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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Notes
- 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
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
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
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
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
Delhaize E, Ma JF, Ryan PR (2012) Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci 17:341–348
Doebley J (2004) The genetics of maize evolution. Ann Rev Genet 38:37–59
Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321
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
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
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
Foy C (1988) Plant adaptation to acid, aluminum-toxic soils. Soil Sci Plant Anal 19:959–987
Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch S (2005) Genetic structure and diversity in Oryza sativa L. Genetics 169:1631–1638
Grevenstuk T, Romano A (2013) Aluminium speciation and internal detoxification mechanisms in plants: where do we stand? Metallomics 5:1584–1594
Hengl T (2009) A practical guide to geostatistical mapping. Creative Commons Attribution-Noncommercial-No Derivative Works 3.0 License, pp 291
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
Hoekenga OA, Magalhaes JV (2011) Mechanisms of aluminum tolerance. Springer, Berlin
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
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
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
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
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
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
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
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
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
Kochian LV, Piñeros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195
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
Kovach MJ, Sweeney MT, McCouch SR (2007) New insights into the history of rice domestication. Trends Genet 23:578–587
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
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
Ma J, Hiradate S, Nomoto K, Iwashita T, Matsumoto H (1997) Internal detoxification mechanism of Al in Hydrangea. Plant Physiol 113:1033–1039
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
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
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
Matsumoto H (2000) Cell biology of aluminium toxicity and tolerance in higher plants. Int Rev Cytol 200:1–46
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
Miyasaka SC, Hawes MC (2001) Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiol 125:1978–1987
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
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
O’Neill M, Albersheim P, Darvill A (1990) The pectic polysaccharides of primary cell walls. Meth Plant Biochem 2:415–441
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
Panda SK, Baluska F, Matsumoto H (2009) Aluminum stress signaling in plants. Plant Signal Behav 4:592–597
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
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
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
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
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
Von Uexkull HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15
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
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
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
Wen F, Zhu Y, Hawes MC (1999) Effect of pectin methylesterase gene expression on pea root development. Plant Cell 11:1129–1140
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
Xia J, Yamaji N, Ma JF (2013) A plasma membrane-localized small peptide is involved in rice aluminum tolerance. Plant J 76:345–355
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
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
Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146:602–611
Yang 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
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
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
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
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
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
Zheng SJ, Ma JF, Matsumoto H (1998) High aluminum resistance in buckwheat. Plant Physiol 117:745–751
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.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this chapter
Cite this chapter
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
Download citation
DOI: https://doi.org/10.1007/978-3-319-19968-9_8
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-19967-2
Online ISBN: 978-3-319-19968-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)