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Abstract

Aluminum (Al) toxicity in acid soils is a significant limitation to crop production worldwide, as approximately 50% of the world's potentially arable soil is acidic. Because acid soils are such an important constraint to agriculture, understanding the mechanisms and genes conferring resistance to Al toxicity has been a focus of intense research interest in the decade since the last article on crop acid soil tolerance was published in this journal. An impressive amount of progress has been made during that time that has greatly increased our understanding of the diversity of Al resistance genes and mechanisms, how resistance gene expression is regulated and triggered by Al and Al-induced signals, and how the proteins encoded by these genes function and are regulated. This review examines the state of our understanding of the physiological, genetic, and molecular bases for crop Al tolerance, looking at the novel Al resistance genes and mechanisms that have been identified over the past ten years. Additionally, it examines how the integration of molecular and genetic analyses of crop Al resistance is starting to be exploited for the improvement of crop plants grown on acid soils via both molecular-assisted breeding and biotechnology approaches.

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An erratum has been published for this article:
Plant Adaptation to Acid Soils: The Molecular Basis for Crop Aluminum Resistance
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2015-04-29
2024-12-12
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Literature Cited

  1. Aniol A. 1.  1990. Genetics of tolerance to aluminum in wheat (Triticum aestivum L. Thell). Plant Soil 123:223–27 [Google Scholar]
  2. Aniol A, Gustafson JP. 2.  1984. Chromosome location of genes controlling aluminum tolerance in wheat, rye, and triticale. Can. J. Genet. Cytol. 26:701–5 [Google Scholar]
  3. Apel K, Hirt H. 3.  2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55:373–99 [Google Scholar]
  4. Barcelo J, Poschenrieder C. 4.  2002. Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. Environ. Exp. Bot. 48:75–92 [Google Scholar]
  5. Berg JM, Tymoczko JL, Stryer L. 5.  2002. The citric acid cycle. Biochemistry465–87 New York: Freeman, 5th ed.. [Google Scholar]
  6. Cai S, Wu D, Jabeen Z, Huang Y, Huang Y, Zhang G. 6.  2013. Genome-wide association analysis of aluminum tolerance in cultivated and Tibetan wild barley. PLOS ONE 8:e69776 [Google Scholar]
  7. Camargo CEO. 7.  1981. Melhoramento do trigo. I. Hereditariedade da tolerância à toxicidade do alumínio. Bragantia 40:33–45 [Google Scholar]
  8. Caniato FF, Guimaraes CT, Hamblin M, Billot C, Rami J-F. 8.  et al. 2011. The relationship between population structure and aluminum tolerance in cultivated sorghum. PLOS ONE 6:e20830 [Google Scholar]
  9. Caniato FF, Guimaraes CT, Schaffert RE, Alves VMC, Kochian LV. 9.  et al. 2007. Genetic diversity for aluminum tolerance in sorghum. Theor. Appl. Genet. 114:863–76 [Google Scholar]
  10. Caniato FF, Hamblin MT, Guimaraes CT, Zhang Z, Schaffert RE. 10.  et al. 2014. Association mapping provides insights into the origin and the fine structure of the sorghum aluminum tolerance locus, AltSB. PLOS ONE 9:e87438 [Google Scholar]
  11. Chang YC, Yamamoto Y, Matsumoto H. 11.  1999. Accumulation of aluminium in the cell wall pectin in cultured tobacco (Nicotiana tabacum L.) cells treated with a combination of aluminium and iron. Plant Cell Environ. 22:1009–17 [Google Scholar]
  12. Chen ZC, Yokosho K, Kashino M, Zhao FJ, Yamaji N, Ma JF. 12.  2013. Adaptation to acidic soil is achieved by increased numbers of cis-acting elements regulating ALMT1 expression in Holcus lanatus. Plant J. 76:10–23 [Google Scholar]
  13. Collins NC, Shirley NJ, Saeed M, Pallotta M, Gustafson JP. 13.  2008. An ALMT1 gene cluster controlling aluminium tolerance at the Alt4 locus of rye (Secale cereale L.). Genetics 179:669–82Showed that copy-number variation is involved with Al resistance provided by TaALMT1 in rye. [Google Scholar]
  14. Conceição LDHCS, Tessele C, Barbosa Neto JF. 14.  2009. Diallel analysis and mapping of aluminum tolerance in corn inbred lines. Maydica 54:51–64 [Google Scholar]
  15. Dai J, Bai G, Zhang D, Hong D. 15.  2012. Validation of quantitative trait loci for aluminum tolerance in Chinese wheat landrace FSW. Euphytica 192:171–79 [Google Scholar]
  16. De Angeli A, Baetz U, Francisco R, Zhang J, Chaves MM, Regalado A. 16.  2013. The vacuolar channel VvALMT9 mediates malate and tartrate accumulation in berries of Vitis vinifera. Planta 238:283–91 [Google Scholar]
  17. De Angeli A, Zhang J, Meyer S, Martinoia E. 17.  2013. AtALMT9 is a malate-activated vacuolar chloride channel required for stomatal opening in Arabidopsis. Nat. Commun. 4:1804 [Google Scholar]
  18. Delhaize E, Craig S, Beaton CD, Bennet RJ, Jagadish VC, Randall PJ. 18.  1993. Aluminum tolerance in wheat (Triticum asetivum L.): I. Uptake and distribution of aluminum in root apices. Plant Physiol. 103:685–93 [Google Scholar]
  19. Delhaize E, Ma JF, Ryan PR. 19.  2012. Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci. 17:341–48 [Google Scholar]
  20. Delhaize E, Ryan PR, Hebb DM, Yamamoto Y, Sasaki T, Matsumoto H. 20.  2004. Engineering high-level aluminum tolerance in barley with the ALMT1 gene. PNAS 101:15249–54 [Google Scholar]
  21. Delhaize E, Ryan PR, Randall PJ. 21.  1993. Aluminum tolerance in wheat (Triticum aestivum L.): II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol. 103:695–702The seminal paper that demonstrated the major root tip Al exclusion mechanism based on Al-activated OA exudation. [Google Scholar]
  22. Ding ZJ, Yan JY, Xu XY, Li GX, Zheng SJ. 22.  2013. WRKY46 functions as a transcriptional repressor of ALMT1, regulating aluminum-induced malate secretion in Arabidopsis. Plant J. 76:825–35 [Google Scholar]
  23. Dreyer I, Gomez-Porras JL, Riano-Pachon DM, Hedrich R, Geiger D. 23.  2012. Molecular evolution of slow and quick anion channels (SLACs and QUACs/ALMTs). Front. Plant Sci. 3:263 [Google Scholar]
  24. Eticha D, Stass A, Horst WJ. 24.  2005. Cell-wall pectin and its degree of methylation in the maize root-apex: significance for genotypic differences in aluminium resistance. Plant Cell Environ. 28:1410–20 [Google Scholar]
  25. Famoso AN, Clark RT, Shaff JE, Craft E, McCouch SR, Kochian LV. 25.  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. 153:1678–91 [Google Scholar]
  26. Famoso AN, Zhao K, Clark RT, Tung CW, Wright MH. 26.  et al. 2011. Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL mapping. PLOS Genet. 7:e1002221 [Google Scholar]
  27. Fujii M, Yokosho K, Yamaji N, Saisho D, Yamane M. 27.  et al. 2012. Acquisition of aluminium tolerance by modification of a single gene in barley. Nat. Commun. 3:713Identified a cis sequence within the HvAACT1 promoter that enhances gene expression and drives expression to the root tips. [Google Scholar]
  28. Furuichi T, Sasaki T, Tsuchiya Y, Ryan PR, Delhaize E, Yamamoto Y. 28.  2010. An extracellular hydrophilic carboxy-terminal domain regulates the activity of TaALMT1, the aluminum-activated malate transport protein of wheat. Plant J. 64:47–55 [Google Scholar]
  29. Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y. 29.  et al. 2007. An aluminum-activated citrate transporter in barley. Plant Cell Physiol. 48:1081–91Along with Ref. 71, provided the first identification of the second class of root OA transporters involved in Al exclusion (MATEs). [Google Scholar]
  30. Garvin DF, Carver BF. 30.  2003. Role of the genotype in tolerance to acidity and aluminum toxicity. Handbook of Soil Acidity Z Rengel 387–406 New York: Dekker [Google Scholar]
  31. Gruber BD, Ryan PR, Richardson AE, Tyerman SD, Ramesh S. 31.  et al. 2010. HvALMT1 from barley is involved in the transport of organic anions. J. Exp. Bot. 61:1455–67 [Google Scholar]
  32. Guimaraes CT, Simoes CC, Pastina MM, Maron LG, Magalhaes JV. 32.  et al. 2014. Genetic dissection of Al tolerance QTLs in the maize genome by high density SNP scan. BMC Genomics 15:153–67 [Google Scholar]
  33. Henikoff S, Greene EA, Pietrokovski S, Bork P, Attwood TK, Hood L. 33.  1997. Gene families: the taxonomy of protein paralogs and chimeras. Science 278:609–14 [Google Scholar]
  34. Hoekenga OA, Maron LG, Piñeros MA, Cançado GM, Shaff J. 34.  et al. 2006. AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. PNAS 103:9738–43 [Google Scholar]
  35. Huang CF, Yamaji N, Chen Z, Ma JF. 35.  2012. A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice. Plant J. 69:857–67 [Google Scholar]
  36. Huang CF, Yamaji N, Ma JF. 36.  2010. Knockout of a bacterial-type ATP-binding cassette transporter gene, AtSTAR1, results in increased aluminum sensitivity in Arabidopsis. Plant Physiol. 153:1669–77 [Google Scholar]
  37. Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF. 37.  2009. A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21:655–67Identified the first rice Al resistance genes (STAR1 and STAR2) involved in transporting cell wall–modifying substrates from the root cytoplasm. [Google Scholar]
  38. Ito D, Shinkai Y, Kato Y, Kondo T, Yoshida K. 38.  2009. Chemical studies on different color development in blue- and red-colored sepal cells of Hydrangea macrophylla. Biosci. Biotechnol. Biochem. 73:1054–59 [Google Scholar]
  39. Iuchi S, Koyama H, Iuchi A, Kobayashi Y, Kitabayashi S. 39.  et al. 2007. Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. PNAS 104:9900–5Identified the first transcription factor (STOP1) that regulates the Al-induced expression of a suite of Al resistance genes. [Google Scholar]
  40. Johnson JP, Carver BF, Baligar VC. 40.  1997. Expression of aluminum tolerance transferred from Atlas 66 to hard winter wheat. Crop Sci. 37:103–8 [Google Scholar]
  41. Jones DL, Blancaflor EB, Kochian LV, Gilroy S. 41.  2006. Spatial coordination of aluminium uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots. Plant Cell Environ. 29:1309–18 [Google Scholar]
  42. Jones DL, Gilroy S, Larsen PB, Howell SH, Kochian LV. 42.  1998. Effect of aluminum on cytoplasmic Ca2+ homeostasis in root hairs of Arabidopsis thaliana (L.). Planta 206:378–87 [Google Scholar]
  43. Jones DL, Kochian LV, Gilroy S. 43.  1998. Aluminum induces a decrease in cytosolic [Ca2+] in BY-2 tobacco cell cultures. Plant Physiol. 116:81–89 [Google Scholar]
  44. Kang J, Park J, Choi H, Burla B, Kretzschmar T. 44.  et al. 2011. Plant ABC transporters. Arabidopsis Book 9:e0153 [Google Scholar]
  45. Kerridge PC, Kronstad WE. 45.  1968. Evidence of genetic resistance to aluminum toxicity in wheat (Triticum aestivum Vill., Host). Agron. J. 60:710–11 [Google Scholar]
  46. Kidd PS, Llugany M, Poschenrieder C, Gunse B, Barcelo J. 46.  2001. The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). J. Exp. Bot. 52:1339–52 [Google Scholar]
  47. Kobayashi Y, Hoekenga OA, Itoh H, Nakashima M, Saito S. 47.  et al. 2007. Characterization of AtALMT1 expression in aluminum-inducible malate release and its role for rhizotoxic stress tolerance in Arabidopsis. Plant Physiol. 145:843–52 [Google Scholar]
  48. Kobayashi Y, Ohyama Y, Kobayashi Y, Ito H, Iuchi S. 48.  et al. 2014. STOP2 activates transcription of several genes for Al- and low pH-tolerance that are regulated by STOP1 in Arabidopsis. Mol. Plant 7:311–22 [Google Scholar]
  49. Kochian LV, Hoekenga OA, Piñeros MA. 49.  2004. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu. Rev. Plant Biol. 55:459–93 [Google Scholar]
  50. Kollmeier M, Dietrich P, Bauer CS, Horst WJ, Hedrich R. 50.  2001. Aluminum activates a citrate-permeable anion channel in the aluminum-sensitive zone of the maize root apex. A comparison between an aluminum-sensitive and an aluminum-resistant cultivar. Plant Physiol. 126:397–410 [Google Scholar]
  51. Kovermann P, Meyer S, Hortensteiner S, Picco C, Scholz-Starke J. 51.  et al. 2007. The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J. 52:1169–80 [Google Scholar]
  52. Larsen PB, Cancel J, Rounds M, Ochoa V. 52.  2007. Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta 225:1447–58 [Google Scholar]
  53. Larsen PB, Geisler MJ, Jones CA, Williams KM, Cancel JD. 53.  2005. ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. Plant J. 41:353–63 [Google Scholar]
  54. Li JY, Liu J, Dong D, Jia X, McCouch SR, Kochian LV. 54.  2014. Natural variation underlies alterations in Nramp aluminum transporter (NRAT1) expression and function that play a key role in rice aluminum tolerance. PNAS 111:6503–8 [Google Scholar]
  55. Liang C, Piñeros MA, Tian J, Yao Z, Sun L. 55.  et al. 2013. Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils. Plant Physiol. 161:1347–61 [Google Scholar]
  56. Ligaba A, Dreyer I, Margaryan A, Schneider DJ, Kochian LV, Piñeros M. 56.  2013. Functional, structural and phylogenetic analysis of domains underlying the Al sensitivity of the aluminum-activated malate/anion transporter, TaALMT1. Plant J. 76:766–80 [Google Scholar]
  57. Ligaba A, Katsuhara M, Ryan PR, Shibasaka M, Matsumoto H. 57.  2006. The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporters that enhance the aluminum resistance of plant cells. Plant Physiol. 142:1294–303 [Google Scholar]
  58. Ligaba A, Kochian LV, Piñeros M. 58.  2009. Phosphorylation at S384 regulates the activity of the TaALMT1 malate transporter that underlies aluminum resistance in wheat. Plant J. 60:411–23 [Google Scholar]
  59. Ligaba A, Maron L, Shaff J, Kochian LV, Piñeros M. 59.  2012. Maize ZmALMT2 is a root anion transporter that mediates constitutive root malate efflux. Plant Cell Environ. 35:1185–200 [Google Scholar]
  60. Liu J, Magalhaes JV, Shaff J, Kochian LV. 60.  2009. Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J. 57:389–99Demonstrated that a transcriptional link between AtMATE and AtALMT1 provided by STOP1 uncovers common regulatory networks that influence distinct transporter families. [Google Scholar]
  61. Luo MC, Dvorak J. 61.  1996. Molecular mapping of an aluminum tolerance locus on chromosome 4D of Chinese Spring wheat. Euphytica 91:31–35 [Google Scholar]
  62. Ma JF. 62.  2000. Role of organic acids in detoxification of aluminum in higher plants. Plant Cell Physiol. 41:383–90 [Google Scholar]
  63. Ma JF. 63.  2007. Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. Int. Rev. Cytol. 264:225–52 [Google Scholar]
  64. Ma JF, Hiradate S. 64.  2000. Form of aluminium for uptake and translocation in buckwheat (Fagopyrum esculentum Moench). Planta 211:355–60 [Google Scholar]
  65. Ma JF, Hiradate S, Nomoto K, Iwashita T, Matsumoto H. 65.  1997. Internal detoxification mechanism of Al in hydrangea: identification of Al form in the leaves. Plant Physiol. 113:1033–39 [Google Scholar]
  66. Ma JF, Nagao S, Huang CF, Nishimura M. 66.  2005. Isolation and characterization of a rice mutant hypersensitive to Al. Plant Cell Physiol. 46:1054–61 [Google Scholar]
  67. Ma JF, Ryan PR, Delhaize E. 67.  2001. Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 6:273–78 [Google Scholar]
  68. Ma JF, Shen R, Zhao Z, Wissuwa M, Takeuchi Y. 68.  et al. 2002. Response of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant Cell Physiol. 43:652–59 [Google Scholar]
  69. Ma JF, Zheng SJ, Matsumoto H, Hiradate S. 69.  1997. Detoxifying aluminium with buckwheat. Nature 390:569–70 [Google Scholar]
  70. Magalhaes JV, Garvin DF, Wang Y, Sorrells ME, Klein PE. 70.  et al. 2004. Comparative mapping of a major aluminum tolerance gene in sorghum and other species in the poaceae. Genetics 167:1905–14 [Google Scholar]
  71. Magalhaes JV, Liu J, Guimaraes CT, Lana UGP, Alves VMC. 71.  et al. 2007. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat. Genet. 39:1156–61Along with Ref. 29, provided the first identification of the second class of root OA transporters involved in Al exclusion (MATEs). [Google Scholar]
  72. Magnavaca R, Gardner CO, Clark RB. 72.  1987. Inheritance of aluminum tolerance in maize. Genetic Aspects of Mineral Nutrition HW Gabelman, BC Loughman 201–12 Dordrecht, Neth: Nijhoff [Google Scholar]
  73. Maron LG, Guimaraes CT, Kirst M, Albert PS, Birchler JA. 73.  et al. 2013. Aluminum tolerance in maize is associated with higher MATE1 gene copy number. PNAS 110:5241–46Showed that copy-number variation is involved in the transcriptional control of ZmMATE1 in maize. [Google Scholar]
  74. Maron LG, Piñeros MA, Guimaraes CT, Magalhaes JV, Pleiman JK. 74.  et al. 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. 61:728–40 [Google Scholar]
  75. Martinoia E, Klein M, Geisler M, Bovet L, Forestier C. 75.  et al. 2002. Multifunctionality of plant ABC transporters—more than just detoxifiers. Planta 214:345–55 [Google Scholar]
  76. Matonyei TK, Cheprot RK, Liu J, Piñeros MA, Shaff JE. 76.  et al. 2014. Physiological and molecular analysis of aluminum tolerance in selected Kenyan maize lines. Plant Soil 377:357–67 [Google Scholar]
  77. Melo JO, Lana UGP, Piñeros MA, Alves VMC, Guimaraes CT. 77.  et al. 2013. Incomplete transfer of accessory loci influencing SbMATE expression underlies genetic background effects for aluminum tolerance in sorghum. Plant J. 73:276–88 [Google Scholar]
  78. Meyer S, De Angeli A, Fernie AR, Martinoia E. 78.  2010. Intra- and extra-cellular excretion of carboxylates. Trends Plant Sci. 15:40–47 [Google Scholar]
  79. Meyer S, Mumm P, Imes D, Endler A, Weder B. 79.  et al. 2010. AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. Plant J. 63:1054–62 [Google Scholar]
  80. Meyer S, Scholz-Starke J, De Angeli A, Kovermann P, Burla B. 80.  et al. 2011. Malate transport by the vacuolar AtALMT6 channel in guard cells is subject to multiple regulation. Plant J. 67:247–57 [Google Scholar]
  81. Minella E, Sorrells ME. 81.  1992. Aluminum tolerance in barley: genetic relationships among genotypes of diverse origin. Crop Sci. 32:593–98 [Google Scholar]
  82. Miyasaka SC, Buta JG, Howell RK, Foy CD. 82.  1991. Mechanism of aluminum tolerance in snapbeans: root exudation of citric acid. Plant Physiol. 96:737–43 [Google Scholar]
  83. Motoda H, Sasaki T, Yamamoto Y. 83.  2007. Transmembrane topology of wheat ALMT1 transporter. Plant Cell Physiol. 48:S88 [Google Scholar]
  84. Mumm P, Imes D, Martinoia E, Al-Rasheid KAS, Geiger D. 84.  et al. 2013. C-terminus-mediated voltage gating of Arabidopsis guard cell anion channel QUAC1. Mol. Plant 6:1550–63 [Google Scholar]
  85. Negishi T, Oshima K, Hattori M, Kanai M, Mano S. 85.  et al. 2012. Tonoplast- and plasma membrane-localized aquaporin-family transporters in blue hydrangea sepals of aluminum hyperaccumulating plant. PLOS ONE 7:e43189 [Google Scholar]
  86. Negishi T, Oshima K, Hattori M, Yoshida K. 86.  2013. Plasma membrane-localized Al-transporter from blue hydrangea sepals is a member of the anion permease family. Genes Cells 18:341–52 [Google Scholar]
  87. Nguyen BD, Brar DS, Bui BC, Nguyen TV, Pham LN, Nguyen HT. 87.  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. 106:583–93 [Google Scholar]
  88. Ninamango-Cárdenas F, Guimarães CT, Martins PR, Parentoni SN, Carneiro NP. 88.  et al. 2003. Mapping QTLs for aluminum tolerance in maize. Euphytica 130:223–32 [Google Scholar]
  89. Osawa H, Endo I, Hara Y, Matsushima Y, Tange T. 89.  2011. Transient proliferation of proanthocyanidin-accumulating cells on the epidermal apex contributes to highly aluminum-resistant root elongation in camphor tree. Plant Physiol. 155:433–46 [Google Scholar]
  90. Osawa H, Matsumoto H. 90.  2001. Possible involvement of protein phosphorylation in aluminium-responsive malate efflux from wheat root apex. Plant Physiol. 126:411–20 [Google Scholar]
  91. Papernik LA, Bethea AS, Singleton TE, Magalhaes JV, Garvin DF, Kochian LV. 91.  2001. Physiological basis of reduced Al tolerance in ditelosomic lines of Chinese Spring wheat. Planta 212:829–34 [Google Scholar]
  92. Pellet DM, Grunes DL, Kochian LV. 92.  1995. Organic-acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196:788–95 [Google Scholar]
  93. Pereira JF, Zhou G, Delhaize E, Richardson T, Zhou M, Ryan PR. 93.  2010. Engineering greater aluminium resistance in wheat by over-expressing TaALMT1. Ann. Bot. 106:205–14 [Google Scholar]
  94. Piñeros MA, Cançado GM, Kochian LV. 94.  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. 147:2131–46 [Google Scholar]
  95. Piñeros MA, Cançado GM, Maron LG, Lyi SM, Menossi M, Kochian LV. 95.  2008. Not all ALMT1-type transporters mediate aluminum-activated organic acid responses: the case of ZmALMT1—an anion-selective transporter. Plant J. 53:352–67 [Google Scholar]
  96. Piñeros MA, Fich E, Offenborn JN, Mähs A, Kudla J, Kochian LV. 96.  2013. A CBL5/CIPK2 calcium sensor/protein kinase complex modulates the transport activity of MATE-type transporters involved in the key plant aluminum resistance mechanism mediated by root organic acid release Presented at Int. Workshop Plant Membr. Biol., 16th, Okayama, Jpn., Mar 26–31 [Google Scholar]
  97. Piñeros MA, Kochian LV. 97.  2001. A patch-clamp study on the physiology of aluminum toxicity and aluminum tolerance in maize. Identification and characterization of Al3+-induced anion channels. Plant Physiol. 125:292–305Demonstrated that an Al-activated and electrogenic anion efflux transporter underlies Al-activated citrate efflux and Al resistance in maize. [Google Scholar]
  98. Piñeros MA, Magalhaes JV, Alves VMC, Kochian LV. 98.  2002. The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation in maize. Plant Physiol. 129:1194–206 [Google Scholar]
  99. Piñeros MA, Shaff JE, Manslank HS, Alves VMC, Kochian LV. 99.  2005. Aluminum resistance in maize cannot be solely explained by root organic acid exudation. A comparative physiological study. Plant Physiol. 137:231–41 [Google Scholar]
  100. Raman H, Stodart B, Ryan PR, Delhaize E, Emebiri L. 100.  et al. 2010. Genome-wide association analyses of common wheat (Triticum aestivum L.) germplasm identifies multiple loci for aluminium resistance. Genome 53:957–66 [Google Scholar]
  101. Rengel Z. 101.  1992. Disturbance of Ca2+ homeostasis as a primary trigger in the Al toxicity syndrome. Plant Cell Environ. 15:931–38 [Google Scholar]
  102. Rengel Z, Zhang W-H. 102.  2003. Role of dynamics of intracellular calcium in aluminium-toxicity syndrome. New Phytol. 159:295–314 [Google Scholar]
  103. Riede CR, Anderson JA. 103.  1996. Linkage of RFLP markers to an aluminum tolerance gene in wheat. Crop Sci. 36:905–9 [Google Scholar]
  104. Rodriguez Milla MA, Gustafson JP. 104.  2001. Genetic and physical characterization of chromosome 4DL in wheat. Genome. Genome 44:883–92 [Google Scholar]
  105. Ryan PR, Delhaize E. 105.  2012. Plant adaptations to aluminium toxicity. Plant Stress Physiology S Shabala 171–93 Wallingford, UK: CABI [Google Scholar]
  106. Ryan PR, Delhaize E, Jones D. 106.  2001. Function and mechanism of organic anion exudation from plant roots. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52:527–60 [Google Scholar]
  107. Ryan PR, Delhaize E, Randall PJ. 107.  1995. Malate efflux from root apices and tolerance aluminum are highly correlated in wheat. Aust. J. Plant Physiol. 22:531–36 [Google Scholar]
  108. Ryan PR, DiTomaso JM, Kochian LV. 108.  1993. Aluminum toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. J. Exp. Bot. 44:437–46 [Google Scholar]
  109. Ryan PR, Raman H, Gupta S, Horst WJ, Delhaize E. 109.  2009. A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol. 149:340–51 [Google Scholar]
  110. Ryan PR, Raman H, Gupta S, Sasaki T, Yamamoto Y, Delhaize E. 110.  2010. The multiple origins of aluminium resistance in hexaploid wheat include Aegilops tauschii and more recent cis mutations to TaALMT1. Plant J. 64:446–55 [Google Scholar]
  111. Ryan PR, Skerrett M, Findlay GP, Delhaize E, Tyerman SD. 111.  1997. Aluminum activates an anion channel in the apical cells of wheat roots. PNAS 94:6547–52Demonstrated that Al-activated anion channels underlie Al-activated malate efflux and Al resistance in wheat. [Google Scholar]
  112. Ryan PR, Tyerman SD, Sasaki T, Yamamoto Y, Zhang WH, Delhaize E. 112.  2011. Identification of aluminium-resistance genes in plants provides an opportunity for enhancing the acid-soil tolerance of crop species. J. Exp. Bot. 62:9–20 [Google Scholar]
  113. Sasaki T, Mori IC, Furuichi T, Munemasa S, Toyooka K. 113.  et al. 2010. Closing plant stomata requires a homolog of an aluminum-activated malate transporter. Plant Cell Physiol. 51:354–65 [Google Scholar]
  114. Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ. 114.  et al. 2004. A wheat gene encoding an aluminum-activated malate transporter. Plant J. 37:645–53Identified the first Al resistance gene, TaALMT1, which encodes an Al-activated malate efflux transporter in wheat root apices. [Google Scholar]
  115. Sasidharan R, Voesenek LACJ, Pierik R. 115.  2011. Cell wall modifying proteins mediate plant acclimatization to biotic and abiotic stresses. Crit. Rev. Plant Sci. 30:548–62 [Google Scholar]
  116. Sawaki Y, Iuchi S, Kobayashi Y, Kobayashi Y, Ikka T. 116.  et al. 2009. STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities. Plant Physiol. 150:281–94 [Google Scholar]
  117. Schmohl N, Pilling J, Fisahn J, Horst WJ. 117.  2000. Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiol. Plant. 109:419–27 [Google Scholar]
  118. Shen RF, Ma JF, Kyo M, Iwashita T. 118.  2002. Compartmentation of aluminium in leaves of an Al-accumulator, Fagopyrum esculentum Moench. Planta 215:394–98 [Google Scholar]
  119. Sibov ST, Gaspar MJ, Ottoboni LMM, Arruda P, Souza AP. 119.  1999. Two genes controlling aluminum tolerance in maize: genetic and molecular mapping analyses. Genome 42:475–82 [Google Scholar]
  120. Sivaguru M, Horst W. 120.  1998. The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize. Plant Physiol. 116:155–63 [Google Scholar]
  121. Sivaguru M, Liu J, Kochian LV. 121.  2013. Targeted expression of SbMATE in the root distal transition zone is responsible for sorghum aluminum resistance. Plant J. 76:297–307 [Google Scholar]
  122. Tahara K, Hashida K, Otsuka Y, Ohara S, Kojima K, Shinohara K. 122.  2014. Identification of a hydrolyzable tannin, oenothein B, as an aluminum-detoxifying ligand in a highly aluminum-resistant tree, Eucalyptus camaldulensis. Plant Physiol. 164:683–93 [Google Scholar]
  123. Tang Y, Garvin DF, Kochian LV, Sorrells ME, Carver BF. 123.  2002. Physiological genetics of aluminum tolerance in the wheat cultivar Atlas 66. Crop Sci. 42:1541–46 [Google Scholar]
  124. Tolrà R, Barcelo J, Poschenrieder C. 124.  2009. Constitutive and aluminium-induced patterns of phenolic compounds in two maize varieties differing in aluminium tolerance. J. Inorg. Biochem. 103:1486–90 [Google Scholar]
  125. Tovkach A, Ryan PR, Richardson AE, Lewis DC, Rathjen TM. 125.  et al. 2013. Transposon-mediated alteration of TaMATE1B expression in wheat confers constitutive citrate efflux from root apices. Plant Physiol. 161:880–92 [Google Scholar]
  126. Tsutsui T, Yamaji N, Feng Ma J. 126.  2011. Identification of a cis-acting element of ART1, a C2H2-type zinc-finger transcription factor for aluminum tolerance in rice. Plant Physiol. 156:925–31 [Google Scholar]
  127. von Uexküll HR, Mutert E. 127.  1995. Global extent, development and economic-impact of acid soils. Plant Soil 171:1–15 [Google Scholar]
  128. Wong MTF, Asseng S, Robertson MJ, Oliver Y. 128.  2008. Mapping subsoil acidity and shallow soil across a field with information from yield maps, geophysical sensing and the grower. Precis. Agric. 9:3–5 [Google Scholar]
  129. Wood S, Sebastian K, Scherr SJ. 129.  2000. Pilot analysis of global ecosystems: agroecosystems Tech. Rep., Int. Food Policy Res. Inst. and World Resour. Inst., Washington, DC [Google Scholar]
  130. Wu P, Liao CY, Hu B, Yi KK, Jin WZ. 130.  et al. 2000. QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theor. Appl. Genet. 100:1295–303 [Google Scholar]
  131. Xia J, Yamaji N, Che J, Shen RF, Ma JF. 131.  2014. Differential expression of Nrat1 is responsible for Al-tolerance QTL on chromosome 2 in rice. J. Exp. Bot. 65:4297–304 [Google Scholar]
  132. Xia J, Yamaji N, Kasai T, Ma JF. 132.  2010. Plasma membrane-localized transporter for aluminum in rice. PNAS 107:18381–85Identified the first Al uptake transporter that underlies a novel Al resistance mechanism. [Google Scholar]
  133. Xia J, Yamaji N, Ma JF. 133.  2011. Further characterization of an aluminum influx transporter in rice. Plant Signal. Behav. 6:160–63 [Google Scholar]
  134. Xia J, Yamaji N, Ma JF. 134.  2013. A plasma membrane-localized small peptide is involved in rice aluminum tolerance. Plant J. 76:345–55 [Google Scholar]
  135. Yamaji N, Huang CF, Nagao S, Yano M, Sato Y. 135.  et al. 2009. A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell 21:3339–49Showed that ART1, the STOP1 homolog in rice, is a transcription factor that regulates the Al-induced expression of genes involved in Al resistance. [Google Scholar]
  136. Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H. 136.  2003. Oxidative stress triggered by aluminum in plant roots. Plant Soil 255:239–43 [Google Scholar]
  137. Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR. 137.  et al. 2008. Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol. 146:602–11 [Google Scholar]
  138. Yang JL, Zhu XF, Peng YX, Zheng C, Li GX. 138.  et al. 2011. Cell wall hemicellulose contributes significantly to aluminum adsorption and root growth in Arabidopsis. Plant Physiol. 155:1885–92 [Google Scholar]
  139. Yang XY, Yang JL, Piñeros MA, Kochian LV, Li GX, Zheng SJ. 139.  2011. A de novo synthesis citrate transporter, Vigna umbellata multidrug and toxic compound extrusion, implicates in Al-activated citrate efflux in rice bean (Vigna umbellata) root apex. Plant Cell Environ. 34:2138–48 [Google Scholar]
  140. Yang XY, Zeng ZH, Yan JY, Fan W, Bian HW. 140.  et al. 2013. Association of specific pectin methylesterases with Al-induced root elongation inhibition in rice. Physiol. Plant. 148:502–11 [Google Scholar]
  141. Yokosho K, Yamaji N, Ma JF. 141.  2010. Isolation and characterisation of two MATE genes in rye. Funct. Plant Biol. 37:296–303 [Google Scholar]
  142. Yokosho K, Yamaji N, Ma JF. 142.  2011. An Al-inducible MATE gene is involved in external detoxification of Al in rice. Plant J. 68:1061–69 [Google Scholar]
  143. Zhang WH, Ryan PR, Sasaki T, Yamamoto Y, Sullivan W, Tyerman SD. 143.  2008. Characterization of the TaALMT1 protein as an Al3+-activated anion channel in transformed tobacco (Nicotiana tabacum L.) cells. Plant Cell Physiol. 49:1316–30 [Google Scholar]
  144. Zhang WH, Ryan PR, Tyerman SD. 144.  2001. Malate-permeable channels and cation channels activated by aluminium in the apical cells of wheat roots. Plant Physiol. 125:1459–72 [Google Scholar]
  145. Zheng SJ, Ma JF, Matsumoto H. 145.  1998. Continuous secretion of organic acids is related to aluminum resistance during relatively long-term exposure to aluminum stress. Physiol. Plant. 103:209–14 [Google Scholar]
  146. Zheng SJ, Ma JF, Matsumoto H. 146.  1998. High aluminum resistance in buckwheat: I. Al-induced specific secretion of oxalic acid from root tips. Plant Physiol. 117:745–51 [Google Scholar]
  147. Zhu XF, Shi YZ, Lei GJ, Fry SC, Zhang BC. 147.  et al. 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 24:4731–47 [Google Scholar]
  148. Zhu XF, Sun Y, Zhang BC, Mansoori N, Wan JX. 148.  et al. 2014. TRICHOME BIREFRINGENCE-LIKE27 affects aluminum sensitivity by modulating the O-acetylation of xyloglucan and aluminum-binding capacity in Arabidopsis. Plant Physiol. 166:181–89 [Google Scholar]
  149. Zhu XF, Wan JX, Sun Y, Shi YZ, Braam J. 149.  et al. 2014. Xyloglucan Endotransglucosylase-Hydrolase17 interacts with Xyloglucan Endotransglucosylase-Hydrolase31 to confer xyloglucan endotransglucosylase action and affect aluminum sensitivity in Arabidopsis. Plant Physiol. 165:1566–74 [Google Scholar]
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