TY - JOUR

T1 - Arsenic redox transformations and cycling in the rhizosphere of Pteris vittata and Pteris quadriaurita

AU - Wagner, Stefan

AU - Hoefer, Christoph

AU - Puschenreiter, Markus

AU - Wenzel, Walter W.

AU - Oburger, Eva

AU - Hann, Stephan

AU - Robinson, Brett

AU - Kretzschmar, Ruben

AU - Santner, Jakob

PY - 2020/5/20

Y1 - 2020/5/20

N2 - Pteris vittata (PV) and Pteris quadriaurita (PQ) are reported to hyperaccumulate arsenic (As) when grown in As-rich soil. Yet, little is known about the impact of their unique As accumulation mechanisms on As transformations and cycling at the soil-root interface. Using a combined approach of two-dimensional (2D), sub-mm scale solute imaging of arsenite (As III), arsenate (As V), phosphorus (P), manganese (Mn), iron (Fe) and oxygen (O 2), we found localized patterns of As III/As V redox transformations in the PV rhizosphere (As III/As V ratio of 0.57) compared to bulk soil (As III/As V ratio of ≤0.04). Our data indicate that the high As root uptake, translocation and accumulation from the As-rich experimental soil (2080 mg kg −1) to PV fronds (6986 mg kg −1) induced As detoxification via As V reduction and As III root efflux, leading to As III accumulation and re-oxidation to As V in the rhizosphere porewater. This As cycling mechanism is linked to the reduction of O 2 and Mn III/IV (oxyhydr)oxides resulting in decreased O 2 levels and increased Mn solubilization along roots. Compared to PV, we found 4-fold lower As translocation to PQ fronds (1611 mg kg −1), 2-fold lower As V depletion in the PQ rhizosphere, and no As III efflux from PQ roots, suggesting that PQ efficiently controls As uptake to avoid toxic As levels in roots. Analysis of root exudates obtained from soil-grown PV showed that As acquisition by PV roots was not associated with phytic acid release. Our study demonstrates that two closely-related As-accumulating ferns have distinct mechanisms for As uptake modulating As cycling in As-rich environments.

AB - Pteris vittata (PV) and Pteris quadriaurita (PQ) are reported to hyperaccumulate arsenic (As) when grown in As-rich soil. Yet, little is known about the impact of their unique As accumulation mechanisms on As transformations and cycling at the soil-root interface. Using a combined approach of two-dimensional (2D), sub-mm scale solute imaging of arsenite (As III), arsenate (As V), phosphorus (P), manganese (Mn), iron (Fe) and oxygen (O 2), we found localized patterns of As III/As V redox transformations in the PV rhizosphere (As III/As V ratio of 0.57) compared to bulk soil (As III/As V ratio of ≤0.04). Our data indicate that the high As root uptake, translocation and accumulation from the As-rich experimental soil (2080 mg kg −1) to PV fronds (6986 mg kg −1) induced As detoxification via As V reduction and As III root efflux, leading to As III accumulation and re-oxidation to As V in the rhizosphere porewater. This As cycling mechanism is linked to the reduction of O 2 and Mn III/IV (oxyhydr)oxides resulting in decreased O 2 levels and increased Mn solubilization along roots. Compared to PV, we found 4-fold lower As translocation to PQ fronds (1611 mg kg −1), 2-fold lower As V depletion in the PQ rhizosphere, and no As III efflux from PQ roots, suggesting that PQ efficiently controls As uptake to avoid toxic As levels in roots. Analysis of root exudates obtained from soil-grown PV showed that As acquisition by PV roots was not associated with phytic acid release. Our study demonstrates that two closely-related As-accumulating ferns have distinct mechanisms for As uptake modulating As cycling in As-rich environments.

UR - http://www.scopus.com/inward/record.url?scp=85086460928&partnerID=8YFLogxK

U2 - 10.1016/j.envexpbot.2020.104122

DO - 10.1016/j.envexpbot.2020.104122

M3 - Article

VL - 177.2020

JO - Environmental and Experimental Botany

JF - Environmental and Experimental Botany

SN - 0098-8472

IS - September

M1 - 104122

ER -