Novel Insights Into the Hyperaccumulation Syndrome in Pycnandra (Sapotaceae)

The discovery of nickel hyperaccumulation, in Pycnandra acuminata, was the start of a global quest in this fascinating phenomenon. Despite recent advances in the physiology and molecular genetics of hyperaccumulation, the mechanisms and tolerance of Ni accumulation in the most extreme example report...

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Main Authors: Sandrine Isnard, Laurent L’Huillier, Adrian L. D. Paul, Jérôme Munzinger, Bruno Fogliani, Guillaume Echevarria, Peter D. Erskine, Vidiro Gei, Tanguy Jaffré, Antony van der Ent
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-09-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2020.559059/full
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author Sandrine Isnard
Sandrine Isnard
Laurent L’Huillier
Adrian L. D. Paul
Jérôme Munzinger
Bruno Fogliani
Bruno Fogliani
Guillaume Echevarria
Guillaume Echevarria
Peter D. Erskine
Vidiro Gei
Tanguy Jaffré
Tanguy Jaffré
Antony van der Ent
Antony van der Ent
author_facet Sandrine Isnard
Sandrine Isnard
Laurent L’Huillier
Adrian L. D. Paul
Jérôme Munzinger
Bruno Fogliani
Bruno Fogliani
Guillaume Echevarria
Guillaume Echevarria
Peter D. Erskine
Vidiro Gei
Tanguy Jaffré
Tanguy Jaffré
Antony van der Ent
Antony van der Ent
author_sort Sandrine Isnard
collection DOAJ
description The discovery of nickel hyperaccumulation, in Pycnandra acuminata, was the start of a global quest in this fascinating phenomenon. Despite recent advances in the physiology and molecular genetics of hyperaccumulation, the mechanisms and tolerance of Ni accumulation in the most extreme example reported to date, P. acuminata, remains enigmatic. We conducted a hydroponic experiment to establish Ni tolerance levels and translocation patterns in roots and shoots of P. acuminata, and analyzed elemental partitioning to gain insights into Ni regulation. We combined a phylogeny and foliar Ni concentrations to assess the incidence of hyperaccumulation within the genus Pycnandra. Hydroponic dosing experiments revealed that P. acuminata can resist extreme Ni concentrations in solution (up to 3,000 µM), and dosing at 100 µM Ni was beneficial to growth. All plant parts were highly enriched in Ni, but the latex had extreme Ni concentrations (124,000 µg g−1). Hyperaccumulation evolved independently in only two subgenera and five species of the genus Pycnandra. The extremely high level of Ni tolerance is posited to derive from the unique properties of laticifers. The evolutionary and ecological significance of Ni hyperaccumulation in Pycnandra is discussed in light of these findings. We suggest that Ni-rich laticifers might be more widespread in the plant kingdom and that more investigation is warranted.
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spelling doaj.art-2e153664323549968fc4a1375b646f322022-12-22T00:40:45ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-09-011110.3389/fpls.2020.559059559059Novel Insights Into the Hyperaccumulation Syndrome in Pycnandra (Sapotaceae)Sandrine Isnard0Sandrine Isnard1Laurent L’Huillier2Adrian L. D. Paul3Jérôme Munzinger4Bruno Fogliani5Bruno Fogliani6Guillaume Echevarria7Guillaume Echevarria8Peter D. Erskine9Vidiro Gei10Tanguy Jaffré11Tanguy Jaffré12Antony van der Ent13Antony van der Ent14AMAP, Université Montpellier, IRD, CIRAD CNRS, INRAE, Montpellier, FranceAMAP, IRD, Herbier de Nouvelle-Calédonie, Nouméa, New CaledoniaInstitut Agronomique néo-Calédonien (IAC), Equipe ARBOREAL (AgricultuRe BiOdiveRsité Et vAlorisation), Paita, New CaledoniaCentre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, St Lucia, QLD, AustraliaAMAP, Université Montpellier, IRD, CIRAD CNRS, INRAE, Montpellier, FranceInstitut Agronomique néo-Calédonien (IAC), Equipe ARBOREAL (AgricultuRe BiOdiveRsité Et vAlorisation), Paita, New CaledoniaInstitute of Exact and Applied Sciences (ISEA), Université de la Nouvelle-Calédonie, Nouméa, New CaledoniaCentre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, St Lucia, QLD, AustraliaUniversité de Lorraine – INRAE, Laboratoire Sols et Environnement, Vandoeuvre-lès-Nancy, FranceCentre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, St Lucia, QLD, AustraliaCentre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, St Lucia, QLD, AustraliaAMAP, Université Montpellier, IRD, CIRAD CNRS, INRAE, Montpellier, FranceAMAP, IRD, Herbier de Nouvelle-Calédonie, Nouméa, New CaledoniaCentre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, St Lucia, QLD, AustraliaUniversité de Lorraine – INRAE, Laboratoire Sols et Environnement, Vandoeuvre-lès-Nancy, FranceThe discovery of nickel hyperaccumulation, in Pycnandra acuminata, was the start of a global quest in this fascinating phenomenon. Despite recent advances in the physiology and molecular genetics of hyperaccumulation, the mechanisms and tolerance of Ni accumulation in the most extreme example reported to date, P. acuminata, remains enigmatic. We conducted a hydroponic experiment to establish Ni tolerance levels and translocation patterns in roots and shoots of P. acuminata, and analyzed elemental partitioning to gain insights into Ni regulation. We combined a phylogeny and foliar Ni concentrations to assess the incidence of hyperaccumulation within the genus Pycnandra. Hydroponic dosing experiments revealed that P. acuminata can resist extreme Ni concentrations in solution (up to 3,000 µM), and dosing at 100 µM Ni was beneficial to growth. All plant parts were highly enriched in Ni, but the latex had extreme Ni concentrations (124,000 µg g−1). Hyperaccumulation evolved independently in only two subgenera and five species of the genus Pycnandra. The extremely high level of Ni tolerance is posited to derive from the unique properties of laticifers. The evolutionary and ecological significance of Ni hyperaccumulation in Pycnandra is discussed in light of these findings. We suggest that Ni-rich laticifers might be more widespread in the plant kingdom and that more investigation is warranted.https://www.frontiersin.org/article/10.3389/fpls.2020.559059/fullhydroponichyperaccumulationlaticifersnickelPycnandraX-ray fluorescence spectroscopy
spellingShingle Sandrine Isnard
Sandrine Isnard
Laurent L’Huillier
Adrian L. D. Paul
Jérôme Munzinger
Bruno Fogliani
Bruno Fogliani
Guillaume Echevarria
Guillaume Echevarria
Peter D. Erskine
Vidiro Gei
Tanguy Jaffré
Tanguy Jaffré
Antony van der Ent
Antony van der Ent
Novel Insights Into the Hyperaccumulation Syndrome in Pycnandra (Sapotaceae)
Frontiers in Plant Science
hydroponic
hyperaccumulation
laticifers
nickel
Pycnandra
X-ray fluorescence spectroscopy
title Novel Insights Into the Hyperaccumulation Syndrome in Pycnandra (Sapotaceae)
title_full Novel Insights Into the Hyperaccumulation Syndrome in Pycnandra (Sapotaceae)
title_fullStr Novel Insights Into the Hyperaccumulation Syndrome in Pycnandra (Sapotaceae)
title_full_unstemmed Novel Insights Into the Hyperaccumulation Syndrome in Pycnandra (Sapotaceae)
title_short Novel Insights Into the Hyperaccumulation Syndrome in Pycnandra (Sapotaceae)
title_sort novel insights into the hyperaccumulation syndrome in pycnandra sapotaceae
topic hydroponic
hyperaccumulation
laticifers
nickel
Pycnandra
X-ray fluorescence spectroscopy
url https://www.frontiersin.org/article/10.3389/fpls.2020.559059/full
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