Abstract
Soil cadmium (Cd), which can occur naturally in the environment or arise from industrial pollution, seriously affects crop quality and threatens human health. Therefore, reducing grain Cd accumulation (GCA) has become an important topic worldwide. To comprehensively assess the research status of GCA, we reviewed the research into physiological and molecular mechanisms of GCA, including the characteristics of Cd uptake, transport, and accumulation from roots to grain; furthermore, literature on GCA-related quantitative trait locus identification and gene functional analysis were reviewed. Based on physiological and molecular mechanisms, two strategies to reduce GCA, namely soil management and genetic improvement, were also critically summarized. It became clear that further research is necessary into the physiological mechanisms of Cd uptake, transportation, and accumulation in grain. It is also important to accelerate the discovery and use of effective functional markers and genes associated with low Cd accumulation and to improve the feasibility and potential value of breeding low Cd grain crops.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Due to the rapid advancement of mining, industrial, and agricultural activities, the severity of soil pollution caused by heavy metals has escalated significantly. This problem arises from various sources, including the discharge of industrial waste water and gas, sewage irrigation, and improper use of chemical fertilizers and pesticides (Yan et al. 2021). In China, approximately 16.1% of the nation’s agricultural land surpasses the safety threshold for soil heavy metal concentration. The primary inorganic pollutants contributing to this alarming statistic are cadmium (Cd), nickel (Ni), and arsenic (As), with 7.0%, 4.8%, and 2.7% of soils exceeding the threshold, respectively (Liu et al. 2016a). Moreover, there is a concerning trend for soil plough layer in China to experience Cd-induced pollution, with its rate for increase averaged as 0.004 mg kg− 1 per year, which may be mainly caused by industrial waste discharge and extensive fertilizer usage (Hu et al. 2016). The rate of soil pollution increase in China far surpasses that observed in Europe (Luo et al. 2009). Accumulation of excessive Cd in crops induced by pollution has given rise to health issues, notably with the emergence of “Cd rice” and “Cd wheat”, prompting widespread concern about the impact on public health.
Cd acts as a nonessential component for both plants and animals, yet it can seriously threaten human health when accumulated in high concentrations using food chain (Dias et al. 2013; Li et al. 2019). Functioning as a plant abiotic stress contaminant, Cd exhibits troublesome characteristics, such as a low soil-adsorption coefficient, a high soil-plant mobility, and a substantial plant accumulation factor (Shahid et al. 2017; Chen et al. 2018). In plants, Cd exerts a role of disrupting some normal metabolisms (Fan et al. 2011; Jaouani et al. 2018), impacting crucial processes like photosynthesis and respiration (Song et al. 2019). This disruption extends to reduced root activity, slowed seedling growth, and the manifestation of small and yellow leaves, ultimately culminating in plant death (Ahmad et al. 2015; Zhang et al. 2021a). Importantly, human exposure to Cd prevailingly occurs via ingesting the plant material contaminated with cadmium, constituting a health threat even at low concentrations. Prolonged Cd exposure has been linked to a higher incidence of lung, prostate, testicular, and kidney cancers (Unsal et al. 2020; Reyes-Hinojosa et al. 2019). Consequently, extensive research efforts are underway globally to develop strategies for controlling grain Cd accumulation (GCA) in crops.
Currently, in most regions globally, the concentration of Cd in grain typically aligns with safety standards, albeit with regional variations. According to relevant criteria for food safety stipulated by the European Union (EU) and China, maximum allowable Cd concentration in rice is set at 0.2 mg kg− 1, while the Codex Alimentations Commission specifies a limit of 0.4 mg kg− 1 (Yang et al. 2019a). Recent global research indicates that the average GCA concentration is 0.093 mg kg− 1, with a 16-fold variation in mean values among regions. Notably, South China exhibits the highest concentration at 0.32 mg kg− 1, followed by Argentina (0.15 mg kg− 1) ≈ Germany (0.13 mg kg− 1) > Japan (0.11 mg kg− 1) > United States (0.064 mg kg− 1) > Central-North China (0.020–0.60 mg kg− 1) ≥ Iran (0.042 mg kg− 1) > Brazil (0.023 mg kg− 1) ≈ South Korea (0.020 mg kg− 1) (Zhang et al. 2021b). However, some studies present contrasting findings, emphasizing concerns about Cd levels exceeding allowable limits. For instance, in West Bengal, a study reported GCA concentrations in rice (between the value being below the threshold to 0.49 mg kg− 1) and in soil samples (1.76 mg kg− 1 to 13.8 mg kg− 1), surpassing the permissible limits (Majumdar et al. 2020). In Germany, an investigation into Cd uptake involving 602 soybean accessions revealed that the average Cd content should be 0.13 mg kg− 1, which was 12.5% higher in contrast to the stipulated threshod in EU (Franzaring et al. 2019). Additionally, in New Zealand, an investigation into the GCA content of 12 wheat varieties collected in various regions showed Cd concentrations can be 0.004–0.205 mg kg− 1, which is averaged as 0.066 mg kg− 1, and 7% of the varieties surpassing 0.1 mg kg− 1 (Gray et al. 2019).
Consequently, addressing the avoidance and mitigation of soil pollution induced by heavy metal in cropland to guarantee the generation and supply of safe food has emerged as a crucial global concern. This review centers on examining the physiological and molecular mechanisms underlying GCA and explores strategies to produce grain crops with low Cd (LCd). The review also highlights the knowledge gaps in basic research at both physiological and molecular levels which require further studies. Ultimately, it advocates for research into crop breeding with LCd, offering a theoretical foundation for producing safe and uncontaminated food.
Physiological mechanisms of GCA
With specific concentration, Cd accumulated in the soil can seriously impact plant metabolism, photosynthesis, respiration, transport, and overall growth (Sandalio et al. 2001; Zhang et al. 2014). Furthermore, it causes GCA, ultimately diminishing both crop yield and quality. The intricate physiological processes involved in GCA in crops have been investigated many times. Figure 1 illustrates the Cd uptake, transport, and accumulation, using rice as an example.
Cd uptake and transport in roots
Generally, available soil Cd is passively or actively absorbed into plant root systems through the symplast pathway. Subsequently, it undergoes transportation to aerial parts of a plant using xylem, facilitated by transpiration, and accumulates in grains via internode phloem (Feng et al. 2018; Liu et al. 2021; Uraguchi et al. 2009). Transporters associated with essential elements involve in mediation of Cd transport in plants, like Zn, Ca, Fe, and Mn. Processes such as Cd uptake and xylem loading in roots, Cd remobilization from leaf blades, and intervascular transfer in nodes play pivotal roles in redirecting Cd transport to the grain, a critical aspect of GCA (Uraguchi and Fujiwara 2013). The root cell wall acts as initial barrier in avoiding entrance of Cd to the stem. However, cell walls, composed of proteins, polysaccharides, lignin, and other phenolic compounds, also serve as a target for heavy metals. Functional groups within cell walls can form covalent or non-covalent bonds with Cd (Parrotta et al. 2015), potentially diminishing the Cd uptake by the roots.
Upon entering cells in plant root, some Cd is encapsulated within vacuoles as a complex with Cd-phytochelatin proteins (Miyadate et al. 2011), whereas the remaining Cd is conveyed to xylem. Sequestering Cd into vacuoles is acknowledged to be efficient for Cd tolerance, contributing to a reduction of Cd transport to the grain (Gao et al. 2016; Xin et al. 2018). Phytochelatins accumulate in plants when exposed to heavy metal ions, forming complexes that minimize the free Cd content in the cytosol (Grill et al. 1987). These Cd-phytochelatin complexes hinder Cd transport by binding Cd ions through metal chelation with organic acids in plants (Saraswat and Rai 2011). For examples, organic acids like malonic and malic acids restrict the Cd flow by forming strong bonds with Cd ions through metal chelation (Osmolovskaya et al. 2018). A one-unit increase in content of malonic and malic acids facilitates the chelation of 5.60 and 2.03 units of Cd in plants (Kocaman 2023). Research indicates that root vacuoles in maize genotypes containing high Cd (HCd) experience more severe damage compared to those in maize genotypes with LCd, which remain largely unaffected. The latter is better equipped to generate Cd chelates and sequester more Cd into vacuoles (Lin et al. 2022). Cd chelation or retention in vacuoles impedes Cd transport from roots to aboveground parts, thereby diminishing GCA.
Cd transport to and accumulation in grain
Cd loading into the grain occurs through phloem-mediated redistribution following the initial transport using the xylem (Vanderschueren et al. 2023; Zhong et al. 2023). In durum wheat, excessive GCA did not exhibit a correlation with seedling root uptake rates or root-to-shoot translocation. Instead, it appears to be linked with Cd transport modulated by phloem to the grain (Hart et al. 1998). However, GCA in rice demonstrated independence from both the root uptake period and the Cd content in soil. While, a strong positive association was observed with the Cd content in xylem. Cd translocation from the root to the shoot via the xylem primarily affects the GCA concentration in rice (Uraguchi et al. 2009). Tanaka et al. (2007) investigated the involvement of rice phloem to Cd transport to the grain and unveiled that 91–100% of the Cd was derived from the topmost internode of rice plants during grain-filling.
When the plants are under reproductive growth, they absorb Cd through their roots and transport it to grain through stems and leaves. In wheat, the early filling stage is deemed as a critical period for transporting accumulated Cd from leaves to the grain (Ma et al. 2022). Nodes serve as core organs responsible for transferring Cd from xylem to phloem, crucially contributing to the Cd accumulation from soil to grain during filling (Harris and Taylor 2013; Zhong et al. 2023). Research conducted by Liu et al. (2021) revealed a positive relationship between GCA in brown rice and that in the upper nodes, along with the efficiency of Cd translocation from roots to nodes. Shi et al. (2019) studied the spatial arrangement and evolving dynamics of Cd concentration in one HCd and one LCd common wheat cultivar. The outcomes indicated substantial differences in GCA concentrations between the two cultivars, while the concentrations in rachis and glumes remained similar. This signifies that the two cultivars exhibit distinct regulatory mechanisms with respect to Cd retransfer and redistribution from rachis and glumes to grain during the reproductive stage.
Molecular mechanisms of GCA
Plant genes exert control over physiological and metabolic responses to Cd stress by managing the production of their specific proteins and functionally related proteins through transcription factors. In the last four decades, the accelerated progress in technologies associated with molecular marker and high-throughput sequencing platforms has advanced the exploration of quantitative trait loci (QTLs) and genes. Identifying QTLs and genes linked to GCA have attracted increasing attention and has garnered escalating interest, emerging as a crucial research domain for pinpointing LCd grain germplasm in molecular breeding programs.
QTL identification for GCA
Linkage mapping (LM) and association mapping (AM) are two essential methods for identifying quantitative trait loci (QTLs), based on the construction of genetic maps from biparental segregation populations and the linkage disequilibrium of natural populations, respectively. While numerous QTLs associated with Cd uptake, transport, and accumulation in crops have been extensively delved into, there is a notable scarcity of reports on QTLs directly controlling GCA. Consequently, only those QTLs directly related to GCA in some common crops like rice (Ishikawa et al. 2005, 2010; Sato et al. 2011; Guo et al. 2019; Wang et al. 2020; Zhang et al. 2018; Zhao et al., 2018; Liu et al. 2019b; Pan et al. 2020), wheat (Knox et al. 2009; Oladzad-Abbasabadi et al. 2018; Ban et al. 2020), soybean (Jegadeesan et al. 2010; Benitez et al. 2010), barley (Wu et al. 2015), and maize (Tang et al. 2021a), are detailed in Table 1. For instance, in rice, 14 QTLs for GCA, with the phenotypic variation explained (PVE) of 2.40−4.82%, were identified on seven chromosomes based on an AM natural population containing 312 rice accessions (Zhao et al. 2018). Another example is in soybean, where a significant QTL for grains with LCd, located on chromosome 9, explained 57.3% of the phenotypic variation, which were derived from constructing an RIL population using HCd and LCd parents (Jegadeesan et al. 2010).
A comprehensive review of previous studies revealed the recurrent detection of certain QTLs for GCA were repeatedly detected across diverse populations, generations, environments, and mapping methods. In rice, QTL qGCd7, demonstrating a significant PVE for GCA of 35.5%, was identified in a recombinant inbred line (RIL) population and consistently confirmed in chromosome segment substitution lines (CSSLs), F2, and germplasm populations (Ishikawa et al. 2010; Zhang et al. 2018). Another rice QTL, qLCdG11, with an average PVE for GCA of 11.16% (9.41% and 12.91%), was repeatedly detected across two generations (Sato et al. 2011). In wheat, the QTL QCdu.spa-B1, exhibiting an average PVE for GCA of 80%, was consistently detected in 2 years of testing (Knox et al. 2009). Two additional wheat QTLs, namely QCdc.4B-kita and QCdc.6B-kita, with PVE values for GCA ranging from 9.4 to 25.4% (chromosome 4B) and 9.0–17.8% (6B), respectively, were recurrently detected over 3 years (Ban et al. 2020). In soybean, the QTL Cda1, boasting a PVE of 57.3%, was consistently identified in 2 years and was further validated in different populations (Jegadeesan et al. 2010). Another soybean QTL Cd1, with the average PVE of 71.3% (82.4%, 56.7%, and 74.9%), was repeatedly detected in three RIL generations and a NIL population. In barley, the two main QTLs, which were 8586 − 1221 and ConsensusGBS0086-5, explaining 12.6%/11.3% and 9.5%/8.5% of the average PVE, respectively, were repeatedly detected in two environments (Wu et al. 2015). In maize, the QTL qCd1, featuring a PVE of 20.03%, was consistently detected across four different environments and was further validated through AM and bulked segregant RNA-seq analyses (Tang et al. 2021a). The above major-effect QTLs exhibit high reliability and hold potential for utilization in marker-assisted selection (MAS) to reduce grain Cd concentration.
Cloning and functional analysis of genes associated with GCA
Growth of crop varieties with LCd accumulation hinges on identifying genes linked to reduced Cd content, necessitating a deeper investigation into Cd uptake and transport mechanisms (Chen and Wu 2020). Studies on genotypes, including mutants with varying Cd accumulation levels, have necessitated the identification of Cd transporter proteins in rice and other grain crops. Numerous genes participated in regulating Cd accumulation were uncovered (Fig. 1), like the heavy metal ATPase (HMA) (Takahashi et al. 2012), the Natural resistance-associated macrophage protein (Nramp) (Takahashi et al. 2011), the Zn/Fe-regulated transporter-like (ZIP) (Guerinot 2000; Zheng et al. 2018), and the low-affinity cation transporter (LCT) (Uraguchi et al. 2011). In our previous investigation, the transcriptomic response was compared at different Cd concentrations in a HCd and a LCd sunflower cultivar, and several Cd-related candidate genes were identified, namely ATP-binding cassette (ABC), ZIP, heavy metal- associated isoprenylated plant protein (HIPP), Nramp, and HMA (Fu et al. 2022). These candidate genes, crucial for understanding Cd response mechanisms, necessitate further functional verification. Notably, significant strides have been taken in unraveling genes correlated with Cd uptake, transport, and accumulation in grains, thereby influencing GCA (Table 2).
OsHMA2 primarily conveys Zn and Cd and is discovered in root pericycle and phloem of diffuse vascular bundles in the nodes (Yamaji et al. 2013). A reduction in function or downshift of OsHMA2 expression has been demonstrated to lower Cd content in grains (Satoh-Nagasawa et al. 2012). OsHMA3, a paralogous gene of OsHMA2 in root cell vacuoles, facilitates high root-to-shoot Cd translocation rates (Miyadate et al. 2011). It acts by restricting Cd translocation from roots to aboveground tissues, selectively sequestering Cd into root vacuoles (Miyadate et al. 2011; Ueno et al. 2010). Liu et al. (2020b) highlighted the significance of sequence variation in the OsHMA3 promoter GCC7 in regulating variations in Cd accumulation between indica and japonica rice accessions. The HCd and LCd accumulation alleles, GCC793-11 and GCC7PA64s, exhibit distinct OsHMA3 initiation activities, leading to varying GCA contents between the two subspecies. Genotypes with knockdown mutant alleles of OsHMA3 show reduced the capability to isolate Cd in vacuoles, causing HCd in shoots and grains (Sui et al. 2019; Yan et al. 2016; Zhao and Wang 2020). The OsHMA3 expression exposed to OsHMA2 promoter increased Cd storage in vacuoles from various parts, greatly lowering GCA in rice (Shao et al., 2018). Tang et al. (2021a) reported a potential gene (i.e., ZmHMA3) capable of influencing GCA in maize. By capitalizing on the inherent sequence variations in ZmHMA3 among a diverse array of maize lines, four PCR-based molecular markers were formed, effectively discerning five haplotypes.
OsNramp5, expressed in roots, is crucial in Cd uptake and transport. Mutations in it remarkably weaken the Cd uptake by roots, diminishing GCA content in rice (Ishikawa et al. 2012). Through CRISPR-Cas9 gene-editing system, a novel indica cultivar with LCd accumulation was developed following the knockout of OsNramp5. The mutant consistently maintained a GCA content below 0.05 mg kg− 1 and demonstrated unaffected yields when cultivated in a Cd-contaminated paddy field, in contrast to the same cultivar grown in uncontaminated soil (Tang et al. 2017). OsNramp1 predominantly expresses on plasma membrane of root cells, excluding central vascular tissues and mesophyll cells. Knockdown of OsNramp1 results in a reduction in Cd accumulation, although its impact is less pronounced than that of OsNramp5. Declined Cd content is more substantial in double mutants of OsNramp1 and OsNramp5 in comparison to either single mutant. Another gene within this family, OsNramp2, expressed in vacuoles, likely encodes a functional Cd transporter (Zhao et al., 2018). The combination of OsNramp1, OsNramp5, and OsHMA3 has been employed in breeding the indica rice variety 93 − 11 with low GCA (Wang et al. 2021).
ZIP can transport various cations, like Zn, Fe, Mn, and Cd. OsZIP1, identified as a metal-detoxifying transporter, is crucial to avoid too much Zn, Cu, and Cd are deposited in rice (Liu et al. 2019a). OsLCT1-OsHMA2-OsZIP3 co-expression effectively diminishes the Cd translocation and accumulation, mitigate oxidative stress triggered by Zn and Cd, ultimately enhancing the quality of rice grain (Tian et al. 2019). OsZIP7 exerts an active effect in loading Zn and Cd into xylem in roots and facilitating inter-vascular transfer in nodes, and its specific function involves preferentially directing Zn and Cd to developing tissues and grains (Tan et al. 2019). Through DNA microarray analysis and confirmation in RNA interference (RNAi) plants, two pivotal genes, HvZIP3 and HvZIP8, have been identified as contributors to low GCA in barley (Sun et al. 2015).
The LCD protein predominantly localizes to the cytoplasm and nucleus, with gene expression occurring in vascular tissues of the roots and cells associated with phloem in leaves. In the Cd-tolerant lcd knockout mutant, the GCA level in rice decreased by approximately 50%, in contrast to the wild type. Importantly, no considerable variation was observed in plant biomass or grain yield between the lcd knockout mutant and the wild type (Shimo et al. 2011).
The gene responsible for cation/Ca exchange, specifically OsCCX2, facilitates the direct transport of Cd from the roots to the grain. The knockout mutant of the OsCCX2 gene led to a notable decrease in Cd content within the grain (Hao et al. 2018). Guo et al. (2020) focusing on Cd distribution in rice cultivar ‘YaHui2816’ exhibited a cultivar with a LCd concentration in grain and HCd concentration in straw. This finding signified that OsHMA2, OsCCX2, and OsZIP7 involved in Cd retention at node II. Consequently, this restrains transporting Cd to the grain.
A rice Cd transporter, OsLCT1, functions at the nodes, where Cd is transported to the grain. The regulation of OsLCT1 has been demonstrated to yield “LCd rice” without influencing agronomic traits. In the model indica cultivar ‘Kasalath’, OsLCT1 was observed to be highly expression in the reproductive stage than in the vegetative stage (Uraguchi et al. 2014). Conversely, OsLCT2 increased the Zn concentrations in roots under an overexpression condition by up-regulating OsZIP9, which reduced GCA by limiting Cd enter the xylem and restraining root-to-shoot Cd translocation in rice (Tang et al. 2021b).
OsCd1 exerts a role in Cd uptake by rice roots and facilitates GCA in rice. The inherent variation observed in OsCd1, characterized by a missense mutation Val449Asp, is accountable for the disparity GCA between the indica and japonica subspecies of rice (Yan et al. 2019).
Strategies to produce LCd grain crops
Enhancing our comprehension of the physiological and molecular mechanisms of GCA can pave the way to produce grain crops with LCd, facilitating the translation from laboratory research to practical field applications. Two strategies have been proposed: soil management and genetic improvement. Soil management endeavors to diminish the effective Cd content in the soil through physical, chemical, or biological methods. This strategy aims to enhance the physiological and metabolic environment in plants as well as modulate Cd absorption, transport, and metabolism in grain crops. On the other hand, genetic improvement focuses on identifying valuable QTLs or alleles associated with LCd. It aims to establish efficient breeding technologies that integrate conventional breeding, molecular marker-assisted breeding, gene editing, and other modern biotechnological approaches, and finally cultivate crop varieties containing LCd.
Soil management
Appropriate utilization of conventional agronomic methods on farmland polluted by Cd has demonstrated the potential to yield crops that meet relevant national stipulations on limiting the Cd content (Kang et al. 2020; Li et al. 2017; Liu et al. 2016b). Effective soil management, encompassing precise control of soil moisture and nutrient levels, along with the regulation of soil pH and redox potential, empowers farmers to curtail Cd migration from soil to roots, thereby contributing to a reduction in GCA (Hussain et al. 2021; Yuan et al. 2020). Strategic control of water and fertilizer is conductive for weakening the utilization of heavy metals in paddy soils. Specifically, flooding is a method to decrease GCA in rice, with additional benefits observed when lime is concurrently applied (Han et al. 2018). However, it’s worth noting that flooding may lead to increased arsenic accumulation in crops (Hu et al. 2013). Notably, the implementation of film mulch technology, as demonstrated by Wang et al. (2015), exhibited a 50% reduction in GCA in rice when comparing to the control. Under the condition of collective use of complementary measures (like biochar and silica foliar fertilizer), the reduction in GCA content is enhanced. Current research is actively exploring effects of various factors, individually or jointly, in controlling Cd contamination in plant tissues a (Tang et al. 2020). While these investigations offer valuable insights, a more systematic approach is required, necessitating further comprehensive research in this domain.
Applying fertilizers and soil conditioners judiciously can enhance the physical and chemical properties of soil, diminish plant Cd uptake from soil, and foster plant growth. The extent of GCA is intricately linked to Cd bioavailability in soil. Within a specific range of soil pH values, soil acidification has been identified as a factor that amplifies the available Cd content in the soil, subsequently elevating GCA (Chen et al. 2021). Conversely, alkaline soil amendments can form Cd complexes, chelates, and precipitates, effectively weakening the bioavailability of soil Cd (Hamid et al. 2019; Jin et al. 2020). Huang et al. (2020) applied quicklime for 4 consecutive years to manage soil acidity in Cd-polluted farm soils. The outcomes revealed an average increase in soil pH by 0.57, a 17% reduction in interchangeable or water-soluble Cd components in soil, a 10% increase in organic binding of Cd components, and a decline in GCA concentration in crops below the threshold (0.2 mg kg− 1). Various physical and biochemical soil amendments, like engineered nanoparticles (Fox et al. 2020), salicylic acid (Li et al. 2019; Majumdar et al. 2020), and melatonin (Lv et al. 2019), have been employed to mitigate plant Cd uptake. Sarwar et al. (2015) demonstrated that spraying a ZnSO4 solution at a specific concentration onto wheat leaves during the booting completes with Cd uptake, effectively reducing the GCA in wheat and crops grown on soil suffering from Cd pollution.
Isolating and identifying Cd-tolerant microorganisms from soil suffering from Cd pollution and exploring the potential of plant-microbial symbiosis for Cd remediation offer promising avenues for soil bioremediation and mitigating GCA (Abbas et al. 2020). Wang et al. (2019) demonstrated that treating soil suffering from Cd pollution the fermentation broth of Bacillus cereus strain M4 could enhance the growth of pot-grown rice seedlings in soil after Cd pollution, resulting in a decrease in the GCA in rice from 0.309 to 0.186 mg kg− 1. Arbuscular mycorrhizal fungi, which naturally colonize in plant roots, contribute to its growth and is key in conferring tolerance to heavy metals (Garg and Bhandari 2014). Pseudomonas taiwanensis WRS8 associated with wheat has been shown to reduce Cd uptake. This is achieved by enhancing the adsorption of Cd on the root surface suppressing the expression of genes linked to Cd uptake and transport in wheat. In contrast to the controls, there was a substantial reduction in Cd levels in both roots (78–85%) and above-ground tissues (88–94%) at days 3 and 10 after inoculation, respectively (Cheng et al. 2021). Li et al. (2020) observed that arbuscular mycorrhizal fungi reduces GCA in maize but may also have adverse effects on maize seedling growth. This highlights the need for further exploration and optimization in the selection and application of microorganisms for soil Cd remediation.
Genetic improvement
The cultivation of crops containing LCd represents a strongly effective approach for mitigating the risk of GCA in crops and safeguarding human health (Grant et al. 2008; Ishikawa 2020; Liu et al. 2020a; ZaidImdad et al. 2018). The breeding technologies employed for crops with LCd have evolved from traditional breeding approaches to a synergistic blend of traditional and molecular breeding methods. This progression signifies a shift from empirical breeding practices to more precise and design-oriented breeding strategies.
Efforts to mitigate grain GCA involve manipulating Cd transporter proteins through strategies such as overexpression or knockout of the transporter genes, and MAS breeding based on genotypic differences in GCA (Ma et al. 2021). Chen et al. (2020) employed molecular marker-assisted breeding to individually introgress the OsHMA3 gene or the qlGCd3 QTL, both associated with LCd accumulation, into the recipient parent rice accession ‘C5S’. The resulting improved material consistently expressed the LCd trait, with the average grain Cd concentration reduced by 52.8% or 50.8% for those carrying OsHMA3 or qlGCd3, respectively, compared to wild-type ‘C5S’. Several studies highlighted negative associations between Cd uptake and the concentrations of other mineral elements when a plant grows (Hou et al. 2021; Jia et al. 2016). HCd accumulation varieties tend to over-accumulate calcium, magnesium, manganese, iron, zinc, and other mineral elements, while wheat grain of LCd varieties may be deficient in essential nutrients (Qin et al. 2021). In rice, OsNramp5 serves as the major transporter for both Cd and manganese (Mn). Yang et al. (2019b) employed the CRISPR-Cas9 gene editing technique to knock out OsNramp5 in two japonica rice cultivars, leading to significantly lower GCA concentrations, albeit with reduced Mn accumulation. This negatively impacted various agronomic traits, including plant height, seed setting rate, and grain number per panicle, resulting in a slight decrease in crop yield. Some LCd cultivars maintain normal concentrations of essential minerals (Luo et al. 2018), making them valuable parental materials for LCd cultivar breeding. Through conventional and molecular breeding techniques, either individually or in combination, valuable alleles, such as lcd, have been selected or designed and integrated into new cultivars to achieve a balance between high yield and quality with low GCA.
Conclusion and future perspectives
The comprehension of physiological regulatory mechanisms in plants exposed to Cd is advancing. However, there is a lack of systematic exploration into the physiological mechanisms governing Cd distribution and accumulation in crops. For example, the mechanisms behind LCd accumulation in the storage roots of sweet potatoes remain unclear. This includes the factors influencing why the Cd absorbed by root is accumulated primarily in the feeder roots rather than storage roots (Zhang et al. 2020). Such uncertainties may be attributed to the limitations in conditions and facilities in the research process. Many studies focusing on the physiology of regulating Cd stress during the seedling stage, but there is a relative scarcity of corresponding research at later growth stages, an important point because GCA is primarily determined during the reproductive stage.
In major crops, predecessors have identified several QTLs for GCA that exhibit stability across multiple populations, generations, environments, and mapping methods. These reliable QTLs hold potential for application in MAS. However, it’s noteworthy that some QTLs for GCA are consistently localized on the same chromosomes across different studies. The absence of bridge markers necessitates further confirmation of the consistency and stability of these QTLs through the accumulation of additional data in future investigations. In conjunction with QTL identification and gene cloning efforts, seven candidate genes, namely OsHMA3, OsNRAMP1, OsNRAMP5, OsLCD, CAL1, OsABCB24, and OsCd1, which co-located with major-effect QTLs, were identified, although this represents a limited number. Consequently, there is a need to identify and validate Cd-related functional markers or regulatory genes with practical breeding significance. At present, most studies involve only the growth or physiological metabolic responses of crops to Cd, with limited attempts to elucidate the physiological regulation routes induced by Cd-related genes in crops. Hence, it is imperative to systematically analyze the molecular foundation of physiological traits related to Cd accumulation.
The strategies aimed at reducing GCA by diminishing Cd bioavailability in the soil through physical, chemical, or biological interventions have been extensively studied and can be promptly applied in the short term to crop production systems. However, research focused on reducing grain Cd concentration in crops at the genetic level is mostl predominantly in the initial or theoretical research stage. In contrast, most of the varieties with LCd have been identified employing traditional screening methods, and there are few reports on the development of varieties with consistently stable LCd grain based on modern biotechnologies. By combining comparative grain Cd concentration evaluation and LCd allelic genotyping, Sun et al. (2022) successfully developed a new variety with LCd (‘Lushansimiao’), which exhibited low GCA content in large-scale field trials. However, the stability of this variety requires further investigation under diverse production conditions, environments, and years. Future breeding endeavors should concentrate on integrating traditional and molecular techniques to accurately pyramid multiple valuable LCd accumulation alleles, and finally giving rise to new crop varieties characterized by high yield, excellent quality, and LCd accumulation.
References
Abbas S, Javed MT, Shahid M, Hussain I, Haider MZ, Chaudhary HJ, Tanwir K, Maqsood A (2020) Acinetobacter sp. SG-5 inoculation alleviates cadmium toxicity in differentially cd tolerant maize cultivars as deciphered by improved physio-biochemical attributes, antioxidants and nutrient physiology. Plant Physiol Biochem 155:815–827. https://doi.org/10.1016/j.plaphy.2020.08.024
Ahmad P, Sarwat M, Bhat NA, Wani MR, Kazi AG, Tran LS (2015) Alleviation of cadmium toxicity in Brassica juncea L. (Czern. & Coss.) by calcium application involves various physiological and biochemical strategies. PLoS One 10 (1):e0114571. https://doi.org/10.1371/journal.pone.0114571
Ban Y, Ishikawa G, Ueda H, Ishikawa N, Kato K, Takata K, Matsuyama M, Handa H, Nakamura T, Yanaka M (2020) Novel quantitative trait loci for low grain cadmium concentration in common wheat (Triticum aestivum L). Breed Sci 70(3):331–341. https://doi.org/10.1270/jsbbs.19150
Benitez ER, Hajika M, Yamada T, Takahashi K, Oki N, Yamada N, Nakamura T, Kanamaru K (2010) A major QTL controlling seed cadmium accumulation in soybean. Crop Sci 50(5):1728–1734. https://doi.org/10.2135/cropsci2009.11.0664
Chang JD, Huang S, Yamaji N, Zhang W, Ma JF, Zhao FJ (2020) OsNRAMP1 transporter contributes to cadmium and manganese uptake in rice. Plant Cell Environ 43(10):2476–2491. https://doi.org/10.1111/pce.13843
Chen HP, Zhang WW, Yang XP, Wang P, McGrath Steve P, Zhao FJ (2018) Effective methods to reduce cadmium accumulation in rice grain. Chemosphere 207:699–707. https://doi.org/10.1016/j.chemosphere.2018.05.143
Chen Q, Wu FB (2020) Breeding for low cadmium accumulatin cereals. J Zhejiang, Univ-Sci B, (Biomedicine & Biotechnology) 21(06):442–459. https://doi.org/10.1631/jzus.B1900576
Chen QH, Tang W, Zeng G, Sheng HW, Shi WJ, Xiao YH (2020) Reduction of cadmium accumulation in the grains of male sterile rice Chuang-5S carrying Pi48 or Pi49 through marker-assisted selection. 3 Biotech 10(12):539. https://doi.org/10.1007/s13205-020-02533-6
Chen JL, Zheng C, Ruan JZ, Zhang CH, Ge Y (2021) Cadmium bioavailability and accumulation in rice grain are controlled by pH and Ca in paddy soils with high geological background of transportation and deposition. B Environ Contam Tox 106(1):92–98. https://doi.org/10.1007/s00128-020-03067-6
Cheng C, Wang Q, Wang QX, He LY, Sheng XF (2021) Wheat-associated Pseudomonas taiwanensis WRS8 reduces cadmium uptake by increasing root surface cadmium adsorption and decreasing cadmium uptake and transport related gene expression in wheat. Environ Pollut 268. https://doi.org/10.1016/j.envpol.2020.115850. (Pt A):115850
Dias MC, Monteiro C, Moutinho-Pereira J, Correia C, Gonçalves B, Santos C (2013) Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta Physiol Plant 35(4):1281–1289. https://doi.org/10.1007/s11738-012-1167-8
Fan JL, Wei XZ, Wan LC, Zhang LY, Zhao XQ, Liu WZ, Hao HQ, Zhang HY (2011) Disarrangement of actin filaments and Ca2+ gradient by CdCl2 alters cell wall construction in Arabidopsis thaliana root hairs by inhibiting vesicular trafficking. J Plant Physiol 168(11):1157–1167. https://doi.org/10.1016/j.jplph.2011.01.031
Feng J, Jia W, Lv S, Bao H, Miao F, Zhang X, Wang J, Li J, Li D, Zhu C, Li S, Li Y (2018) Comparative transcriptome combined with morpho-physiological analyses revealed key factors for differential cadmium accumulation in two contrasting sweet sorghum genotypes. Plant Biotechnol J 16(2):558–571. https://doi.org/10.1111/pbi.12795
Fox JP, Capen Jonathan D, Zhang WL, Ma XM, Rossi L (2020) Effects of cerium oxide nanoparticles and cadmium on corn (Zea mays L.) seedlings physiology and root anatomy. NanoImpact 20:100264. https://doi.org/10.1016/j.impact.2020.100264
Franzaring J, Fangmeier A, Schlosser S, Hahn V (2019) Cadmium concentrations in German soybeans are elevated in conurbations and in regions dominated by mining and the metal industry. J Sci Food Agric 99(7):3711–3715. https://doi.org/10.1002/jsfa.9548
Fu Y, Zhatova H, Li Y, Liu Q, Trotsenko V, Li C (2022) Physiological and transcriptomic comparison of two sunflower (Helianthus annuus L.) cultivars with high/Low cadmium accumulation. Front Plant Sci 13:854386. https://doi.org/10.3389/fpls.2022.854386
Gao L, Chang JD, Chen RJ, Li HB, Lu HF, Tao LX, Xiong J (2016) Comparison on cellular mechanisms of iron and cadmium accumulation in rice: prospects for cultivating Fe-rich but Cd-free rice. Rice (New York NY) 9(1):39. https://doi.org/10.1186/s12284-016-0112-7
Garg N, Bhandari P (2014) Cadmium toxicity in crop plants and its alleviation by arbuscular mycorrhizal (AM) fungi: an overview. Plant Biosyst 148(4):609–621. https://doi.org/10.1080/11263504.2013.788096
Grant CA, Clarke JM, Duguid S, Chaney RL (2008) Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ 390(2–3):301–310. https://doi.org/10.1016/j.scitotenv.2007.10.038
Gray CW, Yi ZC, Munir K, Lehto NJ, Robinson BH, Cavanagh JAE (2019) Cadmium concentrations in New Zealand wheat: effect of cultivar type, soil properties, and crop management. J Environ Qual 48(3):701–708. https://doi.org/10.2134/jeq2018.12.0430
Grill E, Winnacker EL, Zenk MH (1987) Phytochelatins, a class of heavy-metal-binding peptides from plants, are functionally analogous to metallothioneins. PNAS 84(2):439–443. https://doi.org/10.1073/pnas.84.2.439
Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465(1–2):190–198. https://doi.org/10.1016/s0005-2736(00)00138-3
Guo JY, Li K, Zhang XZ, Huang HG, Huang F, Zhang L, Wang YD, Li TX, Yu HY (2019) Genetic properties of cadmium translocation from straw to brown rice in low-grain cadmium rice (Oryza sativa L.) line. Ecotox Environ saf 182:109422. https://doi.org/10.1016/j.ecoenv.2019.109422
Guo JY, Zhang XZ, Ye DH, Huang HH, Wang YD, Zheng ZC, Li TX, Yu HY (2020) Crucial roles of cadmium retention in nodeII for restraining cadmium transport from straw to ear at reproductive period in a grain low-cadmium rice line (Oryza sativa L). Ecotoxicol Environ Saf 205:111323. https://doi.org/10.1016/j.ecoenv.2020.111323
Hamid Y, Tang L, Sohail Muhammad I, Cao XR, Hussain B, Aziz Muhammad Z, Usman M, He ZL, Yang XE (2019) An explanation of soil amendments to reduce cadmium phytoavailability and transfer to food chain. Sci Total Environ 660:80–96. https://doi.org/10.1016/j.scitotenv.2018.12.419
Han XQ, Xiao XY, Guo ZH, Xie YH, Zhu HW, Peng C, Qin LY (2018) Release of cadmium in contaminated paddy soil amended with NPK fertilizer and lime under water management. Ecotox Environ saf 159:38–45. https://doi.org/10.1016/j.ecoenv.2018.04.049
Hao XH, Zeng M, Wang J, Zeng ZW, Dai JL, Xie ZJ, Yang YZ, Tian LF, Chen LB, Li DP (2018) A node-expressed transporter OsCCX2 is involved in grain cadmium accumulation of rice. Front Plant Sci 9:476. https://doi.org/10.3389/fpls.2018.00476
Harris NS, Taylor GJ (2013) Cadmium uptake and partitioning in durum wheat during grain filling. BMC Plant Biol 13:103. https://doi.org/10.1186/1471-2229-13-103
Hart JJ, Welch RM, Norvell WA, Sullivan LA, Kochian LV (1998) Characterization of cadmium binding, uptake, and translocation in intact seedlings of bread and durum wheat cultivars. Plant Physiol 116(4):1413–1420. https://doi.org/10.1104/pp.116.4.1413
Hou QY, Yang ZF, Ji JF, Yu T, Yuan JX (2021) Effects of soil pH and mineral nutrients on cadmium uptake by rice grain in the Pearl River Delta, China. Bull Environ Contam Toxicol 1–10. https://doi.org/10.1007/s00128-020-03057-8
Hu PJ, Huang JX, Ouyang YN, Wu LH, Song J, Wang SF, Li Z, Han CL, Zhou LQ, Huang YJ, Luo YM, Christie P (2013) Water management affects arsenic and cadmium accumulation in different rice cultivars. Environ Geochem Health 35(6):767–778. https://doi.org/10.1007/s10653-013-9533-z
Hu Y, Cheng H, Tao S (2016) The challenges and solutions for cadmium-contaminated rice in China: a critical review. Environ Int 92–93:515–532. https://doi.org/10.1016/j.envint.2016.04.042
Huang Y, Sheng H, Zhou P, Zhu ZY (2020) Remediation of Cd-contaminated acidic paddy fields with four-year consecutive liming. Ecotox Environ Saf 188:109903. https://doi.org/10.1016/j.ecoenv.2019.109903
Hussain B, Umer Muhammad J, Li JM, Ma YB, Abbas Y, Ashraf Muhammad N, Tahir N, Ullah A, Gogoi N, Farooq M (2021) Strategies for reducing cadmium accumulation in rice grains. J Clean Prod 286. https://doi.org/10.1016/J.JCLEPRO.2020.125557
Ishikawa S (2020) Mechanisms of cadmium accumulation in rice grains and molecular breeding for its reduction. Soil Sci Plant Nutr 66(1):28–33. https://doi.org/10.1080/00380768.2020.1719806
Ishikawa S, Ae N, Yano M (2005) Chromosomal regions with quantitative trait loci controlling cadmium concentration in brown rice (Oryza sativa). New Phytol 168(2):345–350. https://doi.org/10.1111/j.1469-8137.2005.01516.x
Ishikawa S, Abe T, Kuramata M, Yamaguchi M, Ando T, Yamamoto T, Yano M (2010) A major quantitative trait locus for increasing cadmium-specific concentration in rice grain is located on the short arm of chromosome 7. J Exp Bot 61(3):923–934. https://doi.org/10.1093/jxb/erp360
Ishikawa S, Ishimaru Y, Igura M, Kuramata M, Abe T, Senoura T, Hase Y, Arao T, Nishizawa NK, Nakanishi H (2012) Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. PNAS 109(47):19166–19171. https://doi.org/10.1073/pnas.1211132109
Jaouani K, Karmous I, Ostrowski M, Ferjani EE, Jakubowska A, Chaoui A (2018) Cadmium effects on embryo growth of pea seeds during germination: investigation of the mechanisms of interference of the heavy metal with protein mobilization-related factors. J Plant Physiol 226:64–76. https://doi.org/10.1016/j.jplph.2018.02.009
Jegadeesan S, Yu KF, Poysa V, Gawalko E, Morrison MJ, Shi C, Cober E (2010) Mapping and validation of simple sequence repeat markers linked to a major gene controlling seed cadmium accumulation in soybean [ Glycine max (L.) Merr]. Theor Appl Genet 121(2):283–294. https://doi.org/10.1007/s00122-010-1309-6
Jia WT, Lv SL, Feng JJ, Li JH, Li Y, Xin, Li SZ (2016) Morphophysiological characteristic analysis demonstrated the potential of sweet sorghum (Sorghum bicolor (L.) Moench) in the phytoremediation of cadmium-contaminated soils. Environ Sci Pollut Res Int 23(18):18823–18831. https://doi.org/10.1007/s11356-016-7083-5
Jin ZH, Zhang M, Li R, Zhang X, Wang GL, Liu XS, Qu JJ, Jin Y (2020) Spent mushroom substrate combined with alkaline amendment passivates cadmium and improves soil property. Environ Sci Pollut Res Int 27(2):16317–16325. https://doi.org/10.1007/s11356-020-08099-3
Kang ZM, Zhang WY, Qin JH, Li S, Yang X, Wei X, Li HS (2020) Yield advantage and cadmium decreasing of rice in intercropping with water spinach under moisture management. Ecotoxicol Environ Saf 190(c):110102. https://doi.org/10.1016/j.ecoenv.2019.110102
Knox RE, Pozniak CJ, Clarke FR, Clarke JM, Houshmand S, Singh AK (2009) Chromosomal location of the cadmium uptake gene (Cdu1) in durum wheat. Genome 52(9):741–747. https://doi.org/10.1139/g09-042
Kocaman A (2023) Combined interactions of amino acids and organic acids in heavy metal binding in plants. Plant Signal Behav 18(1):2064072. https://doi.org/10.1080/15592324.2022.2064072
Li H, Luo N, Li YW, Cai QY, Li HY, Mo CH, Wong MH (2017) Cadmium in rice: transport mechanisms, influencing factors, and minimizing measures. Environ Pollut 224:622–630. https://doi.org/10.1016/j.envpol.2017.01.087
Li Q, Wang G, Wang YR, Yang D, Guan CF, Ji J (2019) Foliar application of salicylic acid alleviate the cadmium toxicity by modulation the reactive oxygen species in potato. Ecotoxicol Environ Saf 172:317–325. https://doi.org/10.1016/j.ecoenv.2019.01.078
Li SB, Cao L, Qin L, He YM, Zhan FD, Li B, Duan HP (2020) Effects of arbuscular mycorrhizal fungi on root traits, photosynthetic physiology and cadmium accumulation of sand-cultured maize seedlings. Microbiol China 47(11):3822–3832
Lin K, Zeng M, Williams DV, Hu W, Shabala S, Zhou M, Cao F (2022) Integration of transcriptome and metabolome analyses reveals the mechanistic basis for cadmium accumulation in maize. iScience 25(12):105484. https://doi.org/10.1016/j.isci.2022.105484
Liu XJ, Tian GJ, Jiang D, Zhang C, Kong LQ (2016a) Cadmium (Cd) distribution and contamination in Chinese paddy soils on national scale. Environ Sci Pollut Res Int 23(18):17941–17952. https://doi.org/10.1007/s11356-016-6968-7
Liu Y, Liu K, Li Y, Yang WQ, Wu FZ, Zhu P, Zhang J, Chen LH, Gao S, Zhang L (2016b) Cadmium contamination of soil and crops is affected by intercropping and rotation systems in the lower reaches of the Minjiang River in south-western China. Environ Geochem Health 38(3):811–820
Liu XS, Feng SJ, Zhang BQ, Wang MQ, Cao HW, Rono JK, Chen X, Yang ZM (2019a) OsZIP1 functions as a metal efflux transporter limiting excess zinc, copper and cadmium accumulation in rice. BMC Plant Biol 19(1):283. https://doi.org/10.1186/s12870-019-1899-3
Liu XY, Chen SL, Chen MX, Zheng GY, Peng Y, Shi XL, Qin P, Xu XY, Teng S (2019b) Association study reveals genetic loci responsible for arsenic, cadmium and lead accumulation in rice grain in contaminated farmlands. Front Plant Sci 10:61. https://doi.org/10.3389/fpls.2019.00061
Liu C, Ding S, Zhang A, Hong K, Jiang H, Yang S, Ruan B, Zhang B, Dong G, Guo L, Zeng D, Qian Q, Gao Z (2020a) Development of nutritious rice with high zinc/selenium and low cadmium in grains through QTL pyramiding. J Integr Plant Biol 62(3):349–359. https://doi.org/10.1111/jipb.12909
Liu CL, Gao ZY, Shang LG, Yang CH, Ruan BP, Zeng DL, Guo LB, Zhao FJ, Huang CF, Qian Q (2020b) Natural variation in the promoter of OsHMA3 contributes to differential grain cadmium accumulation between Indica and Japonica rice. J Integr Plant Biol 62(3):314–329. https://doi.org/10.1111/jipb.12794
Liu T, Sun L, Meng Q, Yu J, Weng L, Li J, Deng L, Zhu Q, Gu X, Chen C, Teng S, Xiao G (2021) Phenotypic and genetic dissection of cadmium accumulation in roots, nodes and grains of rice hybrids. Plant Soil 1–15. https://doi.org/10.1007/S11104-021-04877-1
Luo L, Ma YB, Zhang SZ, Wei DW, Zhu YG (2009) An inventory of trace element inputs to agricultural soils in China. J Environ Manage 90(8):2524–2530. https://doi.org/10.1016/j.jenvman.2009.01.011
Luo JS, Huang J, Zeng DL, Peng JS, Zhang GB, Ma HL, Guan Y, Yi HY, Fu YL, Han B, Lin HX, Qian Q, Gong JM (2018) A defensin-like protein drives cadmium efflux and allocation in rice. Nat Commun 9(1):645. https://doi.org/10.1038/s41467-018-03088-0
Lv XC, Fang YX, Zhang LT, Zhang WY, Xu L, Han JJ, Jin BL, Zhang X, Zhang XQ, Xue DW (2019) Effects of melatonin on growth, physiology and gene expression in rice seedlings under cadmium stress. Phyton-Int J Exp Bot 88(2):91–100. https://doi.org/10.32604/phyton.2019.06622
Ma JF, Shen RF, Shao JF (2021) Transport of cadmium from soil to grain in cereal crops: a review. Pedosphere 31(1):3–10. https://doi.org/10.1016/S1002-0160(20)60015-7
Ma C, Xie P, Yang J, Lin L, Zhang K, Zhang H (2022) Evaluating the contributions of leaf organ to wheat grain cadmium at the filling stage. Sci Total Environ 833:155217. https://doi.org/10.1016/j.scitotenv.2022.155217
Majumdar S, Sachdev S, Kundu R (2020) Salicylic acid mediated reduction in grain cadmium accumulation and amelioration of toxicity in Oryza sativa L. Cv Bandana. Ecotoxicol Environ Saf 205:111167. https://doi.org/10.1016/j.ecoenv.2020.111167
Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, Katou K, Kodama I, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H (2011) OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189(1):190–199. https://doi.org/10.1111/j.1469-8137.2010.03459.x
Oladzad-Abbasabadi A, Kumar A, Pirseyedi S, Salsman E, Dobrydina M, Poudel RS, AbuHammad WA, Chao S, Faris JD, Elias EM (2018) Identification and validation of a new source of low grain cadmium accumulation in durum wheat. G3 (Bethesda) 8 (3):923–932. https://doi.org/10.1534/g3.117.300370
Osmolovskaya N, Viet Vu D, Kuchaeva L (2018) The role of organic acids in heavy metal tolerance in plants. Biol Commun 63(1):9–16. https://doi.org/10.21638/spbu03.2018.103
Pan XW, Li YC, Liu WQ, Liu SX, Min J, Xiong HB, Dong Z, Duan YH, Yu YY, Li XX (2020) QTL mapping and candidate gene analysis of cadmium accumulation in polished rice by genome-wide association study. Sci Rep 10(1):11791. https://doi.org/10.1038/s41598-020-68742-4
Parrotta L, Guerriero G, Sergeant K, Cai G, Hausman JF (2015) Target or barrier? The cell wall of early- and later-diverging plants vs cadmium toxicity: differences in the response mechanisms. Front Plant Sci 6:133. https://doi.org/10.3389/fpls.2015.00133
Qin XM, Xia YT, Hu CX, Yu M, Shabala S, Wu SW, Tan QL, Xu SJ, Sun XC (2021) Ionomics analysis provides new insights into the co-enrichment of cadmium and zinc in wheat grains. Ecotoxicol Environ Saf 223:112623. https://doi.org/10.1016/j.ecoenv.2021.112623
Reyes-Hinojosa D, Lozada-Pérez CA, Cuevas YZ, López-Reyes A, Martínez-Nava G, Fernández-Torres J, Olivos-Meza A, Landa-Solis C, Gutiérrez-Ruiz MC, Castillo ERd K (2019) Toxicity of cadmium in musculoskeletal diseases. Environ Toxicol Pharmacol 72:103219. https://doi.org/10.1016/j.etap.2019.103219
Sandalio LM, Dalurzo HC, Gómez M, Romero MC, hyphen P (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52(364):12. https://doi.org/10.1093/jexbot/52.364.2115
Saraswat S, Rai JPN (2011) Complexation and detoxification of Zn and Cd in metal accumulating plants. Rev Environ Sci Bio/Technol 10(4):327–339. https://doi.org/10.1007/s11157-011-9250-y
Sarwar N, Ishaq W, Farid G, Shaheen MR, Imran M, Geng MJ, Hussain S (2015) Zinc-cadmium interactions: impact on wheat physiology and mineral acquisition. Ecotoxicol Environ Saf 122:528–536. https://doi.org/10.1016/j.ecoenv.2015.09.011
Sato H, Shirasawa S, Maeda H, Nakagomi K, Kaji R, Ohta H, Yamaguchi M, Nishio T (2011) Analysis of QTL for lowering cadmium concentration in rice grains from ‘LAC23’. Breed Sci 61(2):196–200. https://doi.org/10.1270/jsbbs.61.196
Satoh-Nagasawa N, Mori M, Nakazawa N, Kawamoto T, Nagato Y, Sakurai K, Takahashi H, Watanabe A, Akagi H (2012) Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol 53(1):213–224. https://doi.org/10.1093/pcp/pcr166
Shahid M, Dumat C, Khalid S, Niazi NK, Antunes PMC (2017) Cadmium bioavailability, uptake, toxicity and detoxification in soil-plant system. Rev Environ Contam Toxicol 241:73–137. https://doi.org/10.1007/398_2016_8
Shao JF, Xia J, Yamaji N, Shen RF, Ma JF (2018) Effective reduction of cadmium accumulation in rice grain by expressing OsHMA3 under the control of the OsHMA2 promoter. J Exp Bot 69(10):2743–2752. https://doi.org/10.1093/jxb/ery107
Shi GL, Li DJ, Wang YF, Liu CH, Hu ZB, Lou LQ, Rengel Z, Cai QS (2019) Accumulation and distribution of arsenic and cadmium in winter wheat (Triticum aestivum L.) at different developmental stages. Sci Total Environ 667:532–539. https://doi.org/10.1016/j.scitotenv.2019.02.394
Shimo H, Ishimaru Y, An G, Yamakawa T, Nakanishi H, Nishizawa NK (2011) Low cadmium (LCD), a novel gene related to cadmium tolerance and accumulation in rice. J Exp Bot 62(15):5727–5734. https://doi.org/10.1093/jxb/err300
Song X, Yue X, Chen W, Jiang H, Han Y, Li X (2019) Detection of cadmium risk to the photosynthetic performance of Hybrid Pennisetum. Front Plant Sci 10:798. https://doi.org/10.3389/fpls.2019.00798
Sui FQ, Zhao DK, Zhu HT, Gong YF, Tang Z, Huang XY, Zhang GQ, Zhao FJ (2019) Map-based cloning of a new total loss-of-function allele of OsHMA3 causes high cadmium accumulation in rice grain. J Exp Bot 70(10):2857–2871. https://doi.org/10.1093/jxb/erz093
Sun H, Chen Z-H, Chen F, Xie L, Zhang G, Vincze E, Wu F (2015) DNA microarray revealed and RNAi plants confirmed key genes conferring low Cd accumulation in barley grains. BMC Plant Biol 15(1):259. https://doi.org/10.1186/s12870-015-0648-5
Sun L, Wang RG, Tang WB, Chen YC, Zhou JQ, Ma HR, Li S, Deng HB, Han L, Chen YB, Tan YJ, Zhu YX, Lin DS, Zhu QH, Wang JR, Huang DY, Chen CY (2022) Robust identification of low-Cd rice varieties by boosting the genotypic effect of grain cd accumulation in combination with marker-assisted selection. J Hazard Mater 424. https://doi.org/10.1016/j.jhazmat.2021.127703. (Pt D):127703
Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK (2011) The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot 62(14):4843–4850. https://doi.org/10.1093/jxb/err136
Takahashi R, Bashir K, Ishimaru Y, Nishizawa NK, Nakanishi H (2012) The role of heavy-metal ATPases, HMAs, in zinc and cadmium transport in rice. Plant Signal Behav 7(12):1605–1607. https://doi.org/10.4161/psb.22454
Tan L, Zhu YX, Fan T, Peng C, Wang JR, Sun L, Chen CY (2019) OsZIP7 functions in xylem loading in roots and inter-vascular transfer in nodes to deliver Zn/Cd to grain in rice. Biochem Biophys Res Commun 512(1):112–118. https://doi.org/10.1016/j.bbrc.2019.03.024
Tanaka K, Fujimaki S, Fujiwara T, Yoneyama T, Hayashi H (2007) Quantitative estimation of the contribution of the phloem in cadmium transport to grains in rice plants (Oryza sativa L). Soil Sci Plant Nutr 53(1):72–77. https://doi.org/10.1111/j.1747-0765.2007.00116.x
Tang L, Mao B, Li Y, Lv Q, Zhang L, Chen C, He H, Wang W, Zeng X, Shao Y, Pan Y, Hu Y, Peng Y, Fu X, Li H, Xia S, Zhao B (2017) Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep 7(1):14438. https://doi.org/10.1038/s41598-017-14832-9
Tang L, Hamid Y, Zehra A, Shohag MJI, He ZL, Yang XE (2020) Endophytic inoculation coupled with soil amendment and foliar inhibitor ensure phytoremediation and argo-production in cadmium contaminated soil under oilseed rape-rice rotation system. Sci Total Environ 748. https://doi.org/10.1016/j.scitotenv.2020.142481
Tang B, Luo M, Zhang Y, Guo H, Li J, Song W, Zhang R, Feng Z, Kong M, Li H, Cao Z, Lu X, Li D, Zhang J, Wang R, Wang Y, Chen Z, Zhao Y, Zhao J (2021a) Natural variations in the P-type ATPase heavy metal transporter gene ZmHMA3 control cadmium accumulation in maize grains. J Exp Bot 72(18):6230–6246. https://doi.org/10.1093/jxb/erab254
Tang L, Dong JY, Tan LT, Ji ZY, Li Y, Sun YT, Chen CY, Lv QL, Mao BG, Hu YY, Zhao BG (2021b) Overexpression of OsLCT2, a low-affinity cation transporter gene, reduces cadmium accumulation in shoots and grains of rice. Rice (New York NY) 14(1):89. https://doi.org/10.1186/s12284-021-00530-8
Tian SQ, Liang S, Qiao K, Wang FH, Zhang YX, Chai TY (2019) Co-expression of multiple heavy metal transporters changes the translocation, accumulation, and potential oxidative stress of Cd and Zn in rice (Oryza sativa). J Hazard Mater 380:120853. https://doi.org/10.1016/j.jhazmat.2019.120853
Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma JF (2010) Gene limiting cadmium accumulation in rice. PNAS 107(38):16500–16505. https://doi.org/10.1073/pnas.1005396107
Unsal V, Dalkıran T, Çiçek M, Kölükçü E (2020) The role of natural antioxidants against reactive oxygen species produced by cadmium toxicity: a review. Adv Pharm Bull 10(2):184–202. https://doi.org/10.34172/apb.2020.023
Uraguchi S, Fujiwara T (2013) Rice breaks ground for cadmium-free cereals. Curr Opin Plant Biol 16(3):328–334. https://doi.org/10.1016/j.pbi.2013.03.012
Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S (2009) Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 60(9):2677–2688. https://doi.org/10.1093/jxb/erp119
Uraguchi S, Kamiya T, Sakamoto T, Kasai K, Sato Y, Nagamura Y, Yoshida A, Kyozuka J, Ishikawa S, Fujiwara T (2011) Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. PNAS 108(52):20959–20964. https://doi.org/10.1073/pnas.1116531109
Uraguchi S, Kamiya T, Clemens S, Fujiwara T (2014) Characterization of OsLCT1, a cadmium transporter from indica rice (Oryza sativa). Physiol Plant 151(3):339–347. https://doi.org/10.1111/ppl.12189
Vanderschueren R, Wantiez L, Blommaert H, Flores J, Chavez E, Smolders E (2023) Revealing the pathways of cadmium uptake and translocation in cacao trees (Theobroma cacao L.): A 108Cd pulse-chase experiment. Sci Total Environ 869:161816. https://doi.org/10.1016/j.scitotenv.2023.161816
Wang ME, Peng C, Chen WP (2015) Effects of rice cultivar and typical soil improvement measures on the uptake of cd in rice grains. Environ Sci Pollut Res Int 36(11):4283–4290. https://doi.org/10.13227/j.hjkx.2015.11.045
Wang CR, Liu ZQ, Huang YC, Zhang YN, Wang XH, Hu ZY (2019) Cadmium-resistant rhizobacterium Bacillus cereus M4 promotes the growth and reduces cadmium accumulation in rice (Oryza sativa L). Environ Toxicol Pharmacol 72:103265. https://doi.org/10.1016/j.etap.2019.103265
Wang CC, Tang Z, Zhuang JY, Tang Z, Huang XY, Zhao FJ (2020) Genetic mapping of ionomic quantitative trait loci in rice grain and straw reveals OsMOT1;1 as the putative causal gene for a molybdenum QTL qMo8. Mol Genet Genomics 295(2):391–407. https://doi.org/10.1007/s00438-019-01632-1
Wang K, Yan TZ, Xu SL, Yan X, Zhou QF, Zhao XH, Li YF, Wu ZX, Qin P, Fu CJ, Fu J, Zhou YB, Yang YZ (2021) Validating a segment on chromosome 7 of japonica for establishing low-cadmium accumulating indica rice variety. Sci Rep 11(1):6053. https://doi.org/10.1038/s41598-021-85324-0
Wu DZ, Sato K, Ma JF (2015) Genome-wide association mapping of cadmium accumulation in different organs of barley. New Phytol 208(3):817–829. https://doi.org/10.1111/nph.13512
Xin JP, Zhang Y, Tian RN (2018) Tolerance mechanism of Triarrhena sacchariflora (Maxim.) Nakai. Seedlings to lead and cadmium: translocation, subcellular distribution, chemical forms and variations in leaf ultrastructure. Ecotoxicol Environ Saf 165:611–621. https://doi.org/10.1016/j.ecoenv.2018.09.022
Yamaji N, Xia J, Mitani-Ueno N, Yokosho K, Feng Ma J (2013) Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiol 162(2):927–939. https://doi.org/10.1104/pp.113.216564
Yan JL, Wang PT, Wang P, Yang M, Lian XM, Tang Z, Huang CF, Salt David E, Zhao FJ (2016) A loss-of-function allele of OsHMA3 associated with high cadmium accumulation in shoots and grain of Japonica rice cultivars. Plant Cell Environ 39(9):1941–1954. https://doi.org/10.1111/pce.12747
Yan HL, Xu WX, Xie JY, Gao YW, Wu LL, Sun L, Feng L, Chen X, Zhang T, Dai CH, Li T, Lin XN, Zhang ZY, Wang XQ, Li FM, Zhu XY, Li JJ, Li ZC, Chen CY, Ma M, Zhang HL, He ZY (2019) Variation of a major facilitator superfamily gene contributes to differential cadmium accumulation between rice subspecies. Nat Commun 10(1):2562. https://doi.org/10.1038/s41467-019-10544-y
Yan Y, Sun QQ, Yang JJ, Zhang XW (2021) Source attributions of cadmium contamination in rice grains by Cadmium isotope composition analysis: a field study. Ecotoxicol Environl Saf 210:111865. https://doi.org/10.1016/j.ecoenv.2020.111865
Yang WM, Xu GC, Ji LY, Shang YE (2019a) Variation analysis is of cereals heavy metals limit standards of CAC, EU, USA, and China. J Food Sci Technol 37(01):16–19. https://doi.org/10.3969/j.issn.2095-6002.2019.01.003
Yang CH, Zhang Y, Huang CF (2019b) Reduction in cadmium accumulation in japonica rice grains by CRISPR/Cas9-mediated editing of OsNRAMP5. J Integr Agric 18(03):688–697. https://doi.org/10.1016/S2095-3119(18)61904-5
Yuan K, Wang CR, Zhang CB, Huang YC, Wang PP, Liu ZQ (2020) Rice grains alleviate cadmium toxicity by expending glutamate and increasing manganese in the cadmium contaminated farmland. Environ Pollut 262:114236. https://doi.org/10.1016/j.envpol.2020.114236
ZaidImdad U, Zheng X, Li XF (2018) Breeding low-cadmium wheat: progress and perspectives. Agronomy 8(11):249. https://doi.org/10.3390/agronomy8110249
Zhang XF, Gao B, Xia HP (2014) Effect of cadmium on growth, photosynthesis, mineral nutrition and metal accumulation of bana grass and vetiver grass. Ecotoxicol Environ Saf 106:102–108. https://doi.org/10.1016/j.ecoenv.2014.04.025
Zhang GM, Zheng TQ, Chen Z, Wang YL, Wang Y, Shi YM, Wang CC, Zhang LY, Ma JT, Deng LW, Li W, Xu TT, Liang CZ, Xu JL, Li ZK (2018) Joint exploration of favorable haplotypes for mineral concentrations in milled grains of rice (Oryza sativa L). Front Plant Sci 9:447. https://doi.org/10.3389/fpls.2018.00447
Zhang DW, Dong F, Zhang Y, Huang YL, Zhang CF (2020) Mechanisms of low cadmium accumulation in storage root of sweetpotato (Ipomoea batatas L). J Plant Physiol 254:153262–153262. https://doi.org/10.1016/j.jplph.2020.153262
Zhang D, Du Y, He D, Zhou D, Wu J, Peng J, Liu L, Liu Z, Yan M (2021a) Use of comparative transcriptomics combined with physiological analyses to identify key factors underlying cadmium accumulation in Brassica juncea L. Front Genet 12:655885. https://doi.org/10.3389/fgene.2021.655885
Zhang S, Song J, Wu LH, Chen Z (2021b) Worldwide cadmium accumulation in soybean grains and feasibility of food production on contaminated calcareous soils. Environ Pollut 269:116153. https://doi.org/10.1016/j.envpol.2020.116153
Zhao FJ, Wang P (2020) Arsenic and cadmium accumulation in rice and mitigation strategies. Plant Soil 1–21. https://doi.org/10.1007/s11104-019-04374-6
Zhao JL, Yang W, Zhang SH, Yang T, Liu Q, Dong JF, Fu H, Mao XX, Liu B (2018) Genome-wide association study and candidate gene analysis of rice cadmium accumulation in grain in a diverse rice collection. Rice (New York NY) 11(1):61. https://doi.org/10.1186/s12284-018-0254-x
Zheng X, Chen L, Li X (2018) Arabidopsis and rice showed a distinct pattern in ZIPs genes expression profile in response to cd stress. Bot Stud 59(1):22. https://doi.org/10.1186/s40529-018-0238-6
Zhong S, Li X, Li F, Pan D, Liu T, Huang Y, Wang Q, Yin H, Huang F (2023) Cadmium isotope fractionation and gene expression evidence for tracking sources of cd in grains during grain filling in a soil-rice system. Sci Total Environ 873:162325. https://doi.org/10.1016/j.scitotenv.2023.162325
Acknowledgements
The authors would like to thank Professor Zhongwen Huang (Henan Institute of Science and Technology, China) and Professor Dayong Zhang (Nanjing Agricultural University, China) for their scientific and editorial comments on the manuscript.
Funding
This work was supported by the Fundamental Research Project of Shanxi Province (20210302123081), the Key Research and Development Project of the Xinjiang Production and Construction Corps (2021AB010), and the Key Discipline Project of Food Science and Engineering of Yuncheng University (XK-2021013).
Author information
Authors and Affiliations
Contributions
CL wrote the draft. YF performed the literature search and data analysis. HZ drew the illustration. VT and CL revised and edited the work. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interest.
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Communicated by Jiayin Pang.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, C., Fu, Y., Trotsenko, V. et al. Understanding the physiological and molecular mechanisms of grain cadmium accumulation conduces to produce low cadmium grain crops: a review. Plant Growth Regul 103, 257–269 (2024). https://doi.org/10.1007/s10725-023-01105-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-023-01105-x