Intraspecific Variation in Nickel Tolerance and Hyperaccumulation among Serpentine and Limestone Populations of <i>Odontarrhena serpyllifolia</i> (Brassicaceae: Alysseae) from the Iberian Peninsula

<i>Odontarrhena serpyllifolia</i> (Desf.) Jord. & Fourr. (=<i>Alyssum serpyllifolium</i> Desf.) occurs in the Iberian Peninsula and adjacent areas on a variety of soils including both limestone and serpentine (ultramafic) substrates. Populations endemic to serpentine are...

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Main Authors: A. Joseph Pollard, Grace L. McCartha, Celestino Quintela-Sabarís, Thomas A. Flynn, Maria K. Sobczyk, J. Andrew C. Smith
Format: Article
Language:English
Published: MDPI AG 2021-04-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/10/4/800
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author A. Joseph Pollard
Grace L. McCartha
Celestino Quintela-Sabarís
Thomas A. Flynn
Maria K. Sobczyk
J. Andrew C. Smith
author_facet A. Joseph Pollard
Grace L. McCartha
Celestino Quintela-Sabarís
Thomas A. Flynn
Maria K. Sobczyk
J. Andrew C. Smith
author_sort A. Joseph Pollard
collection DOAJ
description <i>Odontarrhena serpyllifolia</i> (Desf.) Jord. & Fourr. (=<i>Alyssum serpyllifolium</i> Desf.) occurs in the Iberian Peninsula and adjacent areas on a variety of soils including both limestone and serpentine (ultramafic) substrates. Populations endemic to serpentine are known to hyperaccumulate nickel, and on account of this remarkable phenotype have, at times, been proposed for recognition as taxonomically distinct subspecies or even species. It remains unclear, however, to what extent variation in nickel hyperaccumulation within this taxon merely reflects differences in the substrate, or whether the different populations show local adaptation to their particular habitats. To help clarify the physiological basis of variation in nickel hyperaccumulation among these populations, 3 serpentine accessions and 3 limestone accessions were cultivated hydroponically under common-garden conditions incorporating a range of Ni concentrations, along with 2 closely related non-accumulator species, <i>Clypeola jonthlaspi</i> L. and <i>Alyssum montanum</i> L. As a group, serpentine accessions of <i>O. serpyllifolia</i> were able to tolerate Ni concentrations approximately 10-fold higher than limestone accessions, but a continuous spectrum of Ni tolerance was observed among populations, with the least tolerant serpentine accession not being significantly different from the most tolerant limestone accession. Serpentine accessions maintained relatively constant tissue concentrations of Ca, Mg, K, and Fe across the whole range of Ni exposures, whereas in the limestone accessions, these elements fluctuated widely in response to Ni toxicity. Hyperaccumulation of Ni, defined here as foliar Ni concentrations exceeding 1g kg<sup>−1</sup> of dry biomass in plants not showing significant growth reduction, occurred in all accessions of <i>O. serpyllifolia</i>, but the higher Ni tolerance of serpentine accessions allowed them to hyperaccumulate more strongly. Of the reference species, <i>C. jonthlaspi</i> responded similarly to the limestone accessions of <i>O. serpyllifolia</i>, whereas <i>A. montanum</i> displayed by far the lowest degree of Ni tolerance and exhibited low foliar Ni concentrations, which only exceeded 1 g kg<sup>−1</sup> in plants showing severe Ni toxicity. The continuous spectrum of physiological responses among these accessions does not lend support to segregation of the serpentine populations of <i>O. serpyllifolia</i> as distinct species. However, the pronounced differences in degrees of Ni tolerance, hyperaccumulation, and elemental homeostasis observed among these accessions under common-garden conditions argues for the existence of population-level adaptation to their local substrates.
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spelling doaj.art-860a58627b0e499396447ea69575a5e22023-11-21T16:10:03ZengMDPI AGPlants2223-77472021-04-0110480010.3390/plants10040800Intraspecific Variation in Nickel Tolerance and Hyperaccumulation among Serpentine and Limestone Populations of <i>Odontarrhena serpyllifolia</i> (Brassicaceae: Alysseae) from the Iberian PeninsulaA. Joseph Pollard0Grace L. McCartha1Celestino Quintela-Sabarís2Thomas A. Flynn3Maria K. Sobczyk4J. Andrew C. Smith5Department of Biology, Furman University, Greenville, SC 29613, USADepartment of Biology, Furman University, Greenville, SC 29613, USADepartment of Soil Science and Agricultural Chemistry, University of Santiago de Compostela, CP 15782 Santiago de Compostela, SpainDepartment of Plant Sciences, University of Oxford, Oxford OX1 3RB, UKDepartment of Plant Sciences, University of Oxford, Oxford OX1 3RB, UKDepartment of Plant Sciences, University of Oxford, Oxford OX1 3RB, UK<i>Odontarrhena serpyllifolia</i> (Desf.) Jord. & Fourr. (=<i>Alyssum serpyllifolium</i> Desf.) occurs in the Iberian Peninsula and adjacent areas on a variety of soils including both limestone and serpentine (ultramafic) substrates. Populations endemic to serpentine are known to hyperaccumulate nickel, and on account of this remarkable phenotype have, at times, been proposed for recognition as taxonomically distinct subspecies or even species. It remains unclear, however, to what extent variation in nickel hyperaccumulation within this taxon merely reflects differences in the substrate, or whether the different populations show local adaptation to their particular habitats. To help clarify the physiological basis of variation in nickel hyperaccumulation among these populations, 3 serpentine accessions and 3 limestone accessions were cultivated hydroponically under common-garden conditions incorporating a range of Ni concentrations, along with 2 closely related non-accumulator species, <i>Clypeola jonthlaspi</i> L. and <i>Alyssum montanum</i> L. As a group, serpentine accessions of <i>O. serpyllifolia</i> were able to tolerate Ni concentrations approximately 10-fold higher than limestone accessions, but a continuous spectrum of Ni tolerance was observed among populations, with the least tolerant serpentine accession not being significantly different from the most tolerant limestone accession. Serpentine accessions maintained relatively constant tissue concentrations of Ca, Mg, K, and Fe across the whole range of Ni exposures, whereas in the limestone accessions, these elements fluctuated widely in response to Ni toxicity. Hyperaccumulation of Ni, defined here as foliar Ni concentrations exceeding 1g kg<sup>−1</sup> of dry biomass in plants not showing significant growth reduction, occurred in all accessions of <i>O. serpyllifolia</i>, but the higher Ni tolerance of serpentine accessions allowed them to hyperaccumulate more strongly. Of the reference species, <i>C. jonthlaspi</i> responded similarly to the limestone accessions of <i>O. serpyllifolia</i>, whereas <i>A. montanum</i> displayed by far the lowest degree of Ni tolerance and exhibited low foliar Ni concentrations, which only exceeded 1 g kg<sup>−1</sup> in plants showing severe Ni toxicity. The continuous spectrum of physiological responses among these accessions does not lend support to segregation of the serpentine populations of <i>O. serpyllifolia</i> as distinct species. However, the pronounced differences in degrees of Ni tolerance, hyperaccumulation, and elemental homeostasis observed among these accessions under common-garden conditions argues for the existence of population-level adaptation to their local substrates.https://www.mdpi.com/2223-7747/10/4/800ultramaficserpentinenickelhyperaccumulationfacultative hyperaccumulatormetal tolerance
spellingShingle A. Joseph Pollard
Grace L. McCartha
Celestino Quintela-Sabarís
Thomas A. Flynn
Maria K. Sobczyk
J. Andrew C. Smith
Intraspecific Variation in Nickel Tolerance and Hyperaccumulation among Serpentine and Limestone Populations of <i>Odontarrhena serpyllifolia</i> (Brassicaceae: Alysseae) from the Iberian Peninsula
Plants
ultramafic
serpentine
nickel
hyperaccumulation
facultative hyperaccumulator
metal tolerance
title Intraspecific Variation in Nickel Tolerance and Hyperaccumulation among Serpentine and Limestone Populations of <i>Odontarrhena serpyllifolia</i> (Brassicaceae: Alysseae) from the Iberian Peninsula
title_full Intraspecific Variation in Nickel Tolerance and Hyperaccumulation among Serpentine and Limestone Populations of <i>Odontarrhena serpyllifolia</i> (Brassicaceae: Alysseae) from the Iberian Peninsula
title_fullStr Intraspecific Variation in Nickel Tolerance and Hyperaccumulation among Serpentine and Limestone Populations of <i>Odontarrhena serpyllifolia</i> (Brassicaceae: Alysseae) from the Iberian Peninsula
title_full_unstemmed Intraspecific Variation in Nickel Tolerance and Hyperaccumulation among Serpentine and Limestone Populations of <i>Odontarrhena serpyllifolia</i> (Brassicaceae: Alysseae) from the Iberian Peninsula
title_short Intraspecific Variation in Nickel Tolerance and Hyperaccumulation among Serpentine and Limestone Populations of <i>Odontarrhena serpyllifolia</i> (Brassicaceae: Alysseae) from the Iberian Peninsula
title_sort intraspecific variation in nickel tolerance and hyperaccumulation among serpentine and limestone populations of i odontarrhena serpyllifolia i brassicaceae alysseae from the iberian peninsula
topic ultramafic
serpentine
nickel
hyperaccumulation
facultative hyperaccumulator
metal tolerance
url https://www.mdpi.com/2223-7747/10/4/800
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