Aluminum Hyperaccumulation in Angiosperms: A Review of Its Phylogenetic Significance
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.