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Plant improvement for tolerance to aluminum in acid soils – a review

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Abstract

Development of acid soils that limit crop production is an increasing problem worldwide. Many factors contribute to phytotoxicity of these soils, however, in acid soils with a high mineral content, aluminum (Al) is the major cause of toxicity. The target of Al toxicity is the root tip, in which Al exposure causes inhibition of cell elongation and cell division, leading to root stunting accompanied by reduced water and nutrient uptake. Natural variation for Al tolerance has been identified in many crop species and in some crops tolerance to Al has been introduced into productive, well-adapted varieties. Aluminum tolerance appears to be a complex multigenic trait. Selection methodology remains a limiting factor in variety development as all methods have particular drawbacks. Molecular markers have been associated with Al tolerance genes or quantitative trait loci in Arabidopsis and in several crops, which should facilitate development of additional tolerant varieties. A variety of genes have been identified that are induced or repressed upon Al exposure. Most induced genes characterized so far are not specific to Al exposure but are also induced by other stress conditions. Ectopic over-expression of some of these genes has resulted in enhanced Al tolerance. Additionally, expression of genes involved in organic acid synthesis has resulted in enhanced production of organic acids and an associated increase in Al tolerance. This review summarizes the three main approaches that have been taken to develop crops with Al tolerance: recurrent selection and breeding, development of Al tolerant somaclonal variants and ectopic expression of transgenes to reduce Al uptake or limit damage to cells by Al.

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References

  • Archambault DJ, Zhang G & Taylor GJ (1996) Accumulation of Al in root mucilage of an Al-resistant and an Al-sensitive cultivar of wheat. Plant Physiol. 112: 1471–1478

    Google Scholar 

  • Archambault DJ, Zhang GC & Taylor GJ (1997) Spatial variation in the kinetics of aluminium (Al) uptake in roots of wheat (Triticum aestivum L.) exhibiting differential resistance to Al-Evidence for metabolism-dependent exclusion of Al. J. Plant Physiol. 151: 668–674

    Google Scholar 

  • Arihara A, Kumagai R, Koyama H & Ojima K (1991) Aluminum-tolerance of carrot (Daucus carota L.) plants regenerated from selected cell cultures. Soil Sci. Plant Nutr. 37: 699–705

    Google Scholar 

  • Baligar VC, Elgin JH & Foy CD (1989) Variability in alfalfa for growth and mineral uptake and efficiency ratios under aluminum stress. Agron. J. 81: 223–229

    Google Scholar 

  • Barceló J & 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

    Google Scholar 

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

    Google Scholar 

  • Basu U, Good AG, Aung T, Slaski J, Basu A, Briggs KG & Taylor GJ (1999) A 23-kDa root exudate polypeptide co-segregates with aluminum resistance in Triticum aestivum. Physiol. Plant 106: 53–61

    Google Scholar 

  • Bianchi-Hall CM, Carter TE Jr., Bailey MA, Mian MAR, Rufty TW, Ashley DA, Boerma HR, Arellano C, Hussey RS & Parrot WA (2000) Aluminum tolerance associated with quantitative trait loci derived from soybean PI 416937 in hydroponics. Crop Sci. 40: 538–545

    Google Scholar 

  • Bianchi-Hall CM, Carter TE Jr., Rufty TW, Arellano C, Boerma HR, Ashley DA & Burton JW (1998) Heritability and resource allocation of aluminum tolerance derived from soybean PI 416937. Crop Sci. 38: 513–522

    Google Scholar 

  • Blamey FPC, Ostatek-Boczynski Z & Kerven GL (1997) Ligand effects on aluminium sorption by calcium pectate. Plant Soil 192: 269–275

    Google Scholar 

  • Blancaflor EB, Jones DL & Gilroy S (1998) Alterations in the cytoskeleton accompany aluminum-induced growth inhibition and morphological changes in primary roots of maize. Plant Physiol. 118: 159–172

    Google Scholar 

  • Bolan NS, Hedley MJ & White RE (1991) Processes of soil acidification during nitrogen cycling with emphasis on legume based pastures. Plant Soil 134: 53–63

    Google Scholar 

  • Bona L & Carver BF (1998) A proposed scale for quantifying aluminum tolerance level in wheat and barley detected by hematoxylin staining. Cereal Res. Commun. 26: 97–99

    Google Scholar 

  • Bouton JH (1996) Screening the alfalfa core collection for acid soil tolerance. Crop Sci. 36: 198–2000

    Google Scholar 

  • Bouton JH & Sumner ME (1983) Alfalfa, Medicago sativa L., in highly weathered, acid soils. V. Field Performance of alfalfa selected for acid tolerance. Plant Soil 74: 431–436

    Google Scholar 

  • Camargo CEdeO, Neto AT, Filho WPF & Felicio JC (2000) Genetic control of aluminum tolerance in mutant lines of the wheat cultivar Anahuac. Euphytica 114: 47–53

    Google Scholar 

  • Canaado GMA, Loguercio LL, Martins PR, Parentoni SN, Paiva E, Borém A & Lopes MA (1999) Hematoxylin staining as a phenotypic index for aluminum tolerance selection in tropical maize (Zea mays L.). Theor. Appl. Genet. 99: 747–754

    Google Scholar 

  • Carver BF & Ownby JD (1995) Acid soil tolerance in wheat. Adv. Agron. 54: 117–173

    Google Scholar 

  • Čiamporová M (2002) Morphological and structural responses of plant roots to aluminium at organ, tissue and cellular levels. Biol. Plant. 45: 161–171

    Google Scholar 

  • Conner AJ & Meredith CP (1985a) Simulating the mineral environ-ment of aluminium toxic soils in plant cell culture. J. Exp. Bot. 36: 870–880

    Google Scholar 

  • Conner AJ & Meredith CP (1985b) Large scale selection of aluminum-resistant mutants from plant cell cultures: expression and inheritance in seedlings. Theor. Appl. Genet. 71: 159–165

    Google Scholar 

  • -glucanase and a fimbrin-like cytoskeletal protein are induced by Al toxicity in wheat roots. Plant Physiol. 114: 1453–1460

    Google Scholar 

  • Dall'Agnol M, Bouton JH & Parrott WA (1996) Screening methods to develop alfalfa germplasms tolerant of acid, aluminum toxic soils. Crop Sci. 36: 64–70

    Google Scholar 

  • de la Fuente-Martínez JM & Herrera-Estrella L (1999) Advances in the understanding of aluminum toxicity and the development of aluminum-tolerant transgenic plants. Adv. Agron. 66: 103–120

    Google Scholar 

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

    Google Scholar 

  • Degenhardt J, Larsen PB, Howell SH & Kochian L (1998) Aluminum resistance in the Arabidopsis mutant alr-104 is caused by an aluminum increase in rhizosphere pH. Plant Phy-siol. 117: 19–27

    Google Scholar 

  • Delhaize E & Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol. 107: 315–321

    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

    Google Scholar 

  • Delhaize E, Hebb DM, Richards KD, Lin J-M, Ryan PR & Gardner RC (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

    Google Scholar 

  • Delhaize E, Hebb DM & Ryan PP (2001) Expression of a Pseudo-monas aeruginosa citrate synthase gene in tobacco is not associ-ated with either enhanced citrate accumulation or efflux. Plant Physiol. 125: 2059–2067

    Google Scholar 

  • Delhaize E, Ryan PR, Hocking PJ & Richardson AE (2003) Effects of altered citrate synthase and isocitrate dehydrogenase expression on internal citrate concentrations and citrate efflux from tobacco (Nicotiana tabacum L.) roots. Plant Soil 248: 137–144

    Google Scholar 

  • Delisle G, Champoux M & Houde M (2001) Characterization of oxalate oxidase and cell death in Al-sensitive and tolerant wheat roots. Plant Cell Physiol. 42: 324–333

    Google Scholar 

  • Devine TE, Foy CD, Fleming AL, Hanson CH, Campbell TA, McMurtrey JE & Schwartz JW (1976) Development of alfalfa strains with differential tolerance to aluminum toxicity. Plant Soil 44: 73–79

    Google Scholar 

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

    Google Scholar 

  • Ezaki B, Katsuhara M, Kawamura M & Matsumoto H (2001) Different mechanisms of four aluminum (Al)-resistant transgenes for Al toxicity in Arabidopsis. Plant Physiol. 127: 918–927

    Google Scholar 

  • Foy CD (1996a) Tolerance of barley cultivars to an acid, aluminum-toxic subsoil related to mineral element concentrations in their shoots. J. Plant Nutr. 19: 1361–1380

    Google Scholar 

  • Foy CD (1996b) Tolerance of durum wheat lines to an acid, aluminum-toxic subsoil. J. Plant Nutr. 19: 1381–1394

    Google Scholar 

  • Foy CD & Murray JJ (1998) Developing aluminum-tolerant strains of tall fescue for acid soils. J. Plant Nutr. 21: 1301–1325

    Google Scholar 

  • Foy CD, Duke JA & Devine TE (1992) Tolerance of soybean germplasm to an acid tatum subsoil. J. Plant Nutr. 15: 527–547

    Google Scholar 

  • Foy CD, Duncan RR, Waskon RM & Miller DR (1993) Tolerance of sorghum genotypes to an acid, aluminum toxic tatum subsoil. J. Plant Nutr. 161: 97–127

    Google Scholar 

  • Garvin DF & Carver BF (2003) Role of the genotype in tolerance to acidity and aluminum toxicity. In: Rengel Z (ed) Handbook of Soil Acidity (pp. 387–407). Marcel Dekker Inc, New York

    Google Scholar 

  • Gaume A, Mächler F & Frossard E (2001) Aluminum resistance in two cultivars of Zea mays L.: Root exudation of organic acids and influence of phosphorus nutrition. Plant Soil 234: 73–81

    Google Scholar 

  • Giaveno CD & Miranda JB (2000) Rapid screening for aluminum tolerance in maize (Zea mays L.). Genet. Mol. Biol. 23: 847–850

    Google Scholar 

  • Hamel F, Breton C & Houde M (1998) Isolation and characteriza-tion of wheat aluminum-regulated genes: possible involvement of aluminum as a pathogenesis response elicitor. Planta 205: 531–538

    Google Scholar 

  • Hartel PG & Bouton JH (1989) Rhizobium meliloti inoculation of alfalfa selected for tolerance to acid, aluminum-rich soils. Plant Soil 116: 283–285

    Google Scholar 

  • Haynes RJ (1983) Soil acidification induced by leguminous crops. Grass Forage Res. 38: 1–11

    Google Scholar 

  • Haynes RJ & Mokolobate MS (2001) Amelioration of Al toxicity and P deficiency in acid soils by additions of organic residues: a critical review of the phenomenon and the mechanisms involved. Nut. Cycl. Agroecosys. 59: 47–63

    Google Scholar 

  • Henderson M & Ownby JD (1991) The role of root cap mucilage secretion in aluminum tolerance in wheat. Curr. Topics Plant Biochem. Physiol. 10: 134–141

    Google Scholar 

  • Horst WJ, Wager A & Marshner H (1982) Mucilage protects root meristems from aluminium injury. Z. Pflanzenphysiol. 105: 435–444

    Google Scholar 

  • Horst WJ, Schmohl N, Kollmeier M, Baluska F & Sivaguru M (1999) Does aluminium affect root growth of maize through interaction with the cell wall-plasma membrane-cytoskeleton continuum? Plant Soil 215: 163–174

    Google Scholar 

  • Howeler RH (1991) Identifying plants adaptable to low pH con-ditions. In: Wright RJ, Baligar VC & Murrmann RP (eds) Plant- Soil Interactions at Low pH (pp. 885–904). Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Huang JW, Grunes DL & Kochian LV (1995) Aluminium and calcium transport interactions in intact roots and root plasmalem-ma vesicles from aluminium-sensitive and tolerant wheat cul-tivars. Plant Soil 171: 131–135

    Google Scholar 

  • Hue NV, Craddock GR & Adams F (1986) Effect of organic acids on aluminum toxicity in subsoil. Soil Sci. Soc. Am. J. 50: 28–34

    Google Scholar 

  • Jensen S, Broadley MR, Robbrecht W & Smets E (2002) Aluminum hyperaccumulation in angiosperms: a review of its phylogenetic significance. Bot. Rev. 68: 235–269

    Google Scholar 

  • Johnson JP, Carver BF & Baligar VC (1997) Productivity in Great Plains acid soils of wheat genotypes selected for aluminium tolerance. Plant Soil 188: 101–106

    Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere - a critical review. Plant Soil 205: 25–44

    Google Scholar 

  • Jones DL & Kochian LV (1995) Aluminum inhibition of the inositol 1,4,5-triphosphate signal transduction pathway in wheat roots: a role in aluminum toxicity? Plant Cell 7: 1913–1922

    Google Scholar 

  • Jones DL, Gilroy S, Larsen PB, Howell SH & Kochian LV (1998) Effect of aluminum on cytoplasmic Ca2+ homeostasis in root hairs of Arabidopsis thaliana (L.). Planta 206: 378–387

    Google Scholar 

  • Kaneko M, Yoshimura E & Nishizawa NK (1999) Time course study of aluminum-induced callose formation in barley roots as observed by digital microscopy and low-vacuum scanning electron microscopy. Soil Sci. Plant Nut. 45: 701–712

    Google Scholar 

  • Kataoka T & Nakanishi TM (2001) Aluminium distribution in soybean root tip for a short time Al treatment. J. Plant Physiol. 158: 731–736

    Google Scholar 

  • Khatiwada SP, Senadhira D, Carpena AL, Zeigler SR & Fernandez PG (1996) Variability and genetics of tolerance for aluminium toxicity in rice (Oryza sativa L.). Theor. Appl. Genet. 93: 738–744

    Google Scholar 

  • Kidd PS & Proctor J (2001) Why plants grow poorly on very acid soils: are ecologists missing the obvious? J. Exp. Bot. 52: 791–799

    Google Scholar 

  • Kim BY, Baier AC, Somers DJ & Gustafson JP (2001) Aluminum tolerance in triticale, wheat and rye. Euphytica 120: 329–337

    Google Scholar 

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

    Google Scholar 

  • Kinraide TB & Sweeney BK (2001) Buffered, phosphate-con-taining media suitable for aluminum toxicity studies. Plant Soil 235: 75–83

    Google Scholar 

  • Kobayashi Y & Koyama H (2002) QTL analysis of Al tolerance in recombinant inbred lines of Arabidopsis thaliana. Plant Cell Physiol. 43: 1526–1533

    Google Scholar 

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

    Google Scholar 

  • Kochian LV & Jones DL (1997) Aluminum toxicity and resistance in plants. In: Yokel RA & Golub MS (eds) Research Issues in Aluminum Toxicity (pp. 69–89). Taylor and Francis Publishers, Washington, DC

    Google Scholar 

  • Kochian LV, Pence NS, Letham LD, Pineros MA, Magalhaes JV, Hoekenga OA & Garvin DF (2002) Mechanisms of metal resistance in plants: aluminum and heavy metals. Plant Soil 247: 109–119

    Google Scholar 

  • Kollmeier M, Felle HH & Horst WJ (2000) 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? Plant Physiol. 122: 945–956

    Google Scholar 

  • Koyama H, Okawara R, Ojima K & Yamaya T (1988) Re-evalua-tion of characteristics of a carrot cell line previously selected as aluminum-tolerant cells. Physiol. Plant 74: 683–687

    Google Scholar 

  • Koyama H, Toda T, Yokota S, Dawair Z & Hara T (1995) Effects of aluminum and pH on root growth and cell viability in Arabidopsis thaliana strain Landsberg in hydroponic culture. Plant Cell Physiol. 36: 201–205

    Google Scholar 

  • Koyama H, Kawamura A, Kihara T, Hara T, Takita E & Shibata D (2000) Overexpression of mitochondrial citrate synthase in Arabidopsis thaliana improved growth on a phosphorus-limited soil. Plant Cell Physiol. 41: 1030–1037

    Google Scholar 

  • Larsen PB, Tai C-Y, Kochian L & Howell SH (1996) Arabidopsis mutants with increased sensitivity to aluminum. Plant Physiol. 110: 743–751

    Google Scholar 

  • Larsen PB, Stenzle LM, Tai C-Y, Degenhardt J, Howell SH & Kochian L (1997) Molecular and physiological analysis of Arabidopsis mutants exhibiting altered sensitivities to aluminum. Plant Soil 192: 3–7

    Google Scholar 

  • Lazof DB & Holland MJ (1999) Evaluation of the aluminium-induced root growth inhibition in isolation from low pH effects in Glycine max, Pisum sativum and Phaseolus vulgaris. Aust. J. Plant Physiol. 26: 147–157

    Google Scholar 

  • Lazof DB, Goldsmith JG, Rufty TW & Linton RW (1996) The early entry of Al into cells of intact soybean roots. A comparison of three developmental root regions using secondary ion mass spectrometry imaging. Plant Physiol. 112: 1289–1300

    Google Scholar 

  • Li XF, Ma JF, Hiradate S & Matsumoto H (2000) Mucilage strongly binds aluminum but does not prevent roots from aluminum injury in Zea mays. Physiol. Plant. 108: 152–160

    Google Scholar 

  • Liu K & Luan S (2001) Internal aluminum block of plant inward K+ channels. Plant Cell 13: 1453–1465

    Google Scholar 

  • López-Bucio J, Nieto-Jacobo MF, Ramírez-Rodríguez V & Herrera-Estrella L (2000) Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Sci. 160: 1–13

    Google Scholar 

  • Luo HM, Watanabe T, Shinano T & Tadano T (1999) Comparison of aluminum tolerance and phosphate absorption between rape (Brassica napus L.) and tomato (Lycopersicum esculentum Mill.) in relation to organic acid exudation. Soil Sci. Plant Nutr. 45: 897–907

    Google Scholar 

  • Ma JF (2000) Role of organic acids in detoxification of aluminum in higher plants. Plant Cell Physiol. 41: 383–390

    Google Scholar 

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

    Google Scholar 

  • Ma JF, Hiradate S & Matsumoto H (1998) High aluminum resistance in buckwheat. II. Oxalic acid detoxifies aluminum internally. Plant Physiol. 117: 753–759

    Google Scholar 

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

    Google Scholar 

  • Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int. Rev. Cytol. 200: 1–46

    Google Scholar 

  • Meredith CP (1978) Response of cultured tomato cells to aluminum. Plant Sci. Lett. 12: 17–24

    Google Scholar 

  • Miller DR, Waskom RM, Duncan RR, Chapman PL, Brick MA, Hanning GE, Timm DA & Nabors MW (1992) Acid soil stress tolerance in tissue culture-derived sorghum lines. Crop Sci. 32: 324–327

    Google Scholar 

  • Miller SS, Driscoll BT, Gregerson RG, Gantt JS & Vance CP (1998) Alfalfa malate dehydrogenase (MDH): molecular cloning and characterization of five different forms reveals a unique nodule-enhanced MDH. Plant J. 15: 173–184

    Google Scholar 

  • Minnella E & Sorrells ME (1992) Aluminum tolerance in barley: genetic relationships among genotypes of diverse origin. Crop Sci. 32: 593–598

    Google Scholar 

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

    Google Scholar 

  • Moon DH, Ottoboni LMM, Souza AP, Sibov ST, Gaspar M & Arruda P (1997) Somaclonal-variation-induced aluminum-sensi-tive mutant from an aluminum-inbred maize tolerant line. Plant Cell Rep. 16: 686–691

    Google Scholar 

  • Murphy A & Taiz L (1995) A new vertical mesh transfer technique for metal-tolerance studies in Arabidopsis. Plant Physiol. 108: 29–38

    Google Scholar 

  • Nguyen VT, Burow MD, Nguyen HT, Le BT, Le TD & Paterson AH (2001) Molecular mapping of genes conferring aluminum tolerance in rice (Oryza sativa L.). Theor. Appl. Genet. 102: 1002–1010

    Google Scholar 

  • Paliwal K., Sivaguru M. and Thiruselvi (1994) Identification of an aluminum tolerant tropical cowpea cultivar by growth and biomass accumulation parameters. J. Plant Nutr. 17: 367–376

    Google Scholar 

  • Parrot WA & Bouton JH (1990) Aluminum tolerance in alfalfa as expressed in tissue culture. Crop Sci. 30: 387–389

    Google Scholar 

  • Pellet DM, Grunes DL & Kochian LV (1995) Organic acid exuda-tion as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196: 788–795

    Google Scholar 

  • Pellet DM, Papernick LA, Jones DL, Darrah PR, Grunes DL & Kochian LV (1997) Involvement of multiple aluminium exclu-sion mechanisms in aluminium tolerance in wheat. Plant Soil 192: 63–68

    Google Scholar 

  • Piñeros MA & Kochian LV (2001) A patch-clamp study of the physiology of aluminum toxicity and aluminum tolerance in maize. Identification and characterization of Al3+-induced anion channels. Plant Physiol. 125: 292–305

    Google Scholar 

  • Piñeros MA, Magalhaes JV, Carvalho Alves VM & Kochian LV (2002) The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation in maize. Plant Physiol. 129: 1194–1206

    Google Scholar 

  • Plieth C, Sattelmacher B, Hansen UP & Knight MR (1999) Low-pH-mediated elevations in cytosolic calcium are inhibited by aluminum: A potential mechanism for aluminum toxicity. Plant J. 18: 643–650

    Google Scholar 

  • Ramgareeb S, Watt MP, Marsh C & Cooke JA (1999) Assessment of Al3+ availability in callus culture media for screening tolerant genotypes of Cynodon dactylon. Plant Cell Tiss. Org. Cult. 56: 65–68

    Google Scholar 

  • Rengel Z & Reid RJ (1997) Uptake of Al across the plasma membrane of plant cells. Plant Soil 192: 31–35

    Google Scholar 

  • Richards KD, Snowden KC & Gardner RC (1994) Wali6 and wali7: genes induced by aluminum in wheat (Triticum aestivum L.) roots. Plant Physiol. 105: 1455–1456

    Google Scholar 

  • Richards KD, Schott EJ, Sharma YK, Davis KR & Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol. 116: 409–418

    Google Scholar 

  • Riede CR & Anderson JA (1996) Linkage of RFLP markers to an aluminum tolerance gene in wheat. Crop Sci. 36: 905–909

    Google Scholar 

  • Rodriguez Milla MAR, Butler E, Huete AR, Wilson CF, Anderson O & Gustafson JP (2002) Expressed sequenced tag-based gene expression analysis under aluminum stress in rye. Plant Physiol. 130: 1706–1716

    Google Scholar 

  • Rout GR, Samantaray S & Das P (2001) Aluminium toxicity in plants: a review. Agronomie 21: 2–21

    Google Scholar 

  • Ryan PR, Ditomaso JM & Kochian LV (1993) Aluminum toxicity in roots: An investigation of spatial sensitivity and the role of the root cap. J. Exp. Bot. 44: 437–446

    Google Scholar 

  • Ryan PR, Delhaize E & Randall PJ (1995) Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196: 103–110

    Google Scholar 

  • Ryan PR, Reid RJ & Smith FA (1997) Direct evaluation of the Ca2+-displacement hypothesis for Al toxicity. Plant Physiol. 113: 1351–1357

    Google Scholar 

  • 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

    Google Scholar 

  • Sasaki M, Kasai M, Yamamoto Y & Matsumoto H (1995) Involvement of plasma membrane potential in the tolerance mechanism of plant roots to aluminium toxicity. Plant Soil 171: 119–124

    Google Scholar 

  • Sibov ST, Gaspar M, Silva MJ, Ottoboni LMM, Arruda P & Souza AP (1999) Two genes control aluminum tolerance in maize: genetic and molecular mapping analyses. Genome 42: 475–482

    Google Scholar 

  • Silva IR, Smyth TJ, Moxley DF, Carter TE, Allen NS & Rufty TW (2000) Aluminum accumulation at nuclei of cells in the root tip. Fluorescence detection using lumogallion and confocal laser scanning microscopy. Plant Physiol. 124: 543–552

    Google Scholar 

  • Sivaguru M & Horst WJ (1998) The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize. Plant Physiol. 116: 155–163

    Google Scholar 

  • Sivaguru M & Paliwal K (1993) Differential aluminum tolerance in some tropical rice cultivars: I. Growth performance. J. Plant Nutr. 16: 1705–1716

    Google Scholar 

  • Sivaguru M, Baluska F, Volkmann D, Felle HH & Horst WJ (1999) Impacts of aluminum on the cytoskeleton of the maize root apex. Short-term effects on the distal part of the transition zone. Plant Physiol. 119: 1073–1082

    Google Scholar 

  • Sivaguru M, Fujiwara T, Samaj J, Baluska F, Yang Z, Osawa H, Maeda T, Mori T, Volkman D & Matsumoto H (2000) Aluminum-induced 1-3-?-D-glucan inhibits cell-to-cell traffick-ing of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiol. 124: 991–1005

    Google Scholar 

  • Sledge MK, Bouton JH, Dall'Agnoll M, Parrott WA & Kocher G (2002) Identification and confirmation of aluminum tolerance QTL in diploid Medicago sativa subsp. coerulea. Crop Sci. 42: 1121–1128

    Google Scholar 

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

    Google Scholar 

  • Snowden KC, Richards KD & Gardner RC (1995) Aluminum-induced genes: Induction by toxic metals, low calcium and wounding and pattern of expression in root tips. Plant Physiol. 107: 341–348

    Google Scholar 

  • Stolen O & Andersen S (1978) Inheritance of tolerance to low soil pH in barley. Hereditas 88: 101–105

    Google Scholar 

  • Sumner ME, Fey MV & Noble AD (1991) Nutrient status and toxicity problems in acid soils. In: Ulrich B & Sumner ME (eds) Soil Acidity (pp. 149–182). Springer-Verlag, Berlin

    Google Scholar 

  • Tabuchi A & Matsumoto H (2001) Changes in cell-wall properties of wheat (Triticum aestivum) roots during aluminum-induced growth inhibition. Physiol. Plant 112: 353–358

    Google Scholar 

  • Tang Y, Sorrells ME, Kochian LV & Garvin DF (2000) Identification of RFLP markers linked to the barley aluminum tolerance gene Alp. Crop Sci. 40: 78–782

    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 

  • Taylor GJ (1991) Current views of the aluminum stress response: The physiological basis of tolerance. Curr. Topics Plant Bichem. Phsyiol. 10: 57–93

    Google Scholar 

  • Teraoka T, Kanek M, Mori S & Yoshimura E (2002) Aluminum rapidly inhibits cellulose synthesis in roots of barley and wheat seedlings. J. Plant Physiol. 159: 17–23

    Google Scholar 

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

    Google Scholar 

  • Toda T, Koyama H, Hori T & Hara T (1999) Aluminum tolerance of Arabidopsis thaliana under hydroponic and soil culture con-ditions. Soil Sci. Plant Nutr. 45: 419–425

    Google Scholar 

  • Vásquez MD, Poschenrieder C, Corrales I & Barcelo J (1999) Change in apoplastic aluminum during the initial growth re-sponse to aluminum by roots of a tolerant maize variety. Plant Physiol. 119: 435–444

    Google Scholar 

  • Villagarcia MR, Carter TE, Rufty TW, Niewoehner AS, Jennette MW & Arrellano C (2001) Genotypic rankings for aluminum tolerance of soybean roots grown in hydroponics and sand culture. Crop Sci. 41: 1499–1507

    Google Scholar 

  • Voigt PW & Mosjidis JA (2002) Acid-soil resistance of forage legumes as assessed by a soil-on-agar method. Crop Sci. 42: 1631–1639

    Google Scholar 

  • Voigt PW, Morris DR & Godwin HW(1997) A soil-on-agar method to evaluate acid-soil resistance in white clover. Crop Sci. 37: 1493–1496

    Google Scholar 

  • von Uexküll HR & Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171: 1–15

    Google Scholar 

  • Wagatsuma T, Ishikawa S, Obata H, Tawaraya K & Katohda S (1995) Plasma membrane of younger and outer cells is the primary specific site for aluminium toxicity in roots. Plant Soil 171: 105–112

    Google Scholar 

  • Waskom RM, Miller DR, Hanning GE, Duncan RR, Voight RL & Nabors MW (1990) Field evaluation of tissue culture derived sorghum for increased tolerance to acid soils and drought stress. Can J. Plant Sci. 70: 997–1004

    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

    Google Scholar 

  • Wu P, Liao CY, Hu B, Yi KK, Jin WZ, Ni JJ & He C (2000) QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theor. Appl. Genet. 100: 1295–1303

    Google Scholar 

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

    Google Scholar 

  • Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S & Matsumoto H (2002) Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol. 128: 63–72

    Google Scholar 

  • Yan F & Schubert S (2000) Soil pH changes after application of plant shoot materials of faba bean and wheat. Plant Soil 220: 279–287

    Google Scholar 

  • Zhang W-H, Ryan PR & Tyerman SD (2001) Malate-permeable channels and cation channels activated by aluminum in the apical cells of wheat roots. Plant Physiol. 125: 1459–1472

    Google Scholar 

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  1. USDA-ARS-Plant Science Research Unit, 1991 Upper Buford Circle, 495 Borlaug Hall, St. Paul, MN, 55108, USA

    Deborah A. Samac & Mesfin Tesfaye

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  1. Deborah A. Samac
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  2. Mesfin Tesfaye
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Correspondence to Deborah A. Samac.

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Samac, D.A., Tesfaye, M. Plant improvement for tolerance to aluminum in acid soils – a review. Plant Cell, Tissue and Organ Culture 75, 189–207 (2003). https://doi.org/10.1023/A:1025843829545

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