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Aluminum Stress Adaptation in Plants pp 187–202Cite as

Physiological and Molecular Regulation of Aluminum Resistance in Woody Plant Species

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Part of the Signaling and Communication in Plants book series (SIGCOMM,volume 24)

Abstract

Aluminum (Al) is the main limiting factor for plant growth in acid soils. Woody plant species are well adapted to acid soils with high Al3+ concentration. The external resistance mechanisms comprise Al immobilization in the rhizosphere (Al excluders) and internal ones include complexation of Al in cells (Al accumulators). This chapter provides a critical analysis of the physiological and molecular regulation of Al-resistance mechanisms in woody plant species.

Keywords

  • Woody Plant Species
  • Organic Acid Anion
  • Highbush Blueberry
  • Vaccinium Corymbosum
  • Photochemical Parameter

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  • Adams WWIII, Zarter CR, Ebbert V, Demmig-Adams B (2004) Photoprotective strategies of overwintering evergreens. Bioscience 54:41–49

    CrossRef  Google Scholar 

  • Ahonen-Jonnarth U, Göransson A, Finlay RD (2003) Growth and nutrient uptake of ectomycorrhizal Pinus sylvestris seedlings in a natural substrate treated with elevated Al concentrations. Tree Physiol 23:157–167

    CrossRef  CAS  PubMed  Google Scholar 

  • Akaya M, Takenaka C (2001) Effects of aluminum stress on photosynthesis of Quercus glauca Thumb. Plant Soil 237:137–146

    CrossRef  CAS  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

    CrossRef  Google Scholar 

  • Basu U, Godbold D, Tayor GJ (1994) Aluminum resistance in Triticum aestivum associated with enhanced exudation of malate. J Plant Physiol 144:747–753

    CrossRef  CAS  Google Scholar 

  • Britez RM, Reismann CB, Silva SM, Athayde SF, Lima RX, de Quadros RMB (1997) Chemical characterization of two forests on the coastal plain of the Ilha do Mel, Paraná, Brazil. In: Ando T, Fujita K, Mae T, Matsumoto H, Mori S, Sekiya J (eds) Plant nutrition – for sustainable food production and environment. Kluwer, Dordrecht, pp 461–462

    CrossRef  Google Scholar 

  • Britez RM, Watanabe T, Jansen S, Reissmann CB, Osaki M (2002) The relationship between aluminium and silicon accumulation in leaves of Faramea marginata (Rubiaceae). New Phytol 156:445–456

    CrossRef  Google Scholar 

  • Chen LS (2006) Physiological responses and tolerance of plant shoot to aluminum toxicity. J Plant Physiol Mol Biol 32:143–155

    Google Scholar 

  • Chen LS, Qi Y-P, Smith BR, Liu X-H (2005a) Aluminium-induced decrease in CO2 in citrus seedlings is unaccompanied by decreased activities of key enzymes involved in CO2 assimilation. Tree Physiol 25:317–324

    CrossRef  CAS  PubMed  Google Scholar 

  • Chen LS, Qi Y-P, Liu X-H (2005b) Effects of aluminum on light energy utilization and photoprotective systems in citrus leaves. Ann Bot 96:35–41

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Cousins AB, Adam NR, Wall GW, Kimball BA, Pinter PJ Jr, Ottman MJ, Leavitt SW, Webber AN (2002) Photosystem II energy use, non-photochemical quenching and the xanthophyll cycle in Sorghum bicolor grown under drought and free-air CO2 enrichment (FACE) conditions. Plant Cell Environ 25:1551–1559

    CrossRef  CAS  Google Scholar 

  • De Medeiros RA, Haridasan M (1985) Seasonal variations in the foliar concentrations of nutrients in some aluminium accumulating and non-accumulating species of the cerrado region of central Brazil. Plant Soil 88:433–436

    CrossRef  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Delhaize E, Ma JP, Ryan PR (2012) Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci 17:341–347

    CrossRef  CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Adams WW III (1996) The role of xantophyll cycle carotenoids in the protection of photosynthesis. Trends Plants Sci 1:21–26

    CrossRef  Google Scholar 

  • 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 aluminium tolerance. Planta 230:355–365

    CrossRef  CAS  PubMed  Google Scholar 

  • 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

    CrossRef  CAS  Google Scholar 

  • Emmanuel D, Peter PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321

    Google Scholar 

  • Eticha D, The C, Welcker C, Narro L, Staß A, Horst WJ (2005) Aluminium-induced callose formation in root apices: inheritance and selection trait for adaptation of tropical maize to acid soils. Field Crops Res 93:252–263

    CrossRef  Google Scholar 

  • Förster B, Osmond CB, Boynton JE (2001) Very high light resistant mutants of Chlamydomonas reinhardtii: responses of photosystem II, nonphotochemical quenching and xanthophyll pigments to light and CO2. Photosynth Res 67:5–15

    CrossRef  PubMed  Google Scholar 

  • González-Santana IH, Márquez-Guzmán J, Cram-Heydrich S, Cruz-Ortega R (2012) Conostegia xalapensis (Melastomataceae): an aluminum accumulator plant. Physiol Plant 144:134–145

    CrossRef  PubMed  CAS  Google Scholar 

  • Grisel N, Zoller S, Künzli-Gontarczyk M, Lampart T, Münsterkötter M, Brunner I, Bovet L, Métraux JP, Sperisen C (2010) Transcriptome responses to aluminum stress in roots of aspen (Populus tremula). Plant Biol 10:185

    Google Scholar 

  • Hanson JB (1984) The functions of calcium in plant nutrition. In: Tinker PB, Lauchli A (eds) Advances in plant nutrition, vol 1. Praeger Scientific, New York, NY, pp 149–208

    Google Scholar 

  • Haridasan M (2008) Nutritional adaptations of native plants of the cerrado biome in acid soils. Rev Brasil Fisiol Veg 20:183–195

    Google Scholar 

  • Heim A, Brunner I, Frey B, Frossard E, Luster J (2001) Root exudation, organic acids, and element distribution in roots of Norway spruce seedlings treated with aluminium in hydroponics. J Plant Nutr Soil Sci 164:519–526

    CrossRef  CAS  Google Scholar 

  • Heim A, Brunner I, Frossard E, Luster J (2003) Aluminum effects on Picea abies at low solution concentrations. Soil Sci Soc Am J 67:895–898

    CrossRef  CAS  Google Scholar 

  • Hirano Y, Graf-Pannatier E, Zimmermann S, Brunner I (2004) Induction of callose in roots of Norway spruce seedlings after short-term exposure to aluminum. Tree Physiol 24:1279–1283

    CrossRef  CAS  PubMed  Google Scholar 

  • 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

    CrossRef  CAS  PubMed  Google Scholar 

  • Hirano Y, Frey B, Brunner I (2012) Contrasting reactions of roots of two coniferous tree species to aluminum stress. Environ Exp Bot 77:2–18

    CrossRef  CAS  Google Scholar 

  • Horst WJ (1995) The role of the apoplast in aluminium toxicity and resistance of higher plants: a review. Zeitschrift für Pflanzenernährung und Bodenkunde 158:419–428

    CrossRef  CAS  Google Scholar 

  • Horst WJ, Püschel AK, Schmohl N (1997) Induction of callose formation is a sensitive marker for genotypic aluminium sensitivity in maize. Plant Soil 192:23–30

    CrossRef  CAS  Google Scholar 

  • Ikka T, Ogawa T, Li D, Hiradate S, Morita A (2013) Effect of aluminum on metabolism of organic acids and chemical forms of aluminum in root tips of Eucalyptus camaldulensis Dehnh. Phytochemistry 94:142–147

    CrossRef  CAS  PubMed  Google Scholar 

  • Inostroza-Blancheteau C, Aquea F, Reyes-Díaz M, Alberdi M, Arce-Johnson P (2011) Identification of aluminum-regulated genes by cDNA-AFLP analysis of roots in two contrasting genotypes of highbush blueberry (Vaccinium corymbosum L.). Mol Biotechnol 49:32–41

    CrossRef  CAS  PubMed  Google Scholar 

  • Inostroza-Blancheteau C, Rengel Z, Alberdi M, Mora ML, Aquea F, Arce-Johnson P, Reyes-Díaz M (2012) Molecular and physiological strategies to increase aluminum resistance in plants. Mol Biol Rep 39:2069–2079

    CrossRef  CAS  PubMed  Google Scholar 

  • Inostroza-Blancheteau C, Aquea F, Loyola R, Slovin J, Josway S, Rengel Z, Reyes-Díaz M, Alberdi M, Arce-Johnson P (2013) Molecular characterisation of a calmodulin gene, VcCaM1, that is differentially expressed under aluminium stress in highbush blueberry. Plant Biol 15:1013–1018

    CrossRef  CAS  PubMed  Google Scholar 

  • Iuchi S, Koyama H, Iuchi A, Kobayashi Y, Kitabayashi S, Kobayashi Y, Ikka T, Hirayama T, Shinozaki K, Kobayashi M (2007) Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc Natl Acad Sci U S A 14:9900–9905

    CrossRef  CAS  Google Scholar 

  • Jansen S, Watanabe T, Dessein S, Smets E, Robbrecht E (2003) A comparative study of metal levels in leaves of some Al-accumulating Rubiaceae. Ann Bot 91:657–663

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Jiang HX, Chen LS, Zheng JG, Han S, Tang N, Smith B (2008) Aluminum-induced effects on photosystem II photochemistry in Citrus leaves assessed by the chlorophyll a fluorescence transient. Tree Physiol 28:1863–1871

    CrossRef  CAS  PubMed  Google Scholar 

  • Jiang H-X, Tang N, Zheng J-G, Li Y, Chen L-S (2009) Phosphorus alleviates aluminum-induced inhibition of growth and photosynthesis in Citrus grandis seedlings. Physiol Plant 137:298–311

    CrossRef  CAS  PubMed  Google Scholar 

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

    CrossRef  CAS  PubMed  Google Scholar 

  • Jorns AC, Hecht-Buchholz C, Wissemeier AH (1991) Aluminum-induced callose formation in root tips of Norway spruce (Picea abies (L.) Karst.). Z Pflanzenernähr Bodenk 154:349–353

    CrossRef  CAS  Google Scholar 

  • Kasai M, Sasaki M, Yamamoto Y, Matsumoto H (1992) Al increases K+ efflux and activities of ATP-dependent and PPi-dependent H+ pumps of tonoplast-enriched vesicles from barley roots. Plant Cell Physiol 33:1035–1039

    CAS  Google Scholar 

  • Kaus H (1987) Some aspects of calcium dependent regulation in plant metabolism. Annu Rev Plant Physiol 38:47–72

    CrossRef  Google Scholar 

  • Keltjens WG, Ulden PSR (1987) Effect of Al on nitrogen (NH4 + and NO3 −) uptake, nitrate reductase activity and proton release in two sorghum cultivars different in Al tolerance. Plant Soil 104:227–234

    CrossRef  CAS  Google Scholar 

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

    CrossRef  CAS  PubMed  Google Scholar 

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

    CrossRef  CAS  Google Scholar 

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

    CrossRef  CAS  PubMed  Google Scholar 

  • Koyama H, Toda T, Hara T (2001) Brief exposure to low-pH stress causes irreversible damage to the growing root in Arabidopsis thaliana: pectin-Ca interaction may play an important role in proton rhizotoxicity. J Exp Bot 52:361–368

    CrossRef  CAS  PubMed  Google Scholar 

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

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Lidon FC, Barreiro MG, Ramalho JDC, Lauriano JA (1999) Effects of aluminium toxicity on nutrient accumulation in maize shoots: implications on photosynthesis. J Plant Nutr 22:397–416

    CrossRef  CAS  Google Scholar 

  • Logan BA, Demmig-Adams B, Adams W III (1998) Antioxidant and xanthophylls cycle-dependent energy dissipation in Cucurbita pepo L. and Vinca major L. upon a sudden increase in growth PPFD in the field. J Exp Bot 49:1881–1888

    CrossRef  CAS  Google Scholar 

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

    CrossRef  CAS  PubMed  Google Scholar 

  • Masunaga T, Kubota T, Hotta M, Wakatsuki T (1998) Mineral composition of leaves and bark in aluminum accumulators in a tropical rain forest in Indonesia. Soil Sci Plant Nutr 44:347–358

    CrossRef  CAS  Google Scholar 

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

    CrossRef  CAS  PubMed  Google Scholar 

  • Matsumoto H, Hirasawa E, Morimura S, Takahashi E (1976) Localization of aluminium in tea leaves. Plant Cell Physiol 17:627–631

    CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. J Exp Bot 51:659–668

    CrossRef  CAS  PubMed  Google Scholar 

  • Mizuno S, Ayabe S, Uchiyama H (2014) Expression of genes encoding transporters and enzyme proteins in response to low-pH and high-aluminum treatments in Acacia mangium, a stress-tolerant legume. Plant Biotechnol 31:61–66

    CrossRef  CAS  Google Scholar 

  • Mora ML, Alfaro M, Williams PH, Stehr W, Demanet R (2004) Effect of fertilizer input on soil acidification in relation to growth and chemical composition of a pasture and animal production. J Soil Sci Plant Nutr (Chile) 4:29–40

    Google Scholar 

  • Mora ML, Demanet R, Vistoso E, Gallardo F (2005) Influence of sulfate concentration in mineral solution on ryegrass grown at different pH and aluminium levels. J Plant Nutr 28:1–16

    CrossRef  CAS  Google Scholar 

  • Morita A, Yanagisawa O, Maeda S, Takatsu S, Ikka T (2011) Tea plant (Camellia sinensis L.) roots secrete oxalic acid and caffeine into medium containing aluminium. Soil Sci Plant Nutr 57:796–802

    CrossRef  CAS  Google Scholar 

  • Moustakas M, Ouzounidou G, Eleftherios PE, Lannoye R (1995) Aluminum effect on photosynthesis and elemental uptake in an aluminum-tolerant and non-tolerant wheat cultivar. J Plant Nutr 18:669–683

    CrossRef  CAS  Google Scholar 

  • Naik D, Smith E, Cumming JR (2009) Rhizosphere carbon deposition, oxidative stress and nutritional changes in two poplar species exposed to aluminum. Tree Physiol 29:423–436

    CrossRef  CAS  PubMed  Google Scholar 

  • Nguyen NT, Nakabayashi K, Thompson J, Fujita K (2003) Role of exudation of organic acids and phosphate in aluminum tolerance of four tropical woody species. Tree Physiol 23:1041–1050

    CrossRef  CAS  PubMed  Google Scholar 

  • Niyogi KK, Björkman O, Grossman AR (1997) The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci U S A 94:14162–14167

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Nunes-Nesi A, Brito DS, Inostroza-Blancheteau C, Fernie AR, Araújo WL (2014) The complex role of mitochondrial metabolism in plant aluminum resistance. Trends Plant Sci 19:399–407

    CrossRef  CAS  PubMed  Google Scholar 

  • 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

    CrossRef  CAS  Google Scholar 

  • Ohyama Y, Ito H, Kobayashi Y, Ikka T, Morita A, Kobayashi M, Imaizumi R, Aoki T, Komatsu K, Sakata Y, Iuchi S, Koyama H (2013) Characterization of AtSTOP1 orthologous genes in tobacco and other plant species. Plant Physiol 162:1937–1946

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Osawa H, Kojima K (2006) Citrate-release-mediated aluminum resistance is coupled to the inducible expression of mitochondrial citrate synthase gene in Paraserianthes falcataria. Tree Physiol 26:565–574

    CrossRef  CAS  PubMed  Google Scholar 

  • Osawa H, Endo I, Hara Y, Matsushima Y, Tange T (2011) Transient proliferation of proanthocyanidin-accumulating cells on the epidermal apex contributes to highly aluminum-resistant root elongation in camphor tree. Plant Physiol 155:433–446

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Peixoto PHP, Da Matta FM, Cambraia J (2002) Responses of the photosynthetic apparatus to aluminum stress in two sorghum cultivars. J Plant Nutr 25:821–832

    CrossRef  CAS  Google Scholar 

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

    CrossRef  CAS  Google Scholar 

  • Pereira WE, de Siqueira DL, Martinez CA, Puiatti M (2000) Gas exchange and chlorophyll fluorescence in four citrus rootstocks under aluminum stress. J Plant Physiol 157:513–520

    CrossRef  CAS  Google Scholar 

  • Pereira WE, Lopes de Siqueira D, Puiatti M, Martínez CA, Salomão LCC, Cecon PR (2003) Growth of citrus rootstocks under aluminium stress in hydroponics. Sci Agric 60:31–41

    CrossRef  CAS  Google Scholar 

  • Piñeros MA, Shaff JE, Manslank S, Carvalho A, Vera M, Kochian LV (2005) Aluminum resistance in maize cannot be solely explained by root organic exudation. A comparative physiological study. Plant Physiol 137:231–241

    CrossRef  PubMed Central  PubMed  CAS  Google Scholar 

  • Qin R, Hirano Y, Brunner I (2007) Exudation of organic acid anions from poplar roots after exposure to Al, Cu and Zn. Tree Physiol 27:313–320

    CrossRef  CAS  PubMed  Google Scholar 

  • Rengel Z (1992) Role of calcium in aluminium toxicity. New Phytol 121:499–513

    CrossRef  CAS  Google Scholar 

  • Rengel Z (1996) Uptake of aluminium by plant cells. New Phytol 134:389–406

    CrossRef  CAS  Google Scholar 

  • Rengel Z, Zhang W-H (2003) Role of dynamics of intracellular calcium in aluminium-toxicity syndrome. New Phytol 159:295–314

    CrossRef  CAS  Google Scholar 

  • Reyes-Diaz M, Alberdi M, Mora ML (2009) Short-term aluminum stress differentially affects the photochemical efficiency of photosystem II in highbush blueberry genotypes. J Am Soc Hort Sci 134:14–21

    Google Scholar 

  • Reyes-Díaz M, Inostroza-Blancheteau C, Millaleo R, Cruces E, Wulff-Zottele C, Alberdi M, Mora ML (2010) Long-term aluminum exposure effects on physiological and biochemical features of highbush blueberry cultivars. J Am Soc Hort Sci 135:212–222

    Google Scholar 

  • Ridolfi M, Garrec JP (2000) Consequences of an excess Al and a deficiency in Ca and Mg for stomatal functioning and net carbon assimilation of beech leaves. Ann For Sci 57:209–218

    CrossRef  Google Scholar 

  • Rout GR, Samantaray S, Das P (2001) Aluminium toxicity in plants: a review. Agronomie 21:3–21

    CrossRef  Google Scholar 

  • Ruban AV, Horton P (1999) The xanthophyll cycle modulates the kinetics of nonphotochemical energy dissipation in isolated light-harvesting complexes, intact chloroplasts, and leaves of spinach. Plant Physiol 119:531–542

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Ryan PR, Delhaize E (2010) The convergent evolution of aluminum resistance in plants exploits a convenient currency. Funct Plant Biol 37:275–284

    CrossRef  CAS  Google Scholar 

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

    CrossRef  CAS  PubMed  Google Scholar 

  • Sawaki Y, Iuchi S, Kobayashi Y, Ikka T, Sakurai N, Fujita M, Shinozaki K, Shibata D, Kobayashi M, Koyama H (2009) STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities. Plant Physiol 150:281–294

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Sawaki Y, Kihara-Doi T, Kobayashi Y, Nishikubo N, Kawazu T, Kobayashi Y, Koyama H, Sato S (2013) Characterization of Al-responsive citrate excretion and citrate-transporting MATEs in Eucalyptus camaldulensis. Planta 237:979–989

    CrossRef  CAS  PubMed  Google Scholar 

  • Sawaki Y, Kobayashi Y, Kihara-Doic T, Nishikubo N, Kawazuc T, Kobayashi M, Kobayashi Y, Iuchi S, Koyama H, Sato S (2014) Identification of a STOP1-like protein in Eucalyptus that regulates transcription of Al tolerance genes. Plant Sci 223:8–15

    CrossRef  CAS  PubMed  Google Scholar 

  • Schroeder JI, Delhaize E, Frommer WB, Guerinot ML, Harrison MJ, Herrera-Estrella L, Horie T, Kochian LV, Munns R, Nishizawa NK, Tsay YF, Sanders D (2013) Using membrane transporters to improve crops for sustainable food production. Nature 497:60–66

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Setlik I, Allakhveridiev SI, Nedbal L, Setlikova E, Klimov VV (1990) Three types of Photosystem II photoinactivation. I. Damaging process on the acceptor side. Photosynth Res 23:39–48

    CrossRef  CAS  PubMed  Google Scholar 

  • Silva IR, Novais RF, Jham GN, Barros NF, Gebrim FO, Nunes FN (2004) Responses of eucalypt species to aluminum: the possible involvement of low molecular weight organic acids in the Al tolerance mechanism. Tree Physiol 24:1267–1277

    CrossRef  CAS  PubMed  Google Scholar 

  • Smith E, Naik D, Cumming JR (2011) Genotypic variation in aluminum resistance, cellular aluminum fractions, callose and pectin formation and organic acid accumulation in roots of Populus hybrids. Environ Exp Bot 72:182–193

    CrossRef  CAS  Google Scholar 

  • Soto-Cerda BJ, Inostroza-Blancheteau C, Mathias M, Penaloza E, Zuñiga J, Muñoz G, Rengel Z, Salvo-Garrido H (2015) Marker-assisted breeding for TaALMT1, a major gene conferring aluminium tolerance to wheat. Biol Plant 59(1):83–91

    CrossRef  CAS  Google Scholar 

  • Stass A, Smit I, Eticha D, Oettler G, Horst WJ (2008) The significance of organic anion exudation for the aluminum resistance of primary triticale derived from wheat and rye parents differing in aluminum resistance. J Plant Nutr Soil Sci 171:634–682

    CrossRef  CAS  Google Scholar 

  • Tahara K, Norisada M, Tange T, Yagi H, Kojima K (2005) Ectomycorrhizal association enhances Al tolerance by inducing citrate secretion in Pinus densiflora. Soil Sci Plant Nutr 51:397–403

    CrossRef  CAS  Google Scholar 

  • Tahara K, Yamanoshita T, Norisada M, Hasegawa I, Kashima H, Sasaki S, Kojima K (2008a) Aluminum distribution and reactive oxygen species accumulation in root tips of two Melaleuca trees differing in aluminum resistance. Plant Soil 307:167–178

    CrossRef  CAS  Google Scholar 

  • Tahara K, Norisada M, Yamanoshita T, Kojima K (2008b) Role of binding ligands in aluminum resistance of Eucalyptus camaldulensis and Melaleuca cajuputi. Plant Soil 302:175–187

    CrossRef  CAS  Google Scholar 

  • Tahara K, Hashida K, Otsuka Y, Ohara S, Kojima K, Shinohara K (2014) Identification of a hydrolyzable tannin, oenothein B, as an aluminum-detoxifying ligand in a highly aluminum-resistant tree, Eucalyptus camaldulensis. Plant Physiol 164:683–693

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Tamás L, Hutttová J, Mistrík I, Simonovicová B (2006) Aluminium-induced drought and oxidative stress in barley roots. J Plant Physiol 163:781–784

    CrossRef  PubMed  CAS  Google Scholar 

  • Taylor GJ, Basu A, Basu U, Slaski JJ, Zhang G, Good A (1997) Al-induced 51-kilodalton membrane-bound proteins are associated with resistance to Al in a segregating population of wheat. Plant Physiol 114:363–372

    PubMed Central  CAS  PubMed  Google Scholar 

  • von Uexkull HR, Mutert E (1995) Global extent, development and economic impact of acid soils. In: Date RA, Grundon NJ, Rayment GE, Probert ME (eds) Plant–soil interactions at low pH: principles and management. Kluwer, Dordrecht, pp 5–19

    CrossRef  Google Scholar 

  • Wagatsuma T, Yamasaka K (1985) Relationship between differential aluminum tolerance and plant-induced pH change of medium among barley cultivars. Soil Sci Plant Nutr 31:521–535

    CrossRef  CAS  Google Scholar 

  • Wannaz ED, Rodriguez JH, Wolfsberger T, Carreras HA, Pignata ML, Fangmeier A, Franzaring J (2012) Accumulation of aluminium and physiological status of tree foliage in the vicinity of a large aluminium smelter. Sci World J 7. doi:10.1100/2012/865927

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

    CrossRef  CAS  Google Scholar 

  • Watanabe T, Osaki M, Yoshihara T, Tadano T (1998) Distribution and chemical speciation of aluminum in the Al accumulator plant, Melastoma malabathricum L. Plant Soil 201:165–173

    CrossRef  CAS  Google Scholar 

  • Wissemeier AH, Klotz F, Horst WJ (1987) Aluminum induced callose synthesis in roots of soybean. J Plant Physiol 129:487–492

    CrossRef  CAS  Google Scholar 

  • Wissemeier AH, Hahn G, Marschner H (1998) Callose in roots of Norway spruce (Picea abies (L.) Karst.) is a sensitive parameter for aluminum supply at a forest site (Höglwald). Plant Soil 199:53–57

    CrossRef  CAS  Google Scholar 

  • Yamaji N, Huang CF, Nagao S, Yano M, Sato Y, Nagamura Y, Ma JF (2009) A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell 21:3339–3349

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

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

    CrossRef  PubMed Central  CAS  PubMed  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

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Yamane Y, Kashino Y, Koile H, Satoh K (1997) Increase in the fluorescence F0 level reversible inhibition of Photosystem II reaction center by high-temperature treatments in higher plants. Photosynth Res 52:57–64

    CrossRef  CAS  Google Scholar 

  • Yang LT, Jiang HX, Tang N, Chen LS (2011) Mechanisms of aluminum-tolerance in two species of citrus: secretion of organic acid anions and immobilization of aluminum by phosphorus in roots. Plant Sci 189:521–530

    CrossRef  CAS  Google Scholar 

  • Yang LT, Jiang H, Qi YP, Chen LS (2012) Differential expression of genes involved in alternative glycolytic pathways, phosphorus scavenging and recycling in response to aluminum and phosphorus interactions in Citrus roots. Mol Biol Rep 39:6353–6366

    CrossRef  CAS  PubMed  Google Scholar 

  • Zúñiga R, Alberdi M, Reyes-Díaz M, Olivares E, Hess S, Bravo LA, Corcuera LJ (2006) Seasonal changes in the photosynthetic performance of two evergreen Nothofagus species in south central Chile. Rev Chil Hist Nat 79:489–504

    CrossRef  Google Scholar 

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Authors and Affiliations

  1. Departamento de Ciencias Químicas y Recursos Naturales, Facultad de Ingeniería y Ciencias, Universidad de La Frontera, 54-D, Temuco, Chile

    Marjorie Reyes-Díaz

  2. Center of Plant, Soil Interaction and Natural Resources Biotechnology, Scientific and Technological Bioresource Nucleus (BIOREN), Universidad de La Frontera, Temuco, Chile

    Marjorie Reyes-Díaz

  3. Núcleo de Investigación en Producción Alimentaria (NIPA), Facultad de Recursos Naturales, Universidad Católica de Temuco, 56-D, Temuco, Chile

    Claudio Inostroza-Blancheteau

  4. Escuela de Agronomía, Facultad de Recursos Naturales, Universidad Católica de Temuco, Temuco, Chile

    Claudio Inostroza-Blancheteau

  5. Soil Science and Plant Nutrition, School of Earth and Environment, The University of Western Australia, Crawley, WA, 6009, Australia

    Zed Rengel

Authors
  1. Marjorie Reyes-Díaz
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  2. Claudio Inostroza-Blancheteau
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  3. Zed Rengel
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Corresponding author

Correspondence to Marjorie Reyes-Díaz .

Editor information

Editors and Affiliations

  1. Assam University, Silchar, India

    Sanjib Kumar Panda

  2. Department of Plant Cell Biology, IZMB, University of Bonn, Bonn, Germany

    František Baluška

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Reyes-Díaz, M., Inostroza-Blancheteau, C., Rengel, Z. (2015). Physiological and Molecular Regulation of Aluminum Resistance in Woody Plant Species. 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_10

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