498 Original Paper The Distribution and Phylogeny of Aluminium Accumulating Plants in the Ericales S. Jansen1, T. Watanabe2, P. Caris1, K. Geuten1, F. Lens1, N. Pyck1, and E. Smets1 1 Laboratory ofPlant Systematics, Institute ofBotany and Microbiology, K.U.Leuven, Kasteelpark Arenberg 31, 3001 Leuven, Belgium 2 Graduate School ofAgriculture, Hokkaido University, Sapporo, 0608589 Japan Received: August 1, 2003; Accepted: April 20,2004 Abstract: The distribution of aluminium (Al) accumulation in the 1000 mg kg±1 in their leaf dry matter can be defined as Al ac- Ericales is surveyed, based on semi-quantitative tests of 114 spe- cumulators. cies and literature data. Al accumulation mainly characterises the families Diapensiaceae, Pentaphylacaceae, Symplocaceae, Al accumulating plants have mainly been studied from an eco- Ternstroemiaceae, and Theaceae. Al accumulation is consistent- logical and physiological point of view because of substantial ly present or absent in most families examined, but the charac- questions about the possible significance of Al accumulation. ter appears to be more variable in a few taxa (e.g., Lecythida- Since little attention has been paid to the systematic distribu- ceae, Myrsinaceae). Although the interfamilial relationships tion and phylogenetic significance of Al accumulators, we have within the Ericales require further research, the ability to accu- previously investigated the evolution of Al accumulation in mulate high levels of Al appears to show considerable taxonom- the Rubiaceae (Gentianales) and Melastomataceae (Myrtales) ic significance. While the majority of Al accumulating Ericales in- (Jansen et al., 2000a, b, 2003; Jansen et al., 2002 b). These two cludes woody, tropical plants, the feature is remarkably present families show by far the highest number of Al accumulators in in several herbaceous Diapensiaceae, which have a distribution angiosperms. The order Ericales represents the third largest in cold to temperate areas. The association of different mycor- group of Al accumulating plants. It is well known, for instance, rhizae types with plant roots is suggested to play a role in the that Al accumulation is present in the tea bush (Camellia sinen- exclusion of high Al levels from the shoot. sis L.), in which Al levels range from 5000 to 30 000 mg kg±1 in mature leaves (Matsumoto et al., 1976). The commercial tea Key words: Aluminium accumulation, Ericales, phylogeny, Dia- plant belongs to the Theaceae family, which is now included pensiaceae, Pentaphylacaceae, Symplocaceae, Ternstroemia- in the enlarged order Ericales (APG II, 2003; Smets and Pyck, ceae, Theaceae. 2003). Chenery (1955) has already paid extensive attention to Al accumulation in the tea bush and several others have inves- tigated the distribution, concentration, and speciation of Al in tea leaves (Memon et al., 1981; Nagata et al., 1992, 1993; Ech- Introduction lin, 1996, 1999; Ruan and Wong, 2001). Furthermore, the oc- currence of Al accumulation has been studied in families such A high proportion of trivalent Al3+ ions generally becomes bio- as the Symplocaceae, Diapensiaceae, and Theaceae (Yoshii and available and detrimental to plants when the soil pH falls Jimbo, 1932), but no study has surveyed this feature in the en- below 5.5 in acid soils (Marschner, 1995). The majority of na- tire order Ericales. tive plants growing in acid soils avoid the toxic effects of high Al levels by excluding this metal from their shoot tissues, Interest in studying Al compounds has increased over recent although several crop plants are well known to be sensitive years due to the possible role of Al in neurodegenerative disor- to high levels of soluble Al (Foy et al., 1978; Roy et al., 1988; ders such as Alzheimers disease, although this link is still de- Kochian, 1995). Indeed, Al toxicity forms the primary factor batable (Exley, 2001, 2003). Since tea is the second most-con- limiting production of wheat, corn, barley, and soybean in acid sumed beverage in the world after water, it is probably the soils. Moreover, about 5% of angiosperms take up Al in their most important single source of dietary Al for many people. aboveground tissues in quantities far above the average of Accordingly, several studies have investigated the impact of 200 mg kg±1. These plants have developed special mechanisms tea on human health (Flaten and édegård, 1988; Flaten, 2002; for the internal detoxification of Al in their shoots (Jansen et Wong et al., 2003). A better understanding of the distribution al., 2002a, 2004; Watanabe and Osaki, 2002). According to of Al accumulation and its underlying physiological mecha- Chenery (1946, 1948a, b), plants that have Al levels of at least nisms may serve as a basis for the development of more resist- ant crop plants. It may also contribute to forest management, soil improvement, and remediation of degraded lands in trop- ical rain forests or savannas. Plant Biology 6 (2004): 498± 505 Georg Thieme Verlag KG Stuttgart ´ New York ISSN 1435-8603 ´ DOI 10.1055/s-2004-820980 Al Accumulation in the Ericales Plant Biology 6 (2004) 499 This paper aims to illustrate the distribution and evolution of In general, there was good agreement between our data and Al accumulators in the order Ericales. Since our knowledge of earlier tests. However, the genera Galax and Shortia (Diapen- Al accumulators is limited to a few substantial contributions siaceae), Diospyros (Ebenaceae), Brazzeia (Lecythidaceae), Ra- published more than 50 years ago, we have analysed 114 spe- panea (Myrsinaceae), and Adinandra (Ternstroemiaceae) gave cies from most families distinguished within the Ericales. A negative results according to our analyses, while positive re- summary of the literature data allowed us to compare the sults were previously recorded by Chenery (1948a, b) and Ma- new data with earlier results. The phylogenetic significance of sunaga et al. (1998). Al accumulation in the order is evaluated based on the recent molecular phylogenetic studies of Anderberg et al. (2002), Discussion Bremer et al. (2002), and Geuten et al., 2004. Finally, some physiological, chemical, and ecological aspects are briefly dis- The distribution of Al accumulators cussed, linking a wide range of topics to the distribution of ac- cumulators and non-accumulators in the study group. Indeed, The combination of our new analyses and literature data pro- a multidisciplinary approach is required to better understand vides a good overview of the occurrence of Al accumulation in the biology of Al accumulating plants. the Ericales. As illustrated by the new record of Al accumu- lation in Pierrina, further sampling will probably reveal other Materials and Methods previously unknown Al accumulators, but the overall distribu- tion seems to be clear. The data obtained may allow us to dis- Herbarium leaves of the Ericales were collected from the her- tinguish two different groups: (1) families in which Al accu- barium of the National Botanic Garden of Belgium (BR). Leaf mulation is exclusively absent, and (2) families in which Al material for the Lissocarpaceae, Pellicieraceae, Sladeniaceae, accumulation is partly to almost entirely present. Most fami- and Tertrameristaceae was not available. All specimens tested lies in the Ericales belong to the group of non-accumulators, are listed in Table 1. We have analysed only one specimen for as the character is exclusively absent in 18 out of 27 families most species because the presence of Al accumulation is gen- (Table 1). The Al accumulating group includes the families Di- erally consistent at the species level (Jansen et al., 2002 a, apensiaceae, Pentaphylacaceae, Symplocaceae, Ternstroemia- 2004). High Al concentrations in leaves were detected using ceae, and Theaceae, which are thought to include strong, pos- the ªaluminonº test as described by Chenery (1948 b) and fol- sibly absolute or obligate Al accumulators. Obligate Al accu- lowed by Jansen et al. (2000 a, 2002b). This simple but ade- mulators can be defined as species in which the Al content of quate test permits assessment by intensity of colour to arrange the shoot is constantly above 1000 mg kg±1, irrespective of the the specimens tested according to Al accumulators (crimson to concentration of soluble Al in the soil or seasonal changes (Jan- dark red or red colour) or non-accumulators (colour varying sen et al., 2002 a). from pink to yellow or dark brown). The distribution of Al ac- cumulating taxa was then plotted on three trees using Mac- While the presence or absence of Al accumulation is of con- Clade 4.0 (Maddison and Maddison, 2000). stant occurrence in most families, the character appears to be more variable in the Lecythidaceae and Myrsinaceae. The low Several Ericales have been reported to accumulate more than number of Al accumulators and the mixed occurrence of posi- 10000 mg kg±1 in their leaves and can therefore be labelled as tive and negative results may suggest that facultative rather Al ªhyperaccumulatorsº. Since precise quantitative data on the than absolute accumulators occur in these families. The inter- Al content were not obtained using the semi-quantitative spot nal Al concentration in facultative accumulators more or less tests, we use the term ªaccumulatorsº throughout this paper reflects the external soil level and thus may depend on envi- for all accumulating plants, even if the exact Al content could ronmental conditions such as soil acidity and availability of be far above 10 000 mg kg±1. soluble Al. It was not possible, however, to consider environ- mental aspects in this study because precise ecological data Results on the herbarium specimens studied were not available. Al- though exact analytical data may help to clarify the sporadic A summary of the distribution of Al accumulation in the Eri- occurrence of Al accumulation, this feature seems to be re- cales is presented in Table 1, including our own tests and liter- stricted to Rapanea within the Myrsinaceae, and to Brazzeia ature data. and Pierrina within the Lecythidaceae (including Scytopetala- ceae).