A global database for plants that hyperaccumulate metal and metalloid trace elements - Reeves - 2018 - New Phytologist - Wiley Online Library

Hyperaccumulator plants and the need for a database

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; Krämer, 2010). The ecology of hyperaccumulator plants is also an active field of enquiry, focussing on anti-herbivore 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 are more 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 vittata with 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 (Assunção 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 intra-specific variation in its hyperaccumulation capacity with nickel-hyperaccumulating 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.

Previous attempts at creating hyperaccumulator plant databases

Attempts to produce hyperaccumulator databases have been few and global coverage has been patchy. Notable efforts were Environment Canada's PHYTOREM database and the METALS (metal-accumulating plants) database originally maintained by the Environmental Consultancy, University of Sheffield (now ECUS Ltd, Sheffield, UK). A problem with these earlier efforts has been the attempt to record not only the hyperaccumulators but all species growing on metalliferous soils, that is, all the metal-tolerant species. Such a subset of the plant kingdom clearly includes tens of thousands of species, and is difficult to define because tolerance takes on many physiological guises and is inherently a comparative term, relative to sensitive species. A more easily achievable goal is to confine the database to the hyperaccumulators alone, currently numbering c. 700 species, and which (even with new discoveries from poorly investigated regions of the world) may eventually number no greater than 1000–1500 species. In 2015, the online Global Hyperaccumulator Database (www.hyperaccumulators.org), under administration by the Centre for Mined Land Rehabilitation of The University of Queensland (Brisbane, Australia), went on-line and aims to provide a global database freely available to anyone.

Aims of the Global Hyperaccumulator Database

The new database collates information about all known metal and metalloid hyperaccumulator plant species in a standardized format. The database contains information about the taxonomy, distribution, ecology, collection records, analytical data, and references to other studies on the species. It is not a static resource, but is to be updated continually with new discoveries and further information. It should also serve to: (1) provide access to data from sources that are difficult to locate; (2) give details that may not have been published in the open literature; (3) monitor and update nomenclatural changes; and (4) raise awareness of the plight of many hyperaccumulator species that are under threat of extinction.

Recognition of ‘hyperaccumulator status’ and inclusion in the database

Inclusion of species in the database is based on accepted definitions of trace element hyperaccumulation, that is, plants which contain in their dry weight foliar tissue > 100 μg g−1 cadmium, thallium or selenium, > 300 μg g−1 of cobalt, copper or chromium, > 1000 μg g−1 of nickel, arsenic, lead or rare earth elements (REEs), > 3000 μg g−1 of zinc, or > 10 000 μg g−1 of manganese, when growing in their natural habitat (Baker & Brooks, 1989; Reeves, 2003; van der Ent et al., 2013). These nominal threshold criteria provide a practical operational framework for recognizing hyperaccumulator plant species, and guide the recognition of extreme physiological behaviour (van der Ent et al., 2015ab). The database will not include species where attainment of threshold values has been solely obtained from growing plants under solution dosing regimes (i.e. grown in hydroponic media or ‘spiked’ soils) or where chelating agents have been used to achieve abnormal foliar accumulation.

Finally, there is a particular caution about the potential for contamination of foliar samples with soil or aerial particulates. Such contamination can be a major cause of erroneous hyperaccumulator designation in historic data, particularly for copper, cobalt, lead and chromium. This is especially true of plants sampled close to smelters or active mine sites which have a high probability of being contaminated by airborne metal-rich particles. Many of the early records of copper and cobalt hyperaccumulator plants from Central Africa probably related to contaminated material, and experiments undertaken to remove such contamination have led to far lower concentration values in several species (Faucon et al., 2007).

Global numbers of hyperaccumulator plants

As can be seen in Table 1, in July 2017 the database contains 721 hyperaccumulator species (523 nickel, 53 copper, 42 cobalt, one chromium, 42 manganese, 20 zinc, two rare earth elements, 41 selenium, two thallium, seven cadmium, five arsenic, and eight lead) with some species showing hyperaccumulation of more than one element). These numbers will change as more discoveries are made, or if earlier claims are shown to be spurious. The 721 hyperaccumulator species are from 52 families and c. 130 genera; the families most strongly represented are the Brassicaceae (83 species) and the Phyllanthaceae (59 species). The countries with the greatest numbers of published hyperaccumulator plant species (including some subspecific taxa) are Cuba with 128 (Reeves et al., 1999), New Caledonia with 65 (Jaffré et al., 2013), Turkey with 59 (Reeves & Adıgüzel, 2008) and Brazil with at least 30 (Reeves et al., 2007). In the light of recent pioneering fieldwork in Sabah, Malaysia (24 nickel hyperaccumulator plant species), Southeast Asia is also emerging as a global centre of hyperaccumulator plant diversity (van der Ent et al., 2015b, 2016). Table 2 summarizes the most important families and genera for each element, together with the main regions of hyperaccumulator occurrence.

Table 1. Hyperaccumulator species in the Global Database (as of September 2017) with the global records that are the highest concentrations reported to date

• Ma et al. (2001); Stein et al. (2017); Malaisse et al. (1978); Brooks (1977); Jaffré (1979); Mesjasz-Przybyłowicz et al. (2004); Reeves & Brooks (1983); Shan et al. (2003); Galeas et al. (2006); LaCoste et al. (1999); Reeves et al. (2001).

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Table 2. Important families, genera and regions of occurrence of hyperaccumulators

• The criteria for inclusion were based on families containing three or more hyperaccumulating genera or species, and genera containing three or more hyperaccumulating species (the listing is not exhaustive). In the case of some elements (As, Cd, Pb, Se, Tl, Zn), fewer families or genera with hyperaccumulators are known, in which those with the most species are given.
• a Rare earth elements: cerium (Ce), dysprosium (Dy), erbium (Er), europium (Eu), gadolinium (Gd), holmium (Ho), lanthanum (La), lutetium (Lu), neodymium (Nd), praseodymium (Pr), samarium (Sm), scandium (Sc), terbium (Tb), thulium (Tm), ytterbium (Yb) and yttrium (Y).

Discovering more hyperaccumulator plant species

Globally, the discovery of hyperaccumulator plants has been hindered by the lack of systematic screening of plant species and has been biased towards specific regions around the world (Reeves, 2003; van der Ent et al., 2013). Most focus has been on nickel hyperaccumulator plants, partly due to the existence of a reagent paper screening test based on dimethylglyoxime, and partly due to the widespread occurrence of naturally nickel-rich ultramafic soils in many countries. Historically, much of the analysis of herbarium and field samples was carried out by atomic absorption spectrophotometry (AAS) for only one or a small number of elements of interest (e.g. nickel, cobalt, and sometimes zinc). From the early 1980s much more use was made of inductively-coupled plasma atomic emission spectroscopy (ICP-AES) and inductively-coupled plasma mass spectrometry (ICP-MS), giving a wider range of multi-element data. More recently, nondestructive X-ray fluorescence (XRF) has enabled mass analysis of herbarium specimens (Gei et al., 2017). Although the use of herbarium specimens for discovering hyperaccumulator plants goes back to the 1970s (Brooks et al., 1977; Jaffré et al., 1979), new analytical technology makes it possible to measure herbarium specimens at a rate of c. 300 specimens per day. Therefore, it is now feasible to measure the elemental concentrations of whole collections and to perform the analysis nondestructively. Investigations are aided by the increase in herbarium database development and digitization processes. The poorer sensitivity of XRF, compared to AAS or ICP-AES/MS is less of an issue if the interest is confined to hyperaccumulator species alone. All this points to the possibility of making substantial discoveries in decades to come by systematic screening of existing plant collections in global herbaria. Such studies also serve to highlight those species sparsely represented in the world's herbaria and should stimulate further field exploration, particularly in areas of metalliferous geology that have been poorly investigated.

Future outlook

In many parts of the world, by virtue of their existence solely or significantly on metalliferous soils, hyperaccumulator plants are threatened by habitat loss, especially from mining and mineral extraction (Whiting et al., 2004; Erskine et al., 2012; Wulff et al., 2013). Nowhere is this situation more serious than in Central Africa where copper–cobalt hyperaccumulator plants are under acute threat of extinction due to mining activities (Lange et al., 2016). Mining, forest fires and land clearing activities threaten the habitat of many nickel hyperaccumulator plants in New Caledonia, Cuba, Brazil and Indonesia. Timely identification of hyperaccumulator species, along with other metal-tolerant plants, is therefore necessary to preserve them to study their unique physiological mechanisms, and to take advantage of their unique properties.

Acknowledgements

The authors thank all contributors to the Global Hyperaccumulator Database for their efforts and expertise. A.v.d.E. is the recipient of a Discovery Early Career Researcher Award (DE160100429) from the Australian Research Council.

Author contributions

R.D.R., T.J. and A.v.d.E. contributed data records to the Global Hyperaccumulator Database. R.D.R., A.J.M.B., T.J., P.D.E., G.E. and A.v.d.E. contributed equally to the writing of this Letter.