The discovery of nickel hyperaccumulation in the New Caledonian tree Pycnandra acuminata 40 years on: an introduction to a Virtual Issue.

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The discovery of nickel hyperaccumulation in the New

Caledonian tree Pycnandra acuminata 40 years on: an

introduction to a Virtual Issue.

Tanguy Jaffré, Roger D. Reeves, Alan J. M. Baker, Henk Schat, Antony van

der Ent

To cite this version:

Tanguy Jaffré, Roger D. Reeves, Alan J. M. Baker, Henk Schat, Antony van der Ent. The discovery

of nickel hyperaccumulation in the New Caledonian tree Pycnandra acuminata 40 years on: an

intro-duction to a Virtual Issue.. New Phytologist, Wiley, 2018, 218 (2), pp.397-400. �10.1111/nph.15105�.

�hal-02025847�

Commentary

The discovery of nickel

hyperaccumulation in the New

Caledonian tree Pycnandra

acuminata 40 years on: an

introduction to a Virtual Issue

More than 40 years since the discovery of the spectacular New

Caledonian hyperaccumulator tree Pycnandra acuminata,

knowl-edge on these unusual plants has advanced considerably. Hundreds

of other hyperaccumulators of metal and metalloid elements have

since been reported, and new discoveries continue to be made at an

accelerated pace. The field has matured and is the current subject of

detailed investigations into the molecular biology and physiological

aspects of the hyperaccumulation phenomenon, as well as research

on ecological interactions. Hyperaccumulator plants have also

found useful applications in phyto-extraction technologies,

especially in nickel phytomining.

Discovery of hyperaccumulator plants

More than 40 years have passed since the reporting of an

extraordinary accumulation of nickel in a New Caledonian

endemic tree (Jaffr
e et al., 1976). This tree, Pycnandra (formerly

Sebertia) acuminata accumulates an astonishing 20–25% nickel in

its latex which is coloured blue-green from nickel complexes

(Fig. 1). High plant nickel accumulation was first reported by

Minguzzi & Vergnano (1948) in Alyssum bertolonii from Italy. This

was followed in the 1960s by a similar discovery in two other

Alyssum species, and in the early 1970s in two species from

Zimbabwe and in Hybanthus floribundus from Western Australia.

From the nickel-rich ultramafic areas of New Caledonia, high

nickel concentrations were found in Psychotria douarrei (now

P. gabriellae), in two further species of Hybanthus and two species of

Homalium (Brooks et al., 1974; Jaffr
e & Schmid, 1974). However,

the discovery of P. acuminata was a major driver of research over the

following decades. In its title, the Science article introduced the

word ‘hyperaccumulator’ and the term hyperaccumulation was

subsequently established (Brooks et al., 1977) to denote a plant

nickel uptake of

> 1000 mg kg

in dry tissue. The term was later

widened to include other elements normally occurring in only trace

concentrations in plant tissue, as was reviewed by van der Ent et al.

(2013).

Since 1976, Web of Science lists 2829 publications with

‘hyperaccumulator’ in the topic, and Scopus lists 2264

documents with ‘hyperaccumulator’ in the title, abstract or

keywords (Figure 2). Much effort in the late 1970s focused on

finding more nickel hyperaccumulators in Alyssum in the

Mediter-ranean region and Turkey (Brooks et al., 1979), in New Caledonia

(Jaffr
e, 1980) and elsewhere. To date, 65 hyperaccumulator plants

have been found from New Caledonia (Jaffr
e et al., 2013), 130

from Cuba (Reeves et al., 1996, 1999), and 59 from Turkey

(Reeves & Adıg€uzel, 2008), with smaller numbers from Brazil,

Malaysia, Indonesia, the Philippines and several other countries

(Reeves, 2003; Reeves et al., 2007; van der Ent et al., 2015a). The

search is not over: more hyperaccumulators have recently been

found among herbarium collections using a handheld X-ray

fluorescence instrument (Gei et al., 2017).

Studying hyperaccumulator plants

The extreme behaviour implied by hyperaccumulation results from

specific metal or metalloid transport and sequestering mechanisms.

Inquiries into these processes span all biological sciences, from

genetics and molecular biology to physiology and biochemistry.

Fig. 1 The famous blue-green latex of Pycnandra acuminata that instigated the global search for hyperaccumulator plants over the past four decades.

This article is a Commentary on Reeves et al., 218: 407–411 and van der Ent et al., 218: 432–434.

Much has been learnt about the genetic architecture and molecular

mechanisms of zinc and cadmium hyperaccumulation in the model

species Noccaea caerulescens (Assunc

ß~ao et al., 2001, 2003;

O Lochlainn et al., 2011; Ueno et al., 2011) and Arabidopsis

halleri (Courbot et al., 2007; Willems et al., 2007; Hanikenne

et al., 2008). In general, hyperaccumulation and hypertolerance of

zinc and cadmium seem to rely on elevated expression levels of a

number of genes, most of them encoding zinc transmembrane

transporters that are universally expressed in higher plants. In this

way, studies on hyperaccumulators have also significantly enhanced

our understanding of the zinc homeostasis machinery in

non-hyperaccumulators and the roles of individual transporters therein

(Assunc

ß~ao et al., 2010; Lin et al., 2016). Knowledge on nickel

hyperaccumulation mechanisms is largely lacking. Recent studies

have identified a candidate ‘hyperaccumulation gene’ in Psychotria

gabriellae (Merlot et al., 2014). In P. acuminata and several other

New Caledonian nickel hyperaccumulators, nickel was found to be

associated with citrate as the principal ligand (Lee et al., 1977,

1978), a conclusion reinforced by several studies more recently.

However, abnormal citrate concentrations were not found in the

Alyssum hyperaccumulators, and other organic acids and

hydroxy-acids such as malate and malonate accompanied nickel in the

isolation of nickel-rich extracts (Pelosi et al., 1976; Pancaro et al.,

1978). There appears to be no universal mechanism of uptake and

sequestration among the many nickel hyperaccumulators identified

thus far. The nature of the involvement of amino acids such as

histidine and nicotianamine in the transport and sequestration

processes is still a subject of investigation and debate.

The tissue-level micro-distribution of nickel has been

elucidated in several hyperaccumulator species in Alyssum,

Berkheya, Hybanthus, Noccaea, Phyllanthus and Senecio (for

examples, see Mesjasz-Przybylowicz et al., 1997, 2001, 2007,

2016; Broadhurst et al., 2004; K€upper et al., 2001; Kachenko

et al., 2008). In most hyperaccumulators nickel is preferentially

accumulated in foliar epidermal cells, but in Berkheya coddii

from South Africa it is found mainly in the mesophyll and

vascular bundles (Mesjasz-Przybylowicz et al., 2001). Such

studies have not yet included P. acuminata (but see Perrier

et al. (2004) for a preliminary investigation) or other New

Caledonian hyperaccumulators.

The most popular hypothesis for explaining the evolution of

hyperaccumulation revolves around ‘elemental herbivory

protec-tion’ (Boyd & Martens, 1998), which proposes that elevated metal

or metalloid concentrations in shoots afford protection against

leaf-chewing insects. Experimental studies have provided ample

evidence that hyperaccumulated nickel is toxic to most herbivorous

insects (Martens & Boyd, 2002), but some specialist insects have

been found with high levels of tolerance (Mesjasz-Przybylowicz &

Przybylowicz, 2001; Boyd et al., 2006; Boyd, 2009).

Hyperaccu-mulation may also have antifungal effects, or may reduce the

germination and growth of competing plant species through an

increase in nickel concentrations in the nearby soil, via leaf litter

deposition (Martens & Boyd, 1994; Boyd & Jaffr
e, 2001). In

concert, this could also benefit seedlings of the hyperaccumulator

plant itself (van der Ent et al., 2015a).

In this issue of New Phytologist van der Ent

et al. (pp. 432–452)

outline techniques for elucidating the ecophysiology of

hyperac-cumulator plants using X-ray elemental mapping techniques.

These methods mapping techniques are unique in providing in situ

information, and can play an important role in answering questions

at every level of metal(loid) homeostasis and regulation in

hyperaccumulator plants.

Scientific curiosity to real-life applications: nickel

phytoextraction and phytomining

Nickel hyperaccumulators were initially regarded as a scientific

curiosity, but the potential of these plants for extracting

metallic elements from soil (phytoextraction) has been

estab-lished (Chaney et al., 1997; Brooks, 1998). Phytoextraction has

been proposed and demonstrated for the remediation of soils

contaminated by toxic elements, for biofortification (especially

for zinc) or for conferring hyperaccumulation traits to other

crops (Clemens, 2017). There is clear potential for

phytomin-ing of nickel, in which crops of hyperaccumulators are grown

on soils that are sub-economic for conventional mining, with

260 240 220 200 180 160 140 120 100 80 60 40 20 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998

Years 1981–2018

Number of publicaon each year

1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018

Fig. 2 Scopus publications by year for ‘hyperaccumulator’ in the article title, abstract or keywords.

Commentary

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New

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the harvesting of their biomass to produce a nickel-rich

‘bio-ore’ (van der Ent et al., 2015b). This bio-ore is much richer in

nickel than traditional mined ores and can be used to derive

pure chemicals (Barbaroux et al., 2012) or catalysts (Losfeld

et al., 2012). Phytoextraction applications exist for a range of

other elements for which hyperaccumulator plants are known,

including selenium, thallium and manganese, or for remediating

arsenic- cadmium-, or selenium-polluted soils (Schwartz et al.,

2003; Gonzaga et al., 2008; Schiavon & Pilon-Smits, 2017).

Hyperaccumulator plants are acutely threatened

Many hyperaccumulator plants are rare, with restricted ranges on

metalliferous soils, making them sensitive to destructive forces such

as mining, forestry development, fire or urban expansion (Reeves &

Baker, 2000; Whiting et al., 2004; Baker et al., 2010). The current

situation of P. acuminata illustrates the dire circumstances for the

survival of many hyperaccumulator plants globally. In New

Caledonia, only a fraction of the native rainforest remains, as a

result of logging, fires and mining (van der Ent et al., 2015c).

Pycnandra acuminata persists in fragmented forest patches

sur-rounded by maquis, with probably fewer than several hundred

individuals left. Its fate and that of many other species of the unique

flora of New Caledonia hangs in the balance with the continued

threat of exploitation of the remaining habitat for nickel mining

(Isnard et al., 2016). In this issue of New Phytologist, Reeves et al.

(pp. 407–411) highlight the Global Hyperaccumulator Database,

which, amongst other aims, strives to raise awareness of at-risk

hyperaccumulator species that are threatened by extinction.

A selection of articles published in New Phytologist on

hyperaccu-mulator plants can be found at https://nph.onlinelibrary.wiley.com/

doi/toc/10.1111/(ISSN)1469-8137.HYPERACCUMULATORS.

Acknowledgements

A. van der Ent is the recipient of a Discovery Early Career

Researcher Award (DE160100429) from the Australian Research

Council.

Author contributions

T.J., R.D.R., A.J.M.B., H.S. and A.v.d.E. equally contributed in

writing this manuscript.

ORCID

Antony van der Ent

X

http://orcid.org/0000-0003-0922-5065

Tanguy Jaffr
e

_{, Roger D. Reeves}

_{, Alan J. M. Baker}

_,

Henk Schat

and Antony van der Ent

*

X

1

_{Institut de Recherche pour le D
eveloppement (IRD), UMR}

AMAP, Herbarium NOU, Noum
ea, 98848, New Caledonia;

2

_{Palmerston North, 4410, New Zealand;}

_{Centre for Mined Land Rehabilitation, The University of}

Queensland, St Lucia, Queensland, 4072, Australia;

4

_{Laboratoire Sols et Environnement, Universit
e de Lorraine/}

INRA, Vandoeuvre-les-Nancy, France;

5

_{Department of Ecological Sciences, Faculty of Earth and Life}

Sciences, Vrije Universiteit Amsterdam, Amsterdam,

the Netherlands;

6

_{Laboratory of Genetics, Wageningen University, Wageningen,}

the Netherlands

(*Author for correspondence: tel +61 7 3346 4003;

email a.vanderent@uq.edu.au)

This article is a Commentary on Reeves et al., 218: 407–411 and va

n der Ent et al., 218: 432–434.

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Key words: hyperaccumulator, metallophyte, New Caledonia, nickel, phytomining, virtual issue.

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