Protecting cell walls from binding aluminum by organic acids contributes to aluminum resistance

Journal of Integrative Plant Biology

Volumn 51, Issue 6, 2009, Pages 574-580

  Li, Ya Ying ^a   Zhang, Yue Jiao ^b   Zhou, Yuan ^a   Yang, Jian Li ^b   Zheng, Shao Jian ^b  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

Adsorption and desorption; Aluminum toxicity; Cell wall; Chelation; Detoxification; Organic acid

Indexed keywords

ALUMINUM; CARBOXYLIC ACID; CITRIC ACID; MALIC ACID; MALIC ACID DERIVATIVE; OXALIC ACID DERIVATIVE;

ADSORPTION; ALUMINUM; CELL ORGANELLE; CHELATION; CHEMICAL BINDING; CONCENTRATION (COMPOSITION); DESORPTION; DETOXIFICATION; EXUDATION; INHIBITION; ORGANIC ACID; OXALATE; SECRETION; STRESS RESISTANCE; TOXICITY; WHEAT;

ADSORPTION; ANGIOSPERM; ARTICLE; CELL WALL; CYTOLOGY; DRUG EFFECT; DRUG RESISTANCE; FAGOPYRUM; GROWTH, DEVELOPMENT AND AGING; KINETICS; METABOLISM; PLANT ROOT; SENNA; WHEAT;

ADSORPTION; ALUMINUM; ANGIOSPERMS; CARBOXYLIC ACIDS; CASSIA; CELL WALL; CITRATES; DRUG RESISTANCE; FAGOPYRUM; KINETICS; MALATES; OXALATES; PLANT ROOTS; TRITICUM;

SENNA; TRITICUM AESTIVUM;

EID: 67049107985     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/j.1744-7909.2009.00825.x     Document Type: Article

References (42)

1. BarcelóJ, Poschenrieder C (2002). Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: A review. Environ. Exp. Bot 48, 75-92.
2. Delhaize E, Craig S, Beaton CD, Bennet RJ, Jagadish VC, Randall PJ (1993a). Aluminum tolerance in wheat (Triticum aestivum L.). I. Uptake and distribution of aluminum in root apices. Plant Physiol. 103, 685-693.
3. Delhaize E, Ryan PR Randall PJ (1993b). Aluminum tolerance in wheat (Triticum aestivum L.). II Aluminum stimulated excretion of malic acid from root apices. Plant Physiol. 103, 695-702.
4. Eticha D, Stass A, Horst WJ (2005a). Cell-wall pectin and its degree of methylation in the maize root-apex: Significance for genotypic differences in aluminium resistance. Plant Cell Environ. 28, 1410-1420.
5. Eticha D, Stass A, Horst WJ (2005b). Localization of aluminium in the maize root apex: Can morin detect cell wall-bound aluminium? J. Exp. Bot. 56, 1351-1357.
6. Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K et al. (2007). An aluminum-activated citrate transporter in barley. Plant Cell Physiol. 48, 1081-1091.
7. Hoekenga OA, Maron LG, Piñeros MA, Cancado GMA, Shaff J, Kobayashi Y et al. (2006). AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc. Natl. Acad. Sci. USA 103, 9738-9743.
8. Horst WJ (1995). The role of the apoplast in aluminium toxicity and resistance of higher plants: A review. Z Pflanzenernaehr Bodenkd 158, 419-428.
9. Hue NV, Craddock GR, Adams F (1986). Effect of organic acids on aluminum toxicity in subsoils. Soil Sci. Soc. Am. J. 50, 28-34.
10. Jin CW, You GY, He YF, Tang C, Wu P, Zheng SJ (2007). Iron deficiency-induced secretion of phenolics facilitates the reutilization of root apoplastic iron in red clover. Plant Physiol. 144, 278-285.
11. Kinraide TB (2004). Possible influence of cell walls upon ion concentrations at plasma membrane surfaces. Toward a comprehensive view of cell-surface electrical effects upon ion uptake, intoxication, and amelioration. Plant Physiol. 136, 3804-3813.
12. Kinraide TB, Parker DR, Zobel RW (2005). Organic acid secretion as a mechanism of aluminium resistance: A model incorporating the root cortex, epidermis, and the external unstirred layer. J. Exp. Bot. 56, 1853-1856.
13. Kochian LV (1995). Cellular mechanisms of aluminum toxicity and resistance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 237-260.
14. Kochian LV, Hoekenga OA, Piñeros MA (2004). How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu. Rev. Plant Biol. 55, 459-493.
15. Ligaba A, Katsuhara M, Ryan PR, Shibasaka M, Matusmoto H (2006). The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporter that enhance the aluminum resistance of plant cells. Plant Physiol. 142, 1294-1303.
16. Liu Q, Yang JL, He LS, Li YY, Zheng SJ (2008). Effect of aluminum on cell wall, plasma membrane, antioxidants and root elongation in triticale. Biol. Plant. 52, 87-92.
17. Ma JF (2000). Role of organic acids in detoxification of Al in higher plant. Plant Cell Physiol. 44, 383-390.
18. Ma JF (2007). Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. Int. Rev. Cytol. 264, 225-252.
19. Ma JF, Ryan PR, Delhaize E (2001). Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 6, 273-278.
20. Ma JF, Zheng SJ, Matsumoto H (1997). Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant Cell Physiol. 38, 1019-1025.
21. Magalhaes JV, Liu J, Guimaraes CT, Lana UGP, Alves VM, Wang YH et al. (2007). A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat. Genet. 39, 1156-1161.
22. Mimmo T, Marzadori C, Gessa CE (2009). Does the degree of pectin esterification influence aluminium sorption by the root apoplast? Plant Soil 314, 159-168.
23. Parker DR, Pedler JF (1998). Probing the "malate hypothesis" of differential aluminum tolerance in wheat by using other rhizotoxic ions as proxies for Al. Planta 205, 389-396.
24. Poschenrieder C, GunséB, Corrales I, BarcelóJ (2008). A glance into aluminum toxicity and resistance in plants. Sci. Total Environ. 400, 356-368.
25. Rangel AF, Rao IM, Horst WJ (2007). Spatial aluminium sensitivity of root apices of two common bean (Phaseolus vulgaris L.) genotypes with contrasting aluminum resistance. J. Exp. Bot. 58, 3895-3904.
26. Ryan PR, Delhaize E, Jones DL (2001). Function and mechanism of organic anion exudation from plant roots. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 52, 527-560.
27. Ryan PR, Delhaize E, Randall PJ (1995). Characterization of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196, 103-110.
28. Ryan PR, Ditomaso JM, Kochian LV (1993). Aluminium toxicity in roots: An investigation of spatial sensitivity and the role of the root cap. J. Exp. Bot. 44, 437-446.
29. Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR et al. (2004). A wheat gene encoding an aluminum-activated malate transporter. Plant J. 37, 645-653.
30. Sivaguru M, Horst WJ (1998). The distal part of the transition zone is the most aluminium-sensitive apical root zone of maize. Plant Physiol. 116, 155-163.
31. Taylor GJ (1991). Current views of the aluminum stress response: The physiological basis of tolerance. Curr. Top Plant Biochem. Physiol. 10, 57-93.
32. Taylor GJ, McDonald-Stephens JL, Hunter DB, Bertsch PM, Elmore D, Rengel Z et al. (2000). Direct measurement of aluminum uptake and distribution in single cells of Chara coralline. Plant Physiol. 123, 987-996.
33. Tice KR, Parker DR, Demason DA (1992). Operationally defined apoplastic and symplastic aluminum fractions in root tips of aluminum-intoxicated wheat. Plant Physiol. 100, 309-318.
34. Wehr JB, Menzies NW, Blamey FPC (2003). Model studies on the role of citrate, malate and pectin esterification on the enzymatic degradation of Al- and Ca-pectate gels: Possible implications for Al-tolerance. Plant Physiol. Biochem. 41, 1007-1010.
35. Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P et al. (2008). Cell wall polysaccharides are specifically involved in the exclusion of aluminum from rice root apex. Plant Physiol. 146, 602-611.
36. Yang JL, Zheng SJ, He YF, You JF, Zhang L, Yu XH (2006). Comparative studies on the effect of a protein-synthesis inhibitor on aluminum-induced secretion of organic acids from Fagopyrum esculentum Moench and Cassia tora L. roots. Plant Cell Environ. 29, 240-246.
37. Zhang G, Taylor GJ (1990). Kinetics of aluminum uptake in Triticum aestivum L.: Identity of the linear phase of aluminum uptake by excised roots of aluminum-tolerant and aluminum-sensitive cultivars. Plant Physiol. 94, 577-584.
38. Zheng SJ, Lin XY, Yang JL, Liu Q, Tang CX (2004). The kinetics of aluminum adsorption and desorption by root cell walls of an aluminum resistant wheat (Triticum aestivum L.) cultivar. Plant Soil 261, 85-90.
39. Zheng SJ, Ma JF, Matsumoto H (1998). High aluminum resistance in buckwheat: I. Al-induced special secretion of oxalic acid from root tips. Plant Physiol. 117, 745-751.
40. Zheng SJ, Yang JL (2005). Target sites of aluminum phytotoxicity. Biol. Plant 49, 321-331.
41. Zheng SJ, Yang JL, He YF, Yu XH, Zhang L, You JF et al. (2005). Immobilization of aluminum with phosphorus in roots is associated with high Al resistance in buckwheat. Plant Physiol. 138, 297-303.
42. Zhong H, Läuchli A (1993). Changes of cell wall composition and polymer size in primary roots of cotton seedlings under high salinity. J. Exp. Bot. 4, 773-778.