The Distribution and Phylogeny of Aluminium Accumulating Plants in the Ericales

Abstract

The distribution of aluminium (Al) accumulation in the Ericales is surveyed, based on semi-quantitative tests of 114 species and literature data. Al accumulation mainly characterises the families Diapensiaceae, Pentaphylacaceae, Symplocaceae, Ternstroemiaceae, and Theaceae. Al accumulation is consistently present or absent in most families examined, but the character appears to be more variable in a few taxa (e.g., Lecythidaceae, Myrsinaceae). Although the interfamilial relationships within the Ericales require further research, the ability to accumulate high levels of Al appears to show considerable taxonomic significance. While the majority of Al accumulating Ericales includes woody, tropical plants, the feature is remarkably present in several herbaceous Diapensiaceae, which have a distribution in cold to temperate areas. The association of different mycorrhizae types with plant roots is suggested to play a role in the exclusion of high Al levels from the shoot.

Aluminium accumulation - Ericales - phylogeny - Diapensiaceae - Pentaphylacaceae - Symplocaceae - Ternstroemiaceae - Theaceae.

References

• 1 Anderberg A. A., Rydin C., Källersjö M.. Phylogenetic relationships in the order Ericales s.l.: analysis of molecular data from five genes from the plastid and mitochondrial genomes.  American Journal of Botany. (2002);  89 677-687
• 2 APG II . An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II.  Botanical Journal of the Linnean Society. (2003);  141 399-436
• 3 Appel O.. Scytopetalaceae. Kubitzki, K., ed. The Families and Genera of Vascular Plants, Vol. VI: Flowering Plants. Dicotyledons: Celastrales, Oxalidales, Rosales, Cornales, Ericales. Berlin, Heidelberg; Springer-Verlag (2004): 426-430
• 4 Barceló J., Poschenrieder C.. Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review.  Environmental and Experimental Botany. (2002);  48 75-92
• 5 Bradley R., Burt A. J., Read D. J.. Mycorrhizal infection and resistance to heavy metal toxicity in Calluna vulgaris. .  Nature. (1981);  292 335-337
• 6 Bradley R., Burt A. J., Read D. J.. The biology of mycorrhiza in the Ericaceae. VIII. The role of mycorrhizal infection in heavy metal tolerance.  New Phytologist. (1982);  91 197-209
• 7 Bremer B., Bremer K., Heidari N., Erixon P., Olmstead R. G., Anderberg A. A., Källersjö M., Barkhordarian E.. Phylogenetics of Asterids based on 3 coding and 3 non-coding chloroplast DNA markers and the utility of non-coding DNA at higer taxonomic levels.  Molecular Phylogenetics and Evolution. (2002);  24 274-301
• 8 Caris P., Ronse Decraene L.-P., Smets E., Clinckemaillie D.. The uncertain systematic position of Symplocos (Symplocaceae): evidence from a floral ontogenetic study.  International Journal of Plant Sciences. (2002);  163 67-74
• 9 Chenery E. M.. Are Hydrangea flowers unique?.  Nature. (1946);  158 240-241
• 10 Chenery E. M.. Aluminium in plants and its relation to plant pigments.  Annals of Botany. (1948 a);  12 121-136
• 11 Chenery E. M.. Aluminium in the plant world. Part I, General survey in dicotyledons.  Kew Bulletin. (1948 b);  2 173-183
• 12 Chenery E. M.. A preliminary study of aluminium and the tea bush.  Plant Soil. (1955);  6 174-200
• 13 Chenery E. M., Sporne K. R.. A note on the evolutionary status of aluminium-accumulators among dicotyledons.  New Phytologist. (1976);  76 551-554
• 14 Cullings K. W.. Single phylogenetic origin of ericoid mycorrhizae within the Ericaceae.  Canadian Journal of Botany. (1996);  74 1896-1909
• 15 Echlin P.. Distribution of aluminium in the cells of developing leaves of the tea plant as measured by low-temperature X-ray microanalysis.  Scanning. (1996);  18 197-198
• 16 Echlin P.. Low-voltage energy-dispersive X-ray microanalysis of bulk biological materials.  Microscopy and Microanalysis. (1999);  4 577-584
• 17 Exley C.. Aluminum and Alzheimer's Disease. The Science that Describes the Link. New York; Elsevier Science (2001)
• 18 Exley C.. A biogeochemical cycle for aluminium?.  Journal of Inorganic Biochemistry. (2003);  97 1-7
• 19 Flaten T. P., Ødegård M.. Tea, aluminium and Alzheimer's disease.  Food and Chemical Toxicology. (1988);  26 959-960
• 20 Flaten T. P.. Aluminium in tea - concentration, speciation and bioavailability.  Coordination Chemistry Reviews. (2002);  228 385-395
• 21 Foy C. D., Chaney R. L., White M. C.. The physiology of metal toxicity in plants.  Annual Review of Plant Physiology. (1978);  29 511-566
• 22 Geuten K., Smets E., Schols P., Yuan Y.-M., Janssens S., Küpfer P., Pyck N.. Conflicting phylogenies of balsaminoid families and the polytomy in Ericales: combining data in a Bayesian framework.  Molecular Phyologenetics and Evolution. (2004);  31 711-729
• 23 Haridasan M.. Performance of Miconia albicans (Sw.) Triana, an aluminium accumulating species, in acidic and calcareous soils.  Communications in Soil Science and Plant Analysis. (1988);  19 1091-1103
• 24 Haridasan M., Araújo G. M.. Aluminium accumulating species in two forest communities in the cerrado region of central Brazil.  Forest Ecology and Management. (1987);  24 15-26
• 25 Hutchinson G. E.. The biogeochemistry of aluminum and of certain related elements.  Quarterly Review of Biology. (1943);  18 1-29
• 26 Jansen S., Broadley M., Robbrecht E., Smets E.. Aluminium hyperaccumulation in angiosperms: a review of its phylogenetic significance.  The Botanical Review. (2002 a);  68 235-269
• 27 Jansen S., Dessein S., Piesschaert F., Robbrecht E., Smets E.. Aluminium accumulation in leaves of Rubiaceae: systematic and phylogenetic implications.  Annals of Botany. (2000 a);  85 91-101
• 28 Jansen S., Robbrecht E., Beeckman H., Smets E.. Aluminium accumulation in Rubiaceae: an additional character for the delimitation of the subfamily Rubioideae?.  International Association of Wood Anatomists Journal. (2000 b);  21 197-212
• 29 Jansen S., Watanabe T., Dessein S., Robbrecht E., Smets E.. A comparative study of metal levels in leaves of some Al accumulating Rubiaceae.  Annals of Botany. (2003);  91 657-663
• 30 Jansen S., Watanabe T., Dessein S., Robbrecht E., Smets E.. The evolution of aluminium accumulation in angiosperms. Hemsley, A. and Poole, I., eds. Evolution of Plant Physiology. From Whole Plants to Ecosystems. London; Elsevier Academic Press (2004): 467-479
• 31 Jansen S., Watanabe T., Smets E.. Aluminium accumulation in leaves of 127 species in Melastomataceae with comments on the order Myrtales.  Annals of Botany. (2002 b);  90 53-64
• 32 Kochian L. V.. Cellular mechanisms of aluminum toxicity and resistance in plants.  Annual Review of Plant Physiology and Plant Molecular Biology. (1995);  46 237-260
• 33 Konishi S.. Promotive effects of aluminium on tea plant growth.  Japanese Agricultural Research Quarterly. (1992);  26 26-33
• 34 Konishi S., Miyamato S., Tazi T.. Stimulatory effects of aluminium on tea plants grown under low and high phosphorus supply.  Soil Science and Plant Nutrition. (1985);  31 361-368
• 35 Kubota M., McGonigle T. P., Hyakumachi M.. Clethra barbinervis in the Ericales forms arbuscular mycorrhizae.  Phytopathology. (2001);  91 (Suppl.) 118
• 36 Kukachka B. F., Miller R. B.. A chemical spot-test for aluminum and its value in wood identification.  International Association of Wood Anatomists Bulletin. (1980);  1 104-109
• 37 Liang J.-Y., Shyu T.-H., Lin H.-C.. The aluminum complexes in the xylem sap of tea plant.  Journal of the Chinese Agricultural Chemical Society. (1996);  34 695-702
• 38 Machado J. W. B.. Acumulação de alumínio em Vochysia thyrsoidea Pohl. University of Brasília, Brasília: M.Sc. Thesis. (1985)
• 39 Maddison W. P., Maddison D. R.. MacClade: interactive analysis of phylogeny and character evolution, version 4.0. Sunderland, Massachusetts; Sinauer Associates Inc. (2000)
• 40 Martin F., Rubini P., Cote R., Kottke I.. Aluminium polyphosphate complexes in the mycorrhizal basidiomycete Laccaria bicolor: A 27Al-nuclear magnetic resonance study.  Planta. (1994);  194 241-246
• 41 Marschner H.. Mineral Nutrition of Higher Plants, 2nd ed. London; Academic Press (1995)
• 42 Masunaga T., Kubota D., Hotta M., Wakatsuki T.. Mineral composition of leaves and bark in aluminum accumulators in a tropical rain forest in Indonesia.  Soil Science and Plant Nutrition. (1998);  44 347-358
• 43 Matsumoto H., Hirasawa E., Morimura S., Takahashi E.. Localisation of aluminium in the tea leaf.  Plant Cell Physiology. (1976);  17 627-631
• 44 Memon A. R., Chino M., Yatazawa M.. Micro-distribution of aluminum and manganese in the tea leaf tissues as revealed by x-ray microanalyzer.  Communications in Soil Science and Plant Analysis. (1981);  12 441-452
• 45 Nagata T., Hayatsu M., Kosuge N.. Aluminium kinetics in the tea plant using ²⁷Al and ¹⁹F NMR.  Phytochemistry. (1993);  32 771-775
• 46 Nagata T., Masahito H., Kosuge N.. Identification of aluminium forms in tea leaves by ²⁷Al NMR.  Phytochemistry. (1992);  31 1215-1218
• 47 Nascimento M. T.. Herbivoria foliar em Vochysia divergens Pohl.  Brasil Florestal. (1989);  68 51-84
• 48 Nascimento M. T., Villela D. M., de Lacerda L. D.. Foliar growth, longevity and herbivory in two “cerrado” species near Cuiaba, MT, Brazil.  Revista Brasileira de Botânica. (1990);  13 27-32
• 49 Osaki M., Watanabe T., Tadano T.. Beneficial effect of aluminum on growth of plants adapted to low pH soils.  Soil Science and Plant Nutrition. (1997);  43 551-563
• 50 Pennington T. D.. The Genera of Sapotaceae. Kew: Royal Botanic Gardens,. New York; New York Botanical Gardens (1991)
• 51 Read D. J.. Mycorrhizas in ecosystems.  Experientia. (1991);  47 376-391
• 52 Roy A. K., Sharma A., Talukder G.. Some aspects of aluminum toxicity in plants.  Botanical Review. (1988);  54 145-178
• 53 Ruan J. Y., Wong M. H.. Accumulation of fluoride and aluminium related to different varieties of tea plant.  Environmental Geochemistry and Health. (2001);  23 53-63
• 54 Shaw G.. Iron and aluminium toxicity in the Ericaceae in relation to mycorrhizal infection. University of Sheffield, Sheffield, UK: Ph.D. Thesis. (1987)
• 55 Shaw G., Leake J. R., Baker A. J. M., Read D. J.. The biology of mycorrhiza in the Ericaceae. XVII. The role of mycorrhizal infection in the regulation of iron uptake by ericaceous plants.  New Phytologist. (1990);  115 251-258
• 56 Smets E., Pyck N.. Ericales (Rhododendron). In Nature Encyclopedia of Life Sciences. London; Nature Publishing Grouphttp://www.els.net (2003)
• 57 Soltis D. E., Soltis P. S., Chase M. W., Mort M. E., Albach D. C., Zanis M., Savolainen V., Hahn W. H., Hoot S. B., Fay M. F., Axtell M., Swensen S. M., Nixon K. C., Farris J. S.. Angiosperm phylogeny inferred from a combined data set of 18 S rDNA, rbcL, and atpB sequences.  Botanical Journal of the Linnean Society. (2000);  133 381-461
• 58 Tsuji M., Kubai T., Konishi S.. Stimulatory effects of aluminum on the growth of cultured roots of tea.  Soil Science and Plant Nutrition. (1994);  40 471-476
• 59 von Faber F. C.. Untersuchungen über die Physiologie der javanischen Solfataren-Pflanzen.  Flora. (1925);  118 89-110
• 60 Watanabe T., Osaki M.. Mechanisms of adaptation to high Al condition in native plant species growing in acid soils: a review.  Communications in Soil Science and Plant Analysis. (2002);  33 1247-1260
• 61 Watanabe T., Osaki M., Tadano T.. Aluminum-induced growth stimulation in relation to calcium, magnesium and silicate nutrition in Melastoma malabathricum L.  Soil Science and Plant Nutrition. (1997);  43 827-837
• 62 Webb L. J.. Aluminium accumulation in the Australian-New Guinea flora.  Australian Journal of Botany. (1954);  2 176-197
• 63 Wong M. H., Fung K. F., Carr H. P.. Aluminium and fluoride in tea, with emphasis on brick tea and their health implications.  Toxicology Letters. (2003);  137 111-120
• 64 Yoshii Y., Jimbo T.. Mikrochemischer Nachweis von Aluminium und sein Vorkommen im Pflanzenreiche.  The Science Reports of the Tôhoku Imperial University. (1932);  7 65-77

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