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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Nickel hyperaccumulation in populations of Psychotria grandis (Rubiaceae) from serpentine and non-serpentine soils of Puerto Rico

Rachel L. McAlister A , Duane A. Kolterman B and A. Joseph Pollard A C
+ Author Affiliations
- Author Affiliations

A Department of Biology, Furman University, Greenville, 3300 Poinsett Hwy, SC 29613, USA.

B Departamento de Biología, Universidad de Puerto Rico, Mayagüez, PR 00680, USA.

C Corresponding author. Email: joe.pollard@furman.edu

Australian Journal of Botany 63(2) 85-91 https://doi.org/10.1071/BT14337
Submitted: 9 December 2014  Accepted: 19 February 2015   Published: 5 May 2015

Abstract

Metal hyperaccumulators are plants that store heavy metals or metalloids in their leaves, often to concentrations much higher than in the soil. Though most occur exclusively on metalliferous soils, some species are facultative, occurring on both metalliferous and nonmetalliferous soils. Psychotria grandis Sw.(Rubiaceae) occurs from Central America through the Caribbean on many soil types, and hyperaccumulates nickel (Ni) on serpentine soils in several localities. In this study, four Puerto Rican populations of P. grandis – two from serpentine soil and two from non-serpentine soil – were examined to compare Ni accumulation between and within populations. Multiple trees were sampled at most sites, with replicate leaves harvested from each tree. Foliar nickel concentrations were measured by atomic absorption spectrometry. Mean Ni concentration differed significantly among the sites, ranging from <165 µg g–1 on non-serpentine soil to >4000 µg g–1 on serpentine soil. There were also significant differences in Ni concentration among trees within sites, with especially wide variation at one of the serpentine sites known to be geologically heterogeneous. Despite these differences in field-collected leaves, a hydroponic common-garden experiment indicated that the Ni accumulation capacities of the populations were approximately equal. Variation in Ni accumulation between and within these populations in the field is likely to result from variation in Ni availability in the soil.

Additional keywords: facultative hyperaccumulator, intraspecific variation, serpentine soil.


References

Assunção AGL, da Costa Martins P, de Folter S, Vooijs R, Schat H, Aarts MGM (2001) Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant, Cell & Environment 24, 217–226.
Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens.Crossref | GoogleScholarGoogle Scholar |

Assunção AGL, ten Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytologist 159, 411–419.
Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types.Crossref | GoogleScholarGoogle Scholar |

Baker AJM (1981) Accumulators and excluders – strategies in the response of plants to heavy metals. Journal of Plant Nutrition 3, 643–654.
Accumulators and excluders – strategies in the response of plants to heavy metals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhtlemsb8%3D&md5=9707e416a2ab60f6f789d040320dd3dcCAS |

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 soils and waters’. (Eds N Terry, G Bañuelos) pp. 85–107. (CRC Press: Boca Raton, FL, USA)

Bert V, Macnair MR, de Laguerie P, Saumitou-Laprade P, Petit D (2000) Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae). New Phytologist 146, 225–233.
Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktlGlsL0%3D&md5=fb4a0aaa5076843a007fc7a2443a33b9CAS |

Boyd RS, Martens SN (1998) Nickel hyperaccumulation of Thlaspi montanum var. montanum (Brassicaceae): a constitutive trait. American Journal of Botany 85, 259–265.
Nickel hyperaccumulation of Thlaspi montanum var. montanum (Brassicaceae): a constitutive trait.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitFeisb4%3D&md5=ee5ec6235e7ef85843d5fccdb04ce3c0CAS |

Boyd RS, Jaffre T, Odom JW (1999) Variation in nickel content in the nickel-hyperaccumulating shrub Psychotria douarrei (Rubiaceae) from New Caledonia. Biotropica 31, 403–410.
Variation in nickel content in the nickel-hyperaccumulating shrub Psychotria douarrei (Rubiaceae) from New Caledonia.Crossref | GoogleScholarGoogle Scholar |

Brady KU, Kruckeberg AR, Bradshaw HD (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annual Review of Ecology Evolution and Systematics 36, 243–266.
Evolutionary ecology of plant adaptation to serpentine soils.Crossref | GoogleScholarGoogle Scholar |

Campbell LR, Stone CO, Shamsedin NM, Kolterman DA, Pollard AJ (2013) Facultative hyperaccumulation of nickel in Psychotria grandis (Rubiaceae). Caribbean Naturalist 1, 1–8.

van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: Facts and fiction. Plant and Soil 362, 319–334.
Hyperaccumulators of metal and metalloid trace elements: Facts and fiction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2ks7bF&md5=bee356700f51fe2ae7218429ac2a5674CAS |

Gall JE, Rajakaruna N (2013) The physiology, functional genomics, and applied ecology of heavy metal-tolerant Brassicaceae. In ‘Brassicaceae’. (Ed. M Lang) pp. 121–148. (Nova Science Publishers: Hauppauge, NY, USA)

Geology of Puerto Rico (2014) Department of the Interior, US Geological Survey. Available at http://mrdata.usgs.gov/geology/pr/ [Verified 7 December 2014]

Hamilton CW (1989) A revision of Mesoamerican Psychotria subgenus Psychotria (Rubiaceae), part I: Introduction and species 1–16. Annals of the Missouri Botanical Garden 76, 67–111.
A revision of Mesoamerican Psychotria subgenus Psychotria (Rubiaceae), part I: Introduction and species 1–16.Crossref | GoogleScholarGoogle Scholar |

Harrison SP, Rajakaruna N, Eds. (2011) ‘Serpentine: the evolution and ecology of a model system.’ (University of California Press: Berkeley, CA, USA)

Hewitt EJ, Smith TA (1975) ‘Plant mineral nutrition.’ (English Universities Press: London)

Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular 347, 1–32.

Krämer U (2010) Metal hyperaccumulation in plants. Annual Review of Plant Biology 61, 517–534.
Metal hyperaccumulation in plants.Crossref | GoogleScholarGoogle Scholar | 20192749PubMed |

Laó-Dávila DA, Llerandi-Román PA, Anderson TH (2012) Cretaceous-Paleogene thrust emplacement of serpentinite in southwestern Puerto Rico. Geological Society of America Bulletin 124, 1169–1190.
Cretaceous-Paleogene thrust emplacement of serpentinite in southwestern Puerto Rico.Crossref | GoogleScholarGoogle Scholar |

Meerts P, Van Isacker N (1997) Heavy metal tolerance and accumulation in metallicolous and non-metallicolus populations of Thlaspi caerulescens from continental Europe. Plant Ecology 133, 221–231.
Heavy metal tolerance and accumulation in metallicolous and non-metallicolus populations of Thlaspi caerulescens from continental Europe.Crossref | GoogleScholarGoogle Scholar |

Milner MJ, Mitani-Ueno N, Yamaji N, Yokosho K, Craft E, Fei Z, Ebbs S, Zambrano MC, Ma JF, Kochian LV (2014) Root and shoot transcriptome analysis of two ecotypes of Noccaea caerulescens uncovers the role of NcNramp1 in Cd hyperaccumulation. The Plant Journal 78, 398–410.
Root and shoot transcriptome analysis of two ecotypes of Noccaea caerulescens uncovers the role of NcNramp1 in Cd hyperaccumulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmslWrs7s%3D&md5=19d7aed9c535202d3a9ce3dc55ae3bbbCAS | 24547775PubMed |

Ni WZ, Yang XE, Long XX (2004) Comparative studies on zinc tolerance and accumulation between two ecotypes of Sedum alfredii Hance in southeastern China. Journal of Plant Nutrition 27, 627–635.
Comparative studies on zinc tolerance and accumulation between two ecotypes of Sedum alfredii Hance in southeastern China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitFyns70%3D&md5=fdf81ab52614257ec63ea7ffc4ffd7e9CAS |

O’Dell RE, Rajakaruna N (2011) Intraspecific variation, adaptation, and evolution. In ‘Serpentine: the evolution and ecology of a model system’. (Eds Harrison SP, Rajakaruna N) pp. 97–137. (University of California Press: Berkeley, CA, USA)

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=1f35252d72dceb6303f6133d8195f9aaCAS |

Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Science 217–218, 8–17.
Facultative hyperaccumulation of heavy metals and metalloids.Crossref | GoogleScholarGoogle Scholar | 24467891PubMed |

Pošćić F, Marchiol L, Schat H (2013) Hyperaccumulation of thallium is population-specific and uncorrelated with caesium accumulation in the thallium hyperaccumulator, Biscutella laevigata. Plant and Soil 365, 81–91.
Hyperaccumulation of thallium is population-specific and uncorrelated with caesium accumulation in the thallium hyperaccumulator, Biscutella laevigata.Crossref | GoogleScholarGoogle Scholar |

Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Science 180, 169–181.
Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1agtLzI&md5=a615763f6fdee05c050f18799e229d68CAS | 21421358PubMed |

Reeves RD (1992) 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=3aa4a3b1fccc31b40f8804ddaf3af344CAS |

Reeves RD, Baker AJM (1984) Studies on metal uptake by plants from serpentine and nonserpentine populations of Thlaspi goesingense Halacsy (Cruciferae). New Phytologist 98, 191–204.
Studies on metal uptake by plants from serpentine and nonserpentine populations of Thlaspi goesingense Halacsy (Cruciferae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXltVSi&md5=a016df19f9b51396f677934fbd616bdbCAS |

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. (Wiley & Sons: New York)

Reeves RD, Baker AJM, Borhidi A, Berazain 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=fd3caffb6a094cdb888125308d3bafd7CAS |

Reeves RD, Baker AJM, Borhidi A, Berazain 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=6f1477942217c49230dce50fdbfcb529CAS |

Reeves RD, Schwartz C, Morel JL, Edmondson J (2001) Distribution and metal-accumulating behaviour of Thlaspi caerulescens and associated metallophytes in France. International Journal of Phytoremediation 3, 145–172.
Distribution and metal-accumulating behaviour of Thlaspi caerulescens and associated metallophytes in France.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFSit7c%3D&md5=99223f13616e226dafdf3732171c5206CAS |

Richau KH, Schat H (2009) Intraspecific variation of nickel and zinc accumulation and tolerance in the hyperaccumulator Thlaspi caerulescens. Plant and Soil 314, 253–262.
Intraspecific variation of nickel and zinc accumulation and tolerance in the hyperaccumulator Thlaspi caerulescens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVOgsLjO&md5=cc55bde0187edfa27048554798a17b51CAS |

Wright JW, Stanton ML (2011) Local adaptation in heterogeneous landscapes: reciprocal transplant experiments and beyond. In ‘Serpentine: the evolution and ecology of a model system’. (Eds SP Harrison, N Rajakaruna) pp. 97–137. (University of California Press: Berkeley, CA, USA)

Xing JP, Jiang RF, Ueno D, Ma JF, Schat H, McGrath SP, Zhao FJ (2008) Variation in root-to-shoot translocation of cadmium and zinc among different accessions of the hyperaccumulators Thlaspi caerulescens and Thlaspi praecox. New Phytologist 178, 315–325.
Variation in root-to-shoot translocation of cadmium and zinc among different accessions of the hyperaccumulators Thlaspi caerulescens and Thlaspi praecox.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXls1Gqt78%3D&md5=2cd62bc882ea236a8b38a2e20981b3efCAS | 18266619PubMed |

Xue SG, Chen YX, Baker AJM, Reeves RD, Xu XH, Lin Q (2005) Manganese uptake and accumulation by two populations of Phytolacca acinosa Roxb. (Phytolaccaceae). Water, Air, and Soil Pollution 160, 3–14.
Manganese uptake and accumulation by two populations of Phytolacca acinosa Roxb. (Phytolaccaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsFegsrk%3D&md5=549f0690320f02989e541b464cf3d8f7CAS |

Yusuf M, Fariduddin Q, Hayat S, Ahmad A (2011) Nickel: an overview of uptake, essentiality and toxicity in plants. Bulletin of Environmental Contamination and Toxicology 86, 1–17.
Nickel: an overview of uptake, essentiality and toxicity in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjtFCnsg%3D%3D&md5=7fd8a249a84684ec798f30d05c1acbc0CAS | 21170705PubMed |

Zhang M, Senoura T, Yang X, Nishizawa NK (2011) Functional analysis of metal tolerance proteins isolated from Zn/Cd hyperaccumulating ecotype and non-hyperaccumulating ecotype of Sedum alfredii Hance. FEBS Letters 585, 2604–2609.
Functional analysis of metal tolerance proteins isolated from Zn/Cd hyperaccumulating ecotype and non-hyperaccumulating ecotype of Sedum alfredii Hance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVait7nE&md5=46d63d8f7bc534fa2b920e8ebde7a6cfCAS | 21781966PubMed |