A systematic assessment of the metallome of selected plant families in the Queensland (Australia) flora by using X-ray fluorescence spectroscopy
Imam Purwadi A , Farida Abubakari
A , Gillian K. Brown B , Peter D. Erskine A and Antony van der Ent A C *
+ Author Affiliations
- Author Affiliations
A Centre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, Brisbane, Qld 4072, Australia.
B Department of Environment and Science, Queensland Herbarium, Toowong, Qld 4066, Australia.
C Laboratory of Genetics, Wageningen University and Research, The Netherlands; and Laboratoire Sols et Environnement, INRAE, Université de Lorraine, France.
Australian Journal of Botany 71(4) 199-215 https://doi.org/10.1071/BT22028
Submitted: 17 March 2022 Accepted: 31 January 2023 Published: 5 May 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution 4.0 International License (CC BY)
Abstract
Context: Fewer than 10 plant species from Australia were known to hyperaccumulate metal(loid)s, despite metal-rich soils being widespread in Australia. By measuring herbarium specimens with non-destructive portable X-ray fluorescence spectroscopy (XRF) instrumentation their metal(loid)s concentrations can be determined, providing information that could be used to probe the evolution, biogeography, ecology, and physiology of plant species.
Aims: This study aimed to systematically measure herbarium specimens to obtain information on the prevailing concentrations of metal(loid)s in nearly 7000 plant specimens across seven plant families, and to link this data to an assessment of their spatial distribution.
Methods: The raw XRF spectrum of each herbarium specimen was processed using a new data-analysis pipeline recently validated for XRF data of herbarium specimens, to determine the concentrations of the first-row metal transition elements, and other detected elements. The collection localities of each of the herbarium specimens were plotted against rainfall and soil types to assess possible distributional patterns.
Key results: The results showed several newly discovered hyperaccumulator plant species, including 15 for manganese, two for nickel, three for cobalt, three for zinc, two for rare earth elements and one for selenium.
Conclusions and implications: Australia has more hyperaccumulator plant species than previously known and the XRF analysis of herbarium specimens is a powerful tool for their discovery. This research presents a new value proposition for the continued funding of herbarium collections in Australia and could initiate a range of research opportunities to use these data for future studies of plant evolution and adaptation.
Keywords: biogeography, cobalt, herbarium collection, hyperaccumulators, manganese, nickel, phylogenetic diversity, XRF technology, zinc.
References
Abubakari F, Nkrumah PN, Erskine PD, Brown GK, Fernando DR, Echevarria G, van der Ent A (2021a) Manganese (hyper)accumulation within Australian Denhamia (Celastraceae): an assessment of the trait and manganese accumulation under controlled conditions. Plant and Soil 463, 205–223.| Manganese (hyper)accumulation within Australian Denhamia (Celastraceae): an assessment of the trait and manganese accumulation under controlled conditions.Crossref | GoogleScholarGoogle Scholar |
Abubakari F, Nkrumah PN, Fernando DR, Brown GK, Erskine PD, Echevarria G, van der Ent A (2021b) Incidence of hyperaccumulation and tissue-level distribution of manganese, cobalt, and zinc in the genus Gossia (Myrtaceae). Metallomics 13, mfab008
| Incidence of hyperaccumulation and tissue-level distribution of manganese, cobalt, and zinc in the genus Gossia (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Abubakari F, Nkrumah PN, Fernando DR, Erskine PD, van der Ent A (2022) Manganese accumulation and tissue-level distribution in Australian Macadamia (Proteaceae) species. Environmental and Experimental Botany 193, 104668
| Manganese accumulation and tissue-level distribution in Australian Macadamia (Proteaceae) species.Crossref | GoogleScholarGoogle Scholar |
Australian Bureau of Meteorology (2020) Decadal and multi-decadal rainfall. Available at http://www.bom.gov.au/jsp/ncc/climate_averages/decadal-rainfall/index.jsp?maptype=6&period=7605&product=totals#maps
Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements – a review of their distribution, ecology and phytochemistry. Biorecovery 1, 81–126.
Batianoff GN, Reeves RD, Specht RL (1990) Stackhousia tryonii Bailey: a nickel-accumulating serpentine-endemic species of Central Queensland. Australian Journal of Botany 38, 121–130.
| Stackhousia tryonii Bailey: a nickel-accumulating serpentine-endemic species of Central Queensland.Crossref | GoogleScholarGoogle Scholar |
Batianoff GN, Neldner VJ, Singh S (2000) Vascular plant census and floristic analysis of serpentine landscapes in central Queensland. Proceedings of the Royal Society of Queensland 109, 1–30.
Belloeil C, Jouannais P, Malfaisan C, Reyes Fernández R, Lopez S, Navarrete Gutierrez DM, Maeder-Pras S, Villanueva P, Tisserand R, Gallopin M, Alfonso-Gonzalez D, Fuentes Marrero IM, Muller S, Invernon V, Pillon Y, Echevarria G, Berazaín Iturralde R, Merlot S (2021) The X-ray fluorescence screening of multiple elements in herbarium specimens from the Neotropical region reveals new records of metal accumulation in plants. Metallomics 13, mfab045
| The X-ray fluorescence screening of multiple elements in herbarium specimens from the Neotropical region reveals new records of metal accumulation in plants.Crossref | GoogleScholarGoogle Scholar |
Broadhurst L, Coates D (2017) Plant conservation in Australia: current directions and future challenges. Plant Diversity 39, 348–356.
| Plant conservation in Australia: current directions and future challenges.Crossref | GoogleScholarGoogle Scholar |
Brown GK (2021) Introduction to the census of the Queensland flora 2021. (Queensland Government: Brisbane, Qld, Australia) Available at https://www.data.qld.gov.au/dataset/census-of-the-queensland-flora-2020
Brown GK, Bostock PD (2020) ‘Introduction to the census of the Queensland flora 2020.’ (Queensland Department of Environment and Science, Queensland Government, Australia)
Chapman AD (2009) ‘Numbers of living species in Australia and the world.’ (Australian Biodiversity Information Services: Toowoomba. Qld, Australia)
Currie LA (1968) Limits for qualitative detection and quantitative determination. Application to radiochemistry. Analytical Chemistry 40, 586–593.
| Limits for qualitative detection and quantitative determination. Application to radiochemistry.Crossref | GoogleScholarGoogle Scholar |
Dalcorso G, Manara A, Piasentin S, Furini A (2014) Nutrient metal elements in plants. Metallomics 6, 1770–1788.
| Nutrient metal elements in plants.Crossref | GoogleScholarGoogle Scholar |
Do C, Abubakari F, Remigio AC, Brown GK, Casey LW, Burtet-Sarramegna V, Gei V, Erskine PD, van der Ent A (2020) A preliminary survey of nickel, manganese and zinc (hyper)accumulation in the flora of Papua New Guinea from herbarium X-ray fluorescence scanning. Chemoecology 30, 1–13.
| A preliminary survey of nickel, manganese and zinc (hyper)accumulation in the flora of Papua New Guinea from herbarium X-ray fluorescence scanning.Crossref | GoogleScholarGoogle Scholar |
Edwards NP, Manning PL, Bergmann U, Larson PL, Van Dongen BE, Sellers WI, Webb SM, Sokaras D, Alonso-Mori R, Ignatyev K, Barden HE, Van Veelen A, Anné J, Egerton VM, Wogelius RA (2014) Leaf metallome preserved over 50 million years. Metallomics 6, 774–782.
| Leaf metallome preserved over 50 million years.Crossref | GoogleScholarGoogle Scholar |
Erskine P, van der Ent A, Fletcher A (2012) Sustaining metal-loving plants in mining regions. Science 337, 1172–1173.
| Sustaining metal-loving plants in mining regions.Crossref | GoogleScholarGoogle Scholar |
Fernando DR, Marshall AT, Forster PI, Hoebee SE, Siegele R (2013) Multiple metal accumulation within a manganese-specific genus. American Journal of Botany 100, 690–700.
| Multiple metal accumulation within a manganese-specific genus.Crossref | GoogleScholarGoogle Scholar |
Fernando DR, Marshall AT, Green PT (2018) Cellular ion interactions in two endemic tropical rainforest species of a novel metallophytic tree genus. Tree Physiology 38, 119–128.
| Cellular ion interactions in two endemic tropical rainforest species of a novel metallophytic tree genus.Crossref | GoogleScholarGoogle Scholar |
Gei V, Isnard S, Erskine PD, Echevarria G, Fogliani B, Jaffré T, Van Der Ent A (2020) A systematic assessment of the occurrence of trace element hyperaccumulation in the flora of New Caledonia. Botanical Journal of the Linnean Society 194, 1–22.
| A systematic assessment of the occurrence of trace element hyperaccumulation in the flora of New Caledonia.Crossref | GoogleScholarGoogle Scholar |
Greve M, Lykke AM, Fagg CW, Gereau RE, Lewis GP, Marchant R, Marshall AR, Ndayishimiye J, Bogaert J, Svenning J-C (2016) Realising the potential of herbarium records for conservation biology. South African Journal of Botany 105, 317–323.
| Realising the potential of herbarium records for conservation biology.Crossref | GoogleScholarGoogle Scholar |
Heberling JM, Prather LA, Tonsor SJ (2019) The changing uses of herbarium data in an era of global change: an overview using automated content analysis. BioScience 69, 812–822.
| The changing uses of herbarium data in an era of global change: an overview using automated content analysis.Crossref | GoogleScholarGoogle Scholar |
Kalnicky DJ, Singhvi R (2001) Field portable XRF analysis of environmental samples. Journal of Hazardous Materials 83, 93–122.
| Field portable XRF analysis of environmental samples.Crossref | GoogleScholarGoogle Scholar |
Krämer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Letters 581, 2263–2272.
| Transition metal transport.Crossref | GoogleScholarGoogle Scholar |
Lahner B, Gong J, Mahmoudian M, Smith EL, Abid KB, Rogers EE, Guerinot ML, Harper JF, Ward JM, McIntyre L, Schroeder JI, Salt DE (2003) Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nature Biotechnology 21, 1215–1221.
| Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Markowicz A, Haselberger N (2004) XRF analysis of intermediate thickness samples. In ‘Quantifying uncertainty in nuclear analytical measurements’. (International Atomic Energy Agency: Vienna, Austria)
McCartha GL, Taylor CM, van der Ent A, Echevarria G, Navarrete Gutiérrez DM, Pollard AJ (2019) Phylogenetic and geographic distribution of nickel hyperaccumulation in neotropical Psychotria. American Journal of Botany 106, 1377–1385.
| Phylogenetic and geographic distribution of nickel hyperaccumulation in neotropical Psychotria.Crossref | GoogleScholarGoogle Scholar |
Peñuelas J, Fernández-Martínez M, Ciais P, Jou D, Piao S, Obersteiner M, Vicca S, Janssens IA, Sardans J (2019) The bioelements, the elementome, and the biogeochemical niche. Ecology 100, e02652
| The bioelements, the elementome, and the biogeochemical niche.Crossref | GoogleScholarGoogle Scholar |
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 |
Purwadi I, Gei V, Echevarria G, Erskine PD, Mesjasz-Przybyłowicz J, Przybyłowicz WJ, van der Ent A (2021) Tools for the discovery of hyperaccumulator plant species in the field and in the herbarium. In ‘Agromining: farming for metals’. (Eds A van der Ent, AJ Baker, G Echevarria, MO Simonnot, JL Morel) pp. 183–195. (Springer) https://doi.org/10.1007/978-3-030-58904-2_9
Purwadi I, Casey LW, Ryan CG, Erskine PD, van der Ent A (2022) X-ray fluorescence spectroscopy for analysis of the Ionome of herbarium specimens. Plant Methods 18, 139. https://doi.org/10.1186/s13007-022-00958-z
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 |
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, MA, USA)
Reeves RD, Laidlaw WS, Doronila A, Baker AJM, Batianoff (the late) GN (2015) Erratic hyperaccumulation of nickel, with particular reference to the Queensland serpentine endemic Pimelea leptospermoides. Australian Journal of Botany 63, 119–127.
| Erratic hyperaccumulation of nickel, with particular reference to the Queensland serpentine endemic Pimelea leptospermoides.Crossref | GoogleScholarGoogle Scholar |
Reeves RD, Baker AJM, Jaffré T, Erskine PD, Echevarria G, van der Ent A (2018a) A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytologist 218, 407–411.
| A global database for plants that hyperaccumulate metal and metalloid trace elements.Crossref | GoogleScholarGoogle Scholar |
Reeves RD, van der Ent A, Baker AJM (2018b) Global distribution and ecology of hyperaccumulator plants. In ‘Agromining: farming for metals’. (Eds A Van Der Ent, G Echevarria, A Baker, J Morel) pp. 75–92. (Springer: Cham, Switzerland) https://doi.org/10.1007/978-3-319-61899-9_5
Ryan CG (2000) Quantitative trace element imaging using PIXE and the nuclear microprobe. International Journal of Imaging Systems and Technology 11, 219–230.
| Quantitative trace element imaging using PIXE and the nuclear microprobe.Crossref | GoogleScholarGoogle Scholar |
Ryan CG, Clayton E, Griffin WL, Sie SH, Cousens DR (1988) SNIP, a statistics-sensitive background treatment for the quantitative analysis of PIXE spectra in geoscience applications. Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms 34, 396–402.
| SNIP, a statistics-sensitive background treatment for the quantitative analysis of PIXE spectra in geoscience applications.Crossref | GoogleScholarGoogle Scholar |
Ryan CG, Etschmann BE, Vogt S, Maser J, Harland CL, Van Achterbergh E, Legnini D (2005) Nuclear microprobe – Synchrotron synergy: towards integrated quantitative real-time elemental imaging using PIXE and SXRF. Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms 231, 183–188.
| Nuclear microprobe – Synchrotron synergy: towards integrated quantitative real-time elemental imaging using PIXE and SXRF.Crossref | GoogleScholarGoogle Scholar |
Ryan CG, Laird JS, Fisher LA, Kirkham R, Moorhead GF (2015) Improved dynamic analysis method for quantitative PIXE and SXRF element imaging of complex materials. Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms 363, 42–47.
| Improved dynamic analysis method for quantitative PIXE and SXRF element imaging of complex materials.Crossref | GoogleScholarGoogle Scholar |
Searle R (2021) ‘Australian Soil Classification Map.’ (Terrestrial Ecosystem Research Network)
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 |
Sherman J (1955) The theoretical derivation of fluorescent X-ray intensities from mixtures. Spectrochimica Acta 7, 283–306.
| The theoretical derivation of fluorescent X-ray intensities from mixtures.Crossref | GoogleScholarGoogle Scholar |
Souza ENF, Hawkins JA (2017) Comparison of herbarium label data and published medicinal use: herbaria as an underutilized source of ethnobotanical information. Economic Botany 71, 1–12.
| Comparison of herbarium label data and published medicinal use: herbaria as an underutilized source of ethnobotanical information.Crossref | GoogleScholarGoogle Scholar |
Tang RH, Erskine PD, Nkrumah PN, Echevarria G, van der Ent A (2022) Soil–plant relationships of metallophytes of the zinc–lead–copper Dugald River gossan, Queensland, Australia. Plant and Soil 471, 227–245.
| Soil–plant relationships of metallophytes of the zinc–lead–copper Dugald River gossan, Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |
Taylor SR, McLennan SM (1995) The geochemical evolution of the continental crust. Reviews of Geophysics 33, 241–265.
| The geochemical evolution of the continental crust.Crossref | GoogleScholarGoogle Scholar |
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 |
van der Ent A, Jaffré T, L’Huillier L, Gibson N, Reeves RD (2015) The flora of ultramafic soils in the Australia–Pacific region: state of knowledge and research priorities. Australian Journal of Botany 63, 173–190.
| The flora of ultramafic soils in the Australia–Pacific region: state of knowledge and research priorities.Crossref | GoogleScholarGoogle Scholar |
van der Ent A, Echevarria G, Pollard AJ, Erskine PD (2019a) X-Ray fluorescence ionomics of herbarium collections. Scientific Reports 9, 4746
| X-Ray fluorescence ionomics of herbarium collections.Crossref | GoogleScholarGoogle Scholar |
van der Ent A, Ocenar A, Tisserand R, Sugau JB, Echevarria G, Erskine PD (2019b) Herbarium X-ray fluorescence screening for nickel, cobalt and manganese hyperaccumulator plants in the flora of Sabah (Malaysia, Borneo Island). Journal of Geochemical Exploration 202, 49–58.
| Herbarium X-ray fluorescence screening for nickel, cobalt and manganese hyperaccumulator plants in the flora of Sabah (Malaysia, Borneo Island).Crossref | GoogleScholarGoogle Scholar |
van der Ent A, Echevarria G, Nkrumah PN, Erskine PD (2020) Frequency distribution of foliar nickel is bimodal in the ultramafic flora of Kinabalu Park (Sabah, Malaysia). Annals of Botany 126, 1017–1027.
| Frequency distribution of foliar nickel is bimodal in the ultramafic flora of Kinabalu Park (Sabah, Malaysia).Crossref | GoogleScholarGoogle Scholar |
Whiting SN, Reeves RD, Richards D, Johnson MS, Cooke JA, Malaisse F, Paton A, Smith JAC, Angle JS, Chaney RL, Ginocchio R, Jaffré T, Johns R, Mcintyre T, Purvis OW, Salt DE, Schat H, Zhao FJ, Baker AJM (2004) Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation. Restoration Ecology 12, 106–116.
| Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation.Crossref | GoogleScholarGoogle Scholar |
Wickham H (2009) ‘ggplot2: elegant graphics for data analysis.’ (Springer-Verlag)
