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Aluminum hyperaccumulation in angiosperms: A review of its phylogenetic significance

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Abstract

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.

Résumé

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.

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  1. Laboratory of Plant Systematics Institute of Botany and Microbiology, Katholieke Universiteit Leuven, Kasteelpark Arenberg 31, B-3001, Leuven, Belgium

    Steven Jansen & Erik Smets

  2. Horticulture Research International, CV35 9EF, Wellesbourne, Warwick, UK

    Martin R. Broadley

  3. National Botanic Garden of Belgium Domein van Bouchout, B-1860, Meise, Belgium

    Elmar Robbrecht

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Jansen, S., Broadley, M.R., Robbrecht, E. et al. Aluminum hyperaccumulation in angiosperms: A review of its phylogenetic significance. Bot. Rev 68, 235–269 (2002). https://doi.org/10.1663/0006-8101(2002)068[0235:AHIAAR]2.0.CO;2

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