A global database for plants that hyperaccumulate metal and metalloid trace elements.

Hyperaccumulators are unusual plants that accumulate particular metals or metalloids in their living tissues to levels that may be hundreds or thousands of times greater than is normal for most plants (Reeves, 2003; van der Ent et al., 2013). Hyperaccumulator plants are of substantial fundamental interest and practical importance. Hyperaccumulators are exceptional models for fundamental science to understand metal regulation including the physiology of metal uptake, transport and sequestration, as well as evolution and adaptation in extreme environments (Pollard et al., 2002; Kr€amer, 2010). The ecology of hyperaccumulator plants is also an active field of enquiry, focussing on antiherbivore defences, allelopathy and biotic interactions (Martens & Boyd, 1994; Boyd &Martens, 1998; Boyd, 2013). The unique characteristics of hyperaccumulator plants are also exploited in applied biotechnologies including phytomining and phytoremediation (Chaney et al., 2007; van der Ent et al., 2015a), and practical applications in biofortification of essential elements (Clemens, 2016). Most reported hyperaccumulator plants hyperaccumulate nickel and occur on ultramafic soils that are naturally enriched in nickel and cobalt and (in some cases) manganese (Baker & Brooks, 1989; Reeves, 2003). Global centres of distribution for nickel hyperaccumulator plants include the Mediterranean Region, mainly with species in the genus Alyssum (Brassicaceae), and the tropical ultramafic outcrops in Brazil, Cuba, New Caledonia and Southeast Asia, especially with species in the genus Phyllanthus (Phyllanthaceae) (Reeves, 2003). After nickel hyperaccumulators, the largest group of hyperaccumulator plants are those of the copper/cobalt-enriched soils from Central Africa, principally restricted to the Copper Hills in the DR Congo (Brooks et al., 1980), although their status is presently somewhat unclear due to issues with contamination (Faucon et al., 2007). This group of hyperaccumulators is poorly understood, and experimental work has shown that copper and cobalt accumulation in several species follows a low-gradient curve with a certain degree of exclusion (Morrison et al., 1979), and as such they appear to be ‘extremely tolerant excluders’. Zinc and/or cadmium hyperaccumulators occur mainly on metalliferous soils in Europe and China (Baker & Brooks, 1989; Wu et al., 2012). Finally, there are known hyperaccumulators for a range of other elements, including selenium, thallium, manganese and arsenic, occurring in many different countries (Baker & Brooks, 1989; Brooks, 1998; van der Ent et al., 2013). Hyperaccumulator plants often appear to be restricted in their distribution to metalliferous soils, from which they always exhibit hyperaccumulation of some element; these are described as ‘obligate’ hyperaccumulators (Pollard et al., 2002). However, some aremore widespread, with populations that hyperaccumulate from metalliferous soils, and other populations, from nonmetalliferous soils, that do not show unusual accumulation; these are ‘facultative’ hyperaccumulators (Pollard et al., 2014). The latter category includes a number of species that accumulate nickel from ultramafic soils as well as some widespread species that display ‘inadvertent uptake’ when growing on polluted soils (Pollard et al., 2014). Examples are Biscutella laevigata with > 1% thallium (Babst-Kostecka et al., 2016), Pteris vittatawith up to 2.3% arsenic (Ma et al., 2001), and Phytolacca americana which can accumulate > 1% manganese (Xue et al., 2009). A few species appear to show extreme variations in metal uptake, even when confined to metalliferous soils; this behaviour may be a reflection of widely varying metal availability caused by variations in pH or other soil properties, as for Pimelea leptospermoides in Australia (Reeves et al., 2015). However, this applies specifically to nickel hyperaccumulation which is confined to ultramafic soils. A limited number of species have species-wide highly enhanced (hyper)accumulation characteristics, which lead to hyperaccumulation occurring when the species grow on nonmetalliferous soils. This is the case for Noccaea caerulescens which achieves > 1% foliar zinc when growing on soils with only background concentrations of this element (Reeves et al., 2001) and similarly in the case of Arabidopsis halleri (Stein et al., 2017). Examples also exist for facultative hyperaccumulation through intra-ecotypic genetic variation, such as cadmium hyperaccumulation in Noccaea caerulescens growing on metalliferous soils, which is reproducible in hydroponics at low cadmium supply (Assunc ~ao et al., 2003), and in cadmium-spiked soil (Sterckeman et al., 2017). There is also the example of Senecio coronatus from South Africa, which has genetically based intraspecific variation in its hyperaccumulation capacity with nickelhyperaccumulating and nonhyperaccumulating individuals with distinct anatomical differences in the roots (Mesjasz-Przybyłowicz et al., 2007). Widely diffused reporting across academic media means that it is not known precisely how many hyperaccumulator species exist, and information about those species is dispersed in many different types of sources. An online and publicly available inventory of hyperaccumulator plant species, and associated information where available, was therefore desired. The newly launched database is useful in providing background information for any researcher intending to investigate specific hyperaccumulator species.