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Molecular Mechanism of Aluminum Tolerance in Plants: An Overview

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Plant Metal and Metalloid Transporters
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Abstract

Aluminum (Al) is a metal that is abundantly available in the earth’s crust in various forms. Though Al has some beneficial role in selected plants, its toxicity and stress symptoms are a matter of concern to agriculturists. Aluminum at high concentration can severely damage a crop by affecting its root system and limiting the uptake of nutrients. As a consequence, the productivity of the plant is diminished. The plant, however, has devised several tolerance mechanisms through which the can combat stress. These mechanisms primarily involve restriction of Al either outside the plant’s body or compartmentalization of the metal in a subcellular location thereby limiting its reactivity. A wide array of organic acids are involved in this process, and all are exuded by their transporters. These transporter proteins are synthesized from their respective genes, each of which has several transcription factors. This chapter is an attempt to overview the Al tolerance mechanism of a plant at the molecular level. Efforts have been made to highlight the functions of various transporters involved in the process.

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References

  • Ahmed IM, Nadira UA, Cao F, He X, Zhang G, Wu F (2016) Physiological and molecular analysis on root growth associated with the tolerance to aluminum and drought individual and combined in Tibetan wild and cultivated barley. Planta 243(4):973–985

    Article  CAS  PubMed  Google Scholar 

  • Ambachew D, Blair MW (2021) Genome wide association mapping of root traits in the andean genepool of common bean (Phaseolus vulgaris L.) grown with and without aluminum toxicity. Front Plant Sci 12:825

    Article  Google Scholar 

  • Antico CJ, Colon C, Banks T, Ramonell KM (2012) Insights into the role of jasmonic acid-mediated defenses against necrotrophic and biotrophic fungal pathogens. Front Biol 7(1):48–56

    Article  CAS  Google Scholar 

  • Arenhart RA, Margis R, Margis-Pinheiro M (2012) The rice ASR5 protein: a putative role in the response to aluminum photosynthesis disturbance. Plant Signal Behav 7:1263–1266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arenhart RA, Lima JC, Pedron M, Carvalho FE, Silveira JA, Rosa SB, Caverzan A, Andrade CM, Schünemann M, Margis R, Margis-Pinheiro M (2013) Involvement of ASR genes in aluminium tolerance mechanisms in rice. Plant Cell Environ 36(1):52–67

    Article  CAS  PubMed  Google Scholar 

  • Arenhart RA, Schunemann M, Bucker Neto L, Margis R, Wang ZY, Margis-Pinheiro M (2016) Rice ASR1 and ASR5 are complementary transcription factors regulating aluminium responsive genes. Plant Cell Environ 39(3):645–651

    Article  CAS  PubMed  Google Scholar 

  • Awasthi JP, Saha B, Regon P, Sahoo S, Chowra U, Pradhan A, Roy A, Panda SK (2017) Morpho-physiological analysis of tolerance to aluminum toxicity in rice varieties of north East India. PLoS One 12(4):e0176357

    Article  PubMed  PubMed Central  Google Scholar 

  • Blancaflor EB, Jones DL, Gilroy S (1998) Alterations in the cytoskeleton accompany aluminum-induced growth inhibition and morphological changes in primary roots of maize. Plant Physiol 118(1):159–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bojórquez-Quintal E, Escalante-Magaña C, Echevarría-Machado I, Martínez-Estévez M (2017) Aluminum, a friend or foe of higher plants in acid soils. Front Plant Sci 8:1767

    Article  PubMed  PubMed Central  Google Scholar 

  • Bonomelli C, Artacho P (2021) Aluminum toxicity in sweet cherry trees grown in an acidic volcanic soil. Agronomy 11(6):1259

    Article  CAS  Google Scholar 

  • Bose J, Babourina O, Rengel Z (2011) Role of magnesium in alleviation of aluminium toxicity in plants. J Exp Bot 62(7):2251–2264

    Article  CAS  PubMed  Google Scholar 

  • Brunner I, Sperisen C (2013) Aluminum exclusion and aluminum tolerance in woody plants. Front Plant Sci 4:172

    Article  PubMed  PubMed Central  Google Scholar 

  • Cárcamo MP, Reyes-Díaz M, Rengel Z, Alberdi M, Omena-Garcia RP, Nunes-Nesi A, Inostroza-Blancheteau C (2019) Aluminum stress differentially affects physiological performance and metabolic compounds in cultivars of highbush blueberry. Sci Rep 9(1):1–3

    Article  Google Scholar 

  • Che J, Yamaji N, Shen RF, Ma JF (2016) An Al-inducible expansin gene, OsEXPA10 is involved in root cell elongation of rice. Plant J 88:132–142

    Article  CAS  PubMed  Google Scholar 

  • Che J, Tsutsui T, Yokosho K, Yamaji N, Ma JF (2018) Functional characterization of an aluminum (Al)-inducible transcription factor, ART2, revealed a different pathway for Al tolerance in rice. New Phytol 220:209–218

    Article  CAS  PubMed  Google Scholar 

  • Chen ZC, Yamaji N, Motoyama R, Nagamura Y, Ma JF (2012) Up-regulation of a magnesium transporter gene OsMGT1 is required for conferring aluminum tolerance in rice. Plant Physiol 159(4):1624–1633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Q, Wu KH, Wang P, Yi J, Li KZ, Yu YX, Chen LM (2013a) Overexpression of MsALMT1, from the aluminum-sensitive Medicago sativa, enhances malate exudation and aluminum resistance in tobacco. Plant Mol Biol Rep 31(3):769–774

    Article  Google Scholar 

  • Chen ZC, Yokosho K, Kashino M, Zhao FJ, Yamaji N, Ma JF (2013b) Adaptation to acidic soil is achieved by increased numbers of cis-acting elements regulating ALMT1 expression in Holcus lanatus. Plant J 76(1):10–23

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daspute AA, Kobayashi Y, Panda SK, Fakrudin B, Kobayashi Y, Tokizawa M, Iuchi S, Choudhary AK, Yamamoto YY, Koyama H (2018) Characterization of CcSTOP1; a C2H2-type transcription factor regulates Al tolerance gene in pigeon pea. Planta 247:201–214

    Article  CAS  PubMed  Google Scholar 

  • De Angeli A, Zhang J, Meyer S, Martinoia E (2013a) AtALMT9 is a malate-activated vacuolar chloride channel required for stomatal opening in Arabidopsis. Nat Commun 4(1):1

    Article  Google Scholar 

  • De Angeli A, Baetz U, Francisco R, Zhang J, Chaves MM, Regalado A (2013b) The vacuolar channel VvALMT9 mediates malate and tartrate accumulation in berries of Vitis vinifera. Planta 238(2):283–291

    Article  PubMed  Google Scholar 

  • de Silva J, Tuwei G, Zhao FJ (2016) Environmental factors influencing aluminium accumulation in tea (Camellia sinensis L.). Plant Soil 400(1–2):223–230

    Article  Google Scholar 

  • 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(15):4235–4243

    Article  CAS  PubMed  Google Scholar 

  • Ding ZJ, Yan JY, Xu XY, Li GX, Zheng SJ (2013) WRKY46 functions as a transcriptional repressor of ALMT1, regulating aluminum-induced malate secretion in Arabidopsis. Plant J 76(5):825–835

    Article  CAS  PubMed  Google Scholar 

  • Dong B, Niu L, Meng D, Song Z, Wang L, Jian Y, Fan X, Dong M, Yang Q, Fu Y (2019) Genome-wide analysis of MATE transporters and response to metal stress in Cajanus cajan. J Plant Interact 14(1):265–275

    Article  CAS  Google Scholar 

  • Dorneles AO, Pereira AS, Rossato LV, Possebom G, Sasso VM, Bernardy K, Sandri RD, Nicoloso FT, Ferreira PA, Tabaldi LA (2016) Silicon reduces aluminum content in tissues and ameliorates its toxic effects on potato plant growth. Cienc Rural 46:506–512

    Article  CAS  Google Scholar 

  • Du H, Huang Y, Qu M, Li Y, Hu X, Yang W, Li H, He W, Ding J, Liu C, Gao S, Cao M, Lu Y, Zhang S (2020) A maize ZmAT6 gene confers aluminum tolerance via reactive oxygen species scavenging. Front Plant Sci 11:1016

    Article  PubMed  PubMed Central  Google Scholar 

  • Du H, Ryan PR, Liu C, Li H, Hu W, Yan W, Huang Y, He W, Luo B, Zhang X, Gao S, Zhou S, Zhang S (2021) ZmMATE6 from maize encodes a citrate transporter that enhances aluminum tolerance in transgenic Arabidopsis thaliana. Plant Sci 311:111016

    Article  CAS  PubMed  Google Scholar 

  • Emery RJN, Kisiala A (2020) The roles of cytokinins in plants and their response to environmental stimuli. Plants (Basel) 9(9):1158

    Article  CAS  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(2–3):252–263

    Article  Google Scholar 

  • Ezaki B, Takahashi K, Utsumi K, Higashi A (2015) A half-type AvABCG1 transporter derived from Andropogon virginicus L. confers aluminum tolerance. Environ Exp Bot 118:21–31

    Article  CAS  Google Scholar 

  • Fan W, Lou HQ, Gong YL, Liu MY, Cao MJ, Liu Y, Yang JL, Zheng SJ (2015) Characterization of an inducible C2H2-type zinc finger transcription factor VuSTOP1 in rice bean (Vigna umbellata) reveals differential regulation between low pH and aluminum tolerance mechanisms. New Phytol 208:456–468

    Article  CAS  PubMed  Google Scholar 

  • Fan W, Lou HQ, Yang JL, Zheng SJ (2016) The roles of STOP1-like transcription factors in aluminum and proton tolerance. Plant Signal Behav 11(2):e1131371

    Article  PubMed  Google Scholar 

  • Feng X, Liu W, Dai H, Qiu Y, Zhang G, Chen ZH, Wu F (2020) HvHOX9, a novel homeobox leucine zipper transcription factor, positively regulates aluminum tolerance in Tibetan wild barley. J Exp Bot 71(19):6057–6073

    Article  CAS  PubMed  Google Scholar 

  • Fontecha G, Silva-Navas J, Benito C, Mestres MA, Espino FJ, Hernández-Riquer MV, Gallego FJ (2007) Candidate gene identification of an aluminum-activated organic acid transporter gene at the Alt4 locus for aluminum tolerance in rye (Secale cereale L.). Theor Appl Genet 114(2):249–260

    Article  CAS  PubMed  Google Scholar 

  • Gao J, Yan S, Yu H, Zhan M, Guan K, Wang Y, Yang Z (2019) Sweet sorghum (Sorghum bicolor L.) SbSTOP1 activates the transcription of a β-1,3-glucanase gene to reduce callose deposition under Al toxicity: a novel pathway for Al tolerance in plants. Biosci Biotechnol Biochem 83(3):446–455

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Oliveira AL, Benito C, Prieto P, Menezes RDA, Rodrigues-Pousada C, Guedes-Pinto H, Martins-Lopes P (2013) Molecular characterization of TaSTOP1 homoeologues and their response to aluminium and proton (H+) toxicity in bread wheat (Triticum aestivum L.). BMC Plant Biol 13:134

    Article  PubMed  PubMed Central  Google Scholar 

  • Garcia-Oliveira AL, Martins-Lopes P, Tolrá 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(3):441–452

    Article  CAS  PubMed  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). BMC Plant Biol 10(1):1–5

    Article  Google Scholar 

  • Gruber BD, Delhaize E, Richardson AE, Roessner U, James RA, Howitt SM, Ryan PR (2011) Characterisation of HvALMT1 function in transgenic barley plants. Funct Plant Biol 38(2):163–175

    Article  CAS  PubMed  Google Scholar 

  • Guo P, Qi YP, Cai YT, Yang TY, Yang LT, Huang ZR, Chen LS (2018) Aluminum effects on photosynthesis, reactive oxygen species and methylglyoxal detoxification in two citrus species differing in aluminum tolerance. Tree Physiol 38(10):1548–1565

    Article  CAS  PubMed  Google Scholar 

  • Han R, Wei Y, Xie Y, Liu L, Jiang C, Yu Y (2020) Quantitative phosphoproteomic analysis provides insights into the aluminum-responsiveness of Tamba black soybean. PLoS One 15(8):e0237845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasenstein KH, Evans ML (1988) Effects of cations on hormone transport in primary roots of Zea mays. Plant Physiol 86(3):890–894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He H, Oo TL, Huang W, He LF, Gu M (2019) Nitric oxide acts as an antioxidant and inhibits programmed cell death induced by aluminum in the root tips of peanut (Arachis hypogaea L.). Sci Rep 9(1):1–2

    Google Scholar 

  • Heng Y, Wu C, Long Y, Luo S, Ma J, Chen J, Liu J, Zhang H, Ren Y, Wang M, Tan J, Zhu S, Wang J, Lei C, Zhang X, Guo X, Wang H, Cheng Z, Wan J (2018) OsALMT7 maintains panicle size and grain yield in rice by mediating malate transport. Plant Cell 30(4):889–906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirano Y, Pannatier EG, Zimmermann S, Brunner I (2004) Induction of callose in roots of Norway spruce seedlings after short-term exposure to aluminum. Tree Physiol 24(11):1279–1283

    Article  CAS  PubMed  Google Scholar 

  • Hoekenga OA, Maron LG, Piñeros MA, Cancado GMA, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T et al (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci U S A 103:9738–9743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou N, You 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(1):127–137

    Article  CAS  Google Scholar 

  • 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(2):655–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(5):857–867

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Gao J, You J, Liang Y, Guan K, Yan S, Zhan M, Yang Z (2018) Identification of STOP1-like proteins associated with aluminum tolerance in sweet sorghum (Sorghum bicolor L.). Front Plant Sci 9:258

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang Y, He G, Tian W, Li D, Meng L, Wu D, He T (2021a) Genome-wide identification of MATE gene family in potato (Solanum tuberosum L.) and expression analysis in heavy metal stress. Front Genet 12:650500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang J, Li X, Chen X, Guo Y, Liang W, Wang H (2021b) Genome-wide identification of soybean abc transporters relate to aluminum toxicity. Int J Mol Sci 22(12):6556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Illés P, Schlicht M, Pavlovkin J, Lichtscheidl I, Baluska 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 behaviour, and nitric oxide production. J Exp Bot 57(15):4201–4213

    Article  PubMed  Google Scholar 

  • Ito H, Kobayashi Y, Yamamoto YY, Koyama H (2019) Characterization of NtSTOP1-regulating genes in tobacco under aluminum stress. Soil Sci Plant Nutr 65(3):251–258

    Article  CAS  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 104(23):9900–9905

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaskowiak J, Tkaczyk O, Slota M, Kwasniewska J, Szarejko I (2018) Analysis of aluminum toxicity in Hordeum vulgare roots with an emphasis on DNA integrity and cell cycle. PLoS One 13(2):e0193156

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiang HX, Tang N, Zheng JG, Chen LS (2009) Antagonistic actions of boron against inhibitory effects of aluminum toxicity on growth, CO2 assimilation, ribulose-1, 5-bisphosphate carboxylase/oxygenase, and photosynthetic electron transport probed by the JIP-test, of Citrus grandis seedlings. BMC Plant Biol 9(1):1–6

    Article  Google Scholar 

  • Jiang C, Liu L, Li X, Han R, Wei Y, Yu Y (2018) Insights into aluminum-tolerance pathways in Stylosanthes as revealed by RNA-seq analysis. Sci Rep 8(1):1–9

    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 and Environ 29(7):1309–1318

    Article  CAS  Google Scholar 

  • Jung JK, McCouch SR (2013) Getting to the roots of it: genetic and hormonal control of root architecture. Front Plant Sci 4:186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaur S, Kaur N, Siddique KH, Nayyar H (2016) Beneficial elements for agricultural crops and their functional relevance in defence against stresses. Arch Agron Soil Sci 62(7):905–920

    Article  Google Scholar 

  • Kisnierienė V, Lapeikaitė I (2015) When chemistry meets biology: the case of aluminium–a review. Chemija 26(3):148–158

    Google Scholar 

  • Kobayashi Y, Kobayashi Y, Sugimoto M, Lakshmanan V, Iuchi S, Kobayashi M, Bais HP, Koyama H (2013) Characterization of the complex regulation of AtALMT1 expression in response to phytohormones and other inducers. Plant Physiol 162(2):732–740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kochian LV, Piñeros 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

    Article  CAS  PubMed  Google Scholar 

  • Kovermann P, Meyer S, Hörtensteiner S, Picco C, Scholz-Starke J, Ravera S, Lee Y, Martinoia E (2007) The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J 52(6):1169–1180

    Article  CAS  PubMed  Google Scholar 

  • Krewski D, Yokel RA, Nieboer E, Borchelt D, Cohen J, Harry J, Kacew S, Lindsay J, Mahfouz AM, Rondeau V (2007) Human health risk assessment for aluminium, aluminium oxide, and aluminium hydroxide. J Toxicol Environ Health B Crit Rev 10(Suppl 1):1–269. Erratum in: J Toxicol Environ Health B Crit Rev (2008) 11(2):147.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kundu A, Ganesan M (2020) GhMATE1 expression regulates Aluminum tolerance of cotton and overexpression of GhMATE1 enhances acid soil tolerance of Arabidopsis. Curr Plant Biol 24:100160

    Article  Google Scholar 

  • Kundu A, Das S, Basu S, Kobayashi Y, Kobayashi Y, Koyama H, Ganesan M (2019) GhSTOP1, a C2H2 type zinc finger transcription factor is essential for aluminum and proton stress tolerance and lateral root initiation in cotton. Plant Biol (Stuttg) 21(1):35–44

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lei GJ, Yokosho K, Yamaji N, Fujii-Kashino M, Ma JF (2017) Functional characterization of two half-size ABC transporter genes in aluminium-accumulating buckwheat. New Phytol 215(3):1080–1089

    Article  CAS  PubMed  Google Scholar 

  • Li N, Meng H, Xing H, Liang L, Zhao X, Luo K (2017) Genome-wide analysis of MATE transporters and molecular characterization of aluminum resistance in Populus. J Exp Bot 68(20):5669–5683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Li Y, Mai J, Tao L, Qu M, Liu J, Shen R, Xu G, Feng Y, Xiao H, Wu L (2018a) Boron alleviates aluminum toxicity by promoting root alkalization in transition zone via polar auxin transport. Plant Physiol 177(3):1254–1266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li GZ, Wang ZQ, Yokosho K, Ding B, Fan W, Gong QQ, Li GX, Wu YR, Yang JL, Ma JF, Zheng SJ (2018b) Transcription factor WRKY 22 promotes aluminum tolerance via activation of Os FRDL 4 expression and enhancement of citrate secretion in rice (Oryza sativa). New Phytol 219(1):149–162

    Article  CAS  PubMed  Google Scholar 

  • Li D, Ma W, Wei J, Mao Y, Peng Z, Zhang J, Kong X, Han Q, Fan W, Yang Y, Chen J (2019) Magnesium promotes root growth and increases aluminum tolerance via modulation of nitric oxide production in Arabidopsis. Plant Soil 2019:1–3

    Google Scholar 

  • Li W, Du J, Feng H, Wu Q, Xu G, Shabala S, Yu L (2020a) Function of NHX-type transporters in improving rice tolerance to aluminum stress and soil acidity. Planta 251(3):71

    Article  CAS  PubMed  Google Scholar 

  • Li CX, Yan JY, Ren JY, Sun L, Xu C, Li GX, Ding ZJ, Zheng SJ (2020b) A WRKY transcription factor confers aluminum tolerance via regulation of cell wall modifying genes. J Integr Plant Biol 62(8):1176–1192

    Article  CAS  PubMed  Google Scholar 

  • Liang C, Piñeros MA, Tian J, Yao Z, Sun L, Liu J, Shaff J, Coluccio A, Kochian LV, Liao H (2013) Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils. Plant Physiol 161(3):1347–1361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang X, Ou Y, Zhao H, Zhou W, Sun C, Lin X (2021) Lipid peroxide-derived short-chain aldehydes are involved in aluminum toxicity of wheat (Triticum aestivum) roots. J Agric Food Chem 69(36):10496–10505

    Article  CAS  PubMed  Google Scholar 

  • Ligaba A, Katsuhara M, Sakamoto W, Matsumoto H (2007) The BnALMT1 protein that is an aluminum-activated malate transporter is localized in the plasma membrane. Plant Signal Behav 2(4):255–257

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu J, Zhou M (2018) The ALMT gene family performs multiple functions in plants. Agronomy 8(2):20

    Article  Google Scholar 

  • Liu J, 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(3):389–399

    Article  CAS  PubMed  Google Scholar 

  • Liu MY, Chen WW, Xu JM, Fan W, Yang JL, Zheng SJ (2013) The role of VuMATE1 expression in aluminium-inducible citrate secretion in rice bean (Vigna umbellata) roots. J Exp Bot 64(7):1795–1804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu M, Xu J, Lou H, Fan W, Yang J, Zheng S (2016) Characterization of VuMATE1 expression in response to iron nutrition and aluminum stress reveals adaptation of rice bean (Vigna umbellata) to acid soils through cis regulation. Front Plant Sci 7:511

    PubMed  PubMed Central  Google Scholar 

  • Liu J, Zhou M, Delhaize E, Ryan PR (2017) Altered expression of a malate-permeable anion channel, OsALMT4. Disrupts Mineral Nutrition Plant Physiol 175(4):1745–1759

    CAS  PubMed  Google Scholar 

  • Liu MY, Lou HQ, Chen WW, Piñeros MA, Xu JM, Fan W, Kochian LV, Zheng SJ, Yang JL (2018) Two citrate transporters coordinately regulate citrate secretion from rice bean root tip under aluminum stress. Plant Cell Environ 41(4):809–822

    Article  CAS  PubMed  Google Scholar 

  • Liu YT, Shi QH, Cao HJ, Ma QB, Nian H, Zhang XX (2020a) Heterologous expression of a Glycine soja C2H2 Zinc finger gene improves aluminum tolerance in Arabidopsis. Int J Mol Sci 21(8):2754. https://doi.org/10.3390/ijms21082754

    Article  CAS  PubMed Central  Google Scholar 

  • Liu Y, Xu J, Guo S, Yuan X, Zhao S, Tian H, Dai S, Kong X, Ding Z (2020b) AtHB7/12 regulate root growth in response to aluminum stress. Int J Mol Sci 21(11):4080

    Article  CAS  PubMed Central  Google Scholar 

  • Liu W, Feng X, Cao F, Wu D, Zhang G, Vincze E, Wang Y, Chen ZH, Wu F (2021) An ATP binding cassette transporter HvABCB25 confers aluminum detoxification in wild barley. J Hazard Mater 401:123371

    Article  CAS  PubMed  Google Scholar 

  • Lou HQ, Fan W, Jin JF, Xu JM, Chen WW, Yang JL, Zheng SJ (2020) A NAC-type transcription factor confers aluminium resistance by regulating cell wall-associated receptor kinase 1 and cell wall pectin. Plant Cell Environ 43(2):463–478

    Article  CAS  PubMed  Google Scholar 

  • Ma B, Gao L, Zhang H, Cui J, Shen Z (2012) Aluminum-induced oxidative stress and changes in antioxidant defenses in the roots of rice varieties differing in Al tolerance. Plant Cell Rep 31(4):687–696

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Chen ZC, Shen RF (2014) Molecular mechanisms of Al tolerance in gramineous plants. Plant Soil 381(1):1–2

    Article  CAS  Google Scholar 

  • Ma Q, Yi R, Li L, Liang Z, Zeng T, Zhang Y, Huang H, Zhang X, Yin X, Cai Z, Mu Y, Cheng Y, Zeng Q, Li X, Nian H (2018) GsMATE encoding a multidrug and toxic compound extrusion transporter enhances aluminum tolerance in Arabidopsis thaliana. BMC Plant Biol 18(1):212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma X, An F, Wang L, Guo D, Xie G, Liu Z (2020) Genome-wide identification of aluminum-activated malate transporter (ALMT) gene family in rubber trees (Hevea brasiliensis) highlights their involvement in aluminum detoxification. Forests 11(2):142

    Article  Google Scholar 

  • Magalhaes JV, Liu J, Guimarães CT, Lana UG, Alves VM, Wang YH, Schaffert RE, Hoekenga OA, Piñeros 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

    Article  CAS  PubMed  Google Scholar 

  • Maron LG, Piñeros MA, Guimarães CT, Magalhaes JV, Pleiman JK, Mao C, 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

    Article  CAS  PubMed  Google Scholar 

  • Melo JO, Martins LG, Barros BA, Pimenta MR, Lana UG, Duarte CE, Pastina MM, Guimaraes CT, Schaffert RE, Kochian LV, Fontes EP (2019) Repeat variants for the SbMATE transporter protect sorghum roots from aluminum toxicity by transcriptional interplay in cis and trans. Proc Natl Acad Sci 116(1):313–318

    Article  CAS  PubMed  Google Scholar 

  • Meriño-Gergichevich C, Alberdi M, Ivanov AG, Reyes-Díaz M (2010) Al 3+-Ca2+ interaction in plants growing in acid soils: al-phytotoxicity response to calcareous amendments. J Soil Sci Plant Nutr 10(3):217–243

    Google Scholar 

  • Meyer S, Mumm P, Imes D, Endler A, Weder B, Al-Rasheid KA, Geiger D, Marten I, Martinoia E, Hedrich R (2010) AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. Plant J 63(6):1054–1062

    Article  CAS  PubMed  Google Scholar 

  • Meyer S, Scholz-Starke J, De Angeli A, Kovermann P, Burla B, Gambale F, Martinoia E (2011) Malate transport by the vacuolar AtALMT6 channel in guard cells is subject to multiple regulation. Plant J 67(2):247–257

    Article  CAS  PubMed  Google Scholar 

  • Min CW, Khan I, Lee BH (2019) Aluminum stress inhibits root growth and alters physiological and antioxidant enzyme responses in alfalfa (Medicago sativa L.) roots. J Kor Grassl Forage Sci 39(4):298–302

    Article  Google Scholar 

  • Mitsis T, Efthimiadou A, Bacopoulou F, Vlachakis D, Chrousos GP, Eliopoulos E (2020) Transcription factors and evolution: an integral part of gene expression. World Acad Sci J 2(1):3–8

    Google Scholar 

  • Mossor-Pietraszewska T (2001) Effect of aluminium on plant growth and metabolism. Acta Biochim Pol 48(3):673–686

    Article  CAS  PubMed  Google Scholar 

  • Murali Achary VM, Panda BB (2010) Aluminium-induced DNA damage and adaptive response to genotoxic stress in plant cells are mediated through reactive oxygen intermediates. Mutagenesis 25(2):201–209

    Article  CAS  PubMed  Google Scholar 

  • Negishi T, Oshima K, Hattori M, Kanai M, Mano S, Nishimura M, Yoshida K (2012) Tonoplast- and plasma membrane-localized aquaporin-family transporters in blue hydrangea sepals of aluminum hyperaccumulating plant. PLoS One 7(8):e43189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Negishi T, Oshima K, Hattori M, Yoshida K (2013) Plasma membrane-localized Al-transporter from blue hydrangea sepals is a member of the anion permease family. Genes Cells 18(5):341–352

    Article  CAS  PubMed  Google Scholar 

  • Nogueirol RC, Monteiro FA, Azevedo RA (2015) Tropical soils cultivated with tomato: fractionation and speciation of Al. Environ Monit Assess 187(4):160

    Article  PubMed  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer AJ, Baker A, Muench SP (2016) The varied functions of aluminium-activated malate transporters-much more than aluminium resistance. Biochem Soc Trans 44(3):856–862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan WL, Hopkins AG, Jackson WA (1988) Aluminum-inhibited shoot development in soybean: a possible consequence of impaired cytokinin supply. Commun Soil Sci Plant Anal 19(7–12):1143–1153

    Article  CAS  Google Scholar 

  • Panda SK, Baluska F, Matsumoto H (2009) Aluminum stress signaling in plants. Plant Signal Behav 4(7):592–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Panhwar QA, Naher UA, Radziah O, Shamshuddin J, Razi IM (2015) Eliminating aluminum toxicity in an acid sulfate soil for rice cultivation using plant growth promoting bacteria. Molecules 20(3):3628–3646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng W, Wu W, Peng J, Li J, Lin Y, Wang Y, Tian J, Sun L, Liang C, Liao H (2018) Characterization of the soybean GmALMT family genes and the function of GmALMT5 in response to phosphate starvation. J Integr Plant Biol 60(3):216–231

    Article  CAS  PubMed  Google Scholar 

  • Pereira JF, Zhou G, Delhaize E, Richardson T, Zhou M, Ryan PR (2010) Engineering greater aluminium resistance in wheat by over-expressing TaALMT1. Ann Bot 106(1):205–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phukunkamkaew S, Tisarum R, Pipatsitee P, Samphumphuang T, Maksup S, Cha-Um S (2021) Morpho-physiological responses of indica rice (Oryza sativa sub. Indica) to aluminum toxicity at seedling stage. Environ Sci Pollut Res Int 28(23):29321–29331

    Article  CAS  PubMed  Google Scholar 

  • Pilon-Smits EA, Quinn CF, Tapken W, Malagoli M, Schiavon M (2009) Physiological functions of beneficial elements. Curr Opin Plant Biol 12(3):267–274

    Article  CAS  PubMed  Google Scholar 

  • Poot-Poot W, Teresa Hernandez-Sotomayor SM (2011) Aluminum stress and its role in the phospholipid signaling pathway in plants and possible biotechnological applications. IUBMB Life 63(10):864–872

    Article  CAS  PubMed  Google Scholar 

  • Rahman MA, Lee SH, Ji HC, Kabir AH, Jones CS, Lee KW (2018) Importance of mineral nutrition for mitigating aluminum toxicity in plants on acidic soils: current status and opportunities. Int J Mol Sci 19(10):3073

    Article  PubMed Central  Google Scholar 

  • Ramesh SA, Tyerman SD, Xu B, Bose J, Kaur S, Conn V, Domingos P, Ullah S, Wege S, Shabala S, Feijó JA (2015) GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters. Nat Commun 6(1):1

    Google Scholar 

  • Ranjan A, Sinha R, Lal SK, Bishi SK, Singh AK (2021a) Phytohormone signalling and cross-talk to alleviate aluminium toxicity in plants. Plant Cell Rep 40(8):1331–1343

    Article  CAS  PubMed  Google Scholar 

  • Ranjan A, Sinha R, Sharma TR, Pattanayak A, Singh AK (2021b) Alleviating aluminum toxicity in plants: implications of reactive oxygen species signaling and crosstalk with other signaling pathways. Physiol Plant 2021:1–20

    Google Scholar 

  • Reyna-Llorens I, Corrales I, Poschenrieder C, Barcelo J, Cruz-Ortega R (2015) Both aluminum and ABA induce the expression of an ABC-like transporter gene (FeALS3) in the Al-tolerant species Fagopyrum esculentum. Environ Exp Bot 111:74–82

    Article  CAS  Google Scholar 

  • Ribeiro AP, de Souza WR, Martins PK, Vinecky F, Duarte KE, Basso MF, da Cunha BADB, Campanha RB, de Oliveira PA, Centeno DC, Cançado GMA, de Magalhães JV, de Sousa CAF, Andrade AC, Kobayashi AK, Molinari HBC (2017) Overexpression of BdMATE gene improves aluminum tolerance in Setaria viridis. Front Plant Sci 8:865

    Article  PubMed  PubMed Central  Google Scholar 

  • Ribeiro AP, Vinecky F, Duarte KE, Santiago TR, Casari RA, Hell AF, da Cunha BA, Martins PK, da Cruz Centeno D, de Oliveira Molinari PA, de Almeida Cançado GM (2021) Enhanced aluminum tolerance in sugarcane: evaluation of SbMATE overexpression and genome-wide identification of ALMTs in saccharum spp. BMC Plant Biol 21(1):1–5

    Article  Google Scholar 

  • Rogers EE, Wu X, Stacey G, Nguyen HT (2009) Two MATE proteins play a role in iron efficiency in soybean. J Plant Physiol 166(13):1453–1459

    Article  CAS  PubMed  Google Scholar 

  • Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571

    Article  PubMed  PubMed Central  Google Scholar 

  • Saha B, Swain D, Borgohain P, Rout GR, Koyama H, Panda SK (2020) Enhanced exudation of malate in the rhizosphere due to AtALMT1 overexpression in blackgram (Vigna mungo L.) confers increased aluminium tolerance. Plant Biol (Stuttg) 22(4):701–708

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Sawaki Y, Iuchi S, Kobayashi Y, 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(1):281–294

    Article  CAS  PubMed  PubMed Central  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(4):979-89

    Article  PubMed  Google Scholar 

  • Schreiber HD, Jones AH, Lariviere CM, Mayhew KM, Cain JB (2011) Role of aluminum in red-to-blue color changes in Hydrangea macrophylla sepals. Biometals 24(6):1005–1015

    Article  CAS  PubMed  Google Scholar 

  • Sharma T, Dreyer I, Kochian L, Piñeros MA (2016) The ALMT family of organic acid transporters in plants and their involvement in detoxification and nutrient security. Front Plant Sci 7:1488

    Article  PubMed  PubMed Central  Google Scholar 

  • Shetty R, Vidya CS, Prakash NB, Lux A, Vaculík M (2021) Aluminum toxicity in plants and its possible mitigation in acid soils by biochar: a review. Sci Total Environ 765:142744

    Article  CAS  PubMed  Google Scholar 

  • Singh D, Chauhan SK (2011) Organic acids of crop plants in aluminium detoxification. Curr Sci 100(10):1509–1515

    CAS  Google Scholar 

  • Sivaguru M, Pike S, Gassmann W, Baskin TI (2003) Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. Plant Cell Physiol 44(7):667–675

    Article  CAS  PubMed  Google Scholar 

  • Smirnov OE, Kosyan AM, Kosyk OI, Taran NY (2014) Buckwheat stomatal traits under aluminium toxicity. Mod Phytomorphol 6:15–18

    Google Scholar 

  • Sun P, Tian QY, Chen J, Zhang WH (2010) Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. J Exp Bot 61(2):347–356

    Article  CAS  PubMed  Google Scholar 

  • Sun L, Zhang M, Liu X, Mao Q, Shi C, Kochian LV, Liao H (2020) Aluminium is essential for root growth and development of tea plants (Camellia sinensis). J Integr Plant Biol 62(7):984–997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szurman-Zubrzycka M, Chwiałkowska K, Niemira M, Kwaśniewski M, Nawrot M, Gajecka M, Larsen PB, Szarejko I (2021) Aluminum or low pH–which is the bigger enemy of barley? Transcriptome analysis of barley root meristem under Al and low pH stress. Front Genet 12:712

    Article  Google Scholar 

  • Tahara K, Norisada M, Hogetsu T, Kojima K (2005) Aluminum tolerance and aluminum-induced deposition of callose and lignin in the root tips of Melaleuca and Eucalyptus species. J For Res 10(4):325–333

    Article  CAS  Google Scholar 

  • Tietz T, Lenzner A, Kolbaum AE, Zellmer S, Riebeling C, Gürtler R, Jung C, Kappenstein O, Tentschert J, Giulbudagian M, Merkel S (2019) Aggregated aluminium exposure: risk assessment for the general population. Arch Toxicol 93(12):3503–3521

    Article  CAS  PubMed  Google Scholar 

  • Tolrà R, Vogel-Mikuš K, Hajiboland R, Kump P, Pongrac P, Kaulich B, Gianoncelli A, Babin V, Barceló J, Regvar M, Poschenrieder C (2011) Localization of aluminium in tea (Camellia sinensis) leaves using low energy X-ray fluorescence spectro-microscopy. J Plant Res 124(1):165–172

    Article  PubMed  Google Scholar 

  • Tovkach A, Ryan PR, Richardson AE, Lewis DC, Rathjen TM, Ramesh S, Tyerman SD, Delhaize E (2013) Transposon-mediated alteration of TaMATE1B expression in wheat confers constitutive citrate efflux from root apices. Plant Physiol 161:880–892

    Article  CAS  PubMed  Google Scholar 

  • Upadhyay N, Kar D, Deepak Mahajan B, Nanda S, Rahiman R, Panchakshari N, Bhagavatula L, Datta S (2019) The multitasking abilities of MATE transporters in plants. J Exp Bot 70(18):4643–4656

    Article  CAS  PubMed  Google Scholar 

  • Vera-Villalobos H, Lunario-Delgado L, Pérez-Retamal D, Román D, Leiva JC, Zamorano P, Mercado-Seguel A, Gálvez AS, Benito C, Wulff-Zottele C (2020) Sulfate nutrition improves short-term Al3+-stress tolerance in roots of Lolium perenne L. Plant Physiol Biochem 148:103–113

    Article  CAS  PubMed  Google Scholar 

  • Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyay RG, Pandey M, Sharma S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang H, Chen RF, Iwashita T, Shen RF, Ma JF (2015a) Physiological characterization of aluminum tolerance and accumulation in tartary and wild buckwheat. New Phytol 205(1):273–279

    Article  CAS  PubMed  Google Scholar 

  • Wang R, Liu X, Liang S, Ge Q, Li Y, Shao J, Qi Y, An L, Yu F (2015b) A subgroup of MATE transporter genes regulates hypocotyl cell elongation in Arabidopsis. J Exp Bot 66(20):6327–6343

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Yu W, Zhang J, Rengel Z, Xu J, Han Q, Chen L, Li K, Yu Y, Chen Q (2016) Auxin enhances aluminium-induced citrate exudation through upregulation of GmMATE and activation of the plasma membrane H+-ATPase in soybean roots. Ann Bot 118(5):933–940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Li R, Li D, Jia X, Zhou D, Li J, Lyi SM, Hou S, Huang Y, Kochian LV, Liu J (2017) NIP1;2 is a plasma membrane-localized transporter mediating aluminum uptake, translocation, and tolerance in Arabidopsis. Proc Natl Acad Sci U S A 114(19):5047–5052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Liu L, Su H, Guo L, Zhang J, Li Y, Xu J, Zhang X, Guo YD, Zhang N (2020) Jasmonate and aluminum crosstalk in tomato: identification and expression analysis of WRKYs and ALMTs during JA/Al-regulated root growth. Plant Physiol Biochem 154:409–418

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Dong Y, Zhu L, Hao Z, Hu L, Hu X, Wang G, Cheng T, Shi J, Chen J (2021) The role of γ-aminobutyric acid in aluminum stress tolerance in a woody plant, Liriodendron chinense× tulipifera. Hort Res 8(1):1–15

    Google Scholar 

  • Ward CL, Kleinert A, Scortecci KC, Benedito VA, Valentine AJ (2011) Phosphorus-deficiency reduces aluminium toxicity by altering uptake and metabolism of root zone carbon dioxide. J Plant Physiol 168(5):459–465

    Article  CAS  PubMed  Google Scholar 

  • Wei Y, Han R, Xie Y, Jiang C, Yu Y (2021) Recent advances in understanding mechanisms of plant tolerance and response to aluminum toxicity. Sustainability 13(4):1782

    Article  CAS  Google Scholar 

  • Wu X, Li R, Shi J, Wang J, Sun Q, Zhang H, Xing Y, Qi Y, Zhang N, Guo YD (2014) Brassica oleracea MATE encodes a citrate transporter and enhances aluminum tolerance in Arabidopsis thaliana. Plant Cell Physiol 55(8):1426–1436

    Article  CAS  PubMed  Google Scholar 

  • Wu L, Kobayashi Y, Wasaki J, Koyama H (2018a) Organic acid excretion from roots: a plant mechanism for enhancing phosphorus acquisition, enhancing aluminum tolerance, and recruiting beneficial rhizobacteria. Soil Sci Plant Nutr 64(6):697–704

    Article  CAS  Google Scholar 

  • Wu W, Lin Y, Chen Q, Peng W, Peng J, Tian J, Liang C, Liao H (2018b) Functional conservation and divergence of soybean GmSTOP1 members in proton and aluminum tolerance. Front Plant Sci 9:570

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu L, Guo Y, Cai S, Kuang L, Shen Q, Wu D, Zhang G (2020) The zinc finger transcription factor ATF1 regulates aluminum tolerance in barley. J Exp Bot 71(20):6512–6523

    Article  CAS  PubMed  Google Scholar 

  • 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(43):18381–18385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia JX, Yamaji N, Ma JF (2013) A plasma membrane-localized small peptide is involved in rice aluminum tolerance. Plant J 76:345–355

    CAS  PubMed  Google Scholar 

  • Xu M, Gruber BD, Delhaize E, White RG, James RA, You J, Yang Z, Ryan PR (2015) The barley anion channel, HvALMT1, has multiple roles in guard cell physiology and grain metabolism. Physiol Plant 153(1):183–193

    Article  CAS  PubMed  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

    Article  CAS  PubMed  PubMed Central  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(1):63–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan L, Riaz M, Liu J, Yu M, Cuncang J (2020) The aluminum tolerance and detoxification mechanisms in plants; recent advances and prospects. Crit Rev Environ Sci Technol 10:1–37

    CAS  Google Scholar 

  • Yang Y, Wang QL, Geng MJ, Guo ZH, Zhao Z (2011) Effect of indole-3-acetic acid on aluminum-induced efflux of malic acid from wheat (Triticum aestivum L.). Plant Soil 346(1):215–230

    Article  CAS  Google Scholar 

  • Yang M, Tan L, Xu Y, Zhao Y, Cheng F, Ye S, Jiang W (2015) Effect of low pH and aluminum toxicity on the photosynthetic characteristics of different fast-growing Eucalyptus vegetatively propagated clones. PLoS One 10(6):e0130963

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang ZB, He C, Ma Y, Herde M, Ding Z (2017a) Jasmonic acid enhances Al-induced root growth inhibition. Plant Physiol 173(2):1420–1433

    Article  CAS  PubMed  Google Scholar 

  • Yang ZB, Liu G, Liu J, Zhang B, Meng W, Müller B, Hayashi KI, Zhang X, Zhao Z, De Smet I, Ding Z (2017b) Synergistic action of auxin and cytokinin mediates aluminum-induced root growth inhibition in Arabidopsis. EMBO Rep 18(7):1213–1230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang JL, Fan W, Zheng SJ (2019) Mechanisms and regulation of aluminum-induced secretion of organic acid anions from plant roots. J Zhejiang Univ Sci B 20(6):513–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokosho K, Yamaji N, Ma JF (2010) Isolation and characterisation of two MATE genes in rye. Funct Plant Biol 37:296–303

    Article  CAS  Google Scholar 

  • Yokosho K, Yamaji N, Kashino-Fujii M, Ma JF (2016a) Retro transposon-mediated aluminum tolerance through enhanced expression of the citrate transporter OsFRDL4. Plant Physiol 172(4):2327–2336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokosho K, Yamaji N, Miho KF, Ma JF (2016b) Functional analysis of a MATE gene OsFRDL2 revealed its involvement in Al-induced secretion of citrate, but less contribution to Al tolerance in rice. Plant Cell Physiol 57:976–985

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Jin C, Sun C, Wang J, Ye Y, Zhou W, Lu L, Lin X (2016) Inhibition of ethylene production by putrescine alleviates aluminium-induced root inhibition in wheat plants. Sci Rep 6(1):1

    CAS  Google Scholar 

  • Zhang L, Wu XX, Wang J, Qi C, Wang X, Wang G, Li M, Li X, Guo YD (2018) BoALMT1, an Al-induced malate transporter in cabbage, enhances aluminum tolerance in Arabidopsis thaliana. Front Plant Sci 8:2156

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Zhang J, Guo J, Zhou F, Singh S, Xu X, Xie Q, Yang Z, Huang CF (2019) F-box protein RAE1 regulates the stability of the aluminum-resistance transcription factor STOP1 in Arabidopsis. Proc Natl Acad Sci 116(1):319–327

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Li L, Yang C, Cheng Y, Han Z, Cai Z, Nian H, Ma Q (2020) GsMAS1 encoding a MADS-box transcription factor enhances the tolerance to aluminum stress in Arabidopsis thaliana. Int J Mol Sci 21(6):2004

    Article  CAS  PubMed Central  Google Scholar 

  • Zhao XQ, Shen RF (2018) Aluminum–nitrogen interactions in the soil–plant system. Front Plant Sci 18(9):807

    Article  Google Scholar 

  • Zhou G, Delhaize E, Zhou M, Ryan PR (2013) The barley MATE gene, HvAACT1, increases citrate efflux and Al3+ tolerance when expressed in wheat and barley. Ann Bot 112:603–612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou G, Pereira JF, Delhaize E, Zhou M, Magalhaes JV, Ryan PR (2014) Enhancing the aluminium tolerance of barley by expressing the citrate transporter genes SbMATE and FRD3. J Exp Bot 65(9):2381–2390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu XF, Shi YZ, Lei GJ, Fry SC, Zhang BC, Zhou YH, Braam J, Jiang T, Xu XY, Mao CZ, Pan YJ, Yang JL, Wu P, Zheng SJ (2012) XTH31, encoding an in vitro XEH/XET-active enzyme, regulates aluminum sensitivity by modulating in vivo XET action, cell wall xyloglucan content, and aluminum binding capacity in Arabidopsis. Plant Cell 24:4731–4747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Sinha, D., Datta, S. (2022). Molecular Mechanism of Aluminum Tolerance in Plants: An Overview. In: Kumar, K., Srivastava, S. (eds) Plant Metal and Metalloid Transporters. Springer, Singapore. https://doi.org/10.1007/978-981-19-6103-8_9

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