RANDALL, PJ .
PLANT PHYSIOLOGY, 1993, 103 (03) :695-702
[6]   ALUMINUM TOLERANCE IN WHEAT (TRITICUM-AESTIVUM L) .1. UPTAKE AND DISTRIBUTION OF ALUMINUM IN ROOT APICES [J].
DELHAIZE, E ;
CRAIG, S ;
BEATON, CD ;
BENNET, RJ ;
JAGADISH, VC ;
RANDALL, PJ .
PLANT PHYSIOLOGY, 1993, 103 (03) :685-693
[7]   Aluminum-induced organic acids exudation by roots of an aluminum-tolerant tropical maize [J].
Jorge, RA ;
Arruda, P .
PHYTOCHEMISTRY, 1997, 45 (04) :675-&
[8]   CELLULAR MECHANISMS OF ALUMINUM TOXICITY AND RESISTANCE IN PLANTS [J].
KOCHIAN, LV .
ANNUAL REVIEW OF PLANT PHYSIOLOGY AND PLANT MOLECULAR BIOLOGY, 1995, 46 :237-260
[9]   POTASSIUM-TRANSPORT IN CORN ROOTS .2. THE SIGNIFICANCE OF THE ROOT PERIPHERY [J].
KOCHIAN, LV ;
LUCAS, WJ .
PLANT PHYSIOLOGY, 1983, 73 (02) :208-215
[10]   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? [J].
Kollmeier, M ;
Felle, HH ;
Horst, WJ .
PLANT PHYSIOLOGY, 2000, 122 (03) :945-956