PERSPECTIVE ARTICLE published: 26 July 2013 doi: 10.3389/fpls.2013.00279 The metal hyperaccumulators from New Caledonia can broaden our understanding of nickel accumulation in

Tanguy Jaffré 1, Yohan Pillon 2, Sébastien Thomine 3 and Sylvain Merlot 3*

1 Laboratoire de Botanique et D’écologie Végétale Appliquées, Herbarium NOU, UMR AMAP, Institut de Recherche pour le Développement, Nouméa, New Caledonia 2 Tropical Conservation Biology and Environmental Science, University of Hawai‘i at Hilo, Hilo, HI, USA 3 Saclay Sciences Labex, Institut des Sciences du Végétal, Centre National de la Recherche Scientifique, Gif-sur-Yvette, France

Edited by: While an excess of metals such as zinc, cadmium or nickel (Ni) is toxic for most Marc Hanikenne, University of plants, about 500 plant species called hyperaccumulators are able to accumulate high Liège, Belgium amounts of these metals. These plants and the underlying mechanisms are receiving Reviewed by: an increasing interest because of their potential use in sustainable biotechnologies such Thomas J. Bach, Institut Pasteur, France as biofortification, phytoremediation, and phytomining. Among hyperaccumulators, about Damien L. Callahan, The University 400 species scattered in 40 families accumulate Ni. Despite this wide diversity, our current of Melbourne and Deakin Univeristy, knowledge of the mechanisms involved in Ni accumulation is still limited and mostly Australia restricted to temperate herbaceous Brassicaceae. New Caledonia is an archipelago of the Alan E. Pepper, Texas A&M 2 University, USA tropical southwest pacific with a third of its surface (5500 km ) covered by Ni-rich soils *Correspondence: originating from ultramafic rocks. The rich New Caledonia flora contains 2145 species Sylvain Merlot, Institut des Sciences adapted to these soils, among which 65 are Ni hyperaccumulators, including lianas, du Végétal, Centre National de la shrubs or trees, mostly belonging to the orders , , , Recherche Scientifique, Bat. 22, and Gentianales. We present here our current knowledge on Ni hyperaccumulators from avenue de la terrasse, Gif-sur-Yvette, 91198 cedex, France New Caledonia and the latest molecular studies developed to better understand the e-mail: [email protected] mechanisms of Ni accumulation in these plants.

Keywords: nickel hyperaccumulator, New Caledonia, ultramafic soils, adaptation, comparative transcriptomic

INTRODUCTION METAL HYPERACCUMULATORS FROM NEW CALEDONIA: New Caledonia is an archipelago located in the southwest HISTORY AND CURRENT KNOWLEDGE Pacific off the east coast of Australia (20–23 S, 164–167 E). New Unusually high concentration of nickel (Ni) in plants were Caledonia separated from Gondwana in the Cretaceous, and after first reported in the Italian Brassicaceae Alyssum bertolonii a submersion during Paleocene and Eocene, the main island (Minguzzi and Vegnano, 1948)andlaterinHybanthus flori- emerged 37 million years ago (Pelletier, 2006)andwaslikely bundus (Violaceae) from Australia (Severne and Brooks, exclusively re-colonized by plants through long-distance dispersal 1972). Ni concentration exceeding 1% (dry weight) in New (Grandcolas et al., 2008; Cruaud et al., 2012; Pillon, 2012). At the Caledonian plants growing on ultramafic soils was first time of its emersion it was probably entirely covered with ultra- reported in Psychotria gabriellae (previously known as P. douar- mafic rocks that still occupy 34% (5500 km2) of the surface of the rei,Rubiaceae),Hybanthus austrocaledonicus, H. caledonicus main island. The weathering of these rocks produced a variety of (Violaceae), Geissois pruinosa (), and Homalium soils that have a very low level of phosphorus, potassium, calcium guillainii () (Brooks et al., 1974; Jaffré and Schmid, and high level of magnesium and heavy metals including nickel 1974). These plants accumulating more than 1% Ni were then (Ni), cobalt and chromium (Jaffré, 1980; Brooks, 1987). New qualified as “hypernickelophore” (Jaffré and Schmid, 1974). The Caledonia harbors a rich and original vegetation likely result- more widely used term Ni “hyperaccumulator” was first coined ing from the adaptation of plants over a long period of time to by Jaffré et al. (1976) for the description of Pycnandra acuminata these challenging edaphic conditions. New Caledonia is renowned (previously known as Sebertia acuminata, ) in which for its rich, endemic and threatened vascular flora (Morat et al., Ni represents up to 25% of the latex dry weight. The term ‘hyper- 2012) and is therefore considered as one of the world biodiversity accumulator’ was later defined more precisely by Brooks et al. hotspots (Myers et al., 2000). In particular, 2145 species, among (1977) to qualify plants with a concentration of Ni above 0.1% which 80% are endemic, are developing on these metal rich soils (1000 ppm) in dried and extended to other metal accu- (Jaffré et al., 2009). As a consequence, New Caledonia has also mulators, although with different thresholds (Baker and Brooks, been listed among the main hotspots for metallophytes (Whiting 1989; van der Ent et al., 2013a). Following these pioneering stud- et al., 2004). ies, a large number of species that hyperaccumulate Ni were

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described from the New Caledonian flora (Jaffré, 1977a, 1980; soils. This is also the case in New Caledonian Psychotria,in Jaffré et al., 1979a,b; Kersten et al., 1979; Amir et al., 2007). Today, which P. gabriellae is the only Ni hyperaccumulator while 60 we consider that 65 Ni hyperaccumulator taxa scattered in 12 Psychotria species, including P. semper florens, are present on ultra- plant families have been identified (see Supplementary Table), mafic soils (Jaffré, 1980; Baker et al., 1985). In contrast, in New placing New Caledonia, along with Cuba that contains about Caledonian Phyllanthus (Euphorbiaceae; Kersten et al., 1979), and 140 hyperaccumulators (Reeves et al., 1996, 1999), as one of the in Cuban Buxus (Buxaceae; Reeves et al., 1996), a significant most important reservoirs of Ni hyperaccumulators. We can pre- numbers of species growing on ultramafic soils hyperaccumu- dict that the number of Ni hyperaccumulators in New Caledonia lates Ni. In Meditterranean Alyssum sect. Odontarrhena (Cecchi will slightly increase in the coming years considering that the et al., 2010) and in New Caledonian Geissois (Cunoniaceae; Jaffré hyperaccumulator status of known taxa (e.g., Pancheria ferrug- et al., 1979a), almost all species occurring on ultramafic soils inea,Cunoniaceae;Capparis artensis, Capparaceae) was revealed hyperaccumulate nickel, but they are phylogenetically entan- by recent analyses and that new hyperaccumulator taxa, such gled with non-accumulating species restricted to non-ultramafic as Pycnandra caeruleilatex (Swenson and Munzinger, 2010), are soils (Cecchi et al., 2010; Pillon et al., unpublished). In the still being described. The New Caledonian flora also contains Carribean Leucocroton (Euphorbiaceae), mostly diversi- manganese hyperaccumulators (above 1% of dry weight) such fied on Cuba, all 26 species are restricted to ultramafic soils as Denhamia fournieri (previously known as fournieri, and hyperaccumulate nickel (Jestrow et al., 2012). Therefore, ), Alyxia poyaensis (previously a subspecies of Alyxia the link between the adaptation to ultramafic soils and Ni rubricaulis,Apocynaceae),Virotia neurophylla (previously known hyperaccumulation shows some striking variations that are also as Macadamia neurophylla, Proteaceae), and Garcinia amplexi- found within New Caledonian hyperaccumulators. Both charac- caulis from the Clusiaceae family (Jaffré, 1977b, 1979; Fernando ters seem to appear recurrently in some genera in distant areas, et al., 2008, 2010). Interestingly, Denhamia fournieri is also able e.g., in Psychotria and Phyllanthus from New Caledonia, Cuba to hyperaccumulate Ni when growing on ultramafic soil. and other regions (Reeves, 2003). Although no specific study have addressed this question, molecular phylogenetic analyses indi- TAXONOMIC DISTRIBUTION OF NICKEL cated that Phyllanthus and Psychotria species, including nickel HYPERACCUMULATORS AND EVOLUTION OF THE hyperaccumulators, from New Caledonia and the Caribbean HYPERACCUMULATOR TRAIT region belong to distant clades within these genera (Andersson, Worldwide about 400 nickel (Ni) hyperaccumulators scattered 2002; Kathriarachchi et al., 2006; Barrabé, 2013). in more than 40 families have been reported almost exclusively Parallel evolution of the characters at broad taxonomical and in angiosperms (Verbruggen et al., 2009; Krämer, 2010), how- geographical scales may be facilitated by an ancestral fortuitous ever at least one fern of the Adiantum genus (Brooks et al., pre-adaptation, that can be called exaptation, to ultramafic soils 1990), and several epiphytic bryophytes and liverworts growing (Pillon et al., 2010). At a smaller scale, it may have evolved on hyperaccumulating shrubs in New Caledonia can be con- only once and then have been transmitted horizontally through sidered as Ni hyperaccumulators (Boyd et al., 2009), suggesting hybridization and introgression between closely related species, that Ni hyperaccumulation could have appeared early in the as observed for the adaptation to ultramafic soils (Pillon et al., evolution of terrestrial plants. Within angiosperms, Ni hyperac- 2009a,b), in a process that could be qualified as collective evolu- cumulators are mainly found in , although few examples tion (Morjan and Rieseberg, 2004). The great diversity of plants in Magnolianae and Monocots have been described (Figure 1). adapted to ultramafic soils and that can hyperaccumulate Ni in Ni hyperaccumulators are taxonomically scattered, nevertheless New Caledonia, combined with its geographic isolation, makes phylogenetic trends can be observed (Pillon et al., 2010). A this archipelago an ideal system to study the evolution of these third of the Ni hyperaccumulators belongs to the COM clade two characters. (Celastrales, Oxalidales, and Malpighiales) which form part of that account for two third of the Ni hyperaccumulat- MOLECULAR STUDIES ON NEW CALEDONIAN NICKEL ing species. Although this character appeared many times in the HYPERACCUMULATORS course of evolution, it tends to come out more often in certain Our current understanding of the hyperaccumulation of metals in lineages. In New Caledonia, 83% of the Ni hyperaccumulators are plants has been recently recapitulated in excellent review articles from the COM clade while only one hyperaccumulator from each (Verbruggen et al., 2009; Krämer, 2010; Rascio and Navari-Izzo, of the orders Brassicales and Asterales have been identified (see 2011). It now clearly appears that molecular mechanisms involved Supplementary Table). The explanation for this bias remains not in metal chelation and transport play key roles in this remarkable fully understood. adaptation. However, only few mechanisms involved in nickel There are still only few phylogenetic studies that have investi- (Ni) hyperaccumulation have been identified at the molecu- gated how nickel hyperaccumulating species evolved from non- lar level, and this knowledge only originates from studies of accumulating ancestors, and whether the ability to grow on hyperaccumulators from the Brassicaceae family. The study of ultramafic soils is a prerequisite for this character to appear. In Ni hyperaccumulators from other plant families would therefore some genera, such as Australian Stackhousia (Burge and Barker, likely bring new and original information on the mechanisms 2010) or Californian Streptanthus (Mayer and Soltis, 1994), Ni involved in Ni hyperaccumulation in plants. hyperaccumulation is a rare character found only in one species, After the identification of Ni hyperaccumulators in New although several other related species are growing on Ni-rich Caledonia in the early 70’s, one of the first questions was to

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FIGURE 1 | Phylogenetic distribution of nickel hyperaccumulators using number (hyperaccumulating species randomly distributed using a binomial APG III classification. The number of Ni hyperaccumulator in each order is law with a Bonferroni correction for multiple tests). H, indicates the presence presented as a bar (logarithmic scale). The red bar indicates that the of hypernickelophore species accumulating more than 10,000 ppm nickel. observed number of hyperaccumulators significantly exceed the theoretical ∗, indicates the presence of hyperaccumulators from New Caledonia.

identify molecules that are able to chelate Ni and therefore The existence of Ni-citrate complexes in several hyperaccumula- play a role in detoxification. Early analyses of New Caledonian tors was largely confirmed since then in several studies that use hyperaccumulators revealed that Ni was essentially associated state-of-the art techniques of chromatography and mass spec- with organic acids. Citrate was identified as a main ligand for trometry (Sagner et al., 1998; Schaumlöffel et al., 2003; Callahan Ni in the latex of Pycnandra acuminata and in leaves of sev- et al., 2008, 2012). These recent studies also revealed the pres- eral hyperaccumulators in the Homalium and Hybanthus gen- ence of Ni-nicotianamine (NA) complexes in most of the New era (Lee et al., 1977, 1978), while 63% of Ni was bound to Caledonian species that were studied, including P. acuminata malate in leaves of Psychotria gabriellae (Kersten et al., 1980). and P. gabriellae (Schaumlöffel et al., 2003; Callahan et al.,

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2012). Callahan et al. (2008, 2012) developed a metabolic pro- of P. gabriellae was sequenced by the 1KP project in collabora- filing approach based on GC-MS to identify putative ligands tion with the University of New Caledonia (www.onekp.com/ whose abundance in New Caledonian hyperaccumulators cor- index.html). Also, because it is not presently possible to genet- relates with Ni concentration. Putative Ni-metabolite complexes ically manipulate this species, one strategy to target genes of were then directly identified using LC-MS. These analyses iden- interest is to compare its transcriptome with that of a phyloge- tified 2,4,5-trihydroxy-3-methoxy-1,6-hexan-dioic acid as a new netically related, non-accumulating species and thereby identify ligand for Ni in the latex of P. acuminata.IncontrasttoAlyssum genes whose expression is linked to the hyperaccumulation trait. and Noccaea hyperaccumulators (Krämer et al., 1996; Persans Psychotria semperflorens,whichlivesinsympatrywithP. gabriel- et al., 1999), no correlation between the amino acid histidine lae in rain forest on ultramafic soil but does not accumulate Ni and Ni was observed so far in the New Caledonian hyperac- (Figure 2), represents an excellent candidate to conduct com- cumulators. Rather, a significant correlation was observed with parative transcriptomic studies. Interestingly, the flora of Cuba aspartic acid, which has a relatively high association constant for contains at least five Ni hyperaccumulators of the Psychotria genus Ni (lg K = 7.2), but LC-MS analyses failed to directly detect Ni- including P. costivenia and P. clementis (Reeves et al., 1999). The aspartic acid complexes in these species. Analyses of P. gabriellae comparison of the molecular mechanisms involved in Ni adapta- samples revealed several Ni-organic acid complexes, including tion and hyperaccumulation in Psychotria species from the flora malonic and maleic acids, but did not confirm the existence of of Cuba and New Caledonia that have different origins, will help a complex with malic acid. In addition, the authors pointed out to understand the evolution of these traits and possibly reveal that several intense Ni-containing ions could not be identified by LC-MS analysis from P. gabriellae samples (Callahan et al., 2012). These studies confirmed that Ni forms complexes with a plethora of organic acids, which could be of biological signifi- cance for the storage of Ni in vacuoles. NA that is able to bind Ni with a high affinity (lg K = 16), seems to be an ubiquitous Ni ligand in dicotyledon hyperaccumulators and may play an important role in cytoplasmic Ni detoxification and long range transport (Kim et al., 2005; Pianelli et al., 2005; Gendre et al., 2007). In contrast, histidine might not play a significant role in Ni homeostasis in New Caledonian hyperaccumulators and the presence of Ni-complexes with other amino acids still needs to be confirmed. Additional metabolomic studies using alternative extraction and separation methods will be required to validate and identify new Ni-complexes from New Caledonian hyperac- cumulators. Ultimately, the speciation of Ni in New Caledonian hyperaccumulators should be also confirmed in vivo,forexample using X-ray spectrometric methods (Montarges-Pelletier et al., 2008). In parallel to these metabolomic studies, it is also important to identify genes coding for key enzymes in the biosynthesis of Ni lig- ands and for Ni membrane transporters. However, no nucleotide sequences were available until recently for any of the New Caledonian hyperaccumulators. The recent development of Next Generation Sequencing (NGS) technologies and the creation of a molecular biology platform in New Caledonia (Majorel- Loulergue et al., 2009), allowed us to initiate the sequencing of the P. gabriellae transcriptome using Roche GS-FLX titanium technology. We obtained more than 500,000 reads that are pub- licly available at the European Nucleotide Archive under acces- sion number ERP001334. The de novo assembly of the sequence reads generated approximately 30,000 contigs that represented the FIGURE 2 | Psychotria gabriellae and Psychotria semperflorens as a first EST data set for P. gabriellae. We are currently using these model system to study nickel hyperaccumulation. The Ni original sequences to identify putative Ni transporters from the hyperaccumulator P. gabriellae (red tag) and the closely related non-accumulator P. semperflorens (yellow tag) are living in sympatry in rain NRAMP, IREG/FPN, YSL, ZIP/IRT families (Verbruggen et al., forest on ultramafic soil in New Caledonia (A). Both species are 1–3 meters 2009; Krämer, 2010; Rascio and Navari-Izzo, 2011), that might shrub with very similar pink flowers (top right insert: P. semperflorens be involved in nickel tolerance and hyperaccumulation in leaves inflorescence). In natural growth condition, P. gabriellae accumulates up to (Merlot et al., submitted). To identify additional genes impor- 4% Ni in leaves while P. semperflorens accumulates approximately 100 times less Ni. These differences can be semi-quantitatively visualized on tant for Ni accumulation, it will be necessary to sequence the root XRF spectra (B). transcriptome of P. gabriellae. In parallel, the seed transcriptome

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the genetic basis of the exaptation to ultramafic soils. A sim- development are often opposed to the protection of environment ilar approach using New Caledonian species could be used and endangered flora. In every respect, future studies on New to study the evolution of Ni hyperaccumulation mechanisms Caledonian hypernickelophore accumulating more than 1% Ni in the Phyllanthaceae genus Phyllanthus (including Glochidion) and producing a high biomass such as species of Geissois (Fogliani that is also present in Cuba and Indonesia (Kersten et al., et al., 2009)orHomalium,beingrelatedtoPopulus,willbeof 1979). particular interest (Chaney et al., 2007).

CONCLUDING REMARKS ACKNOWLEDGMENTS The hyperaccumulation of nickel (Ni) is a complex trait that Becauseofspacelimitation,wewerenotabletociteallstud- appeared several times during evolution of plants. New Caledonia ies that would have been relevant to this topic, but we would hosts a rich and phylogenetically diverse set of Ni hyper- like to collectively acknowledge researchers from the University of accumulators and offers significant opportunities to broaden New Caledonia (UNC), the neo-Caledonian Agronomic Institute our knowledge of the molecular mechanisms involved in Ni (IAC), IRD, CNRS, or from other institutions and also volunteers hyperaccumulation that was mostly studied so far in European that are acting in New Caledonia to better describe, understand, Brassicaceae. Today, such studies are realistic considering the valorize and protect its peculiar flora. We would like to espe- rapid development of NGS technologies that give access to vir- cially thank Laurent L’Huillier (IAC) for funding some recent tually all plant genomes and also because of the relatively good metal analyses, Laure Barrabé and Nadia Robert for unpublished knowledge of the diversity of New Caledonian hyperaccumula- information and the picture presented in Figure 2, and Fondis tors. The identification of genes involved in Ni accumulation in Bioritech (Guyancourt, France) for the use of the hand-held XRF these species will be important to identify conserved and diver- instrument. The costs for this publication were supported by gent mechanisms involved in Ni hyperaccumulation and also funding from CNRS. adaptation to ultramafic soils. We think these results will support the development of phytoremediation and phytomining tech- SUPPLEMENTARY MATERIAL nologies that are particularly important in regions such as New The Supplementary Material for this article can be found Caledonia (Losfeld et al., 2012) and Indonesia (van der Ent et al., online at: http://www.frontiersin.org/Plant_Physiology/10.3389/ 2013b), where the nickel mining industry and the economical fpls.2013.00279/abstract

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