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Metallomics Integrated Biometal Science Accepted Manuscript View Article Online View Journal Metallomics Integrated biometal science Accepted Manuscript This article can be cited before page numbers have been issued, to do this please use: A. Babst- Kostecka, W. J. Przybyowicz, A. van der Ent, C. G. Ryan, C. C. Dietrich and J. Mesjasz-Przybyowicz, Metallomics, 2019, DOI: 10.1039/C9MT00239A. Volume 10 Number 4 This is an Accepted Manuscript, which has been through the April 2018 Pages 515-652 Royal Society of Chemistry peer review process and has been Metallomics accepted for publication. Integrated biometal science Accepted Manuscripts are published online shortly after acceptance, rsc.li/metallomics before technical editing, formatting and proof reading. Using this free service, authors can make their results available to the community, in citable form, before we publish the edited article. We will replace this Accepted Manuscript with the edited and formatted Advance Article as soon as it is available. You can find more information about Accepted Manuscripts in the Information for Authors. Please note that technical editing may introduce minor changes to the text and/or graphics, which may alter content. The journal’s standard ISSN 1756-591X Terms & Conditions and the Ethical guidelines still apply. In no event PAPER Bin He, Ligang Hu et al. shall the Royal Society of Chemistry be held responsible for any errors Antibacterial mechanism of silver nanoparticles in Pseudomonas aeruginosa: proteomics approach or omissions in this Accepted Manuscript or any consequences arising from the use of any information it contains. rsc.li/metallomics Page 1 of 30 Metallomics 1 2 3 1 Endosperm prevents toxic amounts of Zn from accumulating in the seed embryoView Article Online 4 DOI: 10.1039/C9MT00239A 5 2 6 – an adaptation to metalliferous sites in metal-tolerant Biscutella laevigata 7 3 8 9 4 10 1 2,3 4,5 6 11 5 Alicja Babst-Kostecka , Wojciech J. Przybyłowicz , Antony van der Ent , Chris Ryan , Charlotte 12 6 Dietrich1, Jolanta Mesjasz-Przybyłowicz3 13 14 7 15 16 8 1 W. Szafer Institute of Botany, Polish Academy of Sciences, Department of Ecology, Lubicz 46, 31- 17 18 9 512 Krakow, Poland. 19 10 20 21 11 2AGH University of Science and Technology, Faculty of Physics & Applied Computer Science, 22 23 12 al. Mickiewicza 30, 30-059 Kraków, Poland. 24 25 13 26 14 3Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Manuscript 27 28 15 Matieland 7602, South Africa. 29 30 16 31 17 4Centre for Mined Land Rehabilitation, Sustainable Minerals Institute, 32 33 18 The University of Queensland, Australia. 34 35 19 36 Accepted 5 37 20 Laboratoire Sols et Environnement, Université de Lorraine, France. 38 21 39 40 22 6CSIRO, Mineral Resources, Australia. 41 Published on 07 November 2019. Downloaded by University of Queensland 11/10/2019 10:30:58 PM. 42 23 43 44 24 45 25 46 47 26 48 Metallomics 49 27 Corresponding author: 50 28 51 52 29 Alicja Babst-Kostecka 53 54 30 Tel: +48 12 424 17 04, Fax: +48 12 421 97 90 55 56 31 e-mail: [email protected] 57 32 58 59 33 60 1 Metallomics Page 2 of 30 1 2 3 View Article Online 4 34 Table of contents entry DOI: 10.1039/C9MT00239A 5 6 35 7 36 The pseudometallophyte Biscutella laevigata adapts to metalliferous soils by allocating excess 8 9 37 metal(loid)s to the endosperm (E) of seeds to protect embryonic tissues and improve reproductive 10 11 38 success. 12 39 13 40 14 MiSceroedscpohpoytoSmeiecrdogPriacptuhre SSeeeeddSschematiicc XFXMFM SeseededPmicatupre 15 0.6 16 Ca 0.5 17 E 0.4 18 Hi 19 C 0.3 20 0.2 21 T R 22 0.1 Hy 23 1000 μm wt% 24 41 25 26 Manuscript 27 28 29 30 31 32 33 34 35 36 Accepted 37 38 39 40 41 Published on 07 November 2019. Downloaded by University of Queensland 11/10/2019 10:30:58 PM. 42 43 44 45 46 47 48 Metallomics 49 50 51 52 53 54 55 56 57 58 59 60 2 Page 3 of 30 Metallomics 1 2 3 42 ABSTRACT View Article Online 4 DOI: 10.1039/C9MT00239A 5 43 Seed germination represents the first crucial stage in the life cycle of a plant, and the seed must 6 7 44 contain all necessary transition elements for the development and successful establishment of the 8 45 seedling. Problematically, seed development and germination are often hampered by elevated 9 10 46 metal(loid) concentrations in industrially polluted soils, making their revegetation a challenging task. 11 12 47 Biscutella laevigata L. (Brassicaceae) is a rare perennial pseudometallophyte that can tolerate high 13 14 48 concentrations of trace metal elements. Yet, the strategies of this and other plant species to ensure 15 49 reproductive success at metalliferous sites are poorly understood. Here we characterized several 16 17 50 parameters of germination and used synchrotron X-ray fluorescence microscopy to investigate the 18 19 51 spatial distribution and concentration of elements within B. laevigata seeds from two metallicolous 20 21 52 and two non-metallicolous populations. We find that average germination time was shorter and the 22 53 seed weight was lower in the metallicolous compared to the non-metallicolous populations. By 23 24 54 allowing for at least two generations within one growth season, relatively fast germination at 25 55 metalliferous sites accelerates microevolutionary processes and likely enhances the potential of 26 Manuscript 27 56 metallicolous accessions to adapt to environmental stress. We also identified different strategies of 28 29 57 elemental accumulation within seed tissues between populations. Particularly interesting patterns 30 31 58 were observed for zinc, which was found in 6-fold higher concentrations in the endosperm of 32 33 59 metallicolous compared to non-metallicolous populations. This indicates that the endosperm protects 34 60 the seed embryo from accumulating toxic concentrations of metal(loid)s, which likely improves 35 36 61 reproductive success. Hence, we conclude that elemental uptake regulation by the seed endosperm is Accepted 37 38 62 associated with enhanced metal tolerance and adaptation to metalliferous environments in B. 39 40 63 laevigata. 41 Published on 07 November 2019. Downloaded by University of Queensland 11/10/2019 10:30:58 PM. 64 42 43 65 Significance to Metallomics statement 44 45 66 Plants can only establish in metalliferous environments, if their reproduction is successful. Seeds 46 47 67 must therefore be protected from intoxication by excess metal(loid)s that are abundant in soils at Metallomics 48 68 industrial legacy sites. This study visualizes, quantifies, and compares the distribution of various 49 50 69 elements in Biscutella laevigata seeds from metalliferous and natural habitats. Interestingly, we 51 52 70 found that this species has developed a strategy to allocate zinc and other elements to non-harmful 53 54 71 sections of the seed, using them as a barrier to prevent the intoxication of sensitive parts. This 55 72 enhances our knowledge of how plants can adapt to and tolerate soil pollution. 56 57 58 59 60 3 Metallomics Page 4 of 30 1 2 3 74 1. INTRODUCTION View Article Online 4 DOI: 10.1039/C9MT00239A 5 75 The global industrial revolution has led to an unprecedented release of toxic substances into 6 1 7 76 the environment . The far-reaching consequences of this pollution include soil contamination with 8 77 hazardous waste, which threatens environmental and human health around the world. Among 9 10 78 pollutants, trace metal elements (including arsenic, As, cadmium, Cd, zinc, Zn, lead, Pb, and 11 12 79 thallium, Tl) are of major concern. Negative impacts can arise from direct contact with polluted soil 13 14 80 or ground water, or from ingestion via the food chain (soil-plant-human or soil-plant-animal-human), 15 81 reduction in food quality, and food insecurity resulting from reduced soil fertility and agricultural 16 17 82 production 2-4. Unlike organic contaminants, trace metal elements do not undergo microbial or 18 19 83 chemical degradation and may persist at elevated concentration in soils for a long time after their 20 5 21 84 dissemination . This is particularly problematic in soils in the vicinity of metalliferous mining and 22 85 smelter sites, where trace elements are continuously accumulated upon release 6. Hence, there is a 23 24 86 growing demand for cost-effective and environmentally friendly technologies to remediate 25 87 contaminated sites 7. Revegetation has drawn special attention as a promising “green and clean 26 Manuscript 27 88 technology” for intervention to toxic exposures 8. Plant establishment on mine tailings not only 28 29 89 mitigates hazards associated with wind dispersal of local contaminated dust, but every square meter 30 31 90 of vegetation can effectively remove up to 1 kg of dust per year from the air that moves across the 32 9 33 91 planted region . A lasting plant cover also helps immobilizing contaminants in the ground, with 34 92 positive effects on ground water quality 10, and provides important ecosystem services such as 35 36 93 carbon sequestration, intensified water cycling, and habitat for numerous species. Problematically, Accepted 37 38 94 most plants are sensitive to high soil trace metal element concentrations, which often inhibit seed 39 11-13 40 95 germination and plant growth on mine tailings . 41 Published on 07 November 2019. Downloaded by University of Queensland 11/10/2019 10:30:58 PM. 96 Only a limited number of vascular plant species called ‘metallophytes’ have developed the 42 43 97 ability to survive and reproduce in toxic metalliferous environments 14, 15.
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