The Botanical Review

, Volume 68, Issue 2, pp 235–269 | Cite as

Aluminum hyperaccumulation in angiosperms: A review of its phylogenetic significance

  • Steven Jansen
  • Martin R. Broadley
  • Elmar Robbrecht
  • Erik Smets


Aluminum phytotoxicity and genetically based aluminum resistance has been studied intensively during recent decades because aluminum toxicity is often the primary factor limiting crop productivity on acid soils. Plants that grow on soils with high aluminum concentrations employ three basic strategies to deal with aluminum stress. While excluders effectively prevent aluminum from entering their aerial parts over a broad range of aluminum concentration in the soil, hyperaccumulators take up aluminum in their aboveground tissues in quantities above 1000 ppm; that is, far exceeding those present in the soil or in the nonaccumulating species growing nearby. In between these two extremes are indicator species, representing intermediate responses.

A list of aluminum hyperaccumulators in angiosperms is compiled on the basis of data in the literature. Aluminum hyperaccumulators include mainly woody, perennial taxa from tropical regions. Recent molecular phylogenies are used to evaluate the systematic and phylogenetic implications of the character. As was hypothesized earlier, our preliminary conclusions support the primitive status of aluminum hyperaccumulation. According to the APG classification system, this phytochemical character is found in approximately 45 families, which belong largely to the eudicots. Aluminum hyperaccumulators are particularly common in basal branches of fairly advanced groups such as rosids (Myrtales, Malpighiales, Oxalidales) and asterids (Cornales, Ericales, Gentianales, Aquifoliales), but the character has probably been lost in the most derived taxa. The feature is suggested to characterize approximately 18 families (e.g., Anisophylleaceae, Cunoniaceae, Diapensiaceae, Memecylaceae, Monimiaceae, Rapateaceae, Siparunaceae, Vochysiaceae, and several monogeneric families). In 27 other families, aluminum hyperaccumulation is restricted to subfamilies, tribes, or genera. Further analyses of a broader range of taxa are needed to examine the origin and taxonomic significance of aluminum hyperaccumulation in several clades. Aluminum hyperaccumulation provides an evolutionary model system for the integration of different biological disciplines, such as systematics, ecology, biogeography, physiology, and biochemistry. Therefore, multidisciplinary approaches are needed to make further progress in understanding the biology of aluminum hyperaccumulators.


Botanical Review rbcL rbcL Sequence Rennet Aluminum Level 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


La phytotoxicité et la résistance génétique à l’aluminium ont été étudiées intensivement pendant les dernières décennies en raison du rôle important que joue la toxicité à l’aluminium comme facteur limitant la production des plantes sur les terrains acides. Les végétaux des terres acides ayant une haute concentration d’aluminium, survivent grace à trois stratégies. Les plantes à exclusion d’aluminium empêchent l’élément d’entrer dans les tissus aériens à partir d’un sol à fortes concentrations d’aluminium. Les plantes hyperaccumulatrices d’aluminium cependant contiennent une concentration d’aluminium plus haute que 1000 ppm dans leurs tiges et feuilles, dépassant de beaucoup les concentrations du sol ou des plantes avoisinantes nonaccumulatives. Entre ces deux groupes extrèmes, il y a les plantes indicatrices d’aluminium qui ne font aucun effort pour exclure ou accumuler l’aluminium.

Nous présentons une liste d’angiospermes hyperaccumulateurs d’aluminium sur base d’une analyse des données de la littérature. Les plantes hyperaccumulatrices sont surtout des plantes ligneuses et pérennes des régions tropicales. Nous utilisons les nouvelles phylogenèses moléculaires pour évaluer la signification systématique et phylogénétique du signal phytochimique. Comme il avait été supposé préalablement, nos conclusions préliminaires confirment le statut primitif de l’hyperaccumulation d’aluminium. Selon le système de classification APG, cette caractéristique phytochimique a été rapportée dans environs 45 familles, qui appartiennent surtout aux eudicots. Les familles hyperaccumulatrices d’aluminium sont surtout présentes dans les branches basales de groupes généralement évolués comme les rosides (Myrtales, Malpighiales, Oxalidales) et les astendes (Cornales, Ericales, Gentianales, Aquifoliales), mais le caractère a probablement disparu dans les groupes les plus dérivés. La caractéristique semble être constante dans presque 18 familles, comme les Anisophylleacées, Cunoniacées, Diapensiacées, Memecylacées, Monimiacées, Rapateacées, Siparunacées, Vochysiacées et quelques familles monogénériques. Dans 27 autres familles, l’hyperaccumulation d’aluminium est limitée aux sous-familles, tribus ou genres. De nouvelles analyses de divers taxa sont nécessaires pour déterminer l’origine et la signification taxonomique dans certains groupes de plantes. Finalement, l’hyperaccumulation d’aluminium est une excellente donnée permettant d’intégrer différentes disciplines biologiques comme la botanique systématique, l’écologie, la biogéographie, la physiologie et la biochimie. Seulement une approche multidisciplinaire permettra de comprendre tous les secrets des plantes qui accumulent l’aluminium.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature Cited

  1. Allen, R. C. 1943. Influence of aluminum on the flower colorof Hydrangea macrophylla DC. Contr. Boyce Thompson Inst. Pl. Res. 13: 221–242.Google Scholar
  2. Alva, A. K., D. G. Edwards, C. J. Asher &F. P. Blarney. 1986. Relationships between root length of soybean and calculated activities of aluminum monomers in nutrient solution. Soil Sci. Soc. Amer. J. 50: 959–962.Google Scholar
  3. Andersson, M. E. 1992. Effects of pH and aluminium on growth ofGalium odoratum (L.) Scop, in flowing solution culture. Environm. & Exp. Bot. 32: 497–504.CrossRefGoogle Scholar
  4. —. 1993. Aluminium toxicity as a factor limiting the distribution ofAllium ursinum (L.). Ann. Bot. (London) 72: 607–611.CrossRefGoogle Scholar
  5. Aniol, A. 1984. Induction of aluminum tolerance in wheat seedlings by low doses of aluminum in the nutrient solution. Pl. Physiol. (Lancaster) 76: 551–555.Google Scholar
  6. —. 1990. Genetics of tolerance to aluminum in wheat (Tritcum aestivum L.). Pl. & Soil 123: 223–227.CrossRefGoogle Scholar
  7. — &J. P. Gustafson. 1984. Chromosome location of genes controlling aluminum tolerance in wheat, rye, and triticale. Canad. J. Genet. Cytol. 26: 701–705.Google Scholar
  8. APG (Angiosperm Phytogeny Group). 1998. An ordinal classification for the families of flowering plants. Ann. Missouri Bot. Gard. 85: 531–553.CrossRefGoogle Scholar
  9. Ashida, J., N. Higachi &T. Kikuchi. 1963. An electron microscopic study on copper precipitation by copper resistant yeast cells. Protoplasma 57: 27–32.CrossRefGoogle Scholar
  10. Baas, P., E. Oosterhoud &C. J. L. Scholtes. 1982. Leaf anatomy and classification of the Olacaceae,Octoknema andErythropalum. Allertonia 3: 155–210.Google Scholar
  11. Backlund, M., B. Oxelman &B. Bremer. 2000. Phylogenetic relationships within the Gentianales based on ndhF and rbcL sequences, with particular reference to the Loganiaceae. Amer. J. Bot. 87: 1029–1043.CrossRefGoogle Scholar
  12. Baker, A. J. M. 1981. Accumulators and excluders: Strategies in the response of plants to heavy metals. J. Pl. Nutr. 3: 643–654.Google Scholar
  13. —. 1987. Metal tolerance. New Phytol. 106 (Suppl.): 93–111.Google Scholar
  14. — &R. R. Brooks. 1989. Terrestrial higher plants which hyperaccumulate metallic elements: A review of their distribution, ecology and phytochemistry. Biorecovery 1: 81–126.Google Scholar
  15. —— &R. Reeves. 1989. Growing for gold… and copper… and zinc. New Sci. 1603: 44–48.Google Scholar
  16. —,J. Proctor, M. M. J. van Balgooy &R. D. Reeves. 1992. Hyperaccumulation of nickel by the flora of the ultramafics of Palawan, Republic of the Philippines. Pp. 291–304in A. J. M Baker, J. Proctor, & R. D. Reeves (eds.), The vegetation of ultramafic (serpentine) soils. Intercept, Andover, UK.Google Scholar
  17. Bennet, R. J., C. M. Breen &M. V. Fey. 1985. The primary site of aluminium injury in the root ofZea mays. S. African J. PI. Soil 2: 1–7.Google Scholar
  18. Blarney, F. C. P., D. C. Edmeades &D. M. Wheeler. 1990. Role of root cation-exchange capacity in differential aluminium tolerance ofLotus species. J. Pl. Nutr. 13: 729–744.Google Scholar
  19. Bradley, R., A. J. Burt &D. J. Read. 1981. Mycorrhizal infection and resistance to heavy metal toxic-ity inCalluna vulgaris. Nature 292: 335–337.CrossRefGoogle Scholar
  20. ———. 1982. The biology of mycorrhiza in the Ericaceae, VIII. The role of mycor-rhizal infection in heavy metal tolerance. New Phytol. 91: 197–209.CrossRefGoogle Scholar
  21. Bremer, B., R. K. Jansen, B. Oxelman, M. Backlund, H. Lantz &K. Ki-Joong. 1999. More charac-ters or more taxa for a robust phylogeny: Case study from the coffee family (Rubiaceae). Syst. Biol. 48: 413–435.PubMedCrossRefGoogle Scholar
  22. Brenan, J. P. M. 1953.Soyauxia, a second genus of Medusandraceae. Kew Bull. 1953: 507–511.CrossRefGoogle Scholar
  23. Broadley, M. R., N. J. Willey, J. C. Wilkins, A. J. M. Baker, A. Mead &P. J. White. 2001. Phyloge-netic variation in heavy metal accumulation in angiosperms. New Phytol. 152: 9–27.CrossRefGoogle Scholar
  24. Brooks, R. R., J. Lee, R. D. Reeves &T. Jaffré. 1977. Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J. Geochem. Explor. 7: 49–57.CrossRefGoogle Scholar
  25. Carver, B. F. &J. D. Ownby. 1995. Acid soil tolerance in wheat. Advances Agron. 54: 117–173.CrossRefGoogle Scholar
  26. Chanderbali, A. S., H. van der Werf &S. S. Renner. 2001. Phylogeny and historical biogeography of Lauraceae: Evidence from the chloroplast and nuclear genomes. Ann. Missouri Bot. Gard. 88: 104–134.CrossRefGoogle Scholar
  27. Chase, M. W., D. E. Soltis, P. S. Soltis, P. J. Rudall, M. F. Fay, W. H. Hahn, S. Sullivan, J. Joseph, M. Molvray, P. J. Kores, T. J. Givnish, K. J. Sytsma &J. C. Pires. 2000. Higher-level system-atics of the monocotyledons: An assessment of current knowledge and a new classification. Pp. 3–16in K. L. Wilson & D. A. Morrison (eds.), Monocots: Systematics and evolution. CSIRO, Collingwood, Australia.Google Scholar
  28. —,S. Zmarzty, M. D. Lledó, K. J. Wurdack, S. M. Swensen &M. F. Fay. 2002. When in doubt, put it in Flacourtiaceae: A molecular phylogenetic analysis based on plastid rbcL DNA sequences. Kew Bull. 57: 141–181.CrossRefGoogle Scholar
  29. Chenery, E. M. 1946. AreHydrangea flowers unique? Nature 158: 240–241.CrossRefGoogle Scholar
  30. —. 1948a. Aluminium in plants and its relation to plant pigments. Ann. Bot. (London) 12: 121–136.Google Scholar
  31. —. 1948b. Aluminium in the plant world, I. General survey in dicotyledons. Kew Bull. 1948: 173–183.CrossRefGoogle Scholar
  32. —. 1949. Aluminium in the plant world, II. Monocotyledons and gymnosperms; III. Cryptogams. Kew Bull. 1949: 463–473.CrossRefGoogle Scholar
  33. —. 1955. A preliminary study of aluminium and the tea bush. Pl. & Soil 6: 174–200.CrossRefGoogle Scholar
  34. — &K. R. Sporne. 1976. A note on the evolutionary status of aluminium-accumulators among dicotyledons. New Phytol. 76: 551–554.CrossRefGoogle Scholar
  35. Clausing, G. &S. S. Renner. 2001. Molecular phylogenetics of Melastomataceae and Memecylaceae: Implications for character evolution. Amer. J. Bot. 88: 486–498.CrossRefGoogle Scholar
  36. —,K. Meyer &S. S. Renner. 2000. Correlations among fruit traits and evolution of different fruits within Melastomataceae. Bot. J. Linn. Soc. 133: 303–326.Google Scholar
  37. Conti, E., A. Litt &K. J. Sytsma. 1996. Circumscription of Myrtales and their relationships to other rosids: Evidence from rbcL sequence data. Amer. J. Bot. 83: 221–233.CrossRefGoogle Scholar
  38. ——,P. G. Wilson, S. A. Graham, B. G. Briggs, A. S. Johnson &K. J. Sytsma. 1997. Interfamilial relationships in Myrtales: Molecular phylogeny and patterns of morphological evolu-tion. Syst. Bot. 22: 629–647.CrossRefGoogle Scholar
  39. Cronquist, A. 1980. Chemistry in plant taxonomy: An assessment of where we stand. Pp. 1–27in F.A. Bisby, J. G. Vaughan & C. A. Wright (eds.), Chemosystematics: Principles and practice. Systemat-ics Association Spec. Vol. 16. Academic Press, London.Google Scholar
  40. Cuenca, G. &R. Herrera. 1987. Ecophysiology of aluminium in terrestrial plants, growing in acid and aluminium-rich tropical soils. Ann. Soc. Roy. Zool. de Belgique 117 (Suppl. 1): 57–74.Google Scholar
  41. —— &E. Medina. 1990. Aluminium tolerance in trees of a tropical cloud forest. Pl. & Soil 125: 169–175.CrossRefGoogle Scholar
  42. —— &T. Merida. 1991. Distribution of aluminium in accumulator plants by X-ray mi-croanalysis inRicheria grandis Vahl leaves from a cloud forest in Venezuela. Pl. Cell Environ. 14: 437–441.CrossRefGoogle Scholar
  43. Cullings, K. W. 1996. Single phylogenetic origin of ericoid mycorrhizae within the Ericaceae. Canad. J. Bot. 74: 1896–1909.CrossRefGoogle Scholar
  44. Dahlgren, G. 1989. The last Dahlgrenogram: System of classification of the dicotyledons. Pp. 249–260in K. Tan (ed.), Plant taxonomy, phytogeography and related subjects: The Davis & Hedge festschrift, Edinburgh Univ. Press, Edinburgh.Google Scholar
  45. Dahlgren, R. 1988. Rhizophoraceae and Anisophylleaceae: Summary statement, relationships. Ann. Missouri Bot. Gard. 75: 1259–1277.CrossRefGoogle Scholar
  46. Davis, M. A. &R. S. Boyd. 2000. Dynamics of Ni-based defence and organic defences in the Ni hyperaccumulator,Streptanthus polygaloides (Brassicaceae). New Phytol. 146: 211–217.CrossRefGoogle Scholar
  47. De Lima, M. L. &L. Copeland. 1994. Changes in the ultrastructure of the root tip of wheat following exposure to aluminium. Austral. J. Pl. Physiol. 21: 85–94.CrossRefGoogle Scholar
  48. De Medeiros, R. A. &M. Haridasan. 1985. Seasonal variations in the foliar concentrations of nutrients in some aluminium accumulating and non-accumulating species of the cerrado region of central Brazil. Pl. & Soil 88: 433–436.CrossRefGoogle Scholar
  49. Degenhardt, J., P. B. Larsen, S. H. Howell &L. V. Kochian. 1998. Aluminum resistance in theArabidopsis mutant alr-104 is caused by an aluminum-induced increase in rhizosphere pH. Pl. Physiol. (Lancaster) 117: 19–27.CrossRefGoogle Scholar
  50. Delhaize, E., P. R. Ryan &P. J. Randall. 1993. Aluminum tolerance in wheat (Triticum aestivum L.), II. Aluminum-stimulated excretion of malic acid from root species. PI. Physiol. (Lancaster) 103: 695–702.Google Scholar
  51. Denny, H. J. &D. A. Wilkins. 1987. Zinc tolerance in Betula spp., IV. The mechanism of ectomycorrhizal amelioration of zinc toxicity. New Phytol. 106: 545–553.Google Scholar
  52. Dickinson, T. A. &R. Sattler. 1974. Development of the epiphyllous inflorescence ofPhyllonoma integerrima (Turcz.) Loes.: Implications for comparative morphology. Bot. J. Linn. Soc. 69: 1–13.CrossRefGoogle Scholar
  53. ——. 1975. Development of the epiphyllous inflorescence ofHelwingia japonica (Helwingiaceae). Amer. J. Bot 62: 962–973.CrossRefGoogle Scholar
  54. Duddrige, J. &M. Wainwright. 1980. Heavy metal accumulation by aquatic fungi and reduction in viability ofGammarus pulex fed Cd2+ contaminated mycelium. Water Res. 14: 1605–1611.CrossRefGoogle Scholar
  55. Eriksen, B. 1993. Phylogeny of the Polygalaceae and its taxonomic implications. Pl. Syst. Evol. 186: 33–55.CrossRefGoogle Scholar
  56. Ernst, W. H. O., H. Schat &J. A. C. Verlkeij. 1990. Evolutionary biology of metal resistance inSilene vulgaris. Evol. Trends Pl. 4: 45–51.Google Scholar
  57. Exley, C. 1999. A molecular mechanism of aluminium-induced Alzheimer’s disease? J. Inorg. Biochem. 76: 133–140.PubMedCrossRefGoogle Scholar
  58. —. 2000. Avoidance of aluminium by rainbow trout. Environ. Toxicol. Chem. 19: 933–939.CrossRefGoogle Scholar
  59. Foy, C. D., R. L. Chaney &M. C. White. 1978. The physiology of metal toxicity in plants. Annual Rev. Pl. Physiol. 29: 511–566.CrossRefGoogle Scholar
  60. Geoghegan, I. E. &J. I. Sprent. 1996. Aluminium and nutrient concentrations in species native to cental Brazil. Commun. Soil Sci. Pl. Anal. 27: 2925–2934.Google Scholar
  61. Ghaderian, S. M., A. J. E. Lyon &A. J. M. Baker. 2000. Seedling mortality of metal hyperaccumulator plants resulting from damping-off byPythium spp. New Phytol. 146: 219–224.CrossRefGoogle Scholar
  62. Godbold, D. L., E. Fritz &A. Hütterman. 1988. Aluminum toxicity and forest decline. Proc. Natl. Acad. Sci. U.S.A. 85: 3888–3892.CrossRefGoogle Scholar
  63. Hallier, H. 1922. Beiträge zur Kenntnis der Linaceae. Vide section 18: Die Pentaphylacaceen und Aluminiumpflanzen. Beih. Bot. Centralbl., Abt. 2, 39: 1–178.Google Scholar
  64. Haridasan, M., T. I. Paviani &I. Schiavini. 1986. Localisation of aluminium in the leaves of some aluminium accumulating species. Pl. & Soil 94: 435–437.CrossRefGoogle Scholar
  65. Henderson, M. &J. D. Ownby. 1991. The role of root cap mucilage secretion in aluminum tolerance in wheat. Curr. Topics PI. Biochem. & Physiol. 10: 134–141.Google Scholar
  66. Hillis, W. E. 2000. Vessels inCardwellia sublimis containing aluminium and magnesium salts. Int. Assoc. Wood Anat. J. 21: 121–127.Google Scholar
  67. — &D. de Silva. 1979. Inorganic extraneous constituents of wood. Holzforschung 33: 47–53.Google Scholar
  68. Hoot, S. B. &A. W. Douglas. 1998. Phylogeny of the Proteaceae based on atpB and atpB-rbcL intergenic spacer region sequences. Austral. J. Bot. 11: 301–320.CrossRefGoogle Scholar
  69. —,A. Culham &P. R. Crane. 1995. The utility of atpB gene sequences in resolving phylogenetic relationships: Comparison with rbcL and 18S ribosomal DNA sequences in the Lardizabalaceae. Ann. Missouri Bot. Gard. 82: 194–207.CrossRefGoogle Scholar
  70. —,S. Megallon &P. R. Crane. 1999. Phylogeny of basal eudicots based on three molecular datasets: atpB, rbcL, and 18S nuclear ribosomal DNA sequences. Ann. Missouri Bot. Gard. 86: 1–32.CrossRefGoogle Scholar
  71. Hue, N. V., G. R. Craddock &F. Adams. 1986. Effect of organic acids on aluminum toxicity in sub-soils. Soil Sci. Soc. Amer. J. 50: 28–34.Google Scholar
  72. Hutchinson, G. E. 1943. The biogeochemistry of aluminum and of certain related elements. Quart. Rev. Biol. 18: 1–29.CrossRefGoogle Scholar
  73. —. 1945. Aluminum in soils, plants, and animals. Soil Sci. 60: 29–40.CrossRefGoogle Scholar
  74. — &A. Wollack. 1943. Biological accumulators of aluminum. Trans. Conn. Acad. Arts & Sci. 35: 73–128.Google Scholar
  75. IAWA Committee. 1989. IAWA list of microscopic features for hardwood identification. Int. Assoc. Wood Anat. Bull., n.s. 10: 219–332.Google Scholar
  76. Jansen, S., S. Dessein, R. Piesschaert, E. Robbrecht &E. Smets. 2000a. Aluminium accumulation in leaves of Rubiaceae: Systematic and phylogenetic implications. Ann. Bot. (London) 85: 91–101.CrossRefGoogle Scholar
  77. —,E. Robbrecht, H. Beeckman &E. Smets. 2000b. Aluminium accumulation in Rubiaceae: An additional character for the delimitation of the subfamily Rubioideae? Int. Assoc. Wood Anat. J. 21: 197–212.Google Scholar
  78. —,P. Baas &E. Smets. 2001. Vestures pits, their occurrence and systematic importance in eudicots. Taxon 55: 135–167.CrossRefGoogle Scholar
  79. —,T. Watanabe &E. Smets. 2002. Aluminium accumulation in leaves of 127 species in Melastomataceae, with comments on the order Myrtales. Ann. Bot. (London) 90: 53–64.CrossRefGoogle Scholar
  80. Johnson, L. A. S. &B. G. Briggs. 1975. On the Proteaceae: The evolution and classification of a southern family. Bot. J. Linn. Soc. 70: 83–182.CrossRefGoogle Scholar
  81. Kinraide, T. B. 1991. Identity of the rhizotoxic aluminium species. Pl. & Soil 134: 167–178.Google Scholar
  82. — &D. R. Parker. 1990. Apparent phytotoxicity of mononuclear hydroxyaluminum to four di-cotyledonous species. Physiol. Pl. (Copenhagen) 79: 283–288.CrossRefGoogle Scholar
  83. Kinzel, H. 1983. Influence of limestone, silicates and soil pH on vegetation. Pp. 201–244in O. L.Lange, P. S. Nobel, C. B. Osmond & H. Ziegler (eds.), Physiological plant ecology III: Responses to the chemical and biological environment. Encyclopedia of Plant Physiology, n.s., 12C. Springer-Verlag, Berlin.Google Scholar
  84. Kochian, L. V. 1995. Cellular mechanisms of aluminum toxicity and resistance in plants. Annual Rev. Pl. Physiol. Pl. Molec. Biol. 46: 237–260.CrossRefGoogle Scholar
  85. Konishi, S., S. Miyamoto &T. Taki. 1985. Stimulatory effect of aluminum on tea plants grown under low and high phosphorus supply. Soil Sci. Pl. Nutr. 31: 361–368.Google Scholar
  86. Krämer, U., G. W. Grime, J. A. C. Smith, C. R. Hawes &A. J. M. Baker. 1997. Micro-PIXE as a technique for studying nickel localization in leaves of the hyperaccumulator plantAlyssum lesbiacum. Nucl. Instr. Meth. Physics. Res. B 130: 346–350.CrossRefGoogle Scholar
  87. Kukachka, B. F. &R. B. Miller. 1980. A chemical spot-test for aluminum and its value in wood iden-tification. Int. Assoc. Wood Anat. Bull., n.s. 1: 104–109.Google Scholar
  88. Küpper, H., F. J. Zhao &S. P. McGrath. 1999. Cellular compartmentation of zinc in leaves of the hyperaccumulatorThlaspi caerulescens. Pl. Physiol. (Lancaster) 119: 305–311.CrossRefGoogle Scholar
  89. Larsen, P. B., C.-Y. Tai, L. Stenzler, J. Degenhardt, S. H. Howell &L. V. Kochian. 1998. Alumi-num-resistantArabidopsis mutants that exhibit altered patterns of aluminum accumulation and organic acid release from roots. Pl. Physiol. (Lancaster) 117: 9–18.CrossRefGoogle Scholar
  90. Lemke, D. E. 1988. A synopsis of Flacourtiaceae. Aliso 12: 29–43.Google Scholar
  91. Lindberg, S. 1990. Aluminium interactions with K+ (86Rb+) and45Ca2+ fluxes in three cultivars of sugar beet (Beta vulgaris). Physiol. Pl. (Copenhagen) 79: 275–282.CrossRefGoogle Scholar
  92. Lüttge, U. 1997. Physiological ecology of tropical plants. Springer-Verlag, Berlin.Google Scholar
  93. — &D. T. Clarkson. 1992. Mineral nutrition: Aluminium. Progr. Bot. 53: 63–77.Google Scholar
  94. Ma, J. F. 2000. Role of organic acids in detoxification of aluminum in higher plants. Pl. Cell Physiol. 41: 383–390.Google Scholar
  95. —,S. Hiradate, K. Nomoto, T. Iwashita &H. Matsumoto. 1997a. Internal detoxification mecha-nism of Al inHydrangea. Pl. Physiol. (Lancaster) 113: 1033–1039.Google Scholar
  96. —,S. J. Zheng &H. Matsumoto. 1997b. Specific secretion of citric acid induced by Al stress inCassia tora L. Pl. Cell Physiol. 38: 1019–1025.Google Scholar
  97. ———. 1997c. Detoxifying aluminium with buckwheat. Nature 390: 569–570.CrossRefGoogle Scholar
  98. —,S. Hiradate &H. Matsumoto. 1998. High aluminum resistance in buckwheat. Pl. Physiol. (Lancaster) 117: 753–759.CrossRefGoogle Scholar
  99. —,S. Taketa &Z. M. Yang. 2000. Aluminum tolerance genes on the short arm of chromosome 3 R are linked to organic acid release inTriticale. Pl. Physiol. (Lancaster) 122: 687–694.CrossRefGoogle Scholar
  100. —,P. R. Ryan &E. Delhaize. 2001. Aluminium tolerance in plants and the complexing role of organic acids. Trends PI. Sci. 6: 273–278.CrossRefGoogle Scholar
  101. Macnair, M. R. 1993. The genetics of metal tolerance in vascular plants. New Phytol. 124: 541–559.CrossRefGoogle Scholar
  102. Marschner, H. 1991. Mechanisms of adaptation of plants to acid soils. Pl. & Soil 134: 1–20.Google Scholar
  103. —. 1995. Mineral nutrition of higher plants. Ed. 2. Academic Press, London.Google Scholar
  104. Martin, F., P. Rubini, R. Cote &I. Kottke. 1994. Aluminum polyphosphate complexes in the mycor-rhizal basidiomyceteLaccaria bicolor: A27Al-nuclear magnetic resonance study. Planta 194: 241–246.CrossRefGoogle Scholar
  105. Martin, R. B. 1988. Bioinorganic chemistry of aluminum. Pp. 1–57in H. Sigel & A. Sigel (eds.), Metal ions in biological systems. Vol. 24. Aluminum and its role in biology. Marcel Dekker, New York.Google Scholar
  106. Masunaga, T., D. Kubota, M. Hotta &T. Wakatsuki. 1998a. Mineral composition of leaves and bark in aluminum accumulators in a tropical rain forest in Indonesia. Soil Sci. Pl. Nutr. 44: 347–358.Google Scholar
  107. ——,U. William, M. Hotta, Y. Shinmura &T. Wakatsuki. 1998b. Spatial distribution pattern of trees in relation to soil edaphic status in tropical rain forest in West Sumatra, Indonesia, I. Distribution of accumulating trees. Tropics 7: 209–222.Google Scholar
  108. ——————. 1998c. Spatial distribution pattern of trees in rela-tion to soil edaphic status in tropical rain forest in West Sumatra, Indonesia, II. Distribution of non-accumulating trees. Tropics 8: 17–30.CrossRefGoogle Scholar
  109. Mazorra, M. A., J. J. San Jose, R. Montes, J. G. Miragaya &M. Haridasan. 1987. Aluminium concentration in the biomass of native species of the Morichals (swamp palm community) at the Orinoco Llanos, Venezuela. Pl. & Soil 102: 275–277.CrossRefGoogle Scholar
  110. Meeuse, A. D. J. 1990. The Euphorbiaceae auct. plur.: An unnatural taxon. Eburon, Delft.Google Scholar
  111. Metcalfe, C. R. 1962. Notes on the systematic anatomy ofWhittonia andPeridiscus. Kew Bull. 15: 472–475.CrossRefGoogle Scholar
  112. — &L. Chalk. 1983. Anatomy of the dicotyledons. Vol. 2. Wood structure and conclusion of the general introduction. Ed. 2. Clarendon Press, Oxford.Google Scholar
  113. Miller, R. B. 1975. Systematic anatomy of the xylem and comments on the relationships of Flacourtiaceae. J. Arnold Arbor. 56: 20–102.Google Scholar
  114. Moomaw, J. C., M. T. Nakamura &G. D. Sherman. 1959. Aluminum in some Hawaiian plants. Pacific Sci. 8: 335–341.Google Scholar
  115. Nagata, T., M. Hayatsu &N. Kosuge. 1992. Identification of aluminium forms in tea leaves by27A1 NMR. Phytochemistry 31: 1215–1218.CrossRefGoogle Scholar
  116. Nickrent, D. L., R. J. Duff, A. E. Cohvell, A. D. Wolfe, N. D. Young, K. E. Steiner & C. W.dePamphilis. 1998. Molecular phylogenetic and evolutionary studies of parasitic plants. Pp. 211–241in D.E. Soltis, P. S. Soltis & J. J. Doyle (eds.), Molecular systematics of plants II: DNA sequencing. Kluwer Academic Publishers, Boston.Google Scholar
  117. Olmstead, R. G., B. Bremer, K. M. Scott &J. D. Palmer. 1993. A parsimony analysis of the Asteridae sensu lato based on rbcL sequences. Ann. Missouri Bot. Gard. 80: 700–722.CrossRefGoogle Scholar
  118. Osaki, M., T. Watanabe &T. Tadano. 1997. Beneficial effect of aluminum on growth of plants adapted to low pH soils. Soil Sci. Pl. Nutr. 43: 551–563.Google Scholar
  119. Pavan, M. A. &E. T. Bingham. 1982. Aluminium toxicity in coffee trees cultivated in nutrient solu-tion. Pesq. Agropecu. Brasil 17: 1293–1302.Google Scholar
  120. Pollard, A. J. 2000. Metal hyperaccumulation: A model system for coevolutionary studies. New Phytol. 146: 179–181.CrossRefGoogle Scholar
  121. — &A. J. M. Baker. 1997. Deterrence of herbivory by zinc hyperaccumulation inThlaspi caerulescens. New Phytol. 135: 655–658.CrossRefGoogle Scholar
  122. Puthota, V., R. Cruz-Ortega, J. Johnson &J. Ownby. 1991. An ultrastructural study of the inhibition of mucilage secretion in the wheat root cap by aluminium. Pp. 779–787in R. J. Wright, V. C. Baligar & R. P. Murrmann (eds.), Plant-soil interactions at low pH. Kluwer Academic Publishers, Dordrecht, Netherlands.Google Scholar
  123. Raskin, I., P. B. A. N. Kumar, S. Dushenkov &D. E. Salt. 1994. Bioconcentration of heavy metals by plants. Curr. Opinion Biotechnol. 5: 285–290.CrossRefGoogle Scholar
  124. Read, D. J. 1991. Mycorrhizas in ecosystems. Experientia (Basel) 47: 376–391.Google Scholar
  125. Reeves, R. D. 1992. The hyperaccumulation of nickel by serpentine plants. Pp. 253–277in A. J.M. Baker, J. Proctor, & R. D. Reeves (eds.), The vegetation of ultramafic (serpentine) soils. Intercept, Andover, UK.Google Scholar
  126. — &A. J. M. Baker. 2000. Metal-accumulating plants. Pp. 193–229in I. Raskin & B. D. Ensley (eds.), Phytoremediation of toxic metals: Using plants to clean up the environment. John Wiley, New York.Google Scholar
  127. Renner, S. S. 1999. Circumscription and phylogeny of the Laurales: Evidence from molecular and mor-phological data. Amer. J. Bot. 86: 1301–1315.CrossRefGoogle Scholar
  128. Robinson, W. O. &G. Edgington. 1945. Minor elements in plants, and some accumulator plants. Soil Sci. 60: 15–28.CrossRefGoogle Scholar
  129. Rodrigues, R. K., D. J. Kiemen &L. L. Barton. 1984. Iron metabolism by an ectomycorrhizal fungusCenococcum graniforme. J. Pl. Nutr. 7: 459–468.Google Scholar
  130. Rohwer, J. G. 2000. Toward a phylogenetic classification of the Lauraceae: Evidence from matK se-quences. Syst. Bot. 25: 60–71.CrossRefGoogle Scholar
  131. Roy, A. K., A. Sharma &G. Talukder. 1988. Some aspects of aluminum toxicity in plants. Bot. Rev. (Lancaster) 54: 145–178.CrossRefGoogle Scholar
  132. Royal Botanic Gardens, Kew. 2000. Kew record of taxonomic literature, bibliographies/KR/KRHomeExt.html
  133. Rumphius, G. E. 1743. Herbarium amboinense (Het Amboisch Kruid-boek). Vol. 3. Ed. J. Burmannus. Amsterdam.Google Scholar
  134. Savolainen, V., M. W. Chase, S. B. Hoot, C. M. Morton, D. E. Soltis, C. Bayer, M. F. Fay, A. Y. De Bruijn, S. Sullivan &Y.-L. Qiu. 2000a. Phylogenetics of flowering plants based on combined analysis of plastid atpB and rbcL gene sequences. Syst. Biol. 49: 306–362.PubMedCrossRefGoogle Scholar
  135. —,M. F. Fay, D. C. Albach, A. Backlund, M. van der Bank, K. M. Cameron, S. A. Johnson, M. D. Lledó, J.-C. Pintaud, M. Powell, M. C. Sheahan, D. E. Soltis, P. S. Soltis, P. Weston, W. M. Whitten, K. J. Wurdack &M. W. Chase. 2000b. Phylogeny of the eudicots: A nearly complete familial analysis based on rbcL gene sequences. Kew Bull. 55: 257–309.CrossRefGoogle Scholar
  136. Schöttelndreier, M., M. M. Norddahl, L. Ström &U. Falkengren-Grerup. 2001. Organic acid exuda-tion by wild herbs in response to elevated Al concentrations. Ann. Bot (London) 87: 769–775.CrossRefGoogle Scholar
  137. Shaw, G. 1987. Iron and aluminium toxicity in the Ericaceae in relation to mycorrhizal infection. Ph.D. diss., Univ. of Sheffield.Google Scholar
  138. —,J. R. Leake, A. J. M. Baker &D. J. Read. 1990. The biology of mycorrhiza in the Ericaceae, XVII. The role of mycorrhizal infection in the regulation of iron uptake by ericaceous plants. New Phytol. 115: 251–258.CrossRefGoogle Scholar
  139. Smith, H. G. 1903. Aluminium the chief inorganic element in a proteaceous tree, and the occurrence of aluminium succinate in trees of this species. J. & Proc. Roy. Soc. New South Wales 3: 107–121.Google Scholar
  140. Smith, S. E. &D. J. Read. 1997. Mycorrhizal symbiosis. Ed. 2. Academic Press, San Diego.Google Scholar
  141. Soltls, D. E., P. S. Soltis, M. W. Chase, M. E. Mort, D. C. Albach, M. Zanis, V. Savolainen, W. H. Hahn, S. B. Hoot, M. F. Fay, M. Axtell, S. M. Swensen, K. C. Nixon &J. S. Farris. 2000. Angiosperm phytogeny inferred from a combined data set of 18S rDNA, rbcL, and atpB sequences. Bot. J. Linn. Soc. 133: 381–461.Google Scholar
  142. Stevenson, D. W., J. I. Davis, J. V. Freudenstein, C. R. Hardy, M. P. Simmons &C. D. Specht. 2000. A phylogenetic analysis of the monocotyledons based on morphological and molecular character sets, with comments on the placement ofAcorns and Hydatellaceae. Pp. 17–24in K. L. Wilson & D. A. Morrison (eds.), Monocots: Systematics and evolution. CS1RO, Collingwood, Australia.Google Scholar
  143. Takeda, K., M. Kariuda &H. Itoi. 1985. Blueing of sepal colour ofHydrangea macrophylla. Phy-tochemistry 24: 2251–2254.Google Scholar
  144. Tang, Y., M. E. Sorrels, L. V. Kochian &D. F. Garvin. 2000. Identification of RFLP markers linked to the barley aluminum tolerance gene Alp. Crop Sci. (Madison) 40: 778–782.Google Scholar
  145. Taylor, G. J. 1988a. The physiology of aluminum phytotoxicity. Pp. 123–163in H. Sigel & A. Sigel (eds.), Metal ions in biological systems. Vol. 24. Aluminum and its role in biology. Marcel Dekker, New York.Google Scholar
  146. —. 1988b. Mechanisms of aluminum tolerance inTriticum aestivum L. (wheat), V. Nitrogen nutri-tion, plant-induced pH, and tolerance to aluminum; correlation without causality? Canad. J. Bot. 66: 694–699.Google Scholar
  147. —. 1991. Current views of the aluminum stress response: The physiological basis of tolerance. Pp. 57–93in D. D. Randall, D. G. Blevins & C. D. Miles (eds.), Ultraviolet-B radiation stress, alumi-num stress, toxicity and tolerance, boron requirements, stress and toxicity. Current Topics in Plant Biochemistry and Physiology, 10. Interdisciplinary Plant Biochemistry and Physiology Program, Univ. of Missouri, Columbia.Google Scholar
  148. —. 1995. Overcoming barriers to understanding the cellular basis of aluminium resistance. Pl. & Soil 171: 89–103.CrossRefGoogle Scholar
  149. — &C. D. Foy. 1985. Mechanisms of aluminum tolerance inTriticum aestivum L. (wheat), IV. The role of ammonium and nitrate nutrition. Canad. J. Bot. 63: 2181–2186.CrossRefGoogle Scholar
  150. —,J. L. McDonald-Stephens, D. B. Hunter, P. M. Bertsch, D. Elmore, Z. Rengel &R. J. Reid. 2000. Direct measurement of aluminum uptake and distribution in single cells ofChara corallina. Pl. Physiol. (Lancaster) 123: 987–996.CrossRefGoogle Scholar
  151. Trappe, J. M. 1987. Phylogenetic and écologic aspects of mycotrophy in the angiosperms from an evolutionary standpoint. Pp. 5–25in G. R. Safir (ed.), Ecophysiology of VA mycorrhizal plants. CRC Press, Boca Raton, FL.Google Scholar
  152. Van Staveren, M. G. C. &P. Baas. 1973. Epidermal leaf characters of the Malesian Icacinaceae. Acta Bot. Neerl. 22: 329–359.Google Scholar
  153. Vitorello, V. A. &A. Haug. 1996. Short-term aluminum uptake by tobacco cells: Growth dependence and evidence for internalization in a discrete peripheral region. Physiol. Pl. (Copenhagen) 97: 536–544.CrossRefGoogle Scholar
  154. Von Faber, F. C. 1925. Untersuchungen über die Physiologie der javanischen Solfataren-Pflanzen. Flora 118: 89–110.Google Scholar
  155. Von Uexküll, H. R. &E. Mutert. 1995. Global extent, development and economic impact of acid soils. Pl. & Soil 171: 1–15.CrossRefGoogle Scholar
  156. Watanabe, T., M. Osaki &T. Tadano. 1997. Aluminum-induced growth stimulation in relation to calcium, magnesium, and silicate nutrition inMelastoma malabathricum L. Soil Sci. Pl. Nutr. 43: 827–837.Google Scholar
  157. ——,T. Yoshihara &T. Tadano. 1998. Distribution and chemical speciation of aluminum in the Al accumulator plant,Melastoma malabathricum L. Pl. & Soil 201: 165–173.CrossRefGoogle Scholar
  158. Webb, L. J. 1953. An occurrence of aluminium succinate inCardwellia sublimis F. Muell. Nature 171: 656.PubMedCrossRefGoogle Scholar
  159. —. 1954. Aluminium accumulation in the Australian-New Guinea flora. Aust. J. Bot. 2: 176–197.CrossRefGoogle Scholar
  160. Webster, G. L. 1975. Conspectus of a new classification of the Euphorbiaceae. Taxon 24: 593–601.CrossRefGoogle Scholar
  161. —. 1994. Classification of the Euphorbiaceae. Ann. Missouri Bot. Gard. 81: 3–32.CrossRefGoogle Scholar
  162. Wurdack, K. J. & M. W. Chase. 1999. Spurges split: Molecular systematics and changing concepts of Euphorbiaceae, s.1. Abstr. XVI Int. Bot. Congr., Saint Louis, MO, 12.2.1. p. 142.Google Scholar
  163. Xiang, Q.-Y., D. E. Soltis, D. R. Morgan &P. S. Soltis. 1993. Phylogenetic relationships ofCornus L. sensu lato and putative relatives inferred from rbcL sequence data. Ann. Missouri Bot. Gard. 80: 723–734.CrossRefGoogle Scholar
  164. —— &P. S. Soltis. 1998. Phylogenetic relationships of Cornaceae and close relatives in-ferred from matK and rbcL sequences. Amer. J. Bot. 85: 285–297.CrossRefGoogle Scholar
  165. Yang, Z. M., M. Sivaguru, W. J. Horst &H. Matsumoto. 2000. Aluminium tolerance is achìeved by exudation of citric acid from roots of soybean (Glycine max). Physiol. Pl. (Copenhagen) 110: 72–77.CrossRefGoogle Scholar
  166. Zhang, G. &G. J. Taylor. 1990. Kinetics of aluminum uptake inTrilicum aestivum L.: Identity of the linear phase of aluminum uptake by excised roots of aluminum-tolerant and aluminum-sensitive cultivars. Pl. Physiol. (Lancaster) 94: 577–584.Google Scholar
  167. ——. 1991. Effects of biological inhibitors on kinetics of aluminum uptake by excised roots and purified cell wall material of aluminum-tolerant and aluminum-sensitive cultivars ofTriticum aestivum L. J. Plant Physiol. 138: 533–539.Google Scholar
  168. Zheng, S. J., J. F. Ma &H. Matsumoto. 1998. High aluminum resistance in buckwheat, I. Al-induced specific secretion of oxalic acid from root tips. PI. Physiol. (Lancaster) 117: 745–751.Google Scholar

Copyright information

© The New York Botanical Garden 2002

Authors and Affiliations

  • Steven Jansen
    • 1
  • Martin R. Broadley
    • 2
  • Elmar Robbrecht
    • 3
  • Erik Smets
    • 1
  1. 1.Laboratory of Plant Systematics Institute of Botany and MicrobiologyKatholieke Universiteit LeuvenLeuvenBelgium
  2. 2.Horticulture Research InternationalWellesbourneUK
  3. 3.National Botanic Garden of Belgium Domein van BouchoutMeiseBelgium

Personalised recommendations