Molecular mechanisms underlying the toxicity and detoxification of trace metals and metalloids in plants

Plants take up a wide range of trace metals/metalloids(hereinafter referred to as trace metals)from the soil,some of which are essential but become toxic at high concentrations(e.g.,Cu,Zn,Ni,Co),while others are non-essential and toxic even at relatively low concentrations(e.g.,As,Cd,Cr,Pb,and Hg).Soil contamination of trace metals is an increasing problem worldwide due to intensifying human activities.Trace metal contamination can cause toxicity and growth inhibition in plants,as well as accumulation in the edible parts to levels that threatens food safety and human health.Understanding the mechanisms of trace metal toxicity and how plants respond to trace metal stress is important for improving plant growth and food safety in contaminated soils.The accumulation of excess trace metals in plants can cause oxidative stress,genotoxicity,programmed cell death,and disturbance in multiple physiological processes.Plants have evolved various strategies to detoxify trace metals through cell-wall binding,complexation,vacuolar sequestration,efflux,and translocation.Multiple signal transduction pathways and regulatory responses are involved in plants challenged with trace metal stresses.In this review,we discuss the recent progress in understanding the molecular mechanisms involved in trace metal toxicity,detoxification,and regulation,as well as strategies to enhance plant resistance to trace metal stresses and reduce toxic metal accumulation in food crops.

Rice roots avoid asymmetric heavy metal and salinity stress via an RBOH-ROS-auxin signaling cascade

Root developmental plasticity is crucial for plants to adapt to a changing soil environment,where nutrients and abiotic stress factors are distributed heterogeneously.How plant roots sense and avoid heterogeneous abiotic stress in soil remains unclear.Here,we show that,in response to asymmetric stress of heavy metals(cadmium,copper,or lead)and salt,rice roots rapidly proliferate lateral roots(LRs)in the stress-free area,thereby remodeling root architecture to avoid localized stress.Imaging and quantitative analyses of reactive oxygen species(ROS)showed that asymmetric stress induces a ROS burst in the tips of the exposed roots and simultaneously triggers rapid systemic ROS signaling to the unexposed roots.Addition of a ROS scavenger to either the stressed or stress-free area abolished systemic ROS signaling and LR proliferation induced by asymmetric stress.Asymmetric stress also enhanced cytosolic calcium(Ca^(2+))signaling;blocking Ca^(2+)signaling inhibited systemic ROS propagation and LR branching in the stress-free area.We identified two plasma-membrane-localized respiratory burst oxidase homologs,OsRBOHA and OsRBOHI,as key players in systemic ROS signaling under asymmetric stress.Expression of OsRBOHA and OsRBOHI in roots was upregulated by Cd stress,and knockout of either gene reduced systemic ROS signaling and LR proliferation under asymmetric stress.Furthermore,we demonstrated that auxin signaling and cell wall remodeling act downstream of the systemic ROS signaling to promote LR development.Collectively,our study reveals an RBOH-ROS-auxin signaling cascade that enables rice roots to avoid localized stress of heavy metals and salt and provides new insight into root system plasticity in heterogenous soil.

The Walker & Syers model and the age of soil

Like many people,I am fascinated by the things that have a time dimension,especially those with a long history.During a recent visit to the Chengjiang Biota Fossil Museum in Yunnan,I was struck by the many fossils of the Cumbrian explosion,formed some 530 million years ago.Stil,if the entire history of the Earth is compressed into 24 h,the Chengjiang Biota occurred rather late,at about 9:10 pm,while Homo sapiens arrived at the last minute just before the midnight!

Toxic metals and metalloids:Uptake,transport,detoxification,phytoremediation,and crop improvement for safer food

Agricultural soils are under threat of toxic metal/metalloid contamination from anthropogenic activities,leading to excessive accumulation of arsenic(As),cadmium(Cd),lead(Pb),and mercury(Hg)in food crops that poses significant risks to human health.Understanding how these toxic metals and their methylated species are taken up,translocated,and detoxified is prerequisite to developing strategies to limit their accumulation for safer food.Toxic metals are taken up and transported across different cellular compart-ments and plant tissues via various transporters for essential or beneficial nutrients,e.g.As by phosphate and silicon transporters,and Cd by manganese(Mn),zinc(Zn),and iron(Fe)transporters.These transport processes are subjected to interactions with nutrients and the regulation at the transcriptional and post-translational levels.Complexation with thiol-rich compounds,such as phytochelatins,and sequestration in the vacuoles are the common mechanisms for detoxification and for limiting their translocation.A num-ber of genes involved in toxic metal uptake,transport,and detoxification have been identified,offering tar-gets for genetic manipulation via gene editing or transgenic technologies.Natural variations in toxic metal accumulation exist within crop germplasm,and some of the quantitative trait loci underlying these variations have been cloned,paving the way for marker-assisted breeding of low metal accumulation crops.Using plants to extract and remove toxic metals from soil is also possible,but this phytoremediation approach requires metal hyperaccumulation for efficiency.Knowledge gaps and future research needs are also discussed.

Natural variation in the promoter of OsHMA3 contributes to differential grain cadmium accumulation between Indica and Japonica rice

Rice is a major source of cadmium(Cd) intake for Asian people. Indica rice usually accumulates more Cd in shoots and grains than Japonica rice. However, underlying genetic bases for differential Cd accumulation between Indica and Japonica rice are still unknown. In this study, we cloned a quantitative trait locus(QTL) grain Cd concentration on chromosome 7(GCC7) responsible for differential grain Cd accumulation between two rice varieties by performing QTL analysis and map-based cloning. We found that the two GCC7 alleles, GCC7PA64s and GCC793-11, had different promoter activity of OsHMA3,leading to different OsHMA3 expression and different shoot and grain Cd concentrations. By analyzing the distribution of different haplotypes of GCC7 among diverse rice accessions, we discovered that the high and low Cd accumulation alleles, namely GCC793-11 and GCC7PA64s, were preferentially distributed in Indica and Japonica rice,respectively. We further showed that the GCC7PA64sallele can be used to replace the GCC793-11 allele in the super cultivar 93-11 to reduce grain Cd concentration without adverse effect on agronomic traits. Our results thus reveal that the QTL GCC7 with sequence variation in the OsHMA3 promoter is an important determinant controlling differential grain Cd accumulation between Indica and Japonica rice.

Strategies to manage the risk of heavy metal(loid) contamination in agricultural soils

Soil contamination with heavy metal(loid)sthreatens soil ecological functions, water quality and foodsafety;the latter is the focus of this review. Cadmium (Cd)and arsenic (As) are the toxic elements of most concern forfood safety because they are relatively easily taken up byfood crops. Rice is a major contributor of both Cd and Asintakes to the Chinese population. Contarmination and soilacidification are the main causes of high Cd levels in ricegrains produced in some areas of southern China. The riskof Cd and As accumulation in food crops can be mitigatedthrough agronomic practices and crop breeding. Liming iseffective and economical at reducing Cd uptake by rice inacid soils. Paddy water management can produce oppositeeffects on Cd and As accumulation. Many genes control-ling Cd and As uptake and translocation have beencharacterized, paving the way to breeding low accumulat-ing crop cultivars through marker- -assisted molecularbreeding or genetic engineering. It is important to protectagricultural soils from future contamination. L ong-termmonitoring of anthropogenic additions and accumulationof heavy metal(loid)s in agricultural soils should beundertaken. Mass-balance models should be constructedto evaluate future trends of metal(loid)s in agricultural soilsat a regional scale.

QTL pyramiding for producing nutritious and safe rice grains

Breeding of rice varieties that are enriched with essential micronutrients and simultaneously have reduced levels of toxic elements in grains is largely unexplored in rice breeding practice.In this issue of JIPB,Liu et al.(2020)developed two rice lines with a low level of cadmium and simultaneously high levels of zinc or selenium accumulation in the grains,thus providing elite genetic materials for breeding rice varieties that are important for addressing mineral malnutrition and ensuring food safety.

Cadmium Phytoremediation： Call Rice CALl

Cadmium （Cd） is a toxic heavy metal that has no known biological functions except in some marine diatoms, such as Thalassiosira weissflogii, which can use Cd as a catalytic metal atom in their carbonic anhydrase, presumably conferring an adaptive advantage for diatoms that grow fast in the zinc-poor environment of the ocean surface （Xu et al., 2008）. In the terrestrial environment, Cd is known as a notorious toxin, causing phytotoxicity and human diseases such as renal dysfunction, osteoporosis, and cancers. The best known Cd-induced disease, Itai-itai （renal tubular osteomalacia）, is caused by chronic exposure to Cd via consumption of rice grown in Cd-contaminated paddy soil.

The ferroxidases LPR1 and LPR2 control iron translocation in the xylem of Arabidopsis plants

Iron(Fe)deficiency is common in agricultural crops and affects millions of people worldwide.Translocation of Fe in the xylem is a key step for Fe distribution in plants.The mechanism controlling this process remains largely unknown.Here,we report that two Arabidopsis ferroxidases,LPR1 and LPR2,play a crucial and redundant role in controlling Fe translocation in the xylem.LPR1 and LPR2 are mainly localized in the cell walls of xylem vessels and the surrounding cells in roots,leaves,and stems.Knockout of both LPR1 and LPR2 increased the proportion of Fe(II)in the xylem sap,and caused Fe deposition along the vascular bundles especially in the petioles and main veins of leaves,which was alleviated by blocking blue light.The lpr1 lpr2 double mutant displayed constitutive expression of Fe deficiency response genes and overaccumulation of Fe in the roots and mature leaves under Fe-sufficient supply,but Fe deficiency chlorosis in the new leaves and inflorescences under low Fe supply.Moreover,the lpr1 lpr2 double mutant showed lower Fe concentrations in the xylem and phloem saps,and impaired 57Fe translocation along the xylem.In vitro assays showed that Fe(III)-citrate,the main form of Fe in xylem sap,is easily photoreduced to Fe(II)-citrate,which is unstable and prone to adsorption by cell walls.Taken together,these results indicate that LPR1 and LPR2 are required to oxidize Fe(II)and maintain Fe(III)-citrate stability and mobility during xylem translocation against photoreduction.Our study not only uncovers an essential physiological role of LPR1 and LPR2 but also reveals a new mechanism by which plants maintain Fe mobility during long-distance translocation in the xylem.