Skip to main content

Mechanisms of Aluminum Tolerance

  • Chapter
  • First Online:

Abstract

Aluminum (Al) toxicity limits agricultural productivity over much of the world’s arable land by inhibiting root growth and development. Affected plants have difficulty in acquiring adequate water and nutrition from their soil environments and thus have stunted shoot development and diminished yield. Al toxicity is due to soil acidity and is largely a natural problem; however, it can also result due to excessive use of ammonia-based fertilizers. Many plants utilize Al tolerance mechanisms that depend upon excluding Al from the root tip, which is the most sensitive part of the root system to Al toxicity. Al exclusion is often mediated by citrate or malate release from roots by Al-activated transporters. Recently, major Al tolerance loci have been cloned and represent citrate (Alt SB from Sorghum) or malate (TaALMT1) from wheat transporters. While other Al tolerance mechanisms have some support, systems biology approaches are making good progress to describe them more fully. Thus, it is an exciting time to study the mechanisms of Al tolerance and apply this knowledge to crop improvement via marker-assisted breeding and translational genomics.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Aniol A, Gustafson J (1984) Chromosome location of genes controlling aluminum tolerance in wheat, rye and triticale. Can J Genet Cytol 26:701–705

    Google Scholar 

  • Anoop V, Basu U, McCammon M, McAlister-Henn L, Taylor G (2003) Modulation of citrate metabolism alters aluminum tolerance in yeast and transgenic canola overexpressing a mitochondrial citrate synthase. Plant Physiol 132:2205–2217

    CAS  PubMed  Google Scholar 

  • Basu U, Good A, Taylor G (2001) Transgenic Brassica napus plants overexpressing aluminum-induced mitochondrial manganese superoxide dismutase cDNA are resistant to aluminum. Plant Cell Environ 24:1269–1278

    CAS  Google Scholar 

  • Bot AJ, Nachtergaele FO, Young A (eds) (2000) Land resource potential and constraints at regional and country level. F.A.O. Land and Water Development Division, FAO, Rome. http://www.fao.org/AG/agl/agll/terrastat/Cited 31 Jan 2008

  • Cakmak I, Horst WJ (1991) Effect of aluminum on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468

    CAS  Google Scholar 

  • Chaffai R, Marzouk B, El Ferjani E (2005) Aluminum mediates compositional alterations of polar lipid classes in maize seedlings. Phytochemistry 66:1903–1912

    CAS  PubMed  Google Scholar 

  • Christie PJ, Alfenito MR, Walbot V (1994) Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta 194:541–549

    CAS  Google Scholar 

  • Cosgrove DJ (2000) New genes and new biological roles for expansins. Curr Opin Plant Biol 3:73–78

    CAS  PubMed  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    CAS  PubMed  Google Scholar 

  • da Silva AL, Sperling P, Horst WJ, Franke S, Ott C, Becker D, Stass A, Lorz H, Heinz E (2006) A possible role of sphingolipids in the aluminium resistance of yeast and maize. J Plant Physiol 163:26–38

    PubMed  Google Scholar 

  • Davis W, McCauley M, Byers B (1971) Iron requirements and aluminum sensitivity of an hydrocyamic acid-requiring strain of Bacillus megaterium. J Bacteriol 105:589–594

    CAS  PubMed  Google Scholar 

  • de la Fuente J, Ramirez-Rodriguez V, Cabrera-Ponce J, Herrera-Estrella L (1997) Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276:1566–1568

    PubMed  Google Scholar 

  • Degenhardt J, Larsen P, Howell S, Kochian L (1998) Aluminum resistance in the Arabidopsis mutant alr-104 is caused by an aluminum-induced increase in rhizosphere pH. Plant Physiol 117:19–27

    CAS  PubMed  Google Scholar 

  • Delhaize E, Craig S, Beaton CD, Bennet RJ, Jagadish VC, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.): I. Uptake and distribution of aluminum in root apices. Plant Physiol 103:685–693

    CAS  PubMed  Google Scholar 

  • Delhaize E, Hebb D, Richards K, Lin J, Ryan P, Gardner R (1999) Cloning and expression of a wheat (Triticum aestivum L.) phosphatidylserine synthase cDNA. Overexpression in plants alters the composition of phospholipids. J Biol Chem 274:7082–7088

    CAS  PubMed  Google Scholar 

  • Delhaize E, Hebb DM, Ryan PR (2001) Expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux. Plant Physiol 125:2059–2067

    CAS  PubMed  Google Scholar 

  • Delhaize E, Ryan P, Hebb D, Yamamoto Y, Sasaki T, Matsumoto H (2004) Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proc Natl Acad Sci USA 101:15249–15254

    CAS  PubMed  Google Scholar 

  • Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Lett 581:2255–2262

    CAS  PubMed  Google Scholar 

  • Derbyshire P, McCann MC, Roberts K (2007) Restricted cell elongation in Arabidopsis hypocotyls is associated with a reduced average pectin esterification level. BMC Plant Biol 7:31

    PubMed  Google Scholar 

  • Duncan R (1988) Sequential development of acid soil tolerant Sorghum genotypes under field stress conditions. Commun Soil Sci Plant Anal 19:1295–1305

    CAS  Google Scholar 

  • Duncan R, Clark R, Furlani P (1983) Laboratory and field evaluations of Sorghum for response to aluminum and acid soil. Agron J 75:1023–1026

    CAS  Google Scholar 

  • Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144:197–205

    CAS  PubMed  Google Scholar 

  • Eggert D (1970) The use of morin for fluorescent localization of aluminum in plant tissues. Stain Technol 45:301–303

    CAS  PubMed  Google Scholar 

  • Eticha D, Stass A, Horst WJ (2005) Localization of aluminium in the maize root apex: can morin detect cell wall-bound aluminium? J Exp Bot 56:1351–1357

    CAS  PubMed  Google Scholar 

  • Ezaki B, Gardner R, Ezaki Y, Matsumoto H (2000) Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol 122:657–665

    CAS  PubMed  Google Scholar 

  • Fontecha G, Silva-Navas J, Benito C, Mestres MA, Espino FJ, Hernandez-Riquer MV, Gallego FJ (2007) Candidate gene identification of an aluminum-activated organic acid transporter gene at the Alt4 locus for aluminum tolerance in rye (Secale cereale L.). Theor Appl Genet 114:249–260

    CAS  PubMed  Google Scholar 

  • Frey M, Chomet P, Glawischnig E, Stettner C, Grun S, Winklmair A, Eisenreich W, Bacher A, Meeley RB, Briggs SP, Simcox K, Gierl A (1997) Analysis of a chemical plant defense mechanism in grasses. Science 277:696–699

    CAS  PubMed  Google Scholar 

  • Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF (2007) An aluminum-activated citrate transporter in barley. Plant Cell Physiol 48:1081–1091

    CAS  PubMed  Google Scholar 

  • Gabrielson KM, Cancel JD, Morua LF, Larsen PB (2006) Identification of dominant mutations that confer increased aluminium tolerance through mutagenesis of the Al-sensitive Arabidopsis mutant, als3-1. J Exp Bot 57:943–951

    CAS  PubMed  Google Scholar 

  • Guo P, Bai G, Li R, Carver B, Baum M (2007a) Molecular characterization of Atlas66-derived wheat near-isogenic lines contrasting in aluminum tolerance. Agric Sci China 6:522–528

    CAS  Google Scholar 

  • Guo P, Bai G, Carver B, Li R, Bernardo A, Baum M (2007b) Transcriptional analysis between two wheat near-isogenic lines contrasting in aluminum tolerance under aluminum stress. Mol Genet Genomics 277:1–12

    CAS  PubMed  Google Scholar 

  • Hoekenga OA, Vision TJ, Shaff JE, Monforte AJ, Lee GP, Howell SH, Kochian LV (2003) Identification and characterization of aluminum tolerance loci in Arabidopsis (Landsberg erecta x Columbia) by quantitative trait locus mapping. A physiologically simple but genetically complex trait. Plant Physiol 132:936–948

    CAS  PubMed  Google Scholar 

  • Hoekenga OA, Maron LG, Pineros MA, Cancado GM, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, Matsumoto H, Yamamoto Y, Koyama H, Kochian LV (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

    CAS  PubMed  Google Scholar 

  • Ikka T, Kobayashi Y, Iuchi S, Sakurai N, Shibata D, Kobayashi M, Koyama H (2007) Natural variation of Arabidopsis thaliana reveals that aluminum resistance and proton resistance are controlled by different genetic factors. Theor Appl Genet 115:709–719

    CAS  PubMed  Google Scholar 

  • Iuchi S, Koyama H, Iuchi A, Kobayashi Y, Kitabayashi S, Ikka T, Hirayama T, Shinozaki K, Kobayashi M (2007) Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc Natl Acad Sci USA 104:9900–9905

    PubMed  Google Scholar 

  • Jemo M, Abaidoo RC, Nolte C, Horst WJ (2007) Aluminum resistance of cowpea as affected by phosphorus-deficiency stress. J Plant Physiol 164:442–451

    CAS  PubMed  Google Scholar 

  • Jonczyk R, Schmidt H, Osterrieder A, Fiesselmann A, Schullehner K, Haslbeck M, Sicker D, Hofmann D, Yalpani N, Simmons C, Frey M, Gierl A (2008) Elucidation of the final reactions of DIMBOA-glucoside biosynthesis in maize: characterization of Bx6 and Bx7. Plant Physiol 146:1053–1063

    CAS  PubMed  Google Scholar 

  • Jones DL, Blancaflor EB, Kochian LV, Gilroy S (2006) Spatial coordination of aluminium uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots. Plant Cell Environ 29:1309–1318

    CAS  PubMed  Google Scholar 

  • Keurentjes JJ, Fu J, de Vos CH, Lommen A, Hall RD, Bino RJ, van der Plas LH, Jansen RC, Vreugdenhil D, Koornneef M (2006) The genetics of plant metabolism. Nat Genet 38:842–849

    CAS  PubMed  Google Scholar 

  • Kidd P, Llugany M, Poschenrieder C, Gunse B, Barcelo J (2001) The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). J Exp Bot 52:1339–1352

    CAS  PubMed  Google Scholar 

  • Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50:347–363

    CAS  PubMed  Google Scholar 

  • Kimura M, Yamamoto YY, Seki M, Sakurai T, Sato M, Abe T, Yoshida S, Manabe K, Shinozaki K, Matsui M (2003) Identification of Arabidopsis genes regulated by high light-stress using cDNA microarray. Photochem Photobiol 77:226–233

    CAS  PubMed  Google Scholar 

  • Kinraide TB (1991) Identity of the rhizotoxic aluminum species. Plant Soil 134:167–178

    CAS  Google Scholar 

  • Kobayashi Y, Ikka T, Kimura K, Yasuda O, Koyama H (2007a) Characterization of lanthanum toxicity for root growth of Arabidopsis thaliana from the aspect of natural genetic variation. Funct Plant Biol 34:984–994

    CAS  Google Scholar 

  • Kobayashi Y, Hoekenga OA, Itoh H, Nakashima M, Saito S, Shaff JE, Maron LG, Pineros MA, Kochian LV, Koyama H (2007b) Characterization of AtALMT1 expression in aluminum-inducible malate release and its role for rhizotoxic stress tolerance in Arabidopsis. Plant Physiol 145:843–852

    CAS  PubMed  Google Scholar 

  • Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260

    CAS  Google Scholar 

  • Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Physiol Plant Mol Biol 55:459–493

    CAS  Google Scholar 

  • Kovermann P, Meyer S, Hortensteiner S, Picco C, Scholz-Starke J, Ravera S, Lee Y, Martinoia E (2007) The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J 52:1169–1180

    CAS  PubMed  Google Scholar 

  • Larsen PB, Tai CY, Kochian LV, Howell SH (1996) Arabidopsis mutants with increased sensitivity to aluminum. Plant Physiol 110:743–751

    CAS  PubMed  Google Scholar 

  • Li X, Ma J, Matsumoto H (2000) Pattern of aluminum-induced secretion of organic acids differs between rye and wheat. Plant Physiol 123:1537–1544

    CAS  PubMed  Google Scholar 

  • Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA 97:3730–3734

    CAS  PubMed  Google Scholar 

  • Ma J, Hiradate S (2000) Form of aluminium for uptake and translocation in buckwheat (Fagopyrum esculentum Moench). Planta 211:355–360

    CAS  PubMed  Google Scholar 

  • Ma Z, Miyasaka S (1998) Oxalate exudation by taro in response to Al. Plant Physiol 118:861–865

    PubMed  Google Scholar 

  • Ma JF, Taketa S, Yang ZM (2000) Aluminum tolerance genes on the short arm of chromosome 3R are linked to organic acid release in triticale. Plant Physiol 122:687–694

    CAS  PubMed  Google Scholar 

  • Ma J, Ryan P, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278

    CAS  PubMed  Google Scholar 

  • Ma JF, Shen R, Zhao Z, Wissuwa M, Takeuchi Y, Ebitani T, Yano M (2002) Response of rice to Al stress and identification of quantitative trait Loci for Al tolerance. Plant Cell Physiol 43:652–659

    CAS  PubMed  Google Scholar 

  • Ma JF, Shen R, Nagao S, Tanimoto E (2004a) Aluminum targets elongating cells by reducing cell wall extensibility in wheat roots. Plant Cell Physiol 45:583–589

    CAS  PubMed  Google Scholar 

  • Ma JF, Nagao S, Sato K, Ito H, Furukawa J, Takeda K (2004b) Molecular mapping of a gene responsible for Al-activated secretion of citrate in barley. J Exp Bot 55:1335–1341

    CAS  PubMed  Google Scholar 

  • Magalhaes JV (2006) Aluminum tolerance genes are conserved between monocots and dicots. Proc Natl Acad Sci USA 103:9749–9750

    CAS  PubMed  Google Scholar 

  • Magalhaes JV, Garvin DF, Wang Y, Sorrells ME, Klein PE, Schaffert RE, Li L, Kochian LV (2004) Comparative mapping of a major aluminum tolerance gene in Sorghum and other species in the Poaceae. Genetics 167:1905–1914

    CAS  PubMed  Google Scholar 

  • Magalhaes JV, Liu J, Guimaraes CT, Lana UG, Alves VM, Wang YH, Schaffert RE, Hoekenga OA, Pineros MA, Shaff JE, Klein PE, Carneiro NP, Coelho CM, Trick HN, Kochian LV (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in Sorghum. Nat Genet 39:1156–1161

    CAS  PubMed  Google Scholar 

  • Meyers BC, Lee DK, Vu TH, Tej SS, Edberg SB, Matvienko M, Tindell LD (2004) Arabidopsis MPSS. An online resource for quantitative expression analysis. Plant Physiol 135:801–813

    CAS  PubMed  Google Scholar 

  • Minella E, Sorrells ME (1997) Inheritance and chromosome location of Alp, a gene controlling aluminum tolerance in ‘Dayton’ barley. Plant Breed 116:465–469

    CAS  Google Scholar 

  • Morita A, Horie H, Fujii Y, Takatsu S, Watanabe N, Yagi A, Yokota H (2004) Chemical forms of aluminum in xylem sap of tea plants (Camellia sinensis L.). Phytochemistry 65:2775–2780

    CAS  PubMed  Google Scholar 

  • Morita A, Yanagisawa O, Takatsu S, Maeda S, Hiradate S (2008) Mechanism for the detoxification of aluminum in roots of tea plant (Camellia sinensis (L.) Kuntze). Phytochemistry 69:147–153

    CAS  PubMed  Google Scholar 

  • Nagata T, Hayatsu M, Kosuge N (1992) Identification of aluminum forms in tea leaves by 27Al NMR. Phytochemistry 31:1215–1218

    CAS  Google Scholar 

  • NASS (ed) (2007) Agricultural Statistics U.S.D.A. National Agricultural Statistics Service. US Government Printing Office, Washington DC. http://www.nass.usda.gov/Publications/Ag_Statistics/2007/CHAP01.PDF Cited 31 Jan 2008

  • Osawa H, Matsumoto H (2001) Possible involvement of protein phosphorylation in aluminum-responsive malate efflux from wheat root apex. Plant Physiol 126:411–420

    CAS  PubMed  Google Scholar 

  • Papernik L, Bethea A, Singleton T, Magalhaes J, Garvin D, Kochian L (2001) Physiological basis of reduced Al tolerance in ditelosomic lines of Chinese Spring wheat. Planta 212:829–834

    CAS  PubMed  Google Scholar 

  • Park WJ, Schafer A, Prinsen E, van Onckelen H, Kang BG, Hertel R (2001) Auxin-induced elongation of short maize coleoptile segments is supported by 2, 4-dihydroxy-7-methoxy-1, 4-benzoxazin-3-one. Planta 213:92–100

    CAS  PubMed  Google Scholar 

  • Pellet D, Papernik L, Kochian L (1996) Multiple aluminum-resistance mechanisms in wheat. Roles of root apical phosphate and malate exudation. Plant Physiol 112:591–597

    CAS  PubMed  Google Scholar 

  • Pineros MA, Shaff JE, Manslank HS, Alves VM, Kochian LV (2005) Aluminum resistance in maize cannot be solely explained by root organic acid exudation. A comparative physiological study. Plant Physiol 137:231–241

    CAS  PubMed  Google Scholar 

  • Poschenrieder C, Llugany M, Barcelo J (1995) Short-term effects of pH and aluminium on mineral nutrition in maize varieties differing in proton and aluminium tolerance. J Plant Nutr 18:1495–1507

    CAS  Google Scholar 

  • Poschenrieder C, Tolra RP, Barcelo J (2005) A role for cyclic hydroxamates in aluminium resistance in maize? J Inorg Biochem 99:1830–1836

    CAS  PubMed  Google Scholar 

  • Raman H, Moroni JS, Sato K, Read BJ, Scott BJ (2002) Identification of AFLP and microsatellite markers linked with an aluminium tolerance gene in barley (Hordeum vulgare L.). Theor Appl Genet 105:458–464

    CAS  PubMed  Google Scholar 

  • Raman H, Zhang K, Cakir M, Appels R, Garvin DF, Maron LG, Kochian LV, Moroni JS, Raman R, Imtiaz M, Drake-Brockman F, Waters I, Martin P, Sasaki T, Yamamoto Y, Matsumoto H, Hebb DM, Delhaize E, Ryan PR (2005) Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). Genome 48:781–791

    CAS  PubMed  Google Scholar 

  • Raman H, Ryan PR, Raman R, Stodart BJ, Zhang K, Martin P, Wood R, Sasaki T, Yamamoto Y, Mackay M, Hebb DM, Delhaize E (2007) Analysis of TaALMT1 traces the transmission of aluminum resistance in cultivated common wheat (Triticum aestivum L.). Theor Appl Genet 116:343–354

    PubMed  Google Scholar 

  • Richards K, Schott E, Sharma Y, Davis K, Gardner R (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116:409–418

    CAS  PubMed  Google Scholar 

  • Rogers SA (1986) Methods of evaluation and inheritance of aluminum tolerance in Sorghum. Ph.D. dissertation. Department of Agronomy, Mississippi State University, p 61

    Google Scholar 

  • Ryan PR, Delhaize E, Randall PJ (1995) Malate efflux from root apices and tolerance to aluminum are highly correlated in wheat. Aust J Plant Physiol 22:531–536

    CAS  Google Scholar 

  • Ryan PR, Liu Q, Sperling P, Dong B, Franke S, Delhaize E (2007) A higher plant {delta}8 sphingolipid desaturase with a preference for (z)-isomer formation confers aluminum tolerance to yeast and plants. Plant Physiol 144:1968–1977

    CAS  PubMed  Google Scholar 

  • Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:645–653

    CAS  PubMed  Google Scholar 

  • Sasaki T, Ryan PR, Delhaize E, Hebb DM, Ogihara Y, Kawaura K, Noda K, Kojima T, Toyoda A, Matsumoto H, Yamamoto Y (2006) Sequence upstream of the wheat (Triticum aestivum L.) ALMT1 gene and its relationship to aluminum resistance. Plant Cell Physiol 47:1343–1354

    CAS  PubMed  Google Scholar 

  • Shen R, Ma J, Kyo M, Iwashita T (2002) Compartmentation of aluminium in leaves of an Al-accumulator, Fagopyrum esculentum Moench. Planta 215:394–398

    CAS  PubMed  Google Scholar 

  • Silva I, Smyth T, Raper C, Carter T, Rufty T (2001) Differential aluminum tolerance in soybean: an evaluation of the role of organic acids. Physiol Plant 112:200–210

    CAS  PubMed  Google Scholar 

  • Sivaguru M, Ezaki B, He ZH, Tong H, Osawa H, Baluska F, Volkmann D, Matsumoto H (2003) Aluminum-induced gene expression and protein localization of a cell wall-associated receptor kinase in Arabidopsis. Plant Physiol 132:2256–2266

    CAS  PubMed  Google Scholar 

  • Snowden K, Gardner R (1993) Five genes induced by aluminum in wheat (Triticum aestivum L.) roots. Plant Physiol 103:855–861

    CAS  PubMed  Google Scholar 

  • Szalma SJ, Snook ME, Bushman BS, Houchins K, McMullen MD (2002) Duplicate loci as QTL: the role of chalcone synthase loci in flavone and phenylpropanoid biosynthesis in maize. Crop Sci 42:1679–1687

    CAS  Google Scholar 

  • Takeda K, Yamashita T, Takahashi A, Timberlake C (1990) Stable blue complexes of anthocyanin-aluminium-3-p-coumaroyl- or 3-caffeoyl-quinic acid involved in the blueing of Hydrangea flower. Phytochem 29:1089–1191

    CAS  Google Scholar 

  • Tang Y, Sorrells M, Kochian L, Garvin D (2000) Identification of RFLP markers linked to barley aluminum tolerance gene Alp. Crop Sci 40:778–782

    CAS  Google Scholar 

  • Tang Y, Garvin DF, Kochian LV, Sorrells ME, Carver BF (2002) Physiological genetics of aluminum tolerance in the wheat cultivar Atlas 66. Crop Sci 42:1541–1546

    Google Scholar 

  • Tesfaye M, Temple S, Allan D, Vance C, Samac D (2001) Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum. Plant Physiol 127:1836–1844

    CAS  PubMed  Google Scholar 

  • Wang Y, Stass A, Horst WJ (2004) Apoplastic binding of aluminum is involved in silicon-induced amelioration of aluminum toxicity in maize. Plant Physiol 136:3762–3770

    CAS  PubMed  Google Scholar 

  • Wang JP, Raman H, Zhang GP, Mendham N, Zhou MX (2006) Aluminium tolerance in barley (Hordeum vulgare L.): physiological mechanisms, genetics and screening methods. J Zhejiang Univ Sci 7:769–787

    CAS  Google Scholar 

  • Wang J, Raman H, Zhou M, Ryan PR, Delhaize E, Hebb DM, Coombes N, Mendham N (2007) High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminium tolerance in barley (Hordeum vulgare L.). Theor Appl Genet 115:265–276

    CAS  PubMed  Google Scholar 

  • Watanabe T, Osaki M (2002) Mechanisms of adaptation to high aluminum condition in native plant species growing in acid soils: a review. Commun Soil Sci Plant Anal 33:1247–1260

    CAS  Google Scholar 

  • Wenzl P, Patino G, Chaves A, Mayer J, Rao I (2001) The high level of aluminum resistance in signalgrass is not associated with known mechanisms of external aluminum detoxification in root apices. Plant Physiol 125:1473–1484

    CAS  PubMed  Google Scholar 

  • Wenzl P, Chaves A, Patino G, Mayer J, Rao I, Zhang W, Rengel Z (2002) Aluminum stress stimulates the accumulation of organic acids in root apices of Brachiaria species. J Plant Nutr Soil Sci 165:582–588

    CAS  Google Scholar 

  • Yamaguchi M, Sasaki T, Sivaguru M, Yamamoto Y, Osawa H, Ahn SJ, Matsumoto H (2005) Evidence for the plasma membrane localization of Al-activated malate transporter (ALMT1). Plant Cell Physiol 46:812–816

    CAS  PubMed  Google Scholar 

  • Yamamoto Y, Kobayashi Y, Matsumoto H (2001) Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol 125:199–208

    CAS  PubMed  Google Scholar 

  • Yang Q, Wang Y, Zhang J, Shi W, Qian C, Peng X (2007) Identification of aluminum-responsive proteins in rice roots by a proteomic approach: cysteine synthase as a key player in Al response. Proteomics 7:737–749

    CAS  PubMed  Google Scholar 

  • Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146:602–611

    CAS  PubMed  Google Scholar 

  • Zakir Hossain AK, Koyama H, Hara T (2006) Growth and cell wall properties of two wheat cultivars differing in their sensitivity to aluminum stress. J Plant Physiol 163:39–47

    CAS  PubMed  Google Scholar 

  • Zhang J, He Z, Tian H, Zhu G, Peng X (2007) Identification of aluminium-responsive genes in rice cultivars with different aluminium sensitivities. J Exp Bot 58:2269–2278

    CAS  PubMed  Google Scholar 

  • Zhao Z, Ma JF, Sato K, Takeda K (2003) Differential Al resistance and citrate secretion in barley (Hordeum vulgare L.). Planta 217:794–800

    CAS  PubMed  Google Scholar 

  • Zheng S, Ma J, Matsumoto H (1998a) High aluminum resistance in buckwheat: I. Al-induced specific secretion of oxalic acid from root tips. Plant Physiol 117:745–751

    Google Scholar 

  • Zheng S, Ma J, Matsumoto H (1998b) Continuous secretion of organic acids is related to aluminum resistance during relatively long-term exposure to aluminum stress. Physiol Plant 103:209–214

    CAS  Google Scholar 

  • Zhu JK (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4:401–406

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Owen A. Hoekenga .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Berlin Heidelberg

About this chapter

Cite this chapter

Hoekenga, O.A., Magalhaes, J.V. (2011). Mechanisms of Aluminum Tolerance. In: Costa de Oliveira, A., Varshney, R. (eds) Root Genomics. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-85546-0_6

Download citation

Publish with us

Policies and ethics