Abstract
Aluminum (Al) toxicity limits crop productivity in over 40 % of arable lands on this planet. Understanding the Al signaling and physiological relevance of Al toxicity and tolerance/resistance is fundamental to identify and improve crop productivity which is a better strategy than liming the soils as the latter is labor intensive, ineffective, and expensive. In this chapter, all aspects of Al toxicity and tolerance are discussed in a historic perspective of around a century of research, development, and understanding on this topic; a special section regarding a new function of existing ‘safeners’ and their potential for protection against Al toxicity is also discussed.
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Achary VMM, Parinandi NL, Panda BB (2012) Aluminum induces oxidative burst, cell wall NADH-peroxidase activity, and DNA damage in root cell of Allium cepa L. Environ Molec Mutagen 53:550–560
Ahad A, Nick P (2007) Actin is bundled in activation-tagged tobacco mutants that tolerate aluminum. Planta 225:451–468
Ahn SJ, Matsumoto H (2006) The role of the plasma membrane in the response of plant roots to aluminum toxicity. Plant Signal Behav 1–2:37–45
Ahn SJ, Rengel Z, Matsumoto H (2004) Aluminum-induced plasma membrane surface potential and H+-ATPase activity in near-isogenic wheat lines differing in tolerance to aluminum. New Phytol 162:71–79
Ahn SJ, Sivaguru M, Osawa M, Cheng GC, Matsumoto H (2001) Aluminum inhibits the H+-ATPase activity by permanently altering the plasma membrane surface potential in squash roots. Plant Physiol 126:1381–1390
Akeson MA, Munns DN, Burau RG (1989) Adsorption of Al3+ to phosphatidylcholine vesicles. Biochem Biophys Acta 986:33–40
Almeras E, Stolz S, Vollenweider S, Reymond P, Mene-Saffrane L, Farmer EE (2003) Reactive electrophile species activate defense gene expression in Arabidopsis. Plant J 34:205–216
Amenós M, Corrales I, Poschenrieder C, Illeš P, Baluška F, Barceló J (2009) Different effects of aluminum on the actin cytoskeleton and brefeldin A-sensitive vesicle recycling in root apex cells of two maize varieties differing in root elongation rate and aluminum tolerance. Plant Cell Physiol 50:528–540
Arroyo-Serralta GA, Ku-González A, Hernández-Sotomayor SMT, Aguilar JJZ (2005) Exposure to toxic concentrations of aluminum activates a MAPK-like protein in cell suspension cultures of Coffea arabica. Plant Physiol Biochem 43:27–35
Baluška F, Hlavacka A, Saniaj J, Palme K, Robinson G, Matoh T, McCurdy DW, Menzel D, Volkmann D (2002) F-actin-dependent endocytosis of cell wall pectins in meristematic root cells. Insights from brefeldin A-induced compartments. Plant Physiol 130:422–431
Baluška F, Samaj J, Wojtaszek P, Volkann O, Menzel D (2003) Cytoskeleton-plasma membrane-cell wall continuum in plants. Plant Physiol 133:482–491
Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signaling. J Exp Bot 65:1229–1240
Behringer C, Bartsch K, Schaller A (2011) Safeners recruit multiple signalling pathways for the orchestrated induction of the cellular xenobiotic detoxification machinery in Arabidopsis. Plant Cell Environ 34:1970–1985
Bennet RJ, Breen CM (1991) The aluminium signal: new dimensions to mechanisms of aluminium tolerance. Plant Soil 134:153–166
Bonaventure G, Schuck S, Baldwin IT (2011) Revealing complexity and specificity in the activation of lipase-mediated oxylipin biosynthesis: a specific role of the Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves and roots. Plant Cell Environ 34:1507–1520
Brault M, Amiar Z, Pennarun A-M, Monetiez M, Zhang Z, Cornel D, Dellis O, Knight H, Bouteau F, Rona J-P (2004) Plasma membrane depolarization induced by abscisic acid in Arabidopsis suspension cells involves reduction of proton pumping in addition to anion channel activation, which are both Ca2+ dependent. Plant Physiol 135:231–243
Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468
Chaffai R, Marzouk B, Ferjani E (2005) Aluminum mediates compositional alterations of polar lipid classes in maize seedlings. Phytochem 66:1903–1912
Chee-Gonzalez I, Munoz-Sanchez JA, Racagri-Di Palma G (2009) Effect of phosphate on aluminum-inhibited growth and signal transduction pathway in Coffea arabica suspension cells. J Inorg Biochem 103:1497–1503
Chen Q, Guo C-L, Wang P, Chen X-Q, Wu K-H, Li K-Z, Y-X Y, Chen L-M (2013) Up-regulation and interaction of the plasma membrane H + -ATPaseand the 14-3-3 protein are involved in the regulation of citrate exudation from the broad bean (Vicia faba L.) under Al stress. Plant Physiol Biochem 10:504–511
Christeller JT, Galis I (2014) alpha-Linolenic acid concentration and not wounding per se is the key regulator of octadecanoid (oxylipin) pathway activity in rice (Oryza sativa L.) leaves. Plant Physiol Biochem 83:117–125
Čizková R (1995) Phytohormonal levels in spruce roots under aluminum stress. In: Baluška F et al (eds) Structure and function of roots. Kluwer, The Netherlands, p 335–339
Clarkson DT (1965) The effect of aluminium and some other trivalent metal cations on cell division in the root apices of Allium cepa. Ann Bot 29:309–315
Concado GMA, De Rosa Jr VE, Fernandez JH, Maron LG, Jorge RA, Menossi M (2005) Glutathione S-transferase and aluminum toxicity. Functional Plant Biol 32:1045–1055
Cummins I, Dixon DP, Freitag-Pohl S, Skipsey M, Edwards R (2011) Multiple roles for plant glutathione transferases in xenobiotic detoxification. Drug Metab Rev 43:266–280
da Silva ALS, Sperling P, Horst W, Franke S, Ott C, Becker D, Stass A, Lorz H, Heinz W (2006) A possible role of sphingolipids in the aluminium resistance of yeast and maize. J Plant Physiol 163:26–38
Dave A, Graham IA (2012) Oxylipin signaling: a distinct role for the jasmonic acid precursor cis-(+)-12-oxo-phytodienoic acid (cis-OPDA). Front Plant Sci 3:42
Devi SR, Yamamoto Y, Matsumoto H (2003) An intracellular mechanism of aluminum tolerance associated with antioxidant status in cultured tobacco cells. Inorg Biochem 97:59–68
Davies J, Caseley JC (1999) Herbicide safeners: a review. Pestic Sci 55:1043–1058
Doncheva S, Amenos M, Poschenrieder C, Barcelo J (2005) Root cell patterning: a primary target for aluminium toxicity in maize. J Exp Bot 56:1213–1220
Diao G, Wang Y, Yang C (2010) Functional characterization of a glutathione S-transferase gene from Limonium bicolor in response to several abiotic stresses. Afric J Biotechnol 32:5060–5065
Dixon DP, Skipsey M, Edwards R (2010) Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71:338–350
Dueckershoff K, Mueller S, Mueller MJ, Reinders J (2008) Impact of cyclopentenone-oxylipins on the proteome of Arabidopsis thaliana. Biochim Biophys Acta 1784:1975–1985
Eticha D, Stass A, Horst WJ (2005) Cell-wall pectin and its degree of methylation in the maize root apex: significance for genotypic differences in aluminum resistance. Plant Cell Envir 28:1410–1420
Edwards R, Dixon DP (2005) Plant glutathione transferases. Methods Enzymol 401:169–186
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
Farmer EE, Davoine C (2007) Reactive electrophile species. Curr Opin Plant Biol 10:380–386
Fiskesjo G (1983) Nucleolar dissolution induced by aluminum in root cells of Allium. Physiol Plant 59:508–511
Frantzios G, Galati B, Apostolakos P (2005) Aluminum causes variable responses in actin filament cytoskeleton of the root tip cell of Triticum furigidum. Protoplasma 225:129–140
Frova C (2003) The plant glutathione transferase gene family: genomic structure, functions, expression, and evolution. Physiol Plant 119:469–479
Furuichi J, Sasaki T, Tsuchiya Y, Ryan PR, Delhaize E, Yamamoto Y (2010) An extracellular hydrophilic carboxyl-terminal domain regulates the activity of TaALMT1, the aluminum-actiavated malate transport protein of wheat. Plant J 64:47–55
Grabski S, Schindler M (1995) Aluminum induces rigor within the actin network of soybean cells. Plant Physiol 108:897–901
Grebner W, Stingl NE, Oenel A, Mueller MJ, Berger S (2013) Lipoxygenase6-dependent oxylipin synthesis in roots is required for abiotic and biotic stress resistance of Arabidopsis. Plant Physiol 161:2159–2170
Gutteridge JMC, Quinlan GJ, Clark I, Halliwell B (1985) Aluminium salts accerelate peroxidation of membrane lipids stimulated by iron salts. Biochem Biophys Acta 835:441–447
Hasenstein KH, Evans ML (1988) Effects of cations on hormone transport in primary roots of Zea mays. Plant Physiol 86:890–894
Haug A, Shi B, Vitorello V (1994) Aluminum interaction with phosphoinositide-associated signal transduction. Arch Toxicol 68:1–7
He H, He L, Gu M (2012a) Interactions between nitric oxide and plant hormones in aluminum tolerance. Plant Signal Behav 7:469–471
He H, Zhan J, He L, Gu M (2012b) Nitric oxide signaling in aluminum stress in plants. Protoplasma 249:483–492
Horst WJ (1995) The role of the apoplast in aluminum toxicity and resistance of higher plants. Z Pflanzennernahr Bodenkd 158:419–428
Horst WJ, Schmohl N, Kollemeier M, Baluška F, Sivaguru M (1999) Does aluminum affect root growth of maize through interaction with the cell wall-plasma membrane-cytoskeleton continuum? Plant Soil 215:163–174
Hou N, Yan J, Pang J, Xu M, Chen G, Yang Z (2010) The accumulation and transport of abscisic acid in soybean (Glycine max L.) under aluminum stress. Plant Soil 330:127–137
Illes P, Schlicht M, Pavlovkin J, Lichtschidl I, Baluška F, Ovecka M (2006) Aluminium toxicity in plants: internalization of aluminium into cells of the transition zone in Arabidopsis root apices related to changes in plasma membrane potential, endosomal behavior, and nitric oxide production. J Exp Bot 57:4201–4213
Irzyk GP, Fuerst EP (1993) Purification and characterization of a glutathione S-transferase from benoxacor-treated maize (Zea mays). Plant Physiol 102:803–810
Irzyk GP, Fuerst EP (1997) Characterization and induction of maize glutathione S-transferases involved in herbicide detoxification. In: Hatzios KK (ed) Regulation of enzymatic systems detoxifying xenobiotics in plants. Kluwer, Dordrecht, pp 155–170
Ishikawa S, Wagatsuma T (1998) Plasma membrane permeability of root-tip cells following temporary exposure to Al ions is a rapid measure of Al tolerance among plant species. Plant Cell Physiol 39:516–525
Javelle M, Vernoud V, Rogowsky PM, Ingram GC (2011) Epidermis: the formation and functions of a fundamental plant tissue. New Phytol 189:17–39
Jepson I, Lay VJ, Holt DC, Bright SWJ, Greenland AJ (1994) Cloning and characterization of maize herbicide safener-induced cDNAs encoding subunits of glutathione S-transferase isoforms I, II and IV. Plant Mol Biol 26:1855–1866
Jepson I, Holt DC, Roussel V, Wright SY, Greenland AJ (1997) Transgenic plant analysis as a tool for the study of maize glutathione S-transferases. In: Hatzios KK (ed) Regulation of enzymatic systems detoxifying xenobiotics in plants. Kluwer, Dordrecht, pp 313–323
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 Envirom 29:1309–1318
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
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 7:1913–1921
Kasai M, Sasaki M, Tanakamaru S, Yamamoto Y, Matsumoto H (1993) Possible involvement of abscisic acid in activities of two vacuular H+-pumps in barley roots under aluminum stress. Plant Cell Physiol 34:1335–1338
Kenjebaeva S, Yamamoto Y, Matsumoto H (2000) The impact of aluminum on the distribution of cell wall glycoproteins of pea root tip and their Al-binding capacity. Soil Sci Plant Nutr 47:629–636
Kinraide TB, Yemiyahu U (2007) A scale of metal ion binding strengths correlating with ionic charge, Pauling electronegativity, toxicity, and other physiological effects. Inorg Biochem 101:1201–1213
Klug B, Horst WJ (2010) Spatial characteristics of aluminum uptake and translocation in roots of buckwheat (Fagopyrum esculentum). Physiol Plant 139:181–191
Kobayashi Y, Hoekenga OA, Itoh H, Nakashima M, Saito S, Shoff JE, Maron LG, Pineros MA, Kochian LV, Koyama H (2007) Characterization of AtALMT1 expression in aluminum-inducible malate release and its role for rhizotoxic stress tolerance in Arabidopsis. Plant Physiol 145:843–852
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
Kong X, Zhang M, Xu X, Li X, Li C, Ding Z (2014) System analysis of microRNAs in the development and aluminum stress responses of the maize root system. Plant Biotechnol J 12:1108–1121
Kopittke PM, Blamey FPC, Menzies NW (2008) Toxicities of soluble Al, Cu, and La include ruptures to rhizodermal and root critical cells of cowpea. Plant Soil 303:217–227
Kreuz K, Tommasini R, Martinoia E (1996) Old enzymes for a new job. Herbicide detoxification in plants. Plant Physiol 111:349–353
Larkins BA, Dilkes DP, Dante RA, Coelho CM, Woo Y-M, Liu Y (2001) Investigating the hows and whys of DNA endoreduplication. J Exp Bot 52:183–192
Lazof DB, Goldsmith JG, Linton RW (1997) The in situ analysis of intracellular aluminum in plants. Prog Bot 58:112–149
Lee HO, Davidson JM, Duronio RJ (2009) Endoreplication: polyploidy with purpose. Genes Dev 23:2461–2477
Li J-Y, Liu J, Dong D, Jia X, MxCouch SR, Kochian LV (2014) Natural variation underlies alterations in Nramp aluminum transporter (NRAT1) expression and function that plays a key role in rice aluminum tolerance. Proc Natl Acad Sci U S A 111:6503–6508
Ligaba A, Dreyer I, Margaryan A, Schneider DJ, Kochian L, Pineros M (2013) Functional, structural and phylogenetic analysis of domains underlying the Al sensitivity of the aluminum-activated malate/anion transporter TaALMT1. Plant J 76:766–780
Ligava A, Kochian LV, Pineros M (2009) Phosphorylation at S384 regulates the activity of the TaALMT1 malate transporter that underlies aluminum resistance in wheat. Plant J 60:411–423
Lin C, Yu Y, Kadono T, Iwata M, Umemura K, Furuichi T, Kase M, Isobe M, Yamamoto Y, Matasumoto H, Yoshizuka K, Kawano T (2005) Action of aluminum, novel TPC1-type channel inhibitor, against silicylate-inducd and cold-shock-induced -calcium influx in tobacco BY-2 cells. Biochem Biophys Res Commun 332:823–832
Liu J, Pineros MA, Kochian LV (2014) The role of aluminum sensing and signaling in plant aluminum resistance. J Integrative Plant Biol 56:221–230
Llugany M, Poschenrieder L, Barcelo J (1995) Monitoring of aluminium-induced inhibition of root elongation in four maize cultivars differing in tolerance to aluminium and proton toxicity. Physiol Plant 93:265–271
Loeffler C, Berger S, Guy A, Durand T, Bringmann G, Dreyer M, von Rad U, Durner J, Mueller MJ (2005) B1-phytoprostanes trigger plant defense and detoxification responses. Plant Physiol 137:328–340
Ma JF, Ryan PR, Delhaize E (2001) Aluminum tolerance in plants and the complexity of organic acids. Trends Plant Sci 6:273–278
Magalhaes JV, Liu J, Guimaraes CT, Lana UGP, Alves VMC, Wang Y-H, Schaffert RE, Hoekenga OH, 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
Maron LG, Guimaraes CT, Kirst M, Albert PS, Birchler JA, Bradburya PJ, Buckler ES, Coluccio AE, Danilova TV, Kudrna D, Magalhaes JV, Pineros MA, Schatz MC, Wing RA, Kochian LV (2013) Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proc Natl Acad Sci U S A 110:5241–5246
Martinez-Estévez M, Loyola-Vargas VM, Hervández-Sotomayor SMT (2001) Aluminum increase phosphorylation of particular proteins in cellular suspension cultures of coffee (Coffea arabica). J Plant Physiol 158:1375–1379
Massot N, Nicander B, Barcelo J, Poschenrieder C, Tillberg E (2002) A rapid increase in cytokinin level, and enhanced ethylene evolution precede Al3+-induced inhibition of root growth in bean seedlings (Phaseolus vulgaris L.). Plant Growth Regul 37:105–112
Matsumoto H (1988) Changes of the structure of pea chromatin by aluminum. Plant Cell Physiol 29:281–287
Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol 200:1–46
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
Matsumoto H, Morimura S, Takahashi E (1977) Binding of aluminum to DNP in pea root nuclei. Plant Cell Physiol 18:987–993
Matsumoto H, Motoda H (2012) Aluminum toxicity recovery process in root apices. Possible association with oxidative stress. Plant Sci 185–186:1–8
Matsumoto H, Motoda H (2013) Oxidative stress is associated with aluminum toxicity recovery in apex of pea root. Plant Soil 363:399–410
Matsumoto H, Sivaguru M (2008) Advances in the aluminum toxicity and tolerance of plants for increased productivity in acid soil. In: Debios AN (ed) Soil contamination: new research. Nova Science, New York, NY, pp 1–42
Matsumoto H, Yamamoto Y (2013) Plant roots under aluminum stress: toxicity and tolerance. In: Eshel A, Beckman T (eds) Plant roots: the hidden half, 4th edn. CRC Press/Taylor & Francis Group, Boca Raton, FL, 33-1
Mimmo T, Marzadori C, Gessa CE (2009) Does the degree of pectin esterification influence aluminum sorption by the root apoplast? Plant Soil 314:159–168
Mohanty S, Das AB, Da P, Mohanty P (2004) Effect of a low dose of aluminum on mitotic and meiotic activity, 4C DNA content, and pollen sterility in rice, Oryza sativa L. cv. Lalat. Ecotoxicol Environ Saf 59:70–75
Mosblech A, Feussner I, Heilmann I (2009) Oxylipins: structurally diverse metabolites from fatty acid oxidation. Plant Physiol Biochem 47:511–517
Motoda H, Kano Y, Hiragami F, Kawamura K, Matsumoto H (2010) Changes in the apex of pea roots during and after recovery from aluminum treatment. Plant Soil 333:49–58
Mueller MJ (2004) Archetype signals in plants: the phytoprostanes. Curr Opin Plant Biol 7:441–448
Mueller MJ, Berger S (2009) Reactive electrophilic oxylipins: pattern recognition and signalling. Phytochemistry 70:1511–1521
Mueller S, Hilbert B, Dueckershoff K, Roitsch T, Krischke M, Mueller MJ, Berger S (2008) General detoxification and stress responses are mediated by oxidized lipids through TGA transcription factors in Arabidopsis. Plant Cell 20:768–785
Naidoo G, Stewart J, Med LRJ (1978) Accumulation sites of Al in snapbean and cotton roots. Agron J 70:489–492
Naora H, Naora H, Mirsky AE, Allfrey VG (1961) Magnesium and calcium in isolated cell nuclei. J Gen Physiol 44:713–741
Negishi T, Oshima K, Hattori M, Kanai M, Mano S, Nishimura H, Yoshida R (2012) Tonoplast- and plasma membrane-localized aquaporin-family transporters in blue hydrangea sepals of aluminum hyperaccumulating plant. PLoS One 7:e4389
Nezames CD, Sjogren CA, Barajas JF, Larsen PB (2012) The Arabidopsis cell cycle checkpoint regulators TANMEI/ALT2 and ATR mediates the active process of aluminum-dependent root growth inhibition. Plant Cell 24:608–621
Novascués J, Pérez-Rontomé C, Sánchez DH, Staudinger C, Wienkoop S, Rellan-Alvarez R, Becana M (2012) Oxidative stress is a consequence, not a cause, of aluminum toxicity in the forage legume Lotus csrniculatus. New Phytol 193:625–630
Olivetti GP, Gumming JR, Etherton B (1995) Membrane potential depolarization of root cap cells precedes aluminum tolerance in snap bean. Plant Physiol 109:123–129
Okazaki Y, Saito K (2014) Roles of lipids as signaling molecules and mitigators during stress response in plants. Plant J 79:584–596
Ono K, Yamamoto Y, Haxchiya A, Matsumoto H (1995) Synergistic inhibition of growth by aluminum and iron of tobacco (Nicotiana tobacum L.) cells in suspension culture. Plant Cell Physiol 36:115–125
Osawa H, Matsumoto H (2001) Possible involvement of protein phosphorylation in aluminum-responsive malate efflux from wheat root apex. Plant Physiol 126:411–420
Pan J-W, Zhu M-Y, Chen H (2001) Aluminum-induced cell death in root tip cells of barley. Environ Exp Bot 46:71–79
Panda SK, Baluška F, Matsumoto H (2009) Aluminum stress signaling in plants. Plant Signaling Behav 4:592–597
Papernick LA, Kochian LV (1997) Possible involvement of Al-induced electrical signal in Al tolerance in wheat. Plant Physiol 115:657–667
Pejchar P, Potocky M, Novotná Z, Veselková S, Kocourková D, Valentová O, Schwarzerova K, Martinec J (2010) Aluminium ions inhibit the formation of diacylglycerol generated by phosphatidylcholin-hydrolysing phospholipase C in tobacco cells. New Phytol 188:150–160
Pineros M, Tester M (1993) Plasma membrane Ca2+ channels in roots of higher plants and their role in aluminium toxicity. Plant Soil 155(156):119–122
Qin R, Jiang WS, Liu DH (2013) Aluminum can induce alteration in the cellular localization and expression of three major nucleolar proteins in root tip cells of Allium cepa var. agrogarum L. Chemosphere 90:827–834
Ramel F, Sulmon C, Serra A-A, Gouesbet G, Couee I (2012) Xenobiotic sensing and signaling in higher plants. J Exp Bot 63:3999–4014
Rengel Z (1992a) Distribution of cell Ca2+ homeostasis as a primary target of Al toxicity syndrome. Plant Cell Environ 15:931–938
Rengel Z (1992b) Role of calcium in aluminium toxicity. New Phytol 121:499–513
Rengel Z, Zhang WG (2003) Role of dynamics of intracellular calcium in aluminium-toxicity syndrome. New Phytol 59:295–314
Riechers DE, Irzyk GP, Jones SS, Fuerst EP (1997) Partial characterization of glutathione S-transferases from wheat (Triticum spp.) and purification of a safener-induced glutathione S-transferase from Triticum tauschii. Plant Physiol 114:1461–1470
Riechers DE, Zhang Q, Xu FX, Vaughn KC (2003) Tissue-specific expression and localization of safener-induced glutathione S-transferase proteins in Triticum tauschii. Planta 217:831–840
Riechers DE, Kreuz K, Zhang Q (2010) Detoxification without intoxication: herbicide safeners activate plant defense gene expression. Plant Physiol 153:3–13
Rincón-Zachary M, Teaster ND, Sparks JA, Valster AH, Motes CM, Blancaflor EB (2010) Fluorescence resonance energy transfer-sensitized emission of yellow cameleon 3.60 reveals root zone specific calcium signatures in Arabidopsis in response to aluminum and other trivalent cations. Plant Physiol 152:1442–1458
Rishi A, Muni S, Kapur V, Nelson ND, Goyal A (2004) Identification and analysis of safener-inducible expressed sequence tags in Populus using a cDNA microarray. Planta 220:296–306
Ryan PR, Reid RJ, Smitth FA (1997) Direct evaluation of the Ca2+-displacement hypothesis for Al toxicity. Plant Physiol 113:1351–1357
Sasaki M, Yamamoto Y, Matsumoto H (1996) Lignin deposition induced by aluminum in wheat (Triticum aestivum) roots. Physiol Plant 96:193–198
Sasaki M, Yamamoto Y, Matsumoto H (1997) Aluminum inhibits growth and stability of cortical microtubules in wheat (Triticum aestivum) roots. Soil Sci Plant Nutr 43:469–472
Savchenko T, Kolla VA, Wang C-Q, Nasafi Z, Hicks DR, Phadungchob B, Chehab WE, Brandizzi F, Froehlich J, Dehesh K (2014) Functional convergence of oxylipin and abscisic acid pathways controls stomatal closure in response to drought. Plant Physiol 164:1151–1160
Schaller A, Stintzi A (2009) Enzymes in jasmonate biosynthesis: structure, function, regulation. Phytochemistry 70:1532–1538
Schmohl N, Horst WJ (2000) Cell wall pectin content modulates aluminum sensitivity of Zea mays (L.) cells grown in suspension culture. Plant Cell Envir 23:735–742
Schofield RMS, Pallon J, Fiskesjo G, Karlsson G, Malmqvist KG (1998) Aluminum and calcium distribution patterns in aluminum-intoxicated roots of Allium cepa do not support the calcium-displacement hypothesis and indicate signal-mediated inhibition of root growth. Planta 205:175–180
Schuck S, Kallenbach M, Baldwin IT, Bonaventure G (2014) The Nicotiana attenuata GLA1 lipase controls the accumulation of Phytophthora parasitica-induced oxylipins and defensive secondary metabolites. Plant Cell Environ 37:1703–1715
Schwarzerová K, Zelenková S, Nick P, Opatrny Z (2002) Aluminum-induced rapid changes in the microtubular cytoskeleton of tobacco cell lines. Plant Cell Physiol 43:207–216
Seju K, Lee Y (1998) Aluminum induces changes in the orientation of microtubules and the division plane in root meristem of Zea mays. J Plant Biol 41:269–276
Shen H, He LF, Sasaki T, Yamamoto Y, Zheng SJ, Ligaba A, Yan XL, Ahn SJ, Yamaguchi M, Sasakawa H, Matsumoto H (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress: up-regulation of transcription, translation, and threonine-oriented phosphorylation of plasma membrane H + -ATPase. Plant Physiol 138:287–296
Shen H, Ligaba A, Yamaguchi M, Osawa H, Shibata H, Yan X, Matsumoto H (2004) Effect of K-252a and abscisic acid on the efflux of citrate from soybean roots. J Exp Bot 55:663–671
Simoes CC, Melo JO, Magalhaes JV, Guimaraes CT (2012) Genetic and molecular mechanisms of aluminum tolerance in plants. Genet Mol Res 11:1949–1957
Silva IR, Smyth TJ, Moxley DF, Carter TE, Allen NS, Rufty TW (2002) Aluminum accumulation at nuclei of cells in the root tip. Fluorescence detection using lumogallion and confocal laser scanning microscopy. Plant Physiol 123:543–552
Sivaguru M, Baluska F, Volkmann D, Felle HH, Horst WJ (1999a) 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, Ezaki B, He ZH, Tong H, Osawa H, Baluška F, Volkmann D, Matsumoto H (2003a) Aluminum-induced gene expression and protein localization of a cell wall-associated receptor kinase in Arabidopsis. Plant Physiol 132:1–11
Sivaguru M, Fujiwara T, Samaj J, Baluška F, Yang Z, Osawa H, Maeda T, Mori T, Volkmann D, Matsumoto H (2000) Aluminum-induced 1→3-β-D-glucan inhibits cell-to-cell trafficking of molecules through plasmadesmata: a new mechanism of Al toxicity in plants. Plant Physiol 124:991–1005
Sivaguru M, Horst WJ (1998) The distal part of the transition zone is the most aluminum-sensitive apical zone of maize. Plant Physiol 116:155–163
Sivaguru M, Liu J, Kochian LV (2013) Targeted expression of SbMATE in the root distal transition zone is responsible for sorghum aluminum resistance. Plant J 76:297–307
Sivaguru M, Pike S, Gassmann W, Baskin TI (2003b) Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. Plant Cell Physiol 44:667–6745
Sivaguru M, Yamamoto Y, Matsumoto H (1999b) Diefferential impacts of aluminium on microtubules organization depends on growth phase in suspension-cultured tobacco cells. Physiol Plant 109:110–119
Skipsey M, Knight KM, Brazier-Hicks M, Dixon DP, Steel PG, Edwards R (2011) Xenobiotic responsiveness of Arabidopsis thaliana to a chemical series derived from a herbicide safener. J Biol Chem 286:32268–32276
Sun P, Tian QY, Chen J, Zhang WH (2010) Aluminum induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. J Exp Bot 65:347–356
Sun P, Tian QY, Zhao MG, Dai XY, Huang JH, Li LH, Zhang WH (2007) Aluminum-induced ethylene production is associated with inhibition of root elongation in Lotus japonicus L. Plant Cell Physiol 48:1229–1335
Tabuchi A, Mastumoto H (2001) Changes in cell-wall properties of wheat (Triticum aestivum) roots during aluminum-induced growth inhibition. Physiol Plant 112:353–358
Taki N, Sasaki-Sekimoto Y, Obayashi T, Kikuta A, Kobayashi K, Ainai T, Yagi K, Sakurai N, Suzuki H, Masuda T, Takamiya K-I, Shibata D, Kobayashi Y, Ohta H (2005) 12-Oxophytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis. Plant Physiol 139:1268–1283
Testerink C, Munnik T (2006) Phosphatidic acid: a multifunctional stress-signaling lipid in plants. Trends Plant Sci 10:368–375
Tian Q, Zhang X, Ramesh S, Gilliham M, Tyerman SD, Zhang W-H (2014) Ethylene negatively regulates aluminum-induced malate efflux from wheat roots and tobacco cells transformed with TaLALMT1. J Exp Bot 65:2415–2426
Tian Q-Y, Sun D-H, Zhao M-G, Zhang W-H (2007) Inhibition of nitric oxide synthase (NOS) underlines aluminum-induced inhibition of root elongation in Hibiscus moscheutos. New Phytol 174:322–331
Tice KP, Parker DR, DeMason DA (1992) Operationally defined apoplastic and symplastic aluminum fractions in root tips of aluminum-intoxicated wheat. Plant Physiol 100:309–318
Vicente J, Cascon T, Vicedo B, Garcia-Agustin P, Hamberg M, Castresana C (2012) Role of 9-lipoxygenase and α-dioxygenase oxylipin pathways as modulators of local and systemic defense. Mol Plant 5:914–928
Wagner U, Edwards R, Dixon DP, Mauch F (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol Biol 49:515–532
Walker PR, LeBlanc J, Sikorska M (1989) Effects of aluminum and other cations on the structure of brain and liver chromatin. Biochem 28:3911–39152
Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signalling in plants. Plant Cell Environ 31:622–631
Xia J, Yamaji N, Kasai T, Ma JF (2010) Plasma membrane-localized transporter for aluminum in rice. Proc Natl Acad Sci U S A 107:18381–18385
Xu FX, Lagudah ES, Moose SP, Riechers DE (2002) Tandemly-duplicated safener-induced glutathione S-transferase genes from Triticum tauschii contribute to genome- and organ-specific expression in hexaploid wheat. Plant Physiol 130:362–373
Yamaguchi Y, Yamamoto Y, Matsumoto H (1999) Cell death process initiates by a combination of aluminum and iron in suspension-cultured tobacco cells (Nicotiana tobacum): apoptosis-like cell death mediated by calcium and proteinase. Soil Sci Plant Nutr 45:647–657
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
Yamamoto Y, Kobayashi Y, Rama DS, Rikiishi S, Matasumoto H (2002) Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol 128:63–72
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
Yang JL, Zhu XF, Peng YX, Zheng CJ, Li GX, Liu Y, Shi YZ, Zheng SJ (2011a) Cell wall hemicelluloses contribute significantly to aluminum adsorption and root growth in Arabidopsis. Plant Physiol 155:1885–1892
Yang L, Tian D, Todd CD, Luo Y, Hu X (2013) Comparative proteome analyses reveal that nitric oxide is an important signal molecule in the response of rice to aluminum toxicity. J Proteome Res 1:1316–1330
Yang ZM, Nian H, Sivaguru M, Tanakamaru S, Matsumoto H (2001) Characterization of aluminium-induced citrate secretion in aluminium-tolerant soybean (Glycine max) plants. Physiol Plant 113:64–71
Yang Y, Wang QL, Geng MJ, Guo ZH, Zhao Z (2011b) Effect of indole-3-acetic acid on aluminum-induced efflux of malic acid from wheat (Triticum aestivum L.). Plant Soil 346:215–230
Yin L, Mano J, Wang S, Tsuji W, Tanaka K (2010a) The involvement of lipid peroxide-derived aldehydes in aluminum toxicity of tobacco roots. Plant Physiol 152:1406–1417
Yin L, Wang S, Eltayeb AE, Uddin Md I, Yamamoto Y, Tsuji W, Takeuchi Y, Tanaka K (2010b) Over-expression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231:609–621
Zhan J, He H-Y, Wang T-J, Wang A-Q, Li C-Z, He L-F (2013) Aluminum-induced programmed cell death promoted by AhSAG, a senescence-associated gene in Arachis hypoganea L. Plant Sci 210:108–117
Zhang H, Shi W, You JF, Bian MD, Qin XM, Yu H, Liu Q, Ryan PR, Yang ZM (2015) Transgenic Arabidopsis thaliana plants expressing a β-1,3-glucanase from sweet sorghum (Sorghum bicolor L.) show reduced callose deposition and increase tolerance to aluminum toxicity. Plant Cell Environ 38:1178–1188
Zhang Q, Xu FX, Lambert KN, Riechers DE (2007) Safeners coordinately induce the expression of multiple proteins and MRP transcripts involved in herbicide metabolism and detoxification in Triticum tauschii seedling tissues. Proteomics 7:1261–1278
Zhang SJ, Yang JL (2005) Target sites of aluminum phytotoxicity. Biol Plant 49:321–331
Zhang WH, Rengel Z (1999) Aluminum induces an increase in cytoplasmic calcium in intact wheat root apical cells. Aust J Plant Physiol 26:401–409
Zhao M-G, Tian G-Y, Zhang W-H (2007) Ethylene activates a plasma membrane Ca2+ permeable channel in tobacco suspension cells. New Phytol 174:507–515
Zhou G, Ren N, Qi J, Lu J, Xiang C, Ju H, Cheng J, Lou Y (2014) The 9-lipoxygenase Osr9-LOX1 interacts with the 13-lipoxygenase-mediated pathway to regulate resistance to chewing and piercing-sucking herbivores in rice. Physiol Plant 152:59–69
Zhu XF, Lei GJ, Wang ZW, Shi YZ, Braam J, Li GX, Zheng SJ (2013) Coordination between apoplastic and symplastic detoxification confers plant aluminum resistance. Plant Physiol 162:1947–1955
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Matsumoto, H., Riechers, D.E., Lygin, A.V., Baluška, F., Sivaguru, M. (2015). Aluminum Signaling and Potential Links with Safener-Induced Detoxification in Plants. In: Panda, S., Baluška, F. (eds) Aluminum Stress Adaptation in Plants. Signaling and Communication in Plants, vol 24. Springer, Cham. https://doi.org/10.1007/978-3-319-19968-9_1
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