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Blepharidium guatemalense, an obligate nickel hyperaccumulator plant from non-ultramafic soils in Mexico

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Abstract

Nickel hyperaccumulation in Blepharidium guatemalense Standl. (Rubiaceae) was found in the tropical forests of south-eastern Mexico. This study aimed to document the geographic extent of nickel hyperaccumulation in this species, to understand its process of hyperaccumulation and to explore nickel distribution within the tissues of this plant. To accomplish these objectives, a complete non-destructive elemental screening of herbarium specimens was performed with a hand-held X-ray fluorescence spectrometer. Besides, rhizosphere soils and plant tissues were collected in Mexico and analyzed for physical–chemical parameters. Finally, elemental distribution maps of nickel and other elements in plant tissues were obtained by X-ray fluorescence spectroscopy and microscopy. This study revealed that Blepharidium guatemalense is distributed throughout Chiapas, Tabasco and Campeche, reaching the maximum nickel concentration in leaves (4.3 wt%) followed by roots and seeds (2.0 wt%) and bark (1.8 wt%). Simultaneous hyperaccumulation of cobalt and nickel was found in 15% of the herbarium specimens. Blepharidium guatemalense has uncommon re-distribution mechanisms via phloem since this tissue is the highest nickel-enriched from all parts of the plant (from roots to leaves). A high total nickel (mean of 610 µg g−1) was found in rhizosphere soils even though no evidence of ophiolite emplacement in that area has been reported. Blepharidium guatemalense represents the first hypernickelophore (> 1 wt% Ni) to be reported as growing in soils that are neither ultramafic nor enriched by anthropogenic pollutants.

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Acknowledgements

The authors acknowledge the Centre National de la Recherche Scientifique (CNRS) in France through the X-LIFE Research Program for their financial support. In particular, they wish to thank Dr. Sylvain Merlot (IB2C, CNRS), scientific coordinator of the X-TREM project. The first author conveys her sincere gratitude to the Consejo Nacional de Ciencia y Tecnología (CONACyT) in Mexico and to the French National Research Agency, reference ANR-10-LABX-21—LABEX RESSOURCES21 for PhD funding. The Groupement d’Intérêt Scientifique sur les Friches Industrielles (GISFI) from the Université de Lorraine kindly supplied a hand-held XRF instrument. This research was partly undertaken at P06 at Deutsches Elektronen Synchrotron (DESY), a member of the Helmholtz Association (HGF). The research has been also supported by the project CALIPSOplus under the Grant Agreement 730872 from the EU Framework Programme for Research and Innovation HORIZON 2020. The micro-XRF instrumentation was co-funded by ICEEL (Carnot Institute)-CREGU-LabEX Ressources 21 (ANR-10-LABX 21-LABEX RESSOURCES 21) and FEDER. Special acknowledgments to MSc Blanca V. Juarez Jaimes (MEXU herbarium) for plant identification, to Ing. Francisco Navarrete Torralba for his valuable contribution to this research, to MSc. Jorge A. Ramírez Espinosa, and all the students from the Universidad Tecnológica de la Selva (UTS) (Nancy, Saúl, Sebastián, Simón, Moisés y Francisco) for their enormous help during field surveys. The authors are also grateful to Haley Disinger for the enrichment of the database (XRF screening data from the MO herbarium in Saint Louis), to Vanessa Invernon for her support at the Pherbarium (Muséum National d'Histoire Naturelle in Paris) and to all the technicians from MEXU herbarium for their valuable cooperation. We would like to thank Kathryn Spiers and Jan Garrevoet for their assistance during the experiments. We wish to thank Professor Alan Baker (The Universities of Melbourne and Queensland, Australia) for reviewing the paper and suggesting improvements to the text.

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Authors and Affiliations

  1. Laboratoire Sols et Environnement, Université de Lorraine, INRAE, 54000, Nancy, France

    Dulce Montserrat Navarrete Gutiérrez, Antony van der Ent & Guillaume Echevarria

  2. Universidad Autónoma Chapingo, 56230, Texcoco, Estado de México, Mexico

    Dulce Montserrat Navarrete Gutiérrez & Jesús A. Cuevas Sánchez

  3. Department of Biology, Furman University, Greenville, SC, 29613, USA

    A. Joseph Pollard

  4. Centre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, St Lucia, QLD, 4072, Australia

    Antony van der Ent & Guillaume Echevarria

  5. GeoRessources, Université de Lorraine, CNRS, 54000, Nancy, France

    Michel Cathelineau

  6. Laboratoire Réactions et Génie des Procédés, Université de Lorraine, CNRS, 54000, Nancy, France

    Marie-Noëlle Pons

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  1. Dulce Montserrat Navarrete Gutiérrez
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Navarrete Gutiérrez, D.M., Pollard, A.J., van der Ent, A. et al. Blepharidium guatemalense, an obligate nickel hyperaccumulator plant from non-ultramafic soils in Mexico. Chemoecology 31, 169–187 (2021). https://doi.org/10.1007/s00049-021-00338-4

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