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 plants 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 Plant 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 Celastrales, Oxalidales, Malpighiales, 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 (Cunoniaceae), and Homalium soils that have a very low level of phosphorus, potassium, calcium guillainii (Salicaceae) (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, Sapotaceae) 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 leaves 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 www.frontiersin.org July 2013 | Volume 4 | Article 279 | 1 Jaffré et al. Learning from New Caledonian hyperaccumulators 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 genus 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 Maytenus fournieri, and hyperaccumulate nickel (Jestrow et al., 2012). Therefore, Celastraceae), 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