Evolution of nickel hyperaccumulation by Stackhousia tryonii (Celastraceae), a serpentinite-endemic plant from Queensland, Australia
Dylan O. Burge A C and W. R. Barker B
+ Author Affiliations
- Author Affiliations
A Duke University, Department of Biology, Box 90338, Durham, North Carolina, 27708, USA.
B State Herbarium of South Australia, Hackney Road, Adelaide, SA 5000, Australia and Australian Centre for Evolutionary Biology and Biodiversity, University of Adelaide, SA 5005, Australia.
C Corresponding author. Email: dylan.o.burge@gmail.com
Australian Systematic Botany 23(6) 415-430 https://doi.org/10.1071/SB10029
Submitted: 9 July 2010 Accepted: 5 November 2010 Published: 23 December 2010
Abstract
To elucidate the evolutionary origin of nickel (Ni) hyperaccumulation by the Australian serpentinite-endemic plant Stackhousia tryonii Bailey, phylogenetic analyses of chloroplast and nuclear DNA for Stackhousia and its close relatives were combined with assays of plant-tissue Ni concentrations. Thirty-five plants from 20 taxa were analysed by sequencing nuclear rDNA (ITS) and the plastid trnL–F region. Phylogenetic analysis of sequence data was conducted under maximum parsimony and Bayesian search criteria. In all, 100 plants from 39 taxa, including all 33 Stackhousia species, were analysed for Ni concentration by radial inductively coupled plasma atomic-emission spectrometry (ICP–AES). In phylogenetic analyses, S. tryonii was monophyletic, nested within a monophyletic Stackhousia. Only S. tryonii contained concentrations of Ni above the hyperaccumulation threshold (0.1%; 1000 ppm), containing between 0.25% (2500 ppm) and 4.1% (41 000 ppm) Ni by dry weight. Nickel-hyperaccumulation ability appears to have been acquired once during diversification of Stackhousia, by S. tryonii.
References
Adigüzel N, Reeves RD (2002) A new nickel-accumulating species of Alyssum (Cruciferae) from western Turkey. Edinburgh Journal of Botany 59, 215–219.| A new nickel-accumulating species of Alyssum (Cruciferae) from western Turkey.Crossref | GoogleScholarGoogle Scholar |
Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements – a review of their distribution, ecology and phytochemistry. Biorecovery 1, 81–126.
Baker AJM, Proctor J (1988) Ecological studies on forest over ultrabasic rocks in the Philippines. Bulletin of the British Ecological Society 19, 29–34.
Baker AJM, Brooks RR, Kersten WJ (1985) Accumulation of nickel by Psychotria species from the pacific basin. Taxon 34, 89–95.
| Accumulation of nickel by Psychotria species from the pacific basin.Crossref | GoogleScholarGoogle Scholar |
Baker AJM, Proctor J, van Balgooy MMJ, Reeves RD (1992) Hyperaccumulation of nickel by the flora of the ultramafics of Palawan, Republic of the Philippines. In ‘The vegetation of ultramafic (serpentine) soils’. (Eds AJM Baker, J Proctor, RD Reeves) pp. 291–304. (Intercept: Andover, UK)
Baker AJM, McGrath SP, Reeves RD, Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In ‘Phytoremediation of contaminated soil and water’. (Eds N Terry, G Bañuelos) pp. 85–107. (Lewis Publishers: Boca Raton, FL)
Barker WR (1984) Stackhousiaceae. In ‘Flora of Australia. Vol. 22’. (Ed. AS George) pp. 186–203. (Australian Government Publishing Service: Canberra)
Barker WR (2005) Standardising informal names in Australian publications. Australian Systematic Botany Society Newsletter 122, 11–12.
Barker WR (in press) The taxonomy of subfamily Stackhousioideae (Celastraceae). I. Journal of the Adelaide Botanic Garden
Batianoff GN, Reeves RD, Specht RL (1990) Stackhousia tryonii Bailey, a nickel-accumulating serpentinite-endemic species of central Queensland. Australian Journal of Botany 38, 121–130.
| Stackhousia tryonii Bailey, a nickel-accumulating serpentinite-endemic species of central Queensland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXpslKr&md5=23ea6a62348c542f2517006dca2a416bCAS |
Berazain Iturralde R (1981) Sobre el endemismo de la florula serpentinicola de ‘Lomas de Galindo,’ Canasi, Habana. Revista del Jardín Botánico Nacional 2, 29–59.
Bhatia NP, Orlic I, Siegele R, Ashwath N, Baker AJM, Walsh KB (2003) Elemental mapping using PIXE shows the main pathway of nickel movement is principally symplastic within the fruit of the hyperaccumulator Stackhousia tryonii. New Phytologist 160, 479–488.
| Elemental mapping using PIXE shows the main pathway of nickel movement is principally symplastic within the fruit of the hyperaccumulator Stackhousia tryonii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXps1al&md5=70f9d2aab52fcc6b4a01a798dcea1766CAS |
Bhatia NP, Walsh KB, Orlic I, Siegele R, Ashwath N, Baker AJM (2004) Studies on spatial distribution of nickel in leaves and stems of the metal hyperaccumulator Stackhousia tryonii using nuclear microprobe (micro-PIXE) and EDXS techniques. Functional Plant Biology 31, 1061–1074.
| Studies on spatial distribution of nickel in leaves and stems of the metal hyperaccumulator Stackhousia tryonii using nuclear microprobe (micro-PIXE) and EDXS techniques.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWjt7fL&md5=8d0bf349f471303e14cb8cfea3b0c9d7CAS |
Bhatia NP, Baker AJM, Walsh KB, Midmore DJ (2005a) A role for nickel in osmotic adjustment in drought-stressed plants of the nickel hyperaccumulator Stackhousia tryonii Bailey. Planta 223, 134–139.
| A role for nickel in osmotic adjustment in drought-stressed plants of the nickel hyperaccumulator Stackhousia tryonii Bailey.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Knt77J&md5=193b3c15a8d7d54949b89afe6f50641cCAS | 16200406PubMed |
Bhatia NP, Walsh KB, Baker AJM (2005b) Detection and quantification of ligands involved in nickel detoxification in a herbaceous Ni hyperaccumulator Stackhousia tryonii Bailey. Journal of Experimental Botany 56, 1343–1349.
| Detection and quantification of ligands involved in nickel detoxification in a herbaceous Ni hyperaccumulator Stackhousia tryonii Bailey.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVKmtrs%3D&md5=ff02a85f6d32a4de7616e08cede56c8bCAS | 15767321PubMed |
Bidwell SD (2000) Hyperaccumulation of metal in Australian native plants. PhD Thesis, School of Botany, University of Melbourne, Australia.
Blattner FR (1999) Direct amplification of the entire ITS region from poorly preserved plant material using recombinant PCR. BioTechniques 27, 1180–1185.
Boyd RS (2004) Ecology of metal hyperaccumulation. New Phytologist 162, 563–567.
| Ecology of metal hyperaccumulation.Crossref | GoogleScholarGoogle Scholar |
Boyd RS, Martens SN (1998) Nickel hyperaccumulation by Thalaspi montanum var. montanum (Brassicaceae): a constitutive trait. American Journal of Botany 85, 259–265.
| Nickel hyperaccumulation by Thalaspi montanum var. montanum (Brassicaceae): a constitutive trait.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitFeisb4%3D&md5=957774ab728c03bf23f46d7825e673caCAS |
Bradshaw AD (1952) Populations of Agrostis tenuis resistant to lead and zinc poisoning. Nature 169, 1098
| Populations of Agrostis tenuis resistant to lead and zinc poisoning.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG38%2Fnsl2ruw%3D%3D&md5=321881a8791d60b316bca8cdc192011fCAS | 14947879PubMed |
Broadley MR, Willey NJ, Wilkins JC, Baker AJM, Mead A, White PJ (2001) Phylogenetic variation in heavy metal accumulation in angiosperms. New Phytologist 152, 9–27.
| Phylogenetic variation in heavy metal accumulation in angiosperms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVylsro%3D&md5=a9ada878a9ff40774dee0d504bb99de5CAS |
Brooks RR (1987) ‘Serpentine and its vegetation: a multidisciplinary approach.’ (Dioscorides Press: Portland, OR)
Brooks RR (1995) Specific indicator plants. In ‘Biological systems in mineral exploration and processing’. (Eds RR Brooks, CE Dunn, GEM Hall) pp. 39–70. (Ellis Horwood: New York)
Brooks RR (1998) Geobotany and hyperaccumulators. In ‘Plants that hyperaccumulate heavy metals’. (Ed. RR Brooks) pp. 55–94. (CAB International: Wallingford, UK)
Brooks RR, Radford CC (1978) Nickel accumulation by European species of the genus Alyssum. Proceedings of the Royal Society of London. Series B. Biological Sciences 200, 217–224.
| Nickel accumulation by European species of the genus Alyssum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXhtFOrs7w%3D&md5=1b081b9778f3bd08f27a89e779d335c0CAS |
Brooks RR, Wither ED (1977) Nickel accumulation by Rinorea bengalensis (Wall.) O.K. Journal of Geochemical Exploration 7, 295–300.
| Nickel accumulation by Rinorea bengalensis (Wall.) O.K.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXltVCltr8%3D&md5=fdd2f40dcd99c4c3e0e6547fb2f3d235CAS |
Brooks RR, Yang X-H (1984) Elemental levels and relationships in the endemic serpentine flora of the Great Dyke, Zimbabwe and their significance as controlling factors for the flora. Taxon 33, 392–399.
| Elemental levels and relationships in the endemic serpentine flora of the Great Dyke, Zimbabwe and their significance as controlling factors for the flora.Crossref | GoogleScholarGoogle Scholar |
Brooks RR, Lee J, Reeves RD, Jaffré T (1977a) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. Journal of Geochemical Exploration 7, 49–57.
| Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXkt1KhsL8%3D&md5=101bf7bbfb0ad3fce71655b3b9c487acCAS |
Brooks RR, Wither ED, Zepernick B (1977b) Cobalt and nickel in Rinorea species. Plant and Soil 47, 707–712.
| Cobalt and nickel in Rinorea species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXhtlehsbc%3D&md5=3d66afc83ae5ef037bc67da7fcee440eCAS |
Brooks RR, Morrison RS, Reeves RD, Dudley TR, Akman Y (1979) Hyperaccumulation of nickel by Alyssum Linnaeus (Cruciferae). Proceedings of the Royal Society of London. Series B. Biological Sciences 203, 387–403.
| Hyperaccumulation of nickel by Alyssum Linnaeus (Cruciferae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXhtVSisbk%3D&md5=7c1ac45b57da289eb613089e4fe9a517CAS |
Brooks RR, Reeves RD, Baker AJM, Rizzo JA, Diaz Ferreira H (1990) The Brazilian serpentine plant expedition (BRASPEX), 1988. National Geographic Research 6, 205–219.
Brooks RR, Reeves RD, Baker AJM (1992) The serpentine vegetation of Goiás State, Brazil. In ‘The vegetation of ultramafic (serpentine) soils’. (Eds AJM Baker, J Proctor, RD Reeves) pp. 67–81. (Intercept: Andover, UK)
Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining. Trends in Plant Science 3, 359–362.
| Phytomining.Crossref | GoogleScholarGoogle Scholar |
Cecchi L, Gabbrielli R, Arnetoli M, Gonnelli C, Hasko A, Selvi F (2010) Evolutionary lineages of nickel hyperaccumulation and systematics in European Alysseae (Brassicaceae): evidence from nrDNA sequence data. Annals of Botany 106, 751–767.
| Evolutionary lineages of nickel hyperaccumulation and systematics in European Alysseae (Brassicaceae): evidence from nrDNA sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCltL%2FO&md5=9845cfda1df946b6b5b7b1960ca7210cCAS | 20724306PubMed |
Doksopulo EP (1961) ‘Nickel in rocks, soils, water and plants adjacent to the talc deposits of the Chorchanskaya Group. Tiblisi.’ (Izdatel vo Tbiliskovo Universitet: Tbilisi, Georgia)
Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10, 315–319.
| Testing significance of incongruence.Crossref | GoogleScholarGoogle Scholar |
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
| Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |
Gabbrielli R, Pedani F, Vergnano Gambi O (1987) Ulteriori dati sulla composizione minerale della vegetazione degli affioramenti ofiolitici dell’alta Valle di Ayas. Revue Valdôtaine d’Histoire Naturelle 41, 99–110.
Hendrickx M (2009) Naturally occurring asbestos in eastern Australia: a review of geological occurrence, disturbance and mesothelioma risk. Environmental Geology 57, 909–926.
| Naturally occurring asbestos in eastern Australia: a review of geological occurrence, disturbance and mesothelioma risk.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivFyrtbk%3D&md5=a38db2bd71f70259de542f516e7091c0CAS |
Holmgren PK, Holmgren NH, Barnett LC (1990) ‘Index Herbariorum. I. The herbaria of the world.’ 8th edn. (The New York Botanical Garden: New York)
Homer FA, Reeves RD, Brooks RR, Baker AJM (1991) Characterization of the nickel-rich extract from the nickel hyperaccumulator Dichapetalum gelonioides. Phytochemistry 30, 2141–2145.
| Characterization of the nickel-rich extract from the nickel hyperaccumulator Dichapetalum gelonioides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXks1ymsrs%3D&md5=d400b393898cf1292ce16971a6c2e015CAS |
Jaffré T (1980) Étude écologique du peuplement végétal des sols dérivés de roches ultrabasiques en Nouvelle Calédonie. Travaux et Documents de l’ORSTOM 124, 1–274.
Jaffré T (1992) Floristic and ecological diversity of the vegetation on ultramafic rocks in New Caledonia. In ‘The vegetation of ultramafic (serpentine) soils’. (Eds AJM Baker, J Proctor, RD Reeves) pp. 101–107. (Intercept: Andover, UK)
Jaffré T, Schmid M (1974) Accumulation du nickel par une Rubiacée de Nouvelle Calédonie: Psychotria douarrei (G.Beauvisage) Däniker. Comptes Rendus Hebdomadaires des Séances de l’Académie des Sciences. Série D, Sciences Naturelles 278, 1727–1730.
Jaffré T, Brooks RR, Lee J, Reeves RD (1976) Sebertia acuminata: a hyperaccumulator of nickel from New Caledonia. Science 193, 579–580.
| Sebertia acuminata: a hyperaccumulator of nickel from New Caledonia.Crossref | GoogleScholarGoogle Scholar | 17759588PubMed |
Jaffré T, Brooks RR, Trow JM (1979a) Hyperaccumulation of nickel by Geissois species. Plant and Soil 51, 157–161.
| Hyperaccumulation of nickel by Geissois species.Crossref | GoogleScholarGoogle Scholar |
Jaffré T, Kersten W, Brooks RR, Reeves RD (1979b) Nickel uptake by Flacourtiaceae of New Caledonia. Proceedings of the Royal Society of London. Series B. Biological Sciences 205, 385–394.
| Nickel uptake by Flacourtiaceae of New Caledonia.Crossref | GoogleScholarGoogle Scholar |
Jaireth S, Hoatson DM, Towner RR, Ratajkoski M (2005) ‘Australian nickel resources map.’ (Geoscience Australia: Canberra)
Kelly PC, Brooks RR, Dilli S, Jaffré T (1975) Preliminary observations on the ecology and plant chemistry of some nickel-accumulating plants from New Caledonia. Proceedings of the Royal Society of London. Series B. Biological Sciences 189, 69–80.
| Preliminary observations on the ecology and plant chemistry of some nickel-accumulating plants from New Caledonia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXhtlGks7c%3D&md5=09c92d4143134eacaeac9e0a45f9c5e4CAS |
Kersten WJ, Brooks RR, Reeves RD, Jaffré T (1979) Nickel uptake by New Caledonian species of Phyllanthus. Taxon 28, 529–534.
| Nickel uptake by New Caledonian species of Phyllanthus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhtVOgsbY%3D&md5=07d7db18f64e2537e29dde211819b1c0CAS |
Kruckeberg AR (1951) Intraspecific variability in the response of certain native plant species to serpentine soil. American Journal of Botany 38, 408–419.
| Intraspecific variability in the response of certain native plant species to serpentine soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG3MXltlyjsw%3D%3D&md5=4e8b1852c5db7099165898d36b950e17CAS |
Kruckeberg AR (1986) An essay: the stimulus of unusual geologies for plant speciation. Systematic Botany 11, 455–463.
| An essay: the stimulus of unusual geologies for plant speciation.Crossref | GoogleScholarGoogle Scholar |
Kruckeberg AR, Peterson PJ, Samiullah Y (1993) Hyperaccumulation of nickel by Arenaria rubella (Caryophyllaceace) from Washington State. Madrono 42, 458–469.
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics (Oxford, England) 23, 2947–2948.
| Clustal W and Clustal X version 2.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaqsL%2FM&md5=4a9faf027f4bcf733369f1ff5e23fb88CAS | 17846036PubMed |
Lisanti EL (1952) Contributo allo studio delle morfosi che si riscontrano sui serpentini. Nuovo Giornale Botanico Italiano 14, 349–360.
Mabberley DJ (2008) ‘Mabberley’s plant-book, a portable dictionary of plants, their classifications, and uses.’ 3rd edn. (Cambridge University Press: Cambridge, UK)
Magallón S, Castillo A (2009) Angiosperm diversification through time. American Journal of Botany 96, 349–365.
| Angiosperm diversification through time.Crossref | GoogleScholarGoogle Scholar |
Mason HL (1946) The edaphic factor in narrow endemism. I. The nature of environmental influences. Madrono 8, 209–226.
Menezes de Sequeira E (1969) Toxicity and movement of heavy metals in serpentinic soils (north-Eastern Portugal). Agronomia Lusitana 30, 115–154.
Mengoni A, Baker AJM, Bazzicalupo M, Reeves RD, Adigüzel N, Chianni E, Galardi F, Gabbrielli R, Gonnelli C (2003) Evolutionary dynamics of nickel hyperaccumulation in Alyssum revealed by ITS nrDNA analysis. New Phytologist 159, 691–699.
| Evolutionary dynamics of nickel hyperaccumulation in Alyssum revealed by ITS nrDNA analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXns1Shu7g%3D&md5=96bbc500254951e7f76191cdc9a74bbbCAS |
Minguzzi C, Vergnano O (1948) Il contenuto di nichel nelle ceneri di Alyssum bertolonii. Atti della Società Toscana di Scienze Naturali. Memorie Serie A 55, 49–74.
Morrey DR, Balkwill K, Balkwill M-J (1989) Studies on serpentine flora: preliminary analyses of soils and vegetation associated with serpentinite rock formations in the south-eastern Transvaal. South African Journal of Botany 55, 171–177.
Morrey DR, Balkwill K, Balkwill M-J, Williamson S (1992) A review of some studies of the serpentine flora of southern Africa. In ‘The vegetation of ultramafic (serpentine) soils’. (Eds AJM Baker, J Proctor, RD Reeves) pp. 147–155. (Intercept: Andover, UK)
Murray CG (1969) The petrology of the ultramafic rocks of the Rockhampton district, Queensland. Geological Survey of Queensland 343, 1–13.
Nylander JAA (2004) ‘MrModeltest, v2.’ Program distributed by the author. (Evolutionary Biology Centre, Uppsala University: Uppsala, Sweden)
Pollard AJ, Powell KD, Harper FA, Smith JAC (2002) The genetic basis of metal hyperaccumulation in plants. Critical Reviews in Plant Sciences 21, 539–566.
| The genetic basis of metal hyperaccumulation in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlKitrY%3D&md5=a55d5d51c0b1abfa2ba492bf9456dd2eCAS |
Proctor J, Phillipps C, Duff GK, Heaney A, Robertson FM (1989) Ecological studies on Gunung Silam, a small ultrabasic mountain in Sabah, Malaysia. II. Some forest processes. Journal of Ecology 77, 317–331.
| Ecological studies on Gunung Silam, a small ultrabasic mountain in Sabah, Malaysia. II. Some forest processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXms1al&md5=3a37da21bf144cbdf8bb418322d457c7CAS |
Proctor AJ, van Balgooy MMJ, Fairweather GM, Nagy L, Reeves RD (1994) A preliminary re-investigation of a plant geographical ‘El Dorado’. Tropical Biodiversity 2, 303–316.
Rajakaruna N, Bohm BA (2002) Serpentine and its vegetation: a preliminary study from Sri Lanka. Journal of Applied Botany 76, 20–28.
Ratajkoski M, Huleatt MB, Jaques AL, Jaireth S, Towner R (2005) ‘Mineral density map – Nickel deposits, occurrences, and potential.’ (Geoscience Australia: Canberra)
Reeves RD (1988) Nickel and zinc accumulation by species of Thlaspi L., Cochlearia L., and other genera of the Brassicaceae. Taxon 37, 309–318.
| Nickel and zinc accumulation by species of Thlaspi L., Cochlearia L., and other genera of the Brassicaceae.Crossref | GoogleScholarGoogle Scholar |
Reeves RD (1992) The hyperaccumulation of nickel by serpentine plants. In ‘The vegetation of ultramafic (serpentine) soils’. (Eds AJM Baker, J Proctor, RD Reeves) pp. 253–277. (Intercept: Andover, UK)
Reeves RD (2003) Tropical hyperaccumulators of metals and their potential for phytoextraction. Plant and Soil 249, 57–65.
| Tropical hyperaccumulators of metals and their potential for phytoextraction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsVyrs78%3D&md5=ae93b113c9cd88ffc21fd8139a44b59aCAS |
Reeves RD (2006) Hyperaccumulation of trace elements by plants. In ‘Phytoremediation of metal-contaminated soils, Nato science series (IV): earth and environmental sciences v. 68’. (Eds J-L Morel, G Echevarria, N Goncharova) pp. 25–52. (Springer: Dordrecht, The Netherlands)
Reeves RD, Adigüzel N (2004) Rare plants and nickel accumulators from Turkish serpentine soils, with special reference to Centaurea species. Turkish Journal of Biology 28, 147–153.
Reeves RD, Adigüzel N (2008) The nickel hyperaccumulating plants of the serpentines of Turkey and adjacent areas: a review with new data. Turkish Journal of Biology 32, 143–153.
Reeves RD, Baker AJM (2000) Metal-accumulating plants. In ‘Phytoremediation of toxic metals: using plants to clean up the environment’. (Eds I Raskin, BD Ensley) pp. 193–229. (John Wiley & Sons: New York)
Reeves RD, Brooks RR (1983) European species of Thlaspi L. (Cruciferae) as indicators of nickel and zinc. Journal of Geochemical Exploration 18, 275–283.
| European species of Thlaspi L. (Cruciferae) as indicators of nickel and zinc.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlsl2htbg%3D&md5=83766f7f0358e21fc16bb5ab8821a949CAS |
Reeves RD, Brooks RR, Press JR (1980) Nickel accumulation by species of Peltaria Jacq. (Cruciferae). Taxon 29, 629–633.
| Nickel accumulation by species of Peltaria Jacq. (Cruciferae).Crossref | GoogleScholarGoogle Scholar |
Reeves RD, Brooks RR, MacFarlane RM (1981) Nickel uptake by Californian Streptanthus and Caulanthus with particular reference to the hyperaccumulator S. polygaloides Gray (Brassicaceae). American Journal of Botany 68, 708–712.
| Nickel uptake by Californian Streptanthus and Caulanthus with particular reference to the hyperaccumulator S. polygaloides Gray (Brassicaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXktl2is7w%3D&md5=e6e244db8784971932e91844ca6b867fCAS |
Reeves RD, Brooks RR, Dudley TR (1983a) Uptake of nickel by species of Alyssum, Bornmuellera, and other genera of Old World tribus Alysseae. Taxon 32, 184–192.
| Uptake of nickel by species of Alyssum, Bornmuellera, and other genera of Old World tribus Alysseae.Crossref | GoogleScholarGoogle Scholar |
Reeves RR, MacFarlane RM, Brooks RR (1983b) Accumulation of nickel and zinc by western North American genera containing serpentine-tolerant species. American Journal of Botany 70, 1297–1303.
| Accumulation of nickel and zinc by western North American genera containing serpentine-tolerant species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXitVKltA%3D%3D&md5=ba0c86ce07e52a3a7144e9cbe97d58c1CAS |
Reeves RD, Baker AJM, Borhidi A, Berazaín R (1996) Nickel-accumulating plants from the ancient serpentine soils of Cuba. New Phytologist 133, 217–224.
| Nickel-accumulating plants from the ancient serpentine soils of Cuba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XkvFKlsLc%3D&md5=369a610a16d279fbcf1f16c967e37ce4CAS |
Reeves RD, Baker AJM, Borhidi A, Berazaín R (1999) Nickel hyperaccumulation in the serpentine flora of Cuba. Annals of Botany 83, 29–38.
| Nickel hyperaccumulation in the serpentine flora of Cuba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXht1ajsL4%3D&md5=306bbeb8069f9629cd5d55cdd6406dbfCAS |
Reeves RD, Baker AJM, Becquer T, Echevarria G, Miranda ZJG (2007) The flora and biogeochemistry of the ultramafic soils of Goiás state, Brazil. Plant and Soil 293, 107–119.
| The flora and biogeochemistry of the ultramafic soils of Goiás state, Brazil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltlaktbo%3D&md5=fcee606e08f241b9d18afe8febc88a94CAS |
Roberts BA (1992) Ecology of serpentinized areas, Newfoundland, Canada. In ‘The ecology of areas with serpentinized rocks. A world view’. (Eds BA Roberts, J Proctor) pp. 75–113. (Kluwer Academic Publishers: Dordrecht, The Netherlands)
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=e2562dfd1f8a647bdc0005ecf2b85e99CAS | 12912839PubMed |
Salt DE, Krämer U (2000) Mechanisms of metal hyperaccumulation in plants. In ‘Phytoremediation of toxic metals: using plants to clean up the environment’. (Eds I Raskin, BD Ensley) pp. 231–246. (John Wiley & Sons: New York)
Schmid M (1991) Phyllanthus. In ‘Flore de la Nouvelle-Calédonie et dépendances, v. 17, Euphorbiacées’. pp. 39–40. (Museum National d’Histoire Naturelle: Paris)
Severne BC (1974) Nickel accumulation by Hybanthus floribundus. Nature 248, 807–808.
| Nickel accumulation by Hybanthus floribundus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXks1Sku7g%3D&md5=8c8a0e27a175ff1b875e1d0857702fc8CAS | 4835556PubMed |
Severne BC, Brooks RR (1972) A nickel-accumulating plant from Western Australia. Planta 103, 91–94.
| A nickel-accumulating plant from Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38Xht1Gkurk%3D&md5=ebbc0c15ef2a5449c09f8828f554893cCAS |
Simmons MP, Savolainen V, Clevinger CC, Archer RH, Davis JI (2001) Phylogeny of the Celastraceae inferred from 26S nuclear ribosomal DNA, phytochrome B, rbcl, atpB, and morphology. Molecular Phylogenetics and Evolution 19, 353–366.
| Phylogeny of the Celastraceae inferred from 26S nuclear ribosomal DNA, phytochrome B, rbcl, atpB, and morphology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1Sgt7k%3D&md5=fcd7402f9298addca43b8b36bfee8179CAS | 11399146PubMed |
Simmons MP, Cappa JJ, Archer RH, Ford AJ, Eichstedt D, Clevinger CC (2008) Phylogeny of the Celastreae (Celastraceae) and the relationships of Catha edulis (qat) inferred from morphological characters and nuclear and plastid genes. Molecular Phylogenetics and Evolution 48, 745–757.
| Phylogeny of the Celastreae (Celastraceae) and the relationships of Catha edulis (qat) inferred from morphological characters and nuclear and plastid genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptVOhsro%3D&md5=4d7be36d27ba7ce29e8215933f60cf6fCAS | 18550389PubMed |
Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC, Dowd JM, Martin PG (1995) Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences, USA 92, 2647–2651.
| Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXksl2rs7o%3D&md5=c7ed480927566820ba7a7b594e5cb84aCAS |
Swofford DL (2000) ‘PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4.’ (Sinauer Associates: Sunderland, MA)
Taberlet P, Ludovic G, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology 17, 1105–1109.
| Universal primers for amplification of three non-coding regions of chloroplast DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xhslel&md5=5b634a841e3dedbe1cf2de3518260a0dCAS | 1932684PubMed |
Vergnano Gambi O, Gabbrielli R (1979) Ecophysiological and geochemical aspects of nickel, chromium and cobalt accumulation in the vegetation of some Italian ophiolitic outcrops. Ofioliti 4, 199–208.
Vergnano Gambi O, Gabbrielli R (1981) La composizione minerale della vegetazione degli affloramenti dell’alta Valle di Ayas. Revue Valdôtaine d’Historie Naturelle 35, 51–61.
Vergnano Gambi O, Brooks RR, Radford CC (1979) L’accumulo di nichel nelle specie italiane del genere Alyssum. Webbia 33, 269–277.
Vergnano Gambi O, Gabbrielli R, Pancaro L (1982) Nickel, chromium and cobalt in plants from Italian serpentine areas. Acta Oecologica 3, 291–306.
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In ‘PCR protocols: a guide to methods and applications’. (Eds MA Innis, DH Gelfand, JJ Sninsky, TJ White) pp. 315–322. (Academic Press: San Diego, CA)
Wild H (1970) Geobotanical anomalies in Rhodesia. 3. The vegetation of nickel bearing soils. Kirkia 7, 1–62.
Wild H (1974) Indigenous plants and chromium in Rhodesia. Kirkia 9, 233–241.
Wither ED, Brooks RR (1977) Hyperaccumulation of nickel by some plants of South-east Asia. Journal of Geochemical Exploration 8, 579–583.
| Hyperaccumulation of nickel by some plants of South-east Asia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXkslGjsw%3D%3D&md5=d8ec93243d4ff06148587252f25c6d8eCAS |
Zhang L-B, Simmons MP (2006) Phylogeny and delimitation of the Celastrales inferred from nuclear and plastid genes. Systematic Botany 31, 122–137.
| Phylogeny and delimitation of the Celastrales inferred from nuclear and plastid genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlsVensL4%3D&md5=3052db8b0ba00fd3b2f7f731d5e7b208CAS |
