Toxicity and tolerance of aluminum in plants: tailoring plants to suit to acid soils
Tóm tắt
Từ khóa
Tài liệu tham khảo
Abd El-Moneim D, Contreras R, Silva-Navas J, Gallego FJ, Figueiras AM, Benito C (2014) Pectin methylesterase gene and aluminum tolerance in Secale cereale. Env Exp Bot 107:125–133
Abdel-Haleem H, CarterJr Thomas E, Rufty Thomas W, Roger Boerma H, Li Zenglu (2014) Quantitative trait loci controlling aluminum tolerance in soybean: candidate gene and single nucleotide polymorphism marker discovery. Mol Breed 33:851–862
Aniol A, Gustafson JP (1984) Chromosome location of genes controlling aluminum tolerance in wheat, rye and triticale. Can J Genet Cytol 26:701–705
Anoop VM, Basu U, McCammon MT, McAlister-Henn L, Taylor GJ (2003) Modulation of citrate metabolism alters aluminum tolerance in yeast and transgenic canola overexpressing a mitochondrial citrate synthase. Plant Physiol 132:2205–2217
Arenhart RA, Lima JC, de Pedron M, Carvalho FEL, Silveira JA, Rosa SB, Caverzan A, Andrade CMB, Schunemann M, Margis R (2013) Involvement of ASR genes in aluminum tolerance mechanisms in rice. Plant Cell Env 36:52–67
Arenhart RA, Bai Y, de Oliveira LFV, Neto LB, Schunemann M, Maraschin FS, Mariath J, Silverio A, Sachetto-Martins G, Margis R, Wang ZY, Margis-Pinheiro M (2014) New insights into aluminum tolerance in rice: the ASR5 protein binds the STAR1 promoter and other aluminum-responsive genes. Mol Plant 7:709–721
Babourina O, Rengel Z (2009) Uptake of aluminum into Arabidopsis root cells measured by fluorescent life-time imaging. Ann Bot 104:189–195
Balaji M, Reddy BK, Jogeswar G, Reddy LA, Kavi Kishor PB (2003) Alleviating effect of citrate on aluminum toxicity of rice (Oryza sativa L.) seedlings. Curr Sci 85:383–386
Balaji M, Reddy BK, Rao KR, Kavi Kishor PB (2004) Aluminum induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). J Plant Physiol 161:63–68
Barcelo J, Poschenrieder C (2002) Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminum toxicity and resistance: a review. Environ Exp Bot 48:75–92
Barone PD, Rosellini P, LaFayette J, Bouton FV, Parrott W (2008) Bacterial citrate synthase expression and soil aluminum tolerance in transgenic alfalfa. Plant Cell Rep 27:893–901
Begum HH, Osaki M, Watanabe T, Shinano T (2009) Mechanisms of aluminum tolerance in phosphoenolpyruvate carboxylase transgenic rice. J Plant Nutr 32:84–96
Berihu BA (2015) Histological and functional effect of aluminium on male reproductive system. Int J Pharma Sci Res 6:1122–1132
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
Boscolo PRS, Menossi M, Jorge RA (2003) Aluminum induced oxidative stress in maize. Phytochem 62:181–189
Bose J, Babourina O, Rengel Z (2011) Role of magnesium in alleviation of aluminum toxicity in plants. J Exp Bot 62:2251–2264
Budikova S, Durcekova K (2004) Aluminum accumulation in roots of Al-sensitive barley cultivar changes root cell structure and induces callose synthesis. Biologia 59:215–220
Cakir B, Agasse A, Gaillard C, Saumonneau A, Delrot S, Atanassova R (2003) A grape ASR protein involved in sugar and abscisic acid signalling. Plant Cell 15:2165–2180
Carrari F, Fernie AR, Iusem ND (2004) Heard it through the grapevine? ABA and sugar cross-talk: the ASR story. Trends Plant Sci 9:57–59
Chandran D, Sharopova N, Ivashuta S, Gantt JS, Vanden Bosch KA, Samac DA (2008) Transcriptome profiling identified novel genes associated with aluminum toxicity, resistance and tolerance in Medicago truncatula. Planta 228:151–166
Chang S, Puryear JD, Dias MADL, Funkhouser EA, Newton RJ, Cairney J (1996) Gene expression under water deficit in loblolly pine (Pinus taeda) isolation and characterization of cDNA clones. Physiol Plant 97:139–148
Chen ZC, Ma JF (2013) Magnesium transporters and their role in Al tolerance in plants. Plant Soil 368:51–56. doi: 10.1007/s11104-012-1433
Clark AG et al (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203–218
Collins NC, Shirley NJ, Saeed M, Pallotta M, Gustafson JP (2008) An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 locus of rye (Secale cereale L.). Genetics 179:669–682
Courville P, Chaloupka R, Cellier MF (2006) Recent progress in structure-function analyses of Nramp proton dependent metal-ion transporters. Biochem Cell Biol 84:960–978
Cruz-Ortega R, Cushman JC, Ownby JD (1997) cDNA clones encoding 1, 3-β-glucanase and a fimbrin-like cytoskeletal protein are induced by Al toxicity in wheat roots. Plant Physiol 114:1453–1460
De La Fuente M, Ramirez-Rodriguez V, Cabrera-Ponce JL, Herrera-Estrella L (1997) Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276:1566–1568
Degenhardt J, Larsen PB, Howell SH, Kochian LV (1998) Aluminum resistance in the Arabidopsis mutant alr-104 is caused by an aluminum-induced increase in rhizosphere pH. Plant Physiol 117:19–27
Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.): II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol 103:695–702
Delhaize E, Ryan PR, Hebb DM, 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
Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminum resistance and mineral nutrition. FEBS Lett 581:2255–2262
Deng W, Luo K, Li D, Zheng X, Wei X, Smith W, Thammina C, Lu L, Li Y, Pei Y (2006) Overexpression of an Arabidopsis magnesium transport gene, AtMGT1, in Nicotiana benthamiana confers Al tolerance. J Exp Bot 57:4235–4243
Deng W, Luo K, Li Z, Yang Y, Hu N, Wu Y (2009) Overexpression of Citrus junos mitochondrial citrate synthase gene in Nicotiana benthamiana confers aluminum tolerance. Planta 230:355–365
Devi SR, Yamamoto Y, Matsumoto H (2003) An intracellular mechanism of aluminum tolerance associated with high antioxidant status in cultured tobacco cells. J Inorg Biochem 97:59–68
Doncheva S, Amenos M, Poschenrieder C, Barcel J (2005) Root cell patterning: a primary target for aluminum toxicity in maize. J Exp Bot 56:1213–1220
Dong XY, Shen RF, Chen RF, Zhu ZL, Ma JF (2008) Secretion of malate and citrate from roots is related to high Al resistance in Lespedeza bicolor. Plant Soil 306:139–147
Duressa D, Soliman KM, Chen D (2010) Mechanisms of magnesium amelioration of aluminum toxicity in soybean at the gene expression level. Genome 53:787–797
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
Eldhuset TD, Swensen B, Wickstrøm T, Wollebæk G (2007) Organic acids in root exudates from Picea abies seedlings influenced by mycorrhiza and aluminum. J Plant Nutr Soil Sci 170:645–648
Eticha D, The C, Welcker C, Narro L, Staß A, Horst WJ (2005) Aluminum-induced callose formation in root apices: inheritance and selection trait for adaptation of tropical maize to acid soils. Field Crops Res 93:252–263
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 Physiol 122:657–665
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
Famoso AN, Zhao K, Clark RT, Tung CW, Wright MH, Carlos B, Kochian LV, McCouch SR (2011) Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL mapping. PLoS Gene 7(8):e1002221. doi: 10.1371/journal.pgen.1002221
Frantzios G, Galatis B, Apostolakos P (2000) Aluminum effects on microtubule organization in dividing root-tip cells of Triticum turgidum. I. Mitotic cells. New Phytol 145:211–224
Frantzios G, Galatis B, Apostolakos P (2001) Aluminum effects on microtubule organization in dividing root-tip cells of Triticum turgidum II. Cytokinetic cells J Plant Res 114:157–170
Frantzios G, Galatis B, Apostolakos P (2005) Aluminum causes variable responses in actin filament cytoskeleton of the root tip cells of Triticum turgidum. Protoplasma 225:129–140
Freitas FA, Kopp MM, Sousa RO, Zimmer PD, Carvalho FIF, Oliveira AC (2006) Absorcao de P, Mg, Ca e K e tolerancia de genotipos de arroz submetidos a estresse por aluminio emsistemas hidroponicos. Ciencia Rural 36:72–79
Furukawa J, Yamaji N, Wang H, Mitani N, Murata Sato K (2007) An aluminum-activated citrate transporter in barley. Plant Cell Physiol 48:1081–1091
Garcia-Oliveira AL, Martins-Lopes P, Tolra R, Poschenrieder C, Tarquis M, Guedes-Pinto H, Benito C (2014) Molecular characterization of the citrate transporter gene TaMATE1 and expression analysis of upstream genes involved in organic acid transport under Al stress in bread wheat (Triticum aestivum). Physiol Plant 152:441–452
Ghanati F, Morita A, Yokota H (2005) Effects of aluminum on the growth of tea plant and activation of antioxidant system. Plant Soil 276:133–141
Giannakoula A, Moustakas M, Mylona P, Papadakis I, Yupsanis T (2008) Aluminum tolerance in maize is correlated with increased levels of mineral nutrients, carbohydrates and proline, and decreased levels of lipid peroxidation and Al accumulation. J Plant Physiol 165:385–396
Grabski S, Schindler M (1995) Aluminum induces rigor within the actin network of soybean cells. Plant Physiol 108:897–901
Gruber BD, Ryan PR, Richardson AE, Tyerman SD, Ramesh S (2010) HvALMT1 from barley is involved in the transport of organic anions. J Exp Bot 61:1455–1467
Guo T, Zhang G, Zhou M, Wu F, Chen J (2004) Effects of aluminum and cadmium toxicity on growth and antioxidant enzyme activities of two barley genotypes with different Al resistance. Plant Soil 258:241–248
Gupta N, Gaurav SS, Kumar A (2013) Molecular basis of aluminum toxicity in plants: a review. Am J Plant Sci 4:21–37
Han Y, Zhang W, Zhang B, Zhang S, Wang W, Ming F (2009) One novel mitochondrial citrate synthase from Oryza sativa L. can enhance aluminum tolerance in transgenic tobacco. Mol Biotechnol 42:299–305. doi: 10.1007/s12033-009-9162-z
Hirano Y, Pannatier GE, Zimmermann S, Brunner I (2004) Induction of callose in roots of Norway spruce seedlings after short-term exposure to Al. Tree Physiol 24:1270–1283
Hirano Y, Walthert L, Brunner I (2006) Callose in root apices of European chestnut seedlings; a physiological indicator of aluminum stress. Tree Physiol 26:431–440
Hoekenga O, Maron LG, Pineros MA, Cancado P (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
Horst WJ, Puschel AK, Schmohl N (1997) Induction of callose formation is a sensitive marker for genotypic aluminum sensitivity in maize. Plant Soil 192:23–30
Hossain MA, Hossain AKMZ, Kihara T, Koyama H, Hara T (2005) Aluminum-induced lipid peroxidation and lignin deposition are associated with an increase in H2O2 generation in wheat seedlings. Soil Sci Plant Nutr 51:223–230
Huang JW, Grunes DL, Kochian LV (1992) Aluminum effects on the kinetics of calcium uptake into cells of the wheat root apex. Quantification of calcium fluxes using a calcium-selective vibrating microelectrode. Planta 188:414–421
Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF (2009) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21:655–667
Huang CF, Yamaji N, Chen Z, Ma JF (2012) A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice. Plant J 69:857–867
Husaini Y, Rai LC (1992) pH-dependent aluminum toxicity to Nostoc linckia: studies on phosphate uptake, alkaline and acid phosphatase activity, ATP content, photosynthesis and carbon fixation. J Plant Physiol 139:703–707
Iuchi S, Koyama H, Iuchi A, Kobayashi Y, Kitabayashi S (2007) Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and co-regulates a key gene in aluminum tolerance. Proc Natl Acad Sci USA 104:9900–9905
Iusem ND, Bartholomew DM, Hitz WD, Scolnik PA (1993) Tomato (Lycopersicon esculentum) transcript induced by water deficit and ripening. Plant Physiol 102:1353–1354
Jain LY, Ya YL, Yue JZ, Shan Z, Yun RW, Ping W, Shao JZ (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum form the rice root apex. Plant Physiol 146:602–611
Jones DL, Kochian LV, Gilroy S (1998) Aluminum induces a decrease in cytosolic calcium concentration in BY-2 tobacco cell cultures. Plant Physiol 116:81–89
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
Jorns AC, Hecht-Buchholz C, Wissemeier AH (1991) Aluminum-induced callose formation in root tips of Norway spruce (Picea abies (L.) Karst.). Zeitschrift fur Pflanzenernahrung Bodenkunde 154:349–353
Kalifa Y, Gilad A, Konrad Z, Zaccai M, Scolnik PA (2004) The water- and salt-stress regulated Asr1 (abscisic acid stress ripening) gene encodes a zinc-dependent DNA-binding protein. Biochem J 381:373–378
Keltjens WG, Tan K (1993) Interactions between aluminium, magnesium and calcium with different monocotyledonous and dicotyledonous plant species. Plant Soil 155–156:458–488
Kinraide TB (1997) Reconsidering the rhizotoxicity of hydroxyl, sulphate and fluoride complexes of aluminum. J Exp Bot 48:1115–1124
Kinraide TB (2003) Toxicity factors in acidic forest soils: attempts to evaluate separately the toxic effects of excessive Al3+ and H+ and insufficient Ca2+ and Mg2+ upon root elongation. Eur J Soil Sci 54:323–333
Kinraide TB, Pedler JF, Parker DR (2004) Relative effectiveness of calcium and magnesium in the alleviation of rhizotoxicity in wheat induced by copper, zinc, aluminum, sodium, and low pH. Plant Soil 259:201–208
Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Ann Rev Plant Physiol Plant Mol Biol 46:237–260
Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorus efficiency. Ann Rev Plant Biol 55:459–493
Kochian LV, Pineros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195
Kochian LV, Pineros MA, Liu J, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:571–598
Konarska A (2010) Effects of aluminum on growth and structure of red pepper (Capsicum annuum L.) leaves. Acta Physiol Plant 32:145–151
Koyama H, Takita E, Kawamura A, Hara T, Shibata D (1999) Over expression of mitochondrial citrate synthase gene improves the growth of carrot cells in Alphosphate medium. Plant Cell Physiol 40:482–488
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
Kuo MC, Kao CH (2003) Aluminum effects on lipid peroxidation and antioxidative enzyme activities in rice leaves. Biologia Plant 46:149–152
Larsen PB, Geisler MJB, Jones CA, Williams KM, Cancel JD (2005) ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. Plant J 41:353–363
Larsen PB, Cancel J, Rounds M, Ochoa V (2007) Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta 225:1447–1458
Liao H, Wan H, Shaff J, Wang X, Yan X, Kochian LV (2006) Phosphorus and aluminum interactions in soybean in relation to aluminum tolerance. Exudation of specific organic acids from different regions of the intact root system. Plant Physiol 141:674–684
Ligaba A, Katsuhura M, Ryan PR, Shibasaka M, Matsumoto H (2006) The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporters that enhance the aluminum resistance of plant cells. Plant Physiol 142:1294–1303
Ligaba A, Maron L, Shaff J, Kochian L, Pineros M (2012) Maize ZmALMT2 is a root anion transporter that mediates constitutive root malate efflux. Plant Cell Environ 35:1185–1200
Lin C, Hara A, Comparini D, Bouteau F, Kawano T (2015) Zinc-dependent protection of tobacco and rice cells from aluminum-induced superoxide-mediated cytotoxicity. Front Plant Sci 6:1079 doi:10:3389/fpls.2015.01079
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. Biologia Plant 52:87–92
Liu JP, Magalhaes JV, Shaff J, Kochian LV (2009) Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J 57:389–399
Ma JF (2007) Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. Int Rev Cytol 264:225–252
Ma Q, Rengel Z, Kuo J (2002) Aluminum toxicity in rye (Secale cereale): root growth and dynamics of cytoplasmic Ca2+ in intact root tips. Ann Bot 89:241–244
MacDiarmid CW, Gardner RC (1998) Overexpression of the Saccharomyces cerevisiae magnesium transport system confers resistance to aluminum ion. J Biol Chem 273:1727–1732
Macedo GEC, Jan VVS (2008) Effect of aluminium stress on mineral nutrition in rice cultivars differing in aluminum sensitivity. Revista Brasileira de Engenharia Agricola e Ambiental 12:363–369
Magalhaes J, Garvin D, Wang Y, Sorrells M, Klein P, 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
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
Mancuso S, Marras AM, Mugnai S, Schlicht M, Zarsky V, Li G (2007) Phospholipase Dζ2 drives vesicular secretion of auxin for its polar cell-cell transport in the transition zone of the root apex. Plant Signal Behav 2:240–244
Mariano ED, Jorge RA, Keltjens WG, Menossi M (2005) Metabolism and root exudation of organic acid anions under aluminum stress. Braz J Plant Physiol 17:157–172
Maron LG, Pineros MA, Guimaraes CT, Magalhaes JV, Pleiman JK, Mao CZ, Shaff J, Belicuas SNJ, Kochian LV (2010) Two functionally distinct members of the MATE (multi-drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize. Plant J 61:728–740
Massot N, Llugany M, Poschenrieder C, Barcelo J (1999) Callose production as indicator of aluminum toxicity in bean cultivars. J Plant Nutr 22:1–10
Matsumoto H, Hirasawa E, Torikai H, Takahashi E (1976) Localization of absorbed aluminum in pea root and its binding to nucleic acids. Plant Cell Physiol 17:127–137
Minella E, Sorrells ME (1992) Aluminum tolerance in barley: genetic relationships among genotypes of diverse origin. Crop Sci 32:593–598
Miyasaka SC, Hawes MC (2001) Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiol 125:1978–1987
Miyasaka SJ, Howell BR, Foy CD (1991) Mechanisms of aluminum tolerance in snapbeans (root exudation of citric acid). Plant Physiol 96:737–743
Nagy NE, Dalen LS, Jones DL, Swensen B, Fossdal CG, Eldhuset TD (2004) Cytological and enzymatic responses to aluminum stress in root tips of Norway spruce seedlings. New Phytol 163:595–607
Navakode S, Weidner A, Lohwasser U, Roder MS, Borner A (2009) Molecular mapping of quantitative trait loci (QTLs) controlling aluminum tolerance in bread wheat. Euphytica 166:283–290
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
Nguyen VT, Nguyen BD, Sarkarung S, Martinez C, Paterson AH, Nguyen HT (2002) Mapping of genes controlling aluminum tolerance in rice: comparison of different genetic backgrounds. Mol Genet Gen 267:772–780
Nguyen BD, Brar DS, Bui BC, Nguyen TV, Pham LN, Nguyen HT (2003) Identification and mapping of the QTL for aluminum tolerance introgressed from the new source, Oryza rufipogon Griff., into Indica rice (Oryza sativa L.). Theor Appl Genet 106:583–593
Nichol B, Oliveria LA, Glass ADM, Siddiqi MY (1993) The effects of aluminum on the influx of calcium, potassium, ammonium, nitrate and phosphate in an aluminum-sensitive cultivar of barley (Hordeum vulgare L.). Plant Physiol 101:1263–1266
Ninamango-Cardenas FE, Guimaraes CT, Martins PR (2003) Mapping QTLs for aluminum tolerance in maize. Euphytica 130:223–232
Ofei-Manu P, Wagatsuma T, Ishikawa S, Tawaraya K (2001) The plasma membrane strength of the root-tip cells and root phenolic compounds are correlated with Al tolerance in several common woody plants. Soil Sci Plant Nutr 47:359–375
Olivares E, Penas E, Marcano E (2009) Aluminum accumulation and its relationship with mineral plant nutrients in 12 pteridophytes from Venezuela. Env Exp Bot 65:132–141
Panchangam SS, Mallikarjuna N, Gaur PM, Suravajhala P (2014) Androgenesis in chickpea: anther culture and expressed sequence tags derived annotation. Ind J Exp Biol 52:181–188
Panda SK, Matsumoto H (2007) Molecular physiology of aluminum toxicity and tolerance in plants. Bot Rev 73:326–347
Panda SK, Singha LB, Khan MH (2003) Does aluminum phytotoxicity induce oxidative stress in green gram (Vigna radiata). Bul J Plant Physiol 29:77–86
Peixoto PHP, Cambraia J, Sant’Anna R, Mosquim PR, Moreira MA (1999) Aluminum effects on lipid peroxidation and on the activities of enzymes of oxidative metabolism in sorghum. Revista Brasileira de Fisiologia Vegetal 11:137–143
Pellet DM, Grunes DL, Kochian LV (1995) Organic-acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196:788–795
Pereira LB, Mazzanti CM, Goncalves JF, Cargnelutti D, Tabaldi LA, Becker AG et al (2010) Aluminum-induced oxidative stress in cucumber. Plant Physiol Biochem 48:683–689
Pereira JF, Barichello D, Ferreira JR, Aguilera JG, Consoli L, da Silva Junior JP, Bonow S, Cargnin A (2015) TaALMT1 and TaMATE1B allelic variability in a collection of Brazilian wheat and its association with root growth on acidic soil. Mol Breed 35:169
Pineros MA, Kochian LV (2001) A patch-clamp study on the physiology of aluminum toxicity and aluminum tolerance in maize. Identification and characterization of Al3+-induced anion channels. Plant Physiol 125:292–305
Pineros MA, Magalhaes JV, Alves VMC, Kochian LV (2002) The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation in maize. Plant Physiol 129:1194–1206
Pineros MA, Cancado GMA, Maron LG, Lyi SM, Menossi M, Kochian LV (2008) Not all ALMT1-type transporters mediate aluminum-activated organic acid responses: the case of ZmALMT1– an anion-selective transporter. Plant J 53:352–367
Pournourmohammadi S, Khazaeli P, Eslamizad S, Tajvar A, Mohammadirad A, Abdollahi M (2008) Study on the oxidative stress status among cement plant workers. Hum Exp Toxicol 27:463–469
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 DH, Delhaize E, Ryan PR (2005) Molecular characterization and mapping of ALMT1, the aluminum-tolerance gene of bread wheat (Triticum aestivum L.). Genome 48:781–791
Ramesh SA, Tyerman SD, Xu B, Bose J, Kaur S, Conn V, Domingos P, Ullah S, Wege S, Shabala S, Feijo JA, Ryan PR, Gilliham M (2015) GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters. Nature Commun 6:78–79
Rangel AF, Rao IM, Horst WJ (2007) Spatial aluminum sensitivity of root apices of two common bean (Phaseolus vulgaris L.) genotypes with contrasting aluminum resistance. J Exp Bot 58:3895–3904
Rengel Z, Reid RJ (1997) Uptake of Al across the plasma membrane of plant cells. Plant Soil 192:31–35
Rengel Z, Zhang ZH (2003) Role of dynamic of intracellular calcium in aluminum-toxicity syndrome. New Phytol 159:295–314
Riccardi F, Gazeau D, De Vienne D, Zivy M (1998) Protein changes in response to progressive water deficit in maize: quantitative variation and polypeptide identification. Plant Physiol 117:1253–1263
Rout GR, Samantaray S, Das P (2001) Aluminum toxicity in plants: a review. Agronomie 21:2–21
Ryan PR, Raman H, Gupta S, Horst WJ, Delhaize E (2009) A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol 149:340–351
Ryan PR, Raman H, Gupta S, Sasaki T (2010) The multiple origins of aluminum resistance in hexaploid wheat include Aegilops tauschii and more recent cis-mutations to TaALMT1. Plant J 64:446–455
Ryan PR, Tyerman SD, Sasaki T, Furuichi T, Yamamoto Y, Zhang WH et al (2011) The identification of aluminum-resistance genes provides opportunities for enhancing crop production on acid soils. J Exp Bot 62:9–20
Sasaki M, Yamamoto Y, Matsumoto M (1997) Aluminun inhibits growth and stability of cortical microtubules in wheat (Triticum estivim L.) roots. Soil Sci Plant Nutr 43:469–472
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
Sawaki Y, Iuchi S, Kobayashi Y, Kobayashi Y, Ikka T (2009) STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities. Plant Physiol 150:281–294
Schmohl N, Pilling J, Fisahn J, Horst WJ (2000) Pectin methylesterase modulates aluminum sensitivity in Zea mays and Solanum tuberosum. Physiol Plant 109:419–427
Schreiner KA, Hoddinott J, Taylor GJ (1994) Aluminum-induced deposition of (1, 3)-beta-glucans (callose) in Triticum aestivum L. Plant Soil 162:273–280
Shaw CA, Tomljenovic L (2013) Aluminum in the central nervous system (CNS): toxicity in humans and animals, vaccine adjuvants, and autoimmunity. Immunol Res 56:304–316
Silhavy D, Hutvagner G, Barta E, Banfalvi Z (1995) Isolation and characterization of a water-stress inducible cDNA clone from Solanum chacoense. Plant Mol Biol 27:587–595
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 123:543–552
Silva S, Santos C, Matos M, Pinto-Carnide O (2011) Al toxicity mechanisms in tolerant and sensitive rye genotypes. Env Exp Bot 75:89–97
Silva S, Pinto G, Correia B, Carnide O, Santos C (2013) Rye oxidative stress under long term Al exposure. J Plant Physiol 170:879–889
Simoes CC, Melo JO, Magalhaes JV, Guimaraes CT (2012) Genetic and molecular mechanisms of aluminum tolerance in plants. Genet Mol Res 11:1949–1957
Sivaguru M, Baluska F, Volkman 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
Sivaguru M, Fujiwara T, Samaj J (2000) Aluminum-induced 1→3-beta-D-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiol 124:991–1005
Sivaguru M, Ezaki B, He ZH, Tong HY, 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
Slaski JJ (1995) NAD+ kinase activity in root tips of nearly isogenic lines of wheat (Triticum aestivum L.) that differ in tolerance to aluminum. J Plant Physiol 145:143–147
Sugiharto B, Ermawati N, Mori H, Aoki K, Yonekura-Sakakibara K, Yamaya T, Sugiyama T, Sakakibara H (2002) Identification and characterization of a gene encoding drought inducible protein localizing in the bundle sheath cell of sugarcane. Plant Cell Physiol 43:350–354
Suhadya CG, Haug A (1985) Citrate chelation as a potential mechanism against aluminum toxicity in cells: the role of calmodulin. Can J Biochem Cell Biol 63:1167–1175
Tahara K, Norisada M, Hogetsu T, Kojima K (2005) Aluminum tolerance and 7 aluminum-induced deposition of callose and lignin in the root tips of Melaleuca and 8 Eucalyptus species. J For Res 10:325–333
Tasma IM, Asadi WA (2008) Development and characterization of F2 population for molecular mapping of aluminum toxicity tolerant QTL in soybean. J Agro Biogen 4:1–8
Taylor GJ (1988) The physiology of aluminum tolerance in higher plants. Commu Soil Sci Plant Anal 19:1179–1194
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
Tokizawa M, Kobayashi Y, Saito T, Kobayashi M, Iuchi S, Nomto M, Tada Y, Yamamoto YY, Koyama H (2015) Sensitive to proton rhizotoxicity1, calmodulin binding transcription activator 2, and other transcription factors are involved in aluminum-activated malate transporter 1 expression. Plant Physiol 167:991–1003
Tovkach A, Ryan PR, Richardson AE, Lewis DC, Rathjen TM (2013) Transposon-mediated alteration of TaMATE1B expression in wheat confers constitutive citrate efflux from root apices. Plant Physiol 161:880–892
Trejo-Tellez LI, Stenzel R, Gomez-Merino FC, Schmitt JM (2010) Transgenic tobacco plants overexpressing pyruvate phosphate dikinase increase exudation of organic acids and decrease accumulation of aluminum in the roots. Plant Soil 326:187–198
Vaidyanathan R, Kuruvila S, Thomas G (1999) Characterization and expression pattern of an abscisic acid and osmotic stress responsive gene from rice. Plant Sci 140:25–36
Vardar F, Unal M (2007) Aluminum toxicity and resistance in higher plants. Ann Mol Biol 1:1–12
Wang QF, Zhao Y, Yi QO, Li KZ, Yu YX, Chen LM (2010) Overexpression of malate dehydrogenase in transgenic tobacco leaves: enhanced malate synthesis and augmented Al-resistance. Acta Physiol Plant 32:1209–1220
Wang Y, Xu H, Kou J, Shi L, Zhang C, Fangsen X (2013) Dual effects of transgenic Brassica napus overexpressing CS gene on tolerances to aluminum toxicity and phosphorus deficiency. Plant Soil 362:231–246
Wu P, Liao CY, Hu B, Yi KK, Jin WZ, Nihe JJC (2000) QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theor Appl Genet 100:1295–1303
Xia J, Yamaji N, Kasai T, Ma JF (2010) Plasma membrane localized transporter for aluminum in rice. Proc Nat Acad Sci USA 107:18381–18381
Xue Y, Wan JM, Jiang L, Liu L, Su N, Zhai HQ, Ma JF (2006a) QTLs analysis of aluminum resistance in rice (Oriza sativa L.). Plant Soil 287:375–383
Xue Y, Wan JM, Jiang L, Wang C, Liu L, Zhang Y, Zhai H (2006b) Identification of quantitative trait loci associated with aluminium tolerance in rice (Oryza sativa L.). Euphytica 150:37–45
Xue Y, Jiang L, Su N, Wang J, Deng P, Ma JF, Zhai HG, Wan JM (2007) The genetic basic and finemapping of a stable quantitative-trait loci for aluminium tolerance in rice. Planta 227:255–262
Yamaji N, Huang CF, Nagao S, Yano M, Sato Y (2009) A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell 21:3339–3349
Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H (2003) Oxidative stress triggered by aluminum in plant roots. Plant Soil 255:239–243
Yang H, Knapp J, Koirala P, Rajagopal D, Peer WA, Silbart LK, Murphy A, Gaxiola RA (2007) Enhanced phosphorus nutrition in monocots and dicots over-expressing a phosphorus-responsive type I H+-pyrophosphatase. Plant Biotechnol J 5:735–745
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 146:602–661
Yang JL, Zhu XF, Zheng C, Zhang YJ, Zheng SJ (2011a) Genotypic differences in Al resistance and the role of cell-wall pectin in Al exclusion from the root apex in Fagopyrum tataricum. Ann Bot 107:371–378
Yang JL, Zhu XF, Peng YX, Zheng C, Li GX, Liu Y, Shi YZ, Zheng SJ (2011b) Cell wall hemicellulose contributes significantly to aluminum adsorption and root growth in Arabidopsis. Plant Physiol 155:1885–1892
Yang XY, Zeng ZH, Yan JY, Fan W, Bian HW, Zhu MY, Yang JY, Zheng SJ (2013) Association of specific pectin methylesterases with Al-induced root elongation inhibition in rice. Physiol Plant 148:502–511
Yokosho K, Yamaji N, Ma JF (2010) Isolation and characterization of two MATE genes in rye. Funct Plant Biol 37:296–303
Yokosho K, Yamaji N, Ma JF (2011) An Al-inducible MATE gene is involved in external detoxification of Al in rice. Plant J 68:1061–1069
You J, Zhang H, Liu N, Gao L, Kong L, Yang Z (2011) Transcriptomic responses to aluminum stress in soybean roots. Genome 54:923–933
Zhang B, Liu P, Yang YS, Xu GD (2007) Effect of Al in soil on photosynthesis and related morphological and physiological characteristics of two soybean genotypes. Bot Stud 48:435–444
Zhao Z, Ma JF, Sato K, Takeda K (2003) Differential Al resistance and citrate secretion in barley (Hordeum vulgare L.). Planta 217:794–800
Zhou LL, Bai GH, Ma HX, Carver BF (2007) Quantitative trait loci for aluminum resistance in wheat. Mol Breed 19:153–161
Zhou CP, Qi YP, You X, Yang LT, Guo P (2013) Leaf cDNA-AFLP analysis of two citrus species differing in manganese tolerance in response to long-term manganese toxicity. BMC Genome 14:621