Uncovering the physiology and distribution of thallium in Tl-hyperaccumulating and Tl-sensitive populations of Biscutella laevigata L.

Biscutella laevigata L bioconcentration intraspecific variation metal tolerance phytoextraction synchrotron-based micro-XRF (µXRF)

Journal

Annals of botany
ISSN: 1095-8290
Titre abrégé: Ann Bot
Pays: England
ID NLM: 0372347

Informations de publication

Date de publication:
28 Sep 2024
Historique:
received: 11 04 2024
medline: 28 9 2024
pubmed: 28 9 2024
entrez: 28 9 2024
Statut: aheadofprint

Résumé

Thallium (Tl) is extremely toxic to all lifeforms and an emerging pollutant. Plants in the Brassicaceae family, including edible crops, have an enhanced capacity for Tl accumulation, even from soils with low thallium concentration. The most extreme Tl hyperaccumulator is Biscutella laevigata, capable of attaining >32,000 μg Tl g-1 DW in its leaves. Biscutella laevigata from a non-metallicolous accession (Feltre, Italy) and a metallicolous accession (Les Malines, France) were subjected to a dosing experiment in hydroponics (0, 5, 30 μM Tl), followed by synchrotron-based µXRF analysis to elucidate tissue and cellular-level Tl distribution. Flow cytometric data on the two used accessions showed the Feltre accession has a genome size twice of that of the Les Malines accession (256 and 125 pg/2C respectively), suggesting they are phylogenetically distant populations. The Feltre accession does not accumulate Tl (125 μg Tl g-1 DW on average in leaves) at the 5 µM Tl dose level, whereas the Les Malines accession had a mean of 1750 μg Tl g-1 DW, with peaks of 24,130 μg Tl g-1 DW at the 30 µM Tl dose level. At 30 µM Tl the non-metallicolous accession did not grow, and at 5 µM Tl showed reduced biomasss compared to the metallicolous one. In Les Malines accession, the synchrotron-based µXRF analysis revealed that Tl is localised in the vacuoles of epidermal cells, especially underneath trichomes and in trichome basal cells. Thallium also occurs in solid crystalline deposits (3-5 µm in size, ~40 wt% Tl) that are mainly found in foliar margins and under trichome bases. Biscutella laevigata is an attractive model for studying Tl hypertolerance and hyperaccumulation on account of the extreme expression of this trait, and its marked intraspecific variability.

Sections du résumé

BACKGROUND AND AIMS OBJECTIVE
Thallium (Tl) is extremely toxic to all lifeforms and an emerging pollutant. Plants in the Brassicaceae family, including edible crops, have an enhanced capacity for Tl accumulation, even from soils with low thallium concentration. The most extreme Tl hyperaccumulator is Biscutella laevigata, capable of attaining >32,000 μg Tl g-1 DW in its leaves.
METHODS METHODS
Biscutella laevigata from a non-metallicolous accession (Feltre, Italy) and a metallicolous accession (Les Malines, France) were subjected to a dosing experiment in hydroponics (0, 5, 30 μM Tl), followed by synchrotron-based µXRF analysis to elucidate tissue and cellular-level Tl distribution.
KEY RESULTS RESULTS
Flow cytometric data on the two used accessions showed the Feltre accession has a genome size twice of that of the Les Malines accession (256 and 125 pg/2C respectively), suggesting they are phylogenetically distant populations. The Feltre accession does not accumulate Tl (125 μg Tl g-1 DW on average in leaves) at the 5 µM Tl dose level, whereas the Les Malines accession had a mean of 1750 μg Tl g-1 DW, with peaks of 24,130 μg Tl g-1 DW at the 30 µM Tl dose level. At 30 µM Tl the non-metallicolous accession did not grow, and at 5 µM Tl showed reduced biomasss compared to the metallicolous one. In Les Malines accession, the synchrotron-based µXRF analysis revealed that Tl is localised in the vacuoles of epidermal cells, especially underneath trichomes and in trichome basal cells. Thallium also occurs in solid crystalline deposits (3-5 µm in size, ~40 wt% Tl) that are mainly found in foliar margins and under trichome bases.
CONCLUSIONS CONCLUSIONS
Biscutella laevigata is an attractive model for studying Tl hypertolerance and hyperaccumulation on account of the extreme expression of this trait, and its marked intraspecific variability.

Identifiants

pubmed: 39340339
pii: 7786784
doi: 10.1093/aob/mcae115
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) 2024. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.

Auteurs

Mirko Salinitro (M)

Department of Biological Geological and Environmental Sciences, University of Bologna, Bologna, Italy.

Sandrine Isnard (S)

AMAP, Université de Montpellier, IRD, CIRAD, CNRS, INRAE, Montpellier, France.

Dennis Brueckner (D)

Deutsches Elektronen-Synchrotron DESY, Hamburg, Germany.

Kathryn M Spiers (KM)

Deutsches Elektronen-Synchrotron DESY, Hamburg, Germany.

Mark G M Aarts (MGM)

Laboratory of Genetics, Wageningen University and Research, Wageningen, The Netherlands.

Amelia Corzo Remigio (A)

Centre for Water in the Minerals Industry, Sustainable Minerals Institute, The University of Queensland, Brisbane, Australia.

Antony van der Ent (A)

Laboratory of Genetics, Wageningen University and Research, Wageningen, The Netherlands.

Classifications MeSH