Progress on Molecular Mechanism of Aluminum Resistance in Rice

doi:10.1016/j.rsci.2020.09.003

Abstract

Abstract:

Aluminum (Al) toxicity in acid soils is a significant limitation to crop production worldwide, as 13% of the world’s rice is produced in acid soil with high Al content. Rice is likely the most Al-resistant cereal and also the cereal, where Al resistance is the most genetically complex with external detoxification and internal tolerance. Many Al-resistance genes in rice have been cloned, including Al resistance transcription factor 1 (ART1) and other transcription factors, organic acid transporter genes, and metal ion transporter gene. This review summarized the recent characterized genes affecting Al tolerance in rice and the interrelationships between Al and other plant nutrients.

Key words: rice, aluminum, Al transporter, Al tolerance, Al toxicity

Jingguang Chen, Qi Lai, Baiquan Zeng, Longbiao Guo, Guoyou Ye. Progress on Molecular Mechanism of Aluminum Resistance in Rice[J]. Rice Science, 2020, 27(6): 454-467.

Figures/Tables 3

References 148

[1]	Adamowski M, Friml J.2015. PIN-dependent auxin transport: Action, regulation, and evolution. Plant Cell, 27(1): 20-32.
[2]	Amenós M, Corrales I, Poschenrieder C, Illés P, Baluska 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(3): 528-540.
[3]	Arbelaez J D, Maron L G, Jobe T O, Pineros M A, Famoso A N, Rebelo A R, Singh N, Ma Q Y, Fei Z J, Kochian L V, McCouch S R.2017. ALUMINUM RESISTANCE TRANSCRIPTION FACTOR 1 (ART1) contributes to natural variation in aluminum resistance in diverse genetic backgrounds of rice (O. sativa). Plant Direct, 1(4): e00014.
[4]	Arenhart R A, Margis R, Margis-Pinheiro M.2012. The rice ASR5 protein: A putative role in the response to aluminum photosynthesis disturbance. Plant Signal Behav, 7(10): 1263-1266.
[5]	Arenhart R A, Lima J C, Pedron M, Carvalho F E, Silveira J A, Rosa S B, Caverzan A, Andrade C M, Schunemann M, Margis R, Margis-Pinheiro M.2013. Involvement of ASR genes in aluminium tolerance mechanisms in rice. Plant Cell Environ, 36(1): 52-67.
[6]	Arenhart R A, Bai Y, de Oliveira L F, Neto L B, Schunemann M, Maraschin Fdos S, Mariath J, Silverio A, Sachetto-Martins G, Margis R, Wang Z Y, Margis-Pinheiro M.2014. New insights into aluminum tolerance in rice: The ASR5 protein binds the STAR1 promoter and other aluminum-responsive genes. Mol Plant, 7(4): 709-721.
[7]	Arenhart R A, Schunemann M, Bucker Neto L, Margis R, Wang Z Y, Margis-Pinheiro M.2016. Rice ASR1 and ASR5 are complementary transcription factors regulating aluminium responsive genes. Plant Cell Environ, 39(3): 645-651.
[8]	Awasthi J P, Saha B, Panigrahi J, Yanase E, Koyama H, Panda S K.2019. Redox balance, metabolic fingerprint and physiological characterization in contrasting North East Indian rice for aluminum stress tolerance. Sci Rep, 9(1): 8681.
[9]	Bai B, Bian H W, Zeng Z H, Hou N, Shi B, Wang J H, Zhu M Y, Han N.2017. miR393-mediated auxin signaling regulation is involved in root elongation inhibition in response to toxic aluminum stress in barley. Plant Cell Physiol, 58(3): 426-439.
[10]	Baluska F, Mancuso S, Volkmann D, Barlow P W.2010. Root apex transition zone: A signalling-response nexus in the root. Trends Plant Sci, 15(7): 402-408.
[11]	Barbier-Brygoo H, de Angeli A, Filleur S, Frachisse J M, Gambale F, Thomine S, Wege S.2011. Anion channels/transporters in plants: From molecular bases to regulatory networks. Annu Rev Plant Biol, 62: 25-51.
[12]	Bosch M, Hepler P K.2005. Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell, 17(12): 3219-3226.
[13]	Bose J, Babourina O, Rengel Z.2011. Role of magnesium in alleviation of aluminium toxicity in plants. J Exp Bot, 62(7): 2251-2264.
[14]	Bose J, Babourina O, Shabala S, Rengel Z.2013. Low-pH and aluminum resistance in Arabidopsis correlates with high cytosolic magnesium content and increased magnesium uptake by plant roots. Plant Cell Physiol, 54(7): 1093-1104.
[15]	Che J, Yamaji N, Shen R F, Ma J F.2016. An Al-inducible expansin gene, OsEXPA10 is involved in root cell elongation of rice. Plant J, 88(1): 132-142.
[16]	Che J, Tsutsui T, Yokosho K, Yamaji N, Ma J F.2018. Functional characterization of an aluminum (Al)-inducible transcription factor, ART2, revealed a different pathway for Al tolerance in rice. New Phytol, 220(1): 209-218.
[17]	Chen J, Wang W H, Wu F H, You C Y, Liu T W, Dong X J, He J X, Zheng H L.2013. Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant Soil, 362: 301-318.
[18]	Chen J G, Zhang Y, Tan Y W, Zhang M, Zhu L L, Xu G H, Fan X R.2016. Agronomic nitrogen-use efficiency of rice can be increased by driving OsNRT2.1 expression with the OsNAR2.1 promoter. Plant Biotechnol J, 14(8): 1705-1715.
[19]	Chen J G, Fan X R, Qian K Y, Zhang Y, Song M Q, Liu Y, Xu G H, Fan X R,.2017. pOsNAR2.1:OsNAR2.1 expression enhances nitrogen uptake efficiency and grain yield in transgenic rice plants. Plant Biotechnol J, 15(10): 1273-1283.
[20]	Chen Y N, Fan X R, Song W J, Zhang Y L, Xu G H.2012. Over-expression of OsPIN2 leads to increased tiller numbers, angle and shorter plant height through suppression of OsLAZY1. Plant Biotechnol J, 10(2): 139-149.
[21]	Chen Z C, Zhao X Q, Shen R F.2010. The alleviating effect of ammonium on aluminum toxicity in Lespedeza bicolor results in decreased aluminuminduced malate secretion from roots compared with nitrate. Plant Soil, 337: 389-398.
[22]	Chen Z C, Yamaji N, Motoyama R, Nagamura Y, Ma J F.2012. Up-regulation of a magnesium transporter gene OsMGT1 is required for conferring aluminum tolerance in rice. Plant Physiol, 159(4): 1624-1633.
[23]	Chen Z C, Ma J F.2013. Magnesium transporters and their role in Al tolerance in plants. Plant Soil, 368: 51-56.
[24]	Clarkson D T.1967. Interactions between aluminum and phosphorus on root surface and cell wall material. Plant Soil, 27(3): 347-356.
[25]	de Angeli A, Zhang J B, Meyer S, Martinoia E.2013. AtALMT9 is a malate-activated vacuolar chloride channel required for stomatal opening in Arabidopsis. Nat Commun, 4: 1804.
[26]	Delhaize E, Ryan P R, Hebb D M, Yamamoto Y, Sasaki T, Matsumoto H.2004. Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proc Natl Acad Sci USA, 101(42): 15249-15254.
[27]	Delhaize E, Gruber B D, Pittman J K, White R G, Leung H, Miao Y S, Jiang L W, Ryan P R, Richardson A E.2007. A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. Plant J, 51(2): 198-210.
[28]	Deng W, Luo K M, Li D M, Zheng X L, Wei X Y, Smith W, Thammina C, Lu L T, 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.
[29]	Dreyer I, Gomez-Porras J L, Riano-Pachon D M, Hedrich R, Geiger D.2012. Molecular evolution of slow and quick anion channels (SLACs and QUACs/ALMTs). Front Plant Sci, 3: 263.
[30]	Famoso A N, Clark R T, Shaff J E, Craft E, McCouch S R, Kochian L V.2010. Development of a novel aluminum tolerance phenotyping platform used for comparisons of cereal cluminum tolerance and investigations into rice aluminum tolerance mechanisms. Plant Physiol, 153(4): 1678-1691.
[31]	Famoso A N, Zhao K Y, Clark R T, Tung C W, Wright M H, Bustamante C, Kochian L V, McCouch S R.2011. Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL mapping. PLoS Genet, 7(8): e1002221.
[32]	Fan W, Lou H Q, Gong Y L, Liu M Y, Wang Z Q, Yang J L, Zheng S J.2014. Identification of early Al-responsive genes in rice bean (Vigna umbellata) roots provides new clues to molecular mechanisms of Al toxicity and tolerance. Plant Cell Environ, 37(7): 1586-1597.
[33]	Furuichi T, Sasaki T, Tsuchiya Y, Ryan P R, Delhaize E, Yamamoto Y.2010. An extracellular hydrophilic carboxy-terminal domain regulates the activity of TaALMT1, the aluminum-activated malate transport protein of wheat. Plant J, 64(1): 47-55.
[34]	Gaude N, Brehelin C, Tischendorf G, Kessler F, Dormann P.2007. Nitrogen deficiency in Arabidopsis affects galactolipid composition and gene expression and results in accumulation of fatty acid phytyl esters. Plant J, 49(4): 729-739.
[35]	Grauer U E, Horst W J.1992. Modeling cation amelioration of aluminum phytotoxicity. Soil Sci Soc Am J, 56(1): 166-172.
[36]	Guo L B, Ye G Y.2014. Use of major quantitative trait loci to improve grain yield of rice. Rice Sci, 21(2): 65-82.
[37]	Hu W, Huang C, Deng X M, Zhou S Y, Chen L H, Li Y, Wang C, Ma Z B, Yuan Q Q, Wang Y, Cai R, Liang X Y, Yang G X, He G Y.2013. TaASR1, a transcription factor gene in wheat, confers drought stress tolerance in transgenic tobacco. Plant Cell Environ, 36(8): 1449-1464.
[38]	Huang C F, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma J F.2009. A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell, 21(2): 655-667.
[39]	Huang C F, Yamaji N, Chen Z C, Ma J F.2012. A tonoplastlocalized half-size ABC transporter is required for internal detoxification of aluminum in rice. Plant J, 69(5): 857-867.
[40]	Huang X H, Han B.2014. Natural variations and genome-wide association studies in crop plants. Annu Rev Plant Biol, 65: 531-551.
[41]	Iglesias M J, Terrile M C, Bartoli C G, D’Ippolito S, Casalongue C A.2010. Auxin signaling participates in the adaptative response against oxidative stress and salinity by interacting with redox metabolism in Arabidopsis. Plant Mol Biol, 74(3): 215-222.
[42]	Illéš 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.
[43]	Jiang J J, Ma S H, Ye N H, Jiang M, Cao J S, Zhang J H.2017. WRKY transcription factors in plant responses to stresses. J Integr Plant Biol, 59(2): 86-101.
[44]	Jin Z P, Xue S W, Luo Y N, Tian B H, Fang H H, Li H, Pei Y X.2013. Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem, 62: 41-46.
[45]	Joo J, Lee Y H, Kim Y K, Nahm B H, Song S I.2013. Abiotic stress responsive rice ASR1 and ASR3 exhibit different tissue- dependent sugar and hormone-sensitivities. Mol Cells, 35(5): 421-435.
[46]	Kinraide T B.2003. Toxicity factors in acidic forest soils: Attempts to evaluate separately the toxic effects of excessive Al3+ and H+ and insufficient Ca2+ and Mg2+ upon root elongation. Eur J Soil Sci, 54(2): 323-333.
[47]	Kinraide T B, Pedler J F, Parker D R.2004. Relative effectiveness of calcium and magnesium in the alleviation of rhizotoxicity in wheat induced by copper, zinc, aluminum, sodium, and low pH. Plant Soil, 259: 201-208.
[48]	Kleine-Vehn J, Leitner J, Zwiewka M, Sauer M, Abas L, Luschnig C, Friml J.2008. Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. Proc Natl Acad Sci USA, 105(46): 17812-17817.
[49]	Kochian L V, Hoekenga O A, Pineros M A.2004. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol, 55: 459-493.
[50]	Kochian L V, Piñeros M A, Hoekenga O A.2005. The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil, 274: 175-195.
[51]	Kochian L V, Pineros M A, Liu J, Magalhaes J V.2015. Plant adaptation to acid soils: The molecular basis for crop aluminum resistance. Annu Rev Plant Biol, 66: 571-598.
[52]	Kollmeier M, Felle H H, Horst W J.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(3): 945-956.
[53]	Konrad Z, Bar-Zvi D.2008. Synergism between the chaperone-like activity of the stress regulated ASR1 protein and the osmolyte glycine-betaine. Planta, 227(6): 1213-1219.
[54]	Krishnamurthy A, Rathinasabapathi B.2013. Auxin and its transport play a role in plant tolerance to arsenite-induced oxidative stress in Arabidopsis thaliana. Plant Cell Environ, 36(10): 1838-1849.
[55]	Krtková J, Havelková L, Křepelová A, Fišer R, Vosolsobě S, Novotná Z, Martinec J, Schwarzerová K.2012. Loss of membrane fluidity and endocytosis inhibition are involved in rapid aluminum-induced root growth cessation in Arabidopsis thaliana. Plant Physiol Biochem, 60: 88-97.
[56]	Li G Z, Wang Z Q, Yokosho K, Ding B, Fan W, Gong Q Q, Li G X, Wu Y R, Yang J L, Ma J F, Zheng S J.2018. Transcription factor WRKY22 promotes aluminum tolerance via activation of OsFRDL4 expression and enhancement of citrate secretion in rice(Oryza sativa). New Phytol, 219(1): 149-162.
[57]	Li J Y, Liu J P, Dong D K, Jia X M, McCouch S R, Kochian L V.2014. Natural variation underlies alterations in Nramp aluminum transporter (NRAT1) expression and function that play a key role in rice aluminum tolerance. Proc Natl Acad Sci USA, 111(17): 6503-6508.
[58]	Li X W, Li Y L, Qu M, Xiao H D, Feng Y M, Liu J Y, Wu L S, Yu M.2016. Cell wall pectin and its methyl-esterification in transition zone determine Al resistance in cultivars of pea (Pisum sativum). Front Plant Sci, 7: 39.
[59]	Li X W, Li Y L, Mai J W, Tao L, Qu M, Liu J Y, Shen R F, Xu G L, Feng Y M, Xiao H D, Wu L S, Shi L, Guo S X, Liang J, Zhu Y Y, He Y M, Baluška F, Shabala S, Yu M.2018. Boron alleviates aluminum toxicity by promoting root alkalization in transition zone via polar auxin transport. Plant Physiol, 177(3): 1254-1266.
[60]	Ligaba A, Dreyer I, Margaryan A, Schneider D J, 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(5): 766-780.
[61]	Liu J, Magalhaes J V, Shaff J, Kochian L V.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.
[62]	Liu J, Hou L X, Liu G H, Liu X, Wang X C.2011. Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana. Chin Sci Bull, 56: 3547-3553.
[63]	Liu J, Zhou M X, Delhaize E, Ryan P R.2017. Altered expression of a malate-permeable anion channel, OsALMT4, disrupts mineral nutrition. Plant Physiol, 175(4): 1745-1759.
[64]	Liu J H, Jia C H, Dong F Y, Wang J B, Zhang J B, Xu Y, Xu B Y, Jin Z Q.2013. Isolation of an abscisic acid senescence and ripening inducible gene from litchi and functional characterization under water stress. Planta, 237(4): 1025-1036.
[65]	Liu S, Gao H L, Wu X Y, Fang Q, Chen L, Zhao F J, Huang C F.2016. Isolation and characterization of an aluminum-resistant mutant in rice. Rice, 9(1): 60.
[66]	Liu X W, Lin Y M, Liu D Q, Wang C X, Zhao Z Q, Cui X M, Liu Y, Yang Y.2017. MAPK-mediated auxin signal transduction pathways regulate the malic acid secretion under aluminum stress in wheat (Triticum aestivum L.). Sci Rep, 7(1): 1620.
[67]	Ma J F.2000. Role of organic acids in detoxification of aluminum in higher plants. Plant Cell Physiol, 41(4): 383-390.
[68]	Ma J F, Ryan P R, Delhaize E.2001. Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci, 6(6): 273-278.
[69]	Ma J F, Shen R F, Zhao Z Q, Wissuwa M, Takeuchi Y, Ebitani T, Yano M.2002. Response of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant Cell Physiol, 43(6): 652-659.
[70]	Ma J F, Shen R F, Nagao S, Tanimoto E.2004. Aluminum targets elongating cells by reducing cell wall extensibility in wheat roots. Plant Cell Physiol, 45(5): 583-589.
[71]	Ma J F.2007. Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. Int Rev Cytol, 264: 225-252.
[72]	Ma J F, Chen Z C, Shen R F.2014. Molecular mechanisms of Al tolerance in gramineous plants. Plant Soil, 381: 1-12.
[73]	MacDiarmid C W, Gardner R C.1998. Overexpression of the Saccharomyces cerevisiae magnesium transport system confers resistance to aluminum ion. J Biol Chem, 273(3): 1727-1732.
[74]	Maejima E, Watanabe T, Osaki M, Wagatsuma T.2014. Phosphorus deficiency enhances aluminum tolerance of rice (Oryza sativa) by changing the physicochemical characteristics of root plasma membranes and cell walls. J Plant Physiol, 171(2): 9-15.
[75]	Meng L J, Wang B X, Zhao X Q, Ponce K, Qian Q, Ye G Y.2017. Association mapping of ferrous, zinc, and aluminum tolerance at the seedling stage in indica rice using MAGIC populations. Front Plant Sci, 8: 1822.
[76]	Nagayama T, Nakamura A, Yamaji N, Satoh S, Furukawa J, Iwai H.2019. Changes in the distribution of pectin in root border cells under aluminum stress. Front Plant Sci, 10: 1216.
[77]	Nguyen B D, Brar D S, Bui B C, Nguyen T V, Pham L N, Nguyen H T.2003. Identification and mapping of the QTL for aluminum tolerance introgressed from the new source, Oryza rufipogon Griff., into indica rice(Oryza sativa L.). Theor Appl Genet, 106(4): 583-593.
[78]	Nguyen V T, Burow M D, Nguyen H T, Le B T, Le T D, Paterson A H.2001. Molecular mapping of genes conferring aluminum tolerance in rice (Oryza sativa L.). Theor Appl Genet, 102: 1002-1010.
[79]	Pandey P, Srivastava R K, Dubey R S.2013. Salicylic acid alleviates aluminum toxicity in rice seedlings better than magnesium and calcium by reducing aluminum uptake, suppressing oxidative damage and increasing antioxidative defense. Ecotoxicology, 22(4): 656-670.
[80]	Pineros M A, Cancado G M A, Kochian L V.2008. Novel properties of the wheat aluminum tolerance organic acid transporter (TaALMT1) revealed by electrophysiological characterization in Xenopus oocytes: Functional and structural implications. Plant Physiol, 147(4): 2131-2146.
[81]	Rangel A F, Rao I M, Braun H P, Horst W J.2010. Aluminum resistance in common bean (Phaseolus vulgaris) involves induction and maintenance of citrate exudation from root apices. Physiol Plant, 138(2): 176-190.
[82]	Rangel A F, Rao I M, Horst W J.2009. Intracellular distribution and binding state of aluminum in root apices of two common bean (Phaseolus vulgaris) genotypes in relation to Al toxicity. Physiol Plant, 135(2): 162-173.
[83]	Rengel Z, Robinson D L.1989. Aluminum effects on growth and macronutrient uptake in annual rye grass. Agron J, 81(2): 208-215.
[84]	Riaz M, Yan L, Wu X W, Hussain S, Aziz O, Wang Y H, Imran M, Jiang C C.2018. Boron alleviates the aluminum toxicity in trifoliate orange by regulating antioxidant defense system and reducing root cell injury. J Environ Manage, 208: 149-158.
[85]	Ricardi M M, González R M, Zhong S L, Domínguez P G, Duffy T, Turjanski P G, Salgado Salter J D, Alleva K, Carrari F, Giovannoni J J, Estévez J M, Iusem N D.2014. Genome-wide data (ChIP-seq) enabled identification of cell wall-related and aquaporin genes as targets of tomato ASR1, a drought stress-responsive transcription factor. BMC Plant Biol, 14: 29.
[86]	Roy B, Bhadra S.2014. Effects of toxic levels of aluminium on seedling parameters of rice under hydroponic culture. Rice Sci, 21: 217-223.
[87]	Ruiz J M, Rivero R M, Romero L.2006. Boron increases synthesis of glutathione in sunflower plants subjected to aluminum stress. Plant Soil, 279: 25-30.
[88]	Rushton P J, Somssich I E, Ringler P, Shen Q J.2010. WRKY transcription factors. Trends Plant Sci, 15(5): 247-258.
[89]	Ryan P R, Delhaize E, Jones D L.2001. Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol, 52: 527-560.
[90]	Saha I, Sarkar B, Ghosh A, De A K, Adak M K.2019. Abscisic acid induced cellular responses of sub1A QTL to aluminium toxicity in rice(Oryza sativa L.). Ecotox Environ Safe, 183: 109600.
[91]	Samaj J, Baluska F, Voigt B, Schlicht M, Volkmann D, Menzel D.2004. Endocytosis, actin cytoskeleton, and signaling. Plant Physiol, 135(3): 1150-1161.
[92]	Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn S J, Ryan P R, Delhaize E, Matsumoto H.2004. A wheat gene encoding an aluminum-activated malate transporter. Plant J, 37(5): 645-653.
[93]	Sasidharan R, Voesenek L A C J, Pierik R.2011. Cell wall modifying proteins mediate plant acclimatization to biotic and abiotic stresses. Crit Rev Plant Sci, 30(6): 548-562.
[94]	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: 281-294.
[95]	Schmohl N, Pilling J, Fisahn J, Horst W J.2000. Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiol Plant, 109(4): 419-427.
[96]	Shan C J, Zhang S L, Li D F, Zhao Y Z, Tian X L, Zhao X L, Wu Y X, Wei X Y, Liu R Q.2011. Effects of exogenous hydrogen sulfide on the ascorbate and lutathione metabolism in wheat seedlings leaves under water stress. Acta Physiol Plant, 33: 2533.
[97]	Sun P, Tian Q Y, Chen J, Zhang W H.2010. Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. J Exp Bot, 61(2): 347-356.
[98]	Tamás L, Bočová B, Huttová J, Liptáková Ľ, Mistrík I, Valentovičová K, Zelinová V.2012. Impact of the auxin signaling inhibitor p-chlorophenoxyisobutyric acid on short-term Cd-induced hydrogen peroxide production and growth response in barley root tip. J Plant Physiol, 169(14): 1375-1381.
[99]	Tan J, Wang M L, Shi Z Y, Miao X X.2018. OsEXPA10 mediates the balance between growth and resistance to biotic stress in rice. Plant Cell Rep, 37(7): 993-1002.
[100]	Tan K Z, Keltjens W G, Findenegg G R.1992. Aluminium toxicity with sorghum genotypes in nutrient solutions and its amelioration by magnesium. J Plant Nutr Soil Sci, 155: 81-86.
[101]	Tao Y H, Niu Y N, Wang Y, Chen T X, Naveed S A, Zhang J, Xu J L, Li Z K.2018. Genome-wide association mapping of aluminum toxicity tolerance and fine mapping of a candidate gene for Nrat1 in rice. PLoS One, 13(6): e0198589.
[102]	Tsutsui T, Yamaji N, Ma J F.2011. Identification of a cis-acting element of ART1, a C2H2-type zinc-finger transcription factor for aluminum tolerance in rice. Plant Physiol, 156(2): 925-931.
[103]	Vaahtera L, Brosché M.2011. More than the sum of its parts: How to achieve a specific transcriptional response to abiotic stress. Plant Sci, 180(3): 421-430.
[104]	Wainberg M, Sinnott-Armstrong N, Mancuso N, Barbeira A N, Knowles D A, Golan D, Ermel R, Ruusalepp A, Quertermous T, Hao K, Björkegren J L M, Im H K, Pasaniuc B, Rivas M A, Kundaje A.2019. Opportunities and challenges for transcriptome- wide association studies. Nat Genet, 51(4): 592-599.
[105]	Wang M, Qiao J Y, Yu C L, Chen H, Sun C D, Huang L Z, Li C Y, Geisler M, Qian Q, Jiang D A, Qi Y H.2019. The auxin influx carrier, OsAUX3, regulates rice root development and responses to aluminium stress. Plant Cell Environ, 42(4): 1125-1138.
[106]	Wang S W, Uddin M I, Tanaka K, Yin L N, Shi Z H, Qi Y H, Mano J, Matsui K, Shimomura N, Sakaki T, Deng X P, Zhang S Q.2014. Maintenance of chloroplast structure and function by overexpression of the rice MONOGALACTOSYLDIACYLGLYCEROL SYNTHASE gene leads to enhanced salt tolerance in tobacco. Plant Physiol, 165(3): 1144-1155.
[107]	Wang W, Zhao X Q, Chen R F, Dong X Y, Lan P, Ma J F, Shen R F.2015. Altered cell wall properties are responsible for ammonium-reduced aluminium accumulation in rice roots. Plant Cell Environ, 38(7): 1382-1390.
[108]	Wang Y Q, Li L, Cui W T, Xu S, Shen W B, Wang R.2012. Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil, 351: 107-119.
[109]	Watanabe T, Okada K.2005. Interactive effects of Al, Ca and other cations on root elongation of rice cultivars under low pH. Ann Bot, 95(2): 379-385.
[110]	Wu D M, Shen H, Yokawa K, Baluska F.2014. Alleviation of aluminium-induced cell rigidity by overexpression of OsPIN2 in rice roots. J Exp Bot, 65(18): 5305-5315.
[111]	Wu D M, Shen H, Yokawa K, Baluska F.2015. Overexpressing OsPIN2 enhances aluminium internalization by elevating vesicular trafficking in rice root apex. J Exp Bot, 66(21): 6791-6801.
[112]	Wu P, Liao C Y, Hu B, Yi K K, Jin W Z, Ni J J, He C.2000. QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theor Appl Genet, 100(8): 1295-1303.
[113]	Xia J X, Yamaji N, Kasai T, Ma J F.2010. Plasma membrane- localized transporter for aluminum in rice. Proc Natl Acad Sci USA, 107(43): 18381-18385.
[114]	Xia J X, Yamaji N, Ma J F.2011. Further characterization of an aluminum influx transporter in rice. Plant Signal Behav, 6(1): 160-163.
[115]	Xia J X, Yamaji N, Ma J F.2013. A plasma membrane-localized small peptide is involved in rice Al tolerance. Plant J, 76(2): 345-355.
[116]	Xia J X, Yamaji N, Che J, Shen R F, Ma J F.2014. Differential expression of Nrat1 is responsible for Al-tolerance QTL on chromosome 2 in rice. J Exp Bot, 65(15): 4297-4304.
[117]	Xu G H, Fan X R, Miller A J.2012. Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol, 63: 153-182.
[118]	Xue Y, Jiang L, Su N, Wang J K, Deng P, Ma J F, Zhai H Q, Wan J M.2007. The genetic basic and fine-mapping of a stable quantitative-trait loci for aluminium tolerance in rice. Planta, 227(1): 255-262.
[119]	Xue Y J, Tao L, Yang Z M.2008. Aluminum-induced cell wall peroxidase activity and lignin synthesis are differentially regulated by jasmonate and nitric oxide. J Agric Food Chem, 56(20): 9676-9684.
[120]	Yamaji N, Huang C F, Nagao S, Yano M, Sato Y, Nagamura Y, Ma J F.2009. A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell, 21(10): 3339-3349.
[121]	Yan L, Riaz M, Wu X W, Du C Q, Liu Y L, Jiang C C.2018. Ameliorative effects of boron on aluminum induced variations of cell wall cellulose and pectin components in trifoliate orange (Poncirus trifoliate(L.) Raf.) rootstock. Environ Pollut, 240: 764-774.
[122]	Yang J L, Li Y Y, Zhang Y J, Zhang S S, Wu Y R, Wu P, Zheng S J.2008. Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol, 146(2): 602-611.
[123]	Yang J L, Zhu X F, Peng Y X, Zheng C, Li G X, Liu Y, Shi Y Z, Zheng S J.2011. Cell wall hemicellulose contributes significantly to aluminum adsorption and root growth in Arabidopsis. Plant Physiol, 155(4): 1885-1892.
[124]	Yang X Y, Zeng Z H, Yan J Y, Fan W, Bian H W, Zhu M Y, Yang J L, Zheng S J.2013. Association of specific pectinmethylesterases with Al-induced root elongation inhibition in rice. Physiol Plant, 148(4): 502-511.
[125]	Yang Z B, Geng X Y, He C M, Zhang F, Wang R, Horst W J, Ding Z J.2014. TAA1-regulated local auxin biosynthesis in the root- apex transition zone mediates the aluminum-induced inhibition of root growth in Arabidopsis. Plant Cell, 26(7): 2889-2904.
[126]	Yang Z B, He C, Ma Y, Herde M, Ding Z.2017. Jasmonic acid enhances Al-induced root growth inhibition. Plant Physiol, 173(2): 1420-1433.
[127]	Ye G Y, Smith K F.2010. Marker-assisted gene pyramiding for cultivar development. In: Janick J. Plant Breeding Reviews. Hoboken, USA: John Wiley & Sons: 219-256.
[128]	Yokosho K, Yamaji N, Ma J F.2011. An Al-inducible MATE gene is involved in external detoxification of Al in rice. Plant J, 68(6): 1061-1069.
[129]	Yokosho K, Yamaji N, Fujii-Kashino M, Ma J F.2016a. Functional analysis of a MATE gene OsFRDL2 revealed its involvement in Al-induced secretion of citrate, but a lower contribution to Al tolerance in rice. Plant Cell Physiol, 57(5): 976-985.
[130]	Yokosho K, Yamaji N, Fujii-Kashino M, Ma J F.2016b. Retrotransposon-mediated aluminum tolerance through enhanced expression of the citrate transporter OsFRDL4. Plant Physiol, 172(4): 2327-2336.
[131]	Yu M, Shen R F, Xiao H D, Xu M M, Wang H Z, Wang H Y, Zeng Q L, Bian J F.2008. Boron alleviates aluminum toxicity in pea (Pisum sativum). Plant Soil, 314: 87-98.
[132]	Zhang H, Hu L Y, Hu K D, He Y D, Wang S H, Luo J P.2008. Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol, 50(12): 1518-1529.
[133]	Zhang H, Wang M J, Hu L Y, Wang S H, Hu K D, Bao L J, Luo J P.2010. Hydrogen sulfide promotes wheat seed germination under osmotic stress. Russ J Plant Physiol, 57(4): 532-539.
[134]	Zhang L D, Peng Y Y, Li J, Tian X Y, Chen Z C.2019. OsMGT1 confers resistance to magnesium deficiency by enhancing the import of Mg in rice. Int J Mol Sci, 20(1): 207.
[135]	Zhang M J, Deng X P, Yin L N, Qi L Y, Wang X Y, Wang S W, Li H B.2016. Regulation of galactolipid biosynthesis by overexpression of the rice MGD gene contributes to enhanced aluminum tolerance in tobacco. Front Plant Sci, 7: 337.
[136]	Zhang P, Zhong K Z, Tong H H, Shahid M Q, Li J Q.2016. Association mapping for aluminum tolerance in a core collection of rice landraces. Front Plant Sci, 7: 1415.
[137]	Zhang P, Zhong K Z, Zhong Z Z, Tong H H.2019. Mining candidate gene for rice aluminum tolerance through genome wide association study and transcriptomic analysis. BMC Plant Biol, 19(1): 490.
[138]	Zhang X, Long Y, Huang J J, Xia J X.2019. Molecular mechanisms for coping with Al toxicity in plants. Int J Mol Sci, 20(7): 1551.
[139]	Zhang X C, Wu H H, Chen L M, Liu L L, Wan X C.2018. Maintenance of mesophyll potassium and regulation of plasma membrane H+-ATPase are associated with physiological responses of tea plants to drought and subsequent rehydration. Crop J, 6(6): 611-620.
[140]	Zhao M H, Song J Y, Wu A T, Hu T, Li J Q.2018. Mining beneficial genes for aluminum tolerance within a core collection of rice landraces through genome-wide association mapping with high density SNPs from specific-locus amplified fragment sequencing. Front Plant Sci, 9: 1838.
[141]	Zhao X Q, Shen R F, Sun Q B.2009. Ammonium under solution culture alleviates aluminum toxicity in rice and reduces aluminum accumulation in roots compared with nitrate. Plant Soil, 315: 107-121.
[142]	Zhao X Q, Shen R F.2013. Interactive regulation of nitrogen and aluminum in rice. Plant Signal Behav, 8(6): e24355.
[143]	Zhao X Q, Guo S W, Shinmachi F, Sunairi M, Noguchi A, Hasegawa I, Shen R F.2013. Aluminium tolerance in rice is antagonistic with nitrate preference and synergistic with ammonium preference. Ann Bot, 111(1): 69-77.
[144]	Zhu C Q, Zhang J H, Sun L M, Zhu L F, Abliz B, Hu W J, Zhong C, Bai Z G, Sajid H, Cao X C, Jin Q Y.2018. Hydrogen sulfide alleviates aluminum toxicity via decreasing apoplast and symplast Al contents in rice. Front Plant Sci, 9: 294.
[145]	Zhu C Q, Cao X C, Bai Z G, Zhu L F, Hu W J, Hu A Y, Abliz B, Zhong C, Liang Q D, Huang J, Zhang J H, Jin Q Y.2019a. Putrescine alleviates aluminum toxicity in rice (Oryza sativa) by reducing cell wall Al contents in an ethylene-dependent manner. Physiol Plant, 167(4): 471-487.
[146]	Zhu C Q, Cao X C, Zhu L F, Hu W J, Hu A Y, Abliz B, Bai Z G, Huang J, Liang Q D, Sajid H, Li Y F, Wang L P, Jin Q Y, Zhang J H.2019b. Boron reduces cell wall aluminum content in rice (Oryza sativa) roots by decreasing H2O2 accumulation. Plant Physiol Biochem, 138: 80-90.
[147]	Zhu X F, Shi Y Z, Lei G J, Fry S C, Zhang B C, Zhou Y H, Braam J, Jiang T, Xu X Y, Mao C Z, Pan Y J, Yang J L, Wu P, Zheng S J.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(11): 4731-4747.
[148]	Zhu X F, Lei G J, Wang Z W, Shi Y Z, Braam J, Li G X, Zheng S J.2013. Coordination between apoplastic and symplastic detoxification confers plant aluminum resistance. Plant Physiol, 162(4): 1947-1955.

Gene	Locus in MSU	Function	Subcellular localization	Reference
OsCDT3	LOC_Os01g08300	Bind Al	Plasma membrane	Xia et al, 2013
OsALMT4	LOC_Os01g12210	Transport malate	Plasma membrane	Liu J et al, 2017
OsWRKY22	LOC_Os01g60490	Regulate Al tolerance genes	Nucleus	Li G Z et al, 2018
OsMGT1	LOC_Os01g64890	Transport Mg into the cytoplasm	Plasma membrane	Chen Z C et al, 2012
OsFRDL4	LOC_Os01g69010	Transport citrate	Plasma membrane	Yokosho et al, 2011
Nrat1	LOC_Os02g03900	Transport Al into the cytoplasm	Plasma membrane	Xia et al, 2010, 2014; Li et al, 2014
ASR1	LOC_Os02g33820	Regulate Al tolerance genes	Nucleus, cytoplasm	Arenhart et al, 2016
OsMGD	LOC_Os02g55910	Galactolipid biosynthesis	-	Zhang M J et al, 2016
OsALS1	LOC_Os03g54790	Sequester Al into the vacuoles	Tonoplast	Huang et al, 2012
ART2	LOC_Os04g08290	Regulate Al tolerance genes	Nucleus	Che et al, 2018
OsPME14	LOC_Os04g38560	Regulate pectin methylesterifying degree	-	Yang et al, 2013
OsEXPA10	LOC_Os04g49410	Mediate cell wall loosening	-	Che et al, 2016; Tan et al, 2018
STAR2	LOC_Os05g02750	Transport UDP-glucose to cell wall	Plasma membrane	Huang et al, 2009; Arenhart et al, 2014
OsAUX3	LOC_Os05g37470	Transport auxin	Plasma membrane	Wang et al, 2019
OsPIN2	LOC_Os06g44970	An auxin efflux transporter	Plasma membrane	Wu et al, 2014, 2015
STAR1	LOC_Os06g48060	Transport UDP-glucose to cell wall	Plasma membrane	Huang et al, 2009; Arenhart et al, 2014
OsFRDL2	LOC_Os10g13940	Transport citrate	Unidentified vesicles in cytosol	Yokosho et al, 2016a
ASR5	LOC_Os11g06720	Regulate Al tolerance genes	Nucleus, cytoplasm	Arenhart et al, 2012, 2013
ART1	LOC_Os12g07280	Regulate Al tolerance genes	Nucleus	Yamaji et al, 2009; Tsutsui et al, 2011

Gene	Locus in MSU	Function	Subcellular localization	Reference
OsCDT3	LOC_Os01g08300	Bind Al	Plasma membrane	Xia et al, 2013
OsALMT4	LOC_Os01g12210	Transport malate	Plasma membrane	Liu J et al, 2017
OsWRKY22	LOC_Os01g60490	Regulate Al tolerance genes	Nucleus	Li G Z et al, 2018
OsMGT1	LOC_Os01g64890	Transport Mg into the cytoplasm	Plasma membrane	Chen Z C et al, 2012
OsFRDL4	LOC_Os01g69010	Transport citrate	Plasma membrane	Yokosho et al, 2011
Nrat1	LOC_Os02g03900	Transport Al into the cytoplasm	Plasma membrane	Xia et al, 2010, 2014; Li et al, 2014
ASR1	LOC_Os02g33820	Regulate Al tolerance genes	Nucleus, cytoplasm	Arenhart et al, 2016
OsMGD	LOC_Os02g55910	Galactolipid biosynthesis	-	Zhang M J et al, 2016
OsALS1	LOC_Os03g54790	Sequester Al into the vacuoles	Tonoplast	Huang et al, 2012
ART2	LOC_Os04g08290	Regulate Al tolerance genes	Nucleus	Che et al, 2018
OsPME14	LOC_Os04g38560	Regulate pectin methylesterifying degree	-	Yang et al, 2013
OsEXPA10	LOC_Os04g49410	Mediate cell wall loosening	-	Che et al, 2016; Tan et al, 2018
STAR2	LOC_Os05g02750	Transport UDP-glucose to cell wall	Plasma membrane	Huang et al, 2009; Arenhart et al, 2014
OsAUX3	LOC_Os05g37470	Transport auxin	Plasma membrane	Wang et al, 2019
OsPIN2	LOC_Os06g44970	An auxin efflux transporter	Plasma membrane	Wu et al, 2014, 2015
STAR1	LOC_Os06g48060	Transport UDP-glucose to cell wall	Plasma membrane	Huang et al, 2009; Arenhart et al, 2014
OsFRDL2	LOC_Os10g13940	Transport citrate	Unidentified vesicles in cytosol	Yokosho et al, 2016a
ASR5	LOC_Os11g06720	Regulate Al tolerance genes	Nucleus, cytoplasm	Arenhart et al, 2012, 2013
ART1	LOC_Os12g07280	Regulate Al tolerance genes	Nucleus	Yamaji et al, 2009; Tsutsui et al, 2011