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Aluminum Stress Adaptation in Plants pp 155–168Cite as

Rice Arsenal Against Aluminum Toxicity

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

Abstract

One of the major constraints on crop production is the ability of plants to grow in acidic soils, where aluminum (Al) is soluble in its toxic form (Al3+). However, some plants can address this Al toxicity by utilizing different strategies such as exclusion (an external mechanism) and detoxification (an internal mechanism). Rice, an important food source, is one of the most Al-tolerant crops, but the mechanism of this tolerance is not well understood. In this review, we provide an overview of Al-tolerance mechanisms in rice and show that this species can employ several strategies that together provide tolerance to Al toxicity.

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Notes

  1. 1.

    The soil pH map (from 2000 to 2010) was retrieved from www.globalsoilmap.com and does not represent the pH of the soil 10,000 years ago, during the period in which rice was domesticated. However, until the 1800s, most acidic soil remained untouched and under forest cover. There was only some encroachment into regions with acidic soils in densely populated regions of the world, such as East Asia (Von Uexkull and Mutert 1995). For the map source, please see Hengl (2009).

References

  • Arenhart RA, De Lima JC, Pedron M, Carvalho FEL, Silveira JAG, Rosa SB, Caverzan A, Andrade CMB, Schünemann M, Margis R et al (2013) Involvement of ASR genes in aluminium tolerance mechanisms in rice. Plant Cell Environ 36:52–67

    Article  CAS  PubMed  Google Scholar 

  • Arenhart RA, Bai Y, Oliveira LF, Neto LB, Schunemann M, Maraschin F, Mariath J, Silverio A, Martins G, Margis R et al (2014) New insights into aluminum tolerance in rice: the ASR5 protein binds the STAR1 promoter and other aluminum-responsive genes. Mol Plant 7:709–721

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cai M, Zhang S, Xing C, Wang F, Ning W, Lei Z (2011) Developmental characteristics and aluminum resistance of root border cells in rice seedlings. Plant Sci 180:702–708

    Article  CAS  PubMed  Google Scholar 

  • Cao Y, Lou Y, Han Y, Shi J, Wang Y, Wang W, Ming F (2011) Al toxicity leads to enhanced cell division and changed photosynthesis in Oryza rufipogon L. Mol Biol Rep 38:4839–4846

    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 159:1624–1633

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Delhaize E, Ma JF, Ryan PR (2012) Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci 17:341–348

    Article  CAS  PubMed  Google Scholar 

  • Doebley J (2004) The genetics of maize evolution. Ann Rev Genet 38:37–59

    Article  CAS  PubMed  Google Scholar 

  • Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321

    Article  CAS  PubMed  Google Scholar 

  • Driouich A, Follet-Gueye M-L, Vicré-Gibouin M, Hawes M (2013) Root border cells and secretions as critical elements in plant host defense. Curr Opin Plant Biol 16:489–495

    Article  CAS  PubMed  Google Scholar 

  • Famoso AN, Clark RT, Shaff JE, Craft E, McCouch SR, Kochian LV (2010) Development of a novel aluminum tolerance phenotyping platform used for comparisons of cereal aluminum tolerance and investigations into rice aluminum tolerance mechanisms. Plant Physiol 153:1678–1691

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Famoso AN, Zhao K, Clark RT, Tung C-W, Wright MH, Bustamante C, Kochian LV, McCouch SR (2011) Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL mapping. PLoS Genet 7:e1002221

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Foy C (1988) Plant adaptation to acid, aluminum-toxic soils. Soil Sci Plant Anal 19:959–987

    Article  CAS  Google Scholar 

  • Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch S (2005) Genetic structure and diversity in Oryza sativa L. Genetics 169:1631–1638

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Grevenstuk T, Romano A (2013) Aluminium speciation and internal detoxification mechanisms in plants: where do we stand? Metallomics 5:1584–1594

    Article  CAS  PubMed  Google Scholar 

  • Hengl T (2009) A practical guide to geostatistical mapping. Creative Commons Attribution-Noncommercial-No Derivative Works 3.0 License, pp 291

    Google Scholar 

  • Higham CFW (2002) Languages and farming dispersals: Austroasiatic languages and rice cultivation. In: Bellwood P, Renfrew C (eds) Examining the farming/language dispersal hypothesis. McDonald Institute for Archaeological Research: Cambridge, pp 223–232

    Google Scholar 

  • Hoekenga OA, Magalhaes JV (2011) Mechanisms of aluminum tolerance. Springer, Berlin

    Book  Google Scholar 

  • Huang C, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF (2009a) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21:655–667

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang C-F, Yamaji N, Nishimura M, Tajima S, Ma JF (2009b) A rice mutant sensitive to Al toxicity is defective in the specification of root outer cell layers. Plant Cell Physiol 50:976–985

    Article  CAS  PubMed  Google Scholar 

  • Huang C, Yamaji N, Chen Z, Ma JF (2011) A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice. Plant J 69:857–867

    Article  PubMed  Google Scholar 

  • Huang X, Kurata N, Wei X, Wang Z-X, Wang A, Zhao Q, Zhao Y, Liu K, Lu H, Li W et al (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490:497–501

    Article  CAS  PubMed  Google Scholar 

  • Huynh V-B, Repellin A, Zuily-Fodil Y, Pham-Thi A-T (2012) Aluminum stress response in rice: effects on membrane lipid composition and expression of lipid biosynthesis genes. Physiol Plant 146:272–284

    Article  CAS  PubMed  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 57:4201–4213

    Article  PubMed  Google Scholar 

  • Khan MSH, Tawaraya K, Sekimoto H, Koyama H, Kobayashi Y, Murayama T, Chuba M, Kambayashi M, Shiono Y, Uemura M et al (2009) Relative abundance of Delta(5)-sterols in plasma membrane lipids of root-tip cells correlates with aluminum tolerance of rice. Physiol Plant 135:73–83

    Article  CAS  PubMed  Google Scholar 

  • Kochian LV, Pence NS, Letham DLD, Pineros MA, Magalhaes JV, Hoekenga OA, Garvin DF (2002) Mechanisms of metal resistance in plants: aluminum and heavy metals. Plant Soil 247:109–119

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Kochian LV, Piñeros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195

    Article  CAS  Google Scholar 

  • Kollmeier M, Felle HH, Horst WJ (2000) Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum? Plant Physiol 122:945–956

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kovach MJ, Sweeney MT, McCouch SR (2007) New insights into the history of rice domestication. Trends Genet 23:578–587

    Article  CAS  PubMed  Google Scholar 

  • Li J-Y, Liu J, Dong D, Jia X, McCouch SR, Kochian LV (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 U S A 111:6503–6508

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lu H, Liu Z, Wu N, Berne S, Saito Y, Liu B, Wang L (2002) Rice domestication and climatic change: phytolith evidence from East China. Boreas 31:378–385

    Article  Google Scholar 

  • Ma J, Hiradate S, Nomoto K, Iwashita T, Matsumoto H (1997) Internal detoxification mechanism of Al in Hydrangea. Plant Physiol 113:1033–1039

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ma JF, Shen R, Zhao Z, Wissuwa M, Takeuchi Y, EbitaniT YM (2002) Response of rice to Al stress and identification of quantitative trait Loci for Al tolerance. Plant Cell Physiol 43:652–659

    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 31:687–696

    Article  CAS  PubMed  Google Scholar 

  • Mao C, Yi K, Yang L, Zheng B, Wu Y, Liu F, Wu P (2004) Identification of aluminium-regulated genes by cDNA-AFLP in rice (Oryza sativa L.): aluminium-regulated genes for the metabolism of cell wall components. J Exp Bot 55:137–143

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Meriga B, Reddy BK, Rao KR, Reddy LA, Kishor PBK (2004) Aluminium-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). J Plant Physiol 161:63–68

    Article  CAS  PubMed  Google Scholar 

  • Miyasaka SC, Hawes MC (2001) Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiol 125:1978–1987

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nguyen VT, Nguyen BD, Sarkarung S, Martinez C, Paterson AH, Nguyen HT (2002) Mapping of genes controlling aluminum tolerance in rice: comparison of different genetic backgrounds. Mol Genet Genom 267:772–780

    Article  CAS  Google Scholar 

  • Nguyen BD, Brar DS, Bui BC, Nguyen TV, Pham LN, Nguyen HT (2003) Identification and mapping of the QTL for aluminum tolerance introgressed from the new source, Oryza Rufipogon Griff., into indica rice (Oryza sativa L.). Theor Appl Genet 106:583–593

    CAS  PubMed  Google Scholar 

  • O’Neill M, Albersheim P, Darvill A (1990) The pectic polysaccharides of primary cell walls. Meth Plant Biochem 2:415–441

    Article  Google Scholar 

  • Ozkan H, Brandolini A, Schafer-Pregl R, Salamini F (2002) AFLP analysis of a collection of tetraploid wheats indicates the origin of emmer and hard wheat domestication in southeast Turkey. Mol Biol Evol 19:1797–1801

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pandey P, Srivastava RK, Dubey RS (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 22:656–670

    Article  CAS  PubMed  Google Scholar 

  • Rosa SB, Caverzan A, Teixeira FK, Lazzarotto F, Silveira JAG, Ferreira-Silva SL, Abreu-Neto J, Margis R, Margis-Pinheiro M (2010) Cytosolic APx knockdown indicates an ambiguous redox responses in rice. Phytochemistry 71:548–558

    Article  CAS  PubMed  Google Scholar 

  • Sharma P, Dubey RS (2007) Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Rep 26:2027–2038

    Article  CAS  PubMed  Google Scholar 

  • Stephenson MB, Hawes MC (1994) Correlation of pectin methylesterase activity in root caps of pea with root border cell separation. Plant Physiol 106:739–745

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tsutsui T, Yamaji N, Huang CF, Motoyama R, Nagamura Y, Ma JF (2012) Comparative genome-wide transcriptional analysis of Al-responsive genes reveals novel Al tolerance mechanisms in rice. PLoS One 7:e48197

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Von Uexkull HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15

    Article  Google Scholar 

  • Wagatsuma T, Khan SH, Rao IM, Wenzl P, Tawaraya K, Yamamoto T, Kawamura T, Hosogoe K, Ishikawa S (2005) Methylene blue stainability of root-tip protoplasts as an indicator of aluminum tolerance in a wide range of plant species, cultivars and lines. Soil Sci Plant Nutr 51:991–998

    Article  CAS  Google Scholar 

  • Wang Y-S, Yang Z-M (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923

    Article  CAS  PubMed  Google Scholar 

  • Wang H-H, Huang J-J, Bi Y-R (2010) Nitrate reductase-dependent nitric oxide production is involved in aluminum tolerance in red kidney bean roots. Plant Sci 179:281–288

    Article  CAS  Google Scholar 

  • Wen F, Zhu Y, Hawes MC (1999) Effect of pectin methylesterase gene expression on pea root development. Plant Cell 11:1129–1140

    Article  PubMed Central  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 107:18381–18385

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xia J, 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 

  • 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  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang Q, Wang Y, Zhang J, Shi W, Qian C, Peng X (2007) Identification of aluminum-responsive proteins in rice roots by a proteomic approach: cysteine synthase as a key player in Al response. Proteomics 7:737–749

    Article  CAS  PubMed  Google Scholar 

  • Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146:602–611

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang L, Tian D, Todd CD, Luo Y, Hu X (2013) Comparative proteome analyses reveal that nitric oxide is an important signal molecule in the response of rice to aluminum toxicity. J Proteom Res 12:1316–1330

    Article  CAS  Google Scholar 

  • Yokosho K, Yamaji N, Ma JF (2011) An Al-inducible MATE gene is involved in external detoxification of Al in rice. Plant J 68:1061–1069

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, He Z, Tian H, Zhu G, Peng X (2007) Identification of aluminium-responsive genes in rice cultivars with different aluminium sensitivities. J Exp Bot 58:2269–2278

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Yin Y, Wang Y, Peng X (2010) Identification of rice Al-responsive genes by semi-quantitative polymerase chain reaction using sulfite reductase as a novel endogenous control. J Integr Plant Biol 52:505–514

    CAS  PubMed  Google Scholar 

  • Zhang Z, Wang H, Wang X, Bi Y (2011) Nitric oxide enhances aluminum tolerance by affecting cell wall polysaccharides in rice roots. Plant Cell Rep 30:1701–1711

    Article  CAS  PubMed  Google Scholar 

  • Zhao XQ, Guo SW, Shinmachi F, Sunairi M, Noguchi A, Hasegawa I, Shen RF (2013) Aluminium tolerance in rice is antagonistic with nitrate preference and synergistic with ammonium preference. Ann Bot 111:69–77

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zheng SJ, Ma JF, Matsumoto H (1998) High aluminum resistance in buckwheat. Plant Physiol 117:745–751

    Article  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES: www.capes.gov.br), Fundação de apoio a Pesquisa do Rio Grande do Sul (FAPERGS), and the Brazilian National Council of Technological and Scientific Development (CNPq). This research was partially supported by a grant from the NIH (R01GM066258) to Z.-Y. Wang.

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Authors and Affiliations

  1. Departamento de Genética, Universidade Federal do Rio Grande do Sul, Avenida Bento Gonçalves 9500, sala 207, prédio 43312, 91501–970, Porto Alegre, Brasil

    Rafael Augusto Arenhart, Lauro Bucker-Neto & Marcia Margis-Pinheiro

  2. Departamento de Biofísica e Centro de Biotecnologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brasil

    Rogerio Margis

  3. Department of Plant Biology, Carnegie Institution for Science, Stanford, CA, 94305, USA

    Zhi-Yong Wang

Authors
  1. Rafael Augusto Arenhart
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  2. Lauro Bucker-Neto
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  3. Rogerio Margis
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  4. Zhi-Yong Wang
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  5. Marcia Margis-Pinheiro
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Corresponding author

Correspondence to Marcia Margis-Pinheiro .

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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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Arenhart, R.A., Bucker-Neto, L., Margis, R., Wang, ZY., Margis-Pinheiro, M. (2015). Rice Arsenal Against Aluminum Toxicity. 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_8

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