Focused Review
Recent progress in the research of external Al detoxification in higher plants: a minireview

https://doi.org/10.1016/S0162-0134(03)00245-9Get rights and content

Abstract

Aluminum (Al) is highly toxic to plant growth. The toxicity is characterized by rapid inhibition of root elongation. However, some plant species and cultivars have evolved some mechanisms for detoxifying Al both internally and externally. In this review, the recent progress made in the research of external detoxification of Al is described. Accumulating evidence has shown that organic acids play an important role in the detoxification of Al. Some plant species and cultivars respond to Al by secreting citrate, malate or oxalate from the roots. Recently, the anion channel of malate and citrate in the plasma membrane has been characterized and a gene encoding the malate channel has been cloned. The metabolism of organic acids seems to be poorly correlated with the Al-induced secretion of organic acid anions. A number of QTLs (quantitative trait loci) for Al resistance have been identified in rice, Arabidopsis, and other species. Transgenic plants with enhanced resistance to Al have also been reported, but introduction of multiple genes may be required to gain high Al resistance in future.

Introduction

Aluminum (Al) is the third most abundant element after oxygen and silicon and the most abundant metals in the earth’s crust. Most Al exists as oxides and aluminosilicates and these forms of Al are harmless to plants. However, on the acid soil, which comprises about 40% of the arable land in the world [1], Al is solubilized into the soil solution and exists in the form of trivalent cation, Al3+. At micromolar concentrations, Al3+ can inhibit root elongation within minutes or hours. The subsequent effects on nutrient and water uptake result in poor growth and productivity. The chemistry of Al in solution is complicated because Al hydrolyses in a pH-dependent manner to form various complexes with hydroxyl groups. Although the toxicity of these soluble Al species varies considerably, Al3+ is regarded as the greatest stress to plants (Al3+ will be represented as Al for the remainder of the text). Although it is still under debate in regard to primary mechanism of Al toxicity, all Al-induced inhibition results from a high binding affinity of Al with extracellular and intracellular substances [2].

On the other hand, there is a wide genetic variation, both within and between species, in the resistance of plants to Al, suggesting that Al-resistant species or cultivars possess several mechanisms for detoxifying Al. Two strategies for the detoxification of Al by plants have been suggested [3], [4]. One is the exclusion of Al from the root tips (exclusion mechanism) and the other is tolerance of the Al that enters the plant (internal tolerance mechanism). Several possibilities have been proposed for each type of mechanism, but most of them are highly speculative. However, since 1993, accumulating evidence has shown that organic acids play an important role in detoxifying Al both internally and externally [2], [5]. Some organic acids can form stable complexes with Al, thereby preventing the binding of Al to cellular components. Recently, several reviews on the role of organic acids in Al resistance have been published [2], [5], [6], [7], [8]. Here, we focus on the latest progress made in the research of external detoxification of Al.

Section snippets

New insight into external detoxification of Al

Many Al-resistant species and cultivars respond to Al stress by secreting specific organic acid anions from the roots [2], [5] and a good correlation between organic acid anion secretion and Al resistance has been established (Fig. 1; Ref. [9]). However, the response differs with plant species, such as organic acid species, secretion patterns, temperature sensitivity and dose response. Characteristics of Al-induced organic acid anion secretion from different species are summarized in Table 1.

QTL analysis of Al resistance

As a genetic approach, quantitative trait loci (QTL) for Al resistance have been identified in several plant species. So far, five populations have been used to map Al resistant genes in rice (Oryza sativa L.) (Table 2). Rice is the most Al-resistant species among small-grain cereal crops [20]. Different from other cereal species (e.g. wheat, barley, rye), organic acid anion secretion is not the mechanism of Al resistance in rice [20]. However, the mechanism responsible for high Al resistance

Manipulation of Al resistance

As organic acid anion secretion from the roots has been demonstrated to be involved in Al resistance as described above, an attempt to breed Al-resistant cultivars by manipulating organic acid metabolism has been made (Table 3). Transgenic tobacco lines expressing citrate synthase (CS) gene derived from Pseudomonas aeruginosa showed high CS activity, enhanced citrate efflux and Al resistance [32], [33]. This line showed 10-fold high internal citrate concentration compared with the control line

Acknowledgements

This study was supported in part by a Grant-in-Aid for General Scientific Research (Grant no. 13660067 to J.F.M.) from the Ministry of Education, Sports, Culture, Science and Technology of Japan, by CREST, JST (Japan Science and Technology Cooperation), and NSFC (no. 30228023 to J.F.M.).

References (49)

  • J.F. Ma et al.

    Trends Plant Sci.

    (2001)
  • J. Barcelo et al.

    Environ. Exp. Bot.

    (2002)
  • H. Matsumoto

    Int. Rev. Cytol.

    (2000)
  • J. Lopez-Bucio et al.

    Plant Sci.

    (2000)
  • C.D. Foy et al.

    Annu. Rev. Plant Physiol.

    (1978)
  • J.F. Ma

    Plant Cell Physiol.

    (2000)
  • L.V. Kochian

    Annu. Rev. Plant Physiol. Plant Mol. Biol.

    (1995)
  • G.J. Taylor

    Curr. Top. Plant Biochem. Physiol.

    (1991)
  • P.R. Ryan et al.

    Annu. Rev. Plant Physiol. Plant Mol. Biol.

    (2001)
  • Z. Zhao et al.

    Planta

    (2003)
  • W.H. Zhang et al.

    Plant Physiol.

    (2001)
  • M.A. Pineros et al.

    Plant Physiol.

    (2001)
  • M. Kollmeier et al.

    Plant Physiol.

    (2001)
  • M.A. Pineros et al.

    Plant Physiol.

    (2002)
  • T. Sasaki et al.

    Plant Cell Physiol.

    (2002)
  • H. Osawa et al.

    Plant Physiol.

    (2001)
  • J.F. Ma et al.
  • Z.M. Yang et al.

    Physiol. Plant.

    (2001)
  • X.F. Li et al.

    Plant Physiol.

    (2000)
  • J.E. Hayes et al.

    J. Exp. Bot.

    (2003)
  • J.F. Ma et al.

    Plant Cell Physiol.

    (2002)
  • P. Wu et al.

    Theor. Appl. Genet.

    (2000)
  • V.T. Nguyen et al.

    Theor. Appl. Genet.

    (2001)
  • V.T. Nguyen et al.

    Mol. Genet. Genomics

    (2002)
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