Changes of Cadmium Storage Forms and Isotope Ratios in Rice During Grain Filling

Abstract

Rice poses a major source of the toxic contaminant cadmium (Cd) for humans. Here, we elucidated the role of Cd storage forms (i.e., the chemical Cd speciation) on the dynamics of Cd within rice. In a pot trial, we grew rice on a Cd-contaminated soil in upland conditions and sampled roots and shoots parts at flowering and maturity. Cd concentrations, isotope ratios, Cd speciation (X-ray absorption spectroscopy), and micronutrient concentrations were analyzed. During grain filling, Cd and preferentially light Cd isotopes were strongly retained in roots where the Cd storage form did not change (Cd bound to thiols, Cd–S = 100%). In the same period, no net change of Cd mass occurred in roots and shoots, and the shoots became enriched in heavy isotopes (Δ114/110Cdmaturity–flowering = 0.14 ± 0.04‰). These results are consistent with a sequestration of Cd in root vacuoles that includes strong binding of Cd to thiol containing ligands that favor light isotopes, with a small fraction of Cd strongly enriched in heavy isotopes being transferred to shoots during grain filling. The Cd speciation in the shoots changed from predominantly Cd–S (72%) to Cd bound to O ligands (Cd–O, 80%) during grain filling. Cd–O may represent Cd binding to organic acids in vacuoles and/or binding to cell walls in the apoplast. Despite this change of ligands, which was attributed to plant senescence, Cd was largely immobile in the shoots since only 0.77% of Cd in the shoots were transferred into the grains. Thus, both storage forms (Cd–S and Cd–O) contributed to the retention of Cd in the straw. Cd was mainly bound to S in nodes I and grains (Cd–S > 84%), and these organs were strongly enriched in heavy isotopes compared to straw (Δ114/110Cdgrains/nodes–straw = 0.66–0.72‰) and flag leaves (Δ114/110Cdgrains/nodes–flag leaves = 0.49–0.52‰). Hence, xylem to phloem transfer in the node favors heavy isotopes, and the Cd–S form may persist during the transfer of Cd from node to grain. This study highlights the importance of Cd storage forms during its journey to grain and potentially into the food chain.

Stable Isotope Fractionation of Metals and Metalloids in Plants: A Review

“…In most cases, shoots were isotopically heavier than roots in wheat, barley, rice, cacao, and a Cd accumulator plant ( Wiggenhauser et al, 2016 , 2021a , b ; Wei et al, 2018 ; Imseng et al, 2019 ; Moore et al, 2020 ; Wang et al, 2021 ; Zhong et al, 2021 ; Figure 10 ). The retention of light Cd isotopes in roots of cereals and numerous different cacao genotypes was ascribed to vacuolar sequestration.…”

“…Cd isotope composition in reproductive and shoot organs can strongly differ (Δ 114/110 Cd reproductive-shoot.organ −0.30 to +0.50‰, Figure 10 ). While Rayleigh fractionation modeling for different plants suggests dominantly unidirectional xylem flow from roots to shoots ( Wiggenhauser et al, 2016 ; Wei et al, 2018 ; Moore et al, 2020 ), it has been shown that cereals likely use phloem redistribution on grain filling ( Wiggenhauser et al, 2021b ; Zhong et al, 2021 ). In rice, an important hub for the transfer of Cd from the xylem to the phloem are the nodes ( Yamaji and Ma, 2014 ).…”

“…In rice, an important hub for the transfer of Cd from the xylem to the phloem are the nodes ( Yamaji and Ma, 2014 ). First data on Cd isotopes in nodes indicated that the xylem to phloem transfer of Cd contributes to the enrichment of heavy isotopes in grains ( Wiggenhauser et al, 2021b ; Zhong et al, 2021 ). Additionally, combined isotope and gene expression analyses strongly suggested that membrane proteins (OsHMA2, OsLCT1) that transfer Cd from the xylem to the phloem in the node contribute to the enrichment of heavy Cd in grains ( Zhong et al, 2021 ).…”

“…Additionally, combined isotope and gene expression analyses strongly suggested that membrane proteins (OsHMA2, OsLCT1) that transfer Cd from the xylem to the phloem in the node contribute to the enrichment of heavy Cd in grains ( Zhong et al, 2021 ). The role of Cd speciation in the nodes (mainly Cd-S) on Cd isotope fractionation between nodes, leaves, and grains is not understood yet ( Wiggenhauser et al, 2021b ). In contrast to cereals, Cd loading into cacao beans may use a different mechanism ( Barraza et al, 2019 ) since Cd in cacao beans was found to be isotopically lighter than in the leaves.…”

Water Management Alters Cadmium Isotope Fractionation between Shoots and Nodes/Leaves in a Soil-Rice System

“…12 Recently, node I of rice plants was found to be strongly enriched in heavier isotopes relative to the shoot and flag leaf under drained conditions, even though Cd in node I was exclusively bound to S ligands. 31 It is supposed that membrane transport, rather than Cd speciation, governed the isotope fractionation during xylem-to-phloem transfer in the nodes. 31 Nodes of rice plants serve as a hub for the distribution of minerals, including Cd, to the grains.…”