Ideal Cereals With Lower Arsenic and Cadmium by Accurately Enhancing Vacuolar Sequestration Capacity

Abstract

Cereals are a staple food for many people around the world; however, they are also a major dietary source of toxic metal(loid)s. Many agricultural regions throughout the world are contaminated with toxic metal(loid)s, which can accumulate to high levels in the grains of cereals cultivated in these regions, posing serious health risks to consumers. Arsenic (As) and cadmium (Cd) are efficiently accumulated in cereals through metal transport pathways. Therefore, there is an urgent need to develop crops that contain greatly reduced levels of toxic metal(loid)s. Vacuolar sequestration of toxic metal(loid)s is a primary strategy for reducing toxic metal(loid)s in grains. However, until recently, detailed strategies and mechanisms for reducing toxic metal(loid)s in grain were limited by the lack of experimental data. New strategies to reduce As and Cd in grain by enhancing vacuolar sequestration in specific tissues are critical to develop crops that lower the daily intake of As and Cd, potentially improving human health. This review provides insights and strategies for developing crops with strongly reduced amounts of toxic metal(loid)s without jeopardizing agronomic traits.

Keywords: arsenic; cadmium; cell specificity; crop engineering; food safety; vacuolar sequestration.

FIGURE 1

Tissue-specific expression of OsABCC1 and OsHMA3 reduces As and Cd concentrations in the rice grain. Transporters localized at the plasma membrane and tonoplast are critical for root-to-shoot translocation and grain accumulation of As and Cd. (A) Arsenic taken up by transporters, such as OsPTs and unknown influx transporters (possibly aquaporins) located at the plasma membrane of the root epidermis, is translocated to shoots and grains, or extruded into the rhizosphere. OsABCC1, a major vacuolar PCs-As transporter, delivers As into vacuoles in phloem companion cells of node I, and inhibits As translocation into rice grains (Song et al., 2014a). Rice plants containing low concentrations of As in their grain were generated by expressing OsABCC1 and ScYCF1 specifically in the cortex, internode, and nodes using the OsRCc3 promoter (Deng et al., 2018). (B) Cd is mainly taken up by OsNramp5, which is localized at the distal side of both root exodermis and endodermis cells. In addition, OsIRT1, 2 and OsNramp1 also contribute to Cd uptake. OsHMA3 located at the tonoplast of roots are responsible for the accumulation of Cd within vacuoles and inhibit radial translocation of Cd into the stele. Low Cd-accumulating rice was generated by expressing a functional OsHMA3 transporter under the control of pOsHMA2, a rice root pericycle and nodal phloem-specific promoter (Shao et al., 2018). Epi, epidermis; Endo, endodermis; EVB, enlarged vascular bundles; DVB, diffuse vascular bundles; XTC, xylem transfer cells; PCB, parenchyma cell bridge; NVA, nodal vascular anastomoses; PPC/CC, phloem parenchyma cells and companion cells; P, phloem; V, vacuole.

FIGURE 2

C-type ATP-binding cassette transporters mediate non-protein thiol-dependent As and Cd vacuolar sequestration. Glutathione synthesized by GSH1 is translocated from plastids to the cytosol through CLT1, a putative GSH transporter located at the plastid envelope, while phytochelatins (PCs) are synthesized by phytochelatin synthetases (PCS) in the cytosol. Inorganic arsenic and cadmium form complexes with GSH and PCs. The GS₃-As and GS₂-Cd complexes might be sequestrated into the vacuole by unknown ABC transporters; PC-As can be delivered to the vacuole by AtABCC1, AtABCC2, and OsABCC1; and PC-Cd can be translocated into the vacuole by SpHMT1, AtABCC1, AtABCC2, and AtABCC3. Loss-of-function mutants for Arabidopsis PCS1 and rice CLT1 exhibited hypersensitivity to As and increased As translocation from roots to shoots due to the limited availability of a cytosolic As chelator in roots (Yang et al., 2016; Hayashi et al., 2017). Rice abcc1 and pcs1 mutants accumulated high levels of As in the grain due to the defect in vacuolar As sequestration in node I (Song et al., 2014a; Hayashi et al., 2017).