Focused ReviewRecent progress in the research of external Al detoxification in higher plants: a minireview
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)
- et al.
Trends Plant Sci.
(2001) - et al.
Environ. Exp. Bot.
(2002) Int. Rev. Cytol.
(2000)- et al.
Plant Sci.
(2000) - et al.
Annu. Rev. Plant Physiol.
(1978) Plant Cell Physiol.
(2000)Annu. Rev. Plant Physiol. Plant Mol. Biol.
(1995)Curr. Top. Plant Biochem. Physiol.
(1991)- et al.
Annu. Rev. Plant Physiol. Plant Mol. Biol.
(2001) - et al.
Planta
(2003)
Plant Physiol.
Plant Physiol.
Plant Physiol.
Plant Physiol.
Plant Cell Physiol.
Plant Physiol.
Physiol. Plant.
Plant Physiol.
J. Exp. Bot.
Plant Cell Physiol.
Theor. Appl. Genet.
Theor. Appl. Genet.
Mol. Genet. Genomics
Cited by (155)
Root physiology and morphology of soybean in relation to stress tolerance
2022, Advances in Botanical ResearchMethod for initially selecting Al-tolerant rice varieties based on the charge characteristics of their roots
2020, Ecotoxicology and Environmental SafetyInheritance of aluminum tolerance in the wheat cultivar Toropi and new findings about the introduction of this trait into the Brazilian wheat germplasm
2019, Environmental and Experimental BotanyMechanisms of organic acids and boron induced tolerance of aluminum toxicity: A review
2018, Ecotoxicology and Environmental SafetyCitation Excerpt :It has been demonstrated that aluminum stimulates the efflux of malate from excised root apices of wheat (Triticum aestivum) seedlings and that the response is five- to tenfold greater from Al-tolerant plants than from Al-sensitive plants (Ryan et al., 1995). Therefore, aluminum activated secretion of malate are mediated via transporters (Ma and Furukawa, 2003). The results of previous studies showed that Al-activated secretion of citrate inhibited the citrate exudation in rye bean roots (Secale cereale) by both anion channel and carrier inhibitors, demonstrating the possible role of both citrate carrier and anion channel in aluminum activated citrate exudations (Li et al., 2000).
Role of root exudates in metal acquisition and tolerance
2017, Current Opinion in Plant Biology