Next Article in Journal
Arsenic Neurotoxicity in Humans
Next Article in Special Issue
Selenium Modulates the Level of Auxin to Alleviate the Toxicity of Cadmium in Tobacco
Previous Article in Journal
Increased mtDNA Abundance and Improved Function in Human Barth Syndrome Patient Fibroblasts Following AAV-TAZ Gene Delivery
Previous Article in Special Issue
Heavy Metal Pollutions: State of the Art and Innovation in Phytoremediation
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJMS
Volume 20
Issue 14
10.3390/ijms20143417
ijms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Advances in the Uptake and Transport Mechanisms and QTLs Mapping of Cadmium in Rice

by
Jingguang Chen
1,2,
Wenli Zou
1,
Lijun Meng
1,*,
Xiaorong Fan
2,*,
Guohua Xu
2 and
Guoyou Ye
1,3
1
CAAS-IRRI Joint Laboratory for Genomics-Assisted Germplasm Enhancement, Agricultural Genomics Institute in Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518120, China
2
College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, China
3
Strategic Innovation Platform, International Rice Research Institute, DAPO Box 7777, Metro Manila 1226, Philippines
*
Authors to whom correspondence should be addressed.
Int. J. Mol. Sci. 2019, 20(14), 3417; https://doi.org/10.3390/ijms20143417
Submission received: 28 June 2019 / Revised: 10 July 2019 / Accepted: 11 July 2019 / Published: 11 July 2019
(This article belongs to the Special Issue Heavy Metals Accumulation, Toxicity and Detoxification in Plants)
Browse Figures
Versions Notes

Abstract

:
Cadmium (Cd), as a heavy metal, presents substantial biological toxicity and has harmful effects on human health. To lower the ingress levels of human Cd, it is necessary for Cd content in food crops to be reduced, which is of considerable significance for ensuring food safety. This review will summarize the genetic traits of Cd accumulation in rice and examine the mechanism of Cd uptake and translocation in rice. The status of genes related to Cd stress and Cd accumulation in rice in recent years will be summarized, and the genes related to Cd accumulation in rice will be classified according to their functions. In addition, an overview of quantitative trait loci (QTLs) mapping populations in rice will be introduced, aiming to provide a theoretical reference for the breeding of rice varieties with low Cd accumulation. Finally, existing problems and prospects will be put forward.

1. Introduction

Cadmium (Cd) is a soil contaminant and with a high mobility in living organisms, and is characterized as a toxic heavy metal [1,2]. In China, about 2.786 × 109 m2 of agricultural land is contaminated by Cd [3]. Frequent applications of nitrogen fertilizer in the agricultural land of many areas of China have resulted in more acidic soil, and acidic soil means that cadmium is more easily absorbed by plants [4]. Rice (Oryza sativa L.) is the main food for more than half of the world’s population. Cd is easily transferred from soil to rice and accumulates in rice plants and grains [2,3], and is then enriched in the human body through the food chain, thereby threatening human health [5,6,7], and causing effects such as anemia, cancer, heart failure, hypertension, cerebral infarction, proteinuria, severe lung damage, eye cataract formation, osteoporosis, emphysema, and renal insufficiency [8,9]. It is worth mentioning that Itai-itai disease, which occurred in Japan in the 1950s, was caused by the long-term intake of cadmium-contaminated rice [10]. On average, weekly Cd accumulation was as high as 3–4 mg kg−1 body weight in Japan at that time [11]. Between 1990 and 2015, the average dietary Cd intake of the general population more than doubled in China [12,13]. Therefore, reducing Cd uptake by crops, especially rice, is of great significance to food safety and human health.
The purpose of this review is to explore the mechanism of cadmium uptake and transport and the genetic characteristics of Cd accumulation in rice, and to summarize the research status of genes and QTLs related to cadmium stress and cadmium accumulation in rice. It has important guiding significance for breeding high-quality rice varieties with a low accumulation of Cd in grain and the safe production of rice in mild and moderate Cd-contaminated soil.

2. Toxic Effects of Cadmium Exposure on Rice

Cd stress seriously affects rice germination and growth [2,3,14,15,16,17,18], and it was found that excessive Cd exposure can not only significantly decrease the rice seed germination rate [14], but also cause chlorosis and necrosis in rice plants during the vegetative stage [19,20]. Cd stress causes severe physical and physiological changes in rice plants as it causes a reduction in the length; width; and number of roots, shoots, and leaves. Furthermore, chlorophyll contents, stomatal conductance, and the water use efficiency of rice are also significantly affected [3,17,18,21,22,23]. Cd also affects the absorption and transport of essential nutrients in rice [15,16,18,19,20]. Additionally, Cd can be transported to rice grains, reducing their yield, quality, and nutrients [15,16,24,25,26,27]. In general, Cd stress inhibits rice growth [18,28,29,30].
Rice possesses some tolerance mechanisms to cadmium at physiological and molecular levels [31,32,33,34,35]. As root cell walls of the outermost layer have direct contact with the soil solution, this protects the protoplasts against Cd toxicity [36,37,38]. Furthermore, plants reduce Cd translocation to the shoots by immobilizing Cd in the cell walls and vacuoles of root cells, thus reducing their sensitivity and the harm of Cd to another cellular organelle [39,40,41,42]. Several adenosine triphosphate (ATP)-binding cassette (ABC) proteins have been reported to mediate vacuolar compartmentation of Cd-glutathione and/or phytochelatin (PC) conjugates in Arabidopsis thaliana [43,44]. Rice OsPDR5/ABCG43 is likely to encode ABC-type protein functions in Cd extrusion from the cytoplasm [45]. Overexpression of Cd transporter OsHMA3 located in vacuole membranes in rice roots can increase the tolerance of rice to Cd and reduce the accumulation of Cd in grains [46,47]. Exudates of roots contain metal chelators which play a role in the adjustment of the rhizosphere pH and the metal chelating process [48]. Most of the chelated toxic metals inside plants target vacuoles through metal detoxification processes [38,49]. Organic acids secreted from roots, e.g., malate, citrate, etc., are involved in metal uptake, the long-distance transport of metal, and the transport of metal into vacuoles [50,51]. It was found that chelators play a crucial role in keeping Cd in the rice roots and form a barrier in Cd translocation [52].
Cd stress can induce plants to enhance their antioxidant defense system and regulate ion homeostasis to improve their tolerance to Cd [32,53,54,55,56,57,58]. For example, Cd stress can induce plants to increase the production of glutathione (GSH), abscisic acid (ABA), salicylic acid (SA), jasmonic acid (JA), and nitric oxide (NO) [59,60,61,62,63,64,65]. Mitogen-activated protein kinase OsWJUMK1, OsMSRMK2, OsMSRMK3, and OsMAPK2 can affect rice root growth under Cd stress by regulating auxin signal changes [66,67,68,69]. Auxin transporter OsAUX1 has been reported to be involved in root development and the Cd stress response in rice [34]. In addition, the concentration of iron and cadmium was positively correlated during rice seedling growth [70]. It has been reported that increasing the supply of boron, iron, zinc, silicon, or magnesium can reduce the accumulation and toxicity of cadmium in rice [71,72,73,74,75,76].
In addition, some genes related to Cd stress have been reported in rice (Table 1). OsHMA9 is a copper efflux protein located in the plasma membrane, which may have a cadmium efflux function to excrete Cd from root cells and reduce Cd accumulation in rice [77]. Knock-out of the low cadmium gene (LCD) reduced the accumulation of cadmium and increased the growth of rice under the condition of an excessive cadmium supply, and LCD may be a protein related to cadmium homeostasis [78]. Overexpression of OsCDT1 can increase the growth of Arabidopsis thaliana under cadmium treatment; the cysteine-rich peptide encoded by OsCDT1 is possibly involved in rice Cd tolerance [79]. OsCLT1 probably mediates the export of γ-glutamylcysteine and glutathione from plastids to the cytoplasm, which in turn affects As and Cd detoxification in rice [80].

3. Uptake and Transport Pathway of Cd in Rice

Cadmium is transported from the roots to shoots and then to grains through four steps: (i) uptake by roots; (ii) transportation to shoots through loading to the xylem; (iii) distribution and transportation through nodes; and (iv) transportation to grains through the phloem from leaf blades (Figure 1).

3.1. Functional Analysis of Related Genes

Cd can enter rice plants through the uptake mechanism of essential elements such as Mn, Zn, and Fe, etc. [106,107,119]. Fe2+ transporters OsIRT1 and OsIRT2 display Cd2+ influx activity in yeast, which indicates that OsIRT1 and OsIRT2 may play a role in cadmium uptake in the root system [95,120]. Overexpression of OsIRT1 significantly increased the accumulation of Cd in roots and shoots in Murashige & Skoog (MS) medium containing excess Cd, but no obvious phenotype was observed under field conditions, suggesting that OsIRT1 may be involved in cadmium uptake in roots, but its contribution is largely affected by environmental conditions [96]. Oryza sativa Natural Resistance-Associated Macrophage Protein 5 (OsNramp5), located at the plasma membrane of root cells, was found to be the major transporter of Cd uptake in rice roots, responsible for the transport of Cd from the soil solution to the root cells [106,107]. OsNramp5 is also an Mn transporter, and the knock-out of OsNramp5 can significantly reduce the uptake and accumulation of cadmium in grains, but also lead to the decrease of growth and yield due to manganese deficiency [107,108,109]. Recently, Liu et al. [121] located a major QTL, qGMN7.1, according to the Mn concentration in the grains of a recombinant inbred line (RILS) crossed between 93–11 (low grain Mn) and PA64s (high grain Mn). Fine mapping delimited qGMN7.1 to a 49.3 kb region containing OsNRAMP5, and sequence variations in the OsNRAMP5 promoter caused changes in its transcript level and in grain Mn levels. Tang et al. [110] reported that a series of new indica rice lines with low cadmium accumulation were developed by knocking out the metal transporter OsNramp5 using the CRISPR/CAS9 system. OsNRAMP1, located on the plasma membrane, also exhibits the activity of Cd transport, and participates in the uptake and transport of Cd in root cells [111,112]. OsZIP1, a zinc-regulated/iron-regulated transporter-like protein, expression in yeast can enhance its sensitivity to Cd [84], and the overexpression of OsZIP6 can increase the Cd uptake in X. laevis oocytes [98].
After root absorption, xylem-mediated Cd translocation from the roots to shoots is the main factor determining the cadmium accumulation in shoots [122]. OsHMA2 and OsHMA3 were reported to play a role in this process [46,103,123,124]. OsHMA2 participates in the transport of Cd from the roots to shoots and plays an important role in controlling the distribution of Cd through the phloem to developing tissues [103,104,123]. Compared with wild-type (WT) samples, the Cd concentration in the shoots of an oshma2 mutant was significantly lower [104]. OsHMA3 plays a role in the vacuolar sequestration of Cd in root cells, the overexpression of OsHMA3 reduces the Cd load in the xylem and Cd accumulation in shoots, and the functional deficiency of OsHMA3 results in very high root-to-shoot Cd translocation in rice [46,47,105,125]. Recent reports showed that OsCCX2, a putative cation/calcium (Ca) exchanger, was localized in the plasma membrane and plays an important role in Cd transport by impacting Cd root-to-shoot translocation and the Cd distribution in the shoot tissues, and the knock-out of OsCCX2 resulted in a significant Cd reduction in the grains [94]. Tan et al. [99] reported that OsZIP7 plays a key role in xylem-loading in roots and inter-vascular transfer in nodes to deliver Zn and Cd upward in rice.
Nodes are the central organ of Cd transport from the xylem to phloem, and play an important role in Cd transport to grains [126,127,128]. OsLCT1 is a Cd-efflux transporter on the plasma-membrane involved in phloem Cd transport [101]. OsLCT1 expression was higher in leaf blades and nodes during the reproductive stage, especially in node I. Compared with wild-type (WT), the Cd concentration in phloem exudates and in grains of OsLCT1 RNAi plants decreased significantly, although the Cd concentration in xylem sap did not differ. These results suggest that OsLCT1 in leaf blades functions in Cd remobilization by the phloem, and in node I, OsLCT1 is likely to play a part in intervascular Cd transfer from enlarged large vascular bundles to diffused vascular bundles, which connect to the panicle [101,102]). The positions of cloned cadmium stress-related genes in rice chromosomes are shown in Figure 2.

3.2. Location of Related QTLs

Rice varieties show obvious genetic variation in terms of their cadmium accumulation ability, which is a valuable resource for dissecting functional alleles and genetic improvement [19,20,25]. However, only a few quantitative trait loci (QTLs) related to cadmium accumulation in rice have been reported. OsHMA3, CAL1 (Cd Accumulation in Leaf 1), and OsCd1 are the only Cd-related QTLs cloned so far. OsHMA3 encodes a cadmium transporter located in the vacuole membrane, which transports cadmium into vacuoles for sequestration [105]. Loss of OsHMA3 function significantly increased cadmium transport to rice shoots and grains [101,129]. On the other hand, the overexpression of OsHMA3 can increase the tolerance of rice to Cd and reduce Cd accumulation in grains [46,105,119]. CAL1 (cadmium accumulation in leaf 1) was identified and cloned by Luo et al. [88] as a quantitative trait locus (QTL) in rice, which explained 13% of the variation in leaf cadmium concentration in a doubled haploid population. CAL1 regulates the root-to-shoot translocation of cadmium via the xylem vessels, and knockout mutants of CAL1 significantly reduced the concentration of cadmium in rice leaves [88]. Yan et al. [90] discovered that the gene OsCd1 belongs to the major facilitator superfamily through genome-wide association studies (GWAS), which was associated with divergence in rice grain Cd accumulation. Interestingly, the natural variation OsCd1V449 in Japonica, which is associated with a reduced Cd transport ability and decreased grain Cd accumulation, shows a potential value in low-Cd rice selection [90].
A series of QTLs related to rice varieties that control the Cd concentration in rice have been reported (Table 2). Ishikawa et al. [130] obtained a mapping population consisting of 85 back-cross inbred lines (BIL) from hybridization between a low-cadmium-accumulation variety of Japonica rice (Sasanishiki) and a high-cadmium-accumulation variety of Indica rice (Habataki). Two QTLs were located on chromosomes 2 and 7, separately, with an increased cadmium concentration in grains. qGCd7 plays an important role in increasing the cadmium concentration in grains, which can explain 35.5% of phenotypic variation [130]. Kashiwagi et al. [131] identified two QTLs, known as qcd4–1 and qcd4–2, affecting the cadmium concentration in shoots. Sato et al. [132] reported two QTLs controlling the cadmium concentration in brown rice: qLCdG11 explained 9.4%–12.9% of phenotypic variation and qLCdG3 explained 8.3%–13.9% of phenotypic variation. Yan et al. [133] constructed an recombinant inbred lines (RIL) population of F7 to identify Cd accumulation and distribution. A total of five main effect QTLs (scc10 was correlated with Cd accumulation in shoots; gcc3, gcc9, and gcc11 with Cd accumulation in grains; and sgr5 with the Cd distribution ratio in shoots and roots) were detected. Among them, sgr5 had the greatest effect on the distribution of Cd in grains. Abe et al. [134] used a population consisting of 46 chromosome segment substitution lines (CSSL) to identify eight QTLs related to the grain cadmium content by single-label analysis using ANOVA. The result showed that qlGCd3 had a high F-test value. A recombinant inbred population derived from Xiang 743/Katy was grown in Cd-polluted fields and used to map the QTLs for Cd accumulation in rice grains, and two QTLs, qCd-2 and qCd-7, were identified in 2014 and 2015 [135]. Liu et al. [136] used 276 accessions with 416 K single nucleotide polymorphisms (SNPs) and performed a genome-wide association analysis of grain Cd concentrations in rice grown in heavily multi-contaminated farmlands, and 17 QTLs were found to be responsible for the grain Cd concentration.

4. Future Perspectives

Cadmium is a kind of heavy metal that presents extreme biological toxicity. Cd accumulated in rice can enter the food chain, thereby threatening human health [5,6,7]. Cadmium in rice can be reduced by agronomic practices (including soil amendments, fertilizer management, water management, and tillage management) and bioremediation (including phytoremediation and microbial remediation) [18,145,146,147,148,149,150]. In addition, understanding the mechanism of cadmium translocation and the factors affecting cadmium accumulation in rice are also important for formulating effective strategies to reduce cadmium accumulation in rice. In recent years, some genes related to cadmium transport in rice have been studied, and significant progress has been made in understanding the mechanism of cadmium uptake and transport. In order to understand the mechanism of cadmium transport in rice, it is necessary to identify more unknown transporters or other molecules.
Biotechnology offers a promising approach to reducing the Cd content in rice grains. Mutations of the OsNramp5 gene result in obvious decreases in Cd uptake in roots and Cd accumulation in rice grains [106,108,151]. Using the CRISPR/Cas9 gene editing technology to knock out OsNramp5 in both parental lines, Tang et al. [110] generated a hybrid rice cultivar that accumulated very low levels of Cd in the grain. Another target for gene editing is OsLCT1, which is involved in the phloem transport of Cd from the vegetative tissues to the grains [101]. Knockdown of this gene by RNAi reduced the grain Cd concentration by 30%–50% [101]. Overexpression of functional OsHMA3 in Nipponbare decreased Cd translocation and Cd accumulation in rice grains [46,105]. Overexpression of OsHMA3 is a highly effective method for reducing Cd accumulation in Indica rice, and rice grains produced using this approach are almost Cd-free, with little effect on the grain yield or essential micronutrient concentrations [152].
However, commercial transgenic rice is not commonly accepted by the general public and prohibited in many countries. Ishikawa et al. [151] produced three rice mutants by carbon ion-beam irradiation, where cadmium was hardly detected in mutant seeds when planted in cadmium-contaminated paddy fields and there was no significant difference between the mutant and wild-type (WT) in agronomic traits, which could be directly applied to breeding projects. Another possible strategy is marker-assisted breeding, which uses molecular markers to track the genetic composition of rice and bred rice varieties. For example, identifying a low-cadmium-related QTL and then introducing it into high-cadmium cultivars might be a viable approach [122]. However, only a few of QTLs related to cadmium accumulation in rice have been cloned [90,105], and the natural allele variation of grain cadmium accumulation differences among rice varieties has not been fully explored. Further research is necessary to clone more QTLs for controlling grain Cd accumulation, thus providing tools for the marker-assisted molecular breeding of rice cultivars with a low accumulation of Cd in grains.

Author Contributions

J.C. and W.Z. wrote the first draft of the manuscript and organized the tables and figures; L.M and X.F. conceived and supervised their ideas; G.X. and G.Y. reviewed the manuscript. All authors read and approved the final manuscript.

Acknowledgments

This research was financially supported by the National Natural Science Foundation of China (No. 31601286 to L.M.); the CAAS Innovative Team Award to GY’s team, Shenzhen Science and Technology Projects (No. JSGG20160608160725473 to Q.Q.); the China Postdoctoral Science Foundation (No. 2016M590160 to L.M.); the Fundamental Research Funds for Central Non-profit Scientific Institution (to G.Y.); the Jiangsu Science Fund for Distinguished Young Scholars (Grant BK20160030 to X.F.); and Dapeng district industry development special funds (KY20180218).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. He, S.Y.; He, Z.L.; Yang, X.E.; Stoffella, P.J.; Baligar, V.C. Soil biogeochemistry, plant physiology, and phytoremediation of cadmium-contaminated soils. Adv. Agron. 2015, 134, 135–225. [Google Scholar]
  2. Song, W.E.; Chen, S.B.; Liu, J.F.; Chen, L.; Song, N.N.; Li, N.; Liu, B. Variation of Cd concentration in various rice cultivars and derivation of cadmium toxicity thresholds for paddy soil by species-sensitivity distribution. J. Integr. Agric. 2015, 14, 1845–1854. [Google Scholar] [CrossRef]
  3. Liu, F.; Liu, X.N.; Ding, C.; Wu, L. The dynamic simulation of rice growth parameters under cadmium stress with the assimilation of multi-period spectral indices and crop model. Field Crop. Res. 2015, 183, 225–234. [Google Scholar] [CrossRef]
  4. Zhao, K.L.; Fu, W.J.; Ye, Z.Q.; Zhang, C.S. Contamination and spatial variation of heavy metals in the soil-rice system in Nanxun County, Southeastern China. Int. J. Environ. Res. Public Health. 2015, 12, 1577–1594. [Google Scholar] [CrossRef] [PubMed]
  5. Xie, P.P.; Deng, J.W.; Zhang, H.M.; Ma, Y.H.; Cao, D.J.; Ma, R.X.; Liu, R.J.; Liu, C.; Liang, Y.G. Effects of cadmium on bioaccumulation and biochemical stress response in rice (Oryza sativa L.). Ecotox. Environ. Safe. 2015, 122, 392–398. [Google Scholar] [CrossRef]
  6. Xue, D.W.; Jiang, H.; Deng, X.X.; Zhang, X.Q.; Wang, H.; Xu, X.B.; Hu, J.; Zeng, D.L.; Guo, L.B.; Qian, Q. Comparative proteomic analysis provides new insights into cadmium accumulation in rice grain under cadmium stress. J. Hazard. Mater. 2014, 280, 269–278. [Google Scholar] [CrossRef] [PubMed]
  7. Aziz, R.; Rafiq, M.T.; Li, T.; Liu, D.; He, Z.; Stoffella, P.J.; Sun, K.; Xiaoe, Y. Uptake of cadmium by rice grown on contaminated soils and its bioavailability/toxicity in human cell lines (Caco-2/HL-7702). J. Agric. Food Chem. 2015, 63, 3599–3608. [Google Scholar] [CrossRef]
  8. Godt, J.; Scheidig, F.; Grosse-Siestrup, C.; Esche, V.; Brandenburg, P.; Reich, A.; Groneberg, D.A. The toxicity of cadmium and resulting hazards for human health. J. Occup Med. Toxicol. 2006, 1, 22. [Google Scholar] [CrossRef]
  9. Satarug, S.; Baker, J.R.; Urbenjapol, S.; Haswell-Elkins, M.; Reilly, P.E.; Williams, D.J.; Moore, M.R. A global perspective on cadmium pollution and toxicity in non-occupationally exposed population. Toxicol Lett. 2003, 137, 65–83. [Google Scholar] [CrossRef]
  10. Horiguchi, H.; Teranishi, H.; Niiya, K.; Aoshima, K.; Katoh, T.; Sakuragawa, N.; Kasuya, M. Hypoproduction of erythropoietin contributes to anemia in chronic cadmium intoxication — clinical-study on itai-itai disease in Japan. Arch. Toxicol. 1994, 68, 632–636. [Google Scholar] [CrossRef]
  11. Tsukahara, T.; Ezaki, T.; Moriguchi, J.; Furuki, K.; Shimbo, S.; Matsuda-Inoguchi, N.; Ikeda, M. Rice as the most influential source of cadmium intake among general Japanese population. Sci. Total Environ. 2003, 305, 41–51. [Google Scholar] [CrossRef]
  12. Song, Y.; Wang, Y.; Mao, W.; Sui, H.; Yong, L.; Yang, D.; Jiang, D.; Zhang, L.; Gong, Y. Dietary cadmium exposure assessment among the Chinese population. PLoS ONE 2017, 12, e0177978. [Google Scholar] [CrossRef] [PubMed]
  13. Chen, H.; Yang, X.; Wang, P.; Wang, Z.; Li, M.; Zhao, F.J. Dietary cadmium intake from rice and vegetables and potential health risk: A case study in Xiangtan, southern China. Sci. Total Environ. 2018, 639, 271–277. [Google Scholar] [CrossRef] [PubMed]
  14. Ahsan, N.; Lee, S.H.; Lee, D.G.; Lee, H.; Lee, S.W.; Bahk, J.D.; Lee, B.H. Physiological and protein profiles alternation of germinating rice seedlings exposed to acute cadmiumtoxicity. C. R. Biol. 2007, 330, 735–746. [Google Scholar] [CrossRef] [PubMed]
  15. Li, B.; Wang, X.; Qi, X.; Huang, L.; Ye, Z. Identification of rice cultivars with low brown rice mixed cadmium and lead contents and their interactions with the micronutrients iron, zinc, nickel and manganese. J. Environ. Sci. 2012, 24, 1790–1798. [Google Scholar] [CrossRef]
  16. Li, S.; Yu, J.; Zhu, M.; Zhao, F.; Luan, S. Cadmium impairs ion homeostasis by altering K+ and Ca2+ channel activities in rice root hair cells. Plant Cell Environ. 2012, 35, 1998–2013. [Google Scholar] [CrossRef]
  17. Wang, Y.; Jiang, X.; Li, K.; Wu, M.; Zhang, R.; Zhang, L.; Chen, G. Photosynthetic responses of Oryza sativa L. seedlings to cadmium stress: Physiological, biochemical and ultrastructural analyses. BioMetals 2014, 27, 389–401. [Google Scholar] [CrossRef]
  18. Kanu, A.S.; Ashraf, U.; Bangura, A.; Yang, D.M.; Ngaujah, A.S.; Tang, X. Cadmium (Cd) Stress in Rice; Phyto-Availability, Toxic Effects, and Mitigation Measures-A Critical Review. IOSR-JESTFT 2017, 11, 07–23. [Google Scholar]
  19. Liu, J.; Li, K.; Xu, J.; Liang, J.; Lu, X.; Yang, J.; Zhu, Q. Interaction of Cd and five mineral nutrients for uptake and accumulation in different rice cultivars and genotypes. Field Crop. Res. 2003, 83, 271–281. [Google Scholar] [CrossRef]
  20. Liu, J.G.; Liang, J.S.; Li, K.Q.; Zhang, Z.J.; Yu, B.Y.; Lu, X.L.; Yang, J.C.; Zhu, Q.S. Correlations between cadmium and mineral nutrients in absorption and accumulation in various genotypes of rice under cadmium stress. Chemosphere 2003, 52, 1467–1473. [Google Scholar] [CrossRef]
  21. Rascio, N.; Dalla Vecchia, F.; La Rocca, N.; Barbato, R.; Pagliano, C.; Raviolo, M.; Gonnelli, C.; Gabbrielli, R. Metal accumulation and damage in rice (cv. Vialone nano) seedlings exposed to cadmium. Environ. Exp. Bot. 2008, 62, 267–278. [Google Scholar] [CrossRef]
  22. Yu, H.; Wang, J.; Fang, W.; Yuan, J.; Yang, Z. Cadmiumaccumulation in different rice cultivars and screening for pollution safe cultivars of rice. Sci. Total Environ. 2006, 370, 302–309. [Google Scholar] [CrossRef] [PubMed]
  23. Zhang, X.; Gao, H.; Zhang, Z.; Wan, X. Influences of different ion channel inhibitors on the absorption of fluoride in tea plants (Camellia sinesis L.). Plant Growth Regul. 2013, 69, 99–106. [Google Scholar]
  24. Arao, T.; Ae, N. Genotypic variations in cadmium levels of rice grain. Soil Sci. Plant Nutr. 2003, 49, 473–479. [Google Scholar] [CrossRef]
  25. He, J.; Zhu, C.; Ren, Y.; Yan, Y.; Jiang, D. Genotypic variation in grain cadmium concentration of lowland rice. J. Plant Nutr. Soil Sci. 2006, 169, 711–716. [Google Scholar] [CrossRef]
  26. Liu, H.J.; Zhang, J.L.; Christie, P.; Zhang, F.S. Influence of external zinc and phosphorus supply on Cd uptake by rice (Oryza sativa L.) seedlings with root surface iron plaque. Plant Soil. 2007, 300, 105–115. [Google Scholar] [CrossRef]
  27. Rodda, M.S.; Li, G.; Reid, R.J. The timing of grain Cd accumulation in rice plants: The relative importance of remobilisation within the plant and root Cd uptake post flowering. Plant Soil. 2011, 347, 105–114. [Google Scholar] [CrossRef]
  28. Zhou, H.; Zhou, X.; Zeng, M.; Liao, B.H.; Liu, L.; Yang, W.T.; We, Y.M.; Qiu, Q.Y.; Wang, Y.J. Effects of combined amendments on heavy metal accumulation in rice (Oryza sativa L.) planted on contaminated paddy soil. Ecotoxicol. Environ. Saf. 2014, 101, 226–232. [Google Scholar] [CrossRef]
  29. Mostofa, M.G.; Rahman, A.; Ansary, M.M.U.; Watanabe, A.; Fujita, M.; Tran, L.S.P. Hydrogen sulfide modulates cadmium-induced physiological and biochemical responses to alleviate cadmium toxicity in rice. Sci. Rep. 2015, 5, 14078. [Google Scholar] [CrossRef]
  30. Rehman, M.Z.; Rizwan, M.; Ghafoor, A.; Naeem, A.; Ali, S.; Sabir, M.; Qayyum, M.F. Effect of inorganic amendments for in situ stabilization of cadmium in contaminated soils and its phyto-availability to wheat and rice under rotation. Environ. Sci. Pollut. Res. 2015, 22, 16897–16906. [Google Scholar] [CrossRef]
  31. Shah, K.; Nahakpam, S. Heat exposure alters the expression of SOD, POD, APX and CAT isozymes and mitigates low cadmium toxicity in seedlings of sensitive and tolerant rice cultivars. Plant Physiol. Biochem. 2012, 57, 106–113. [Google Scholar] [CrossRef] [PubMed]
  32. Zhang, C.; Yin, X.; Gao, K.; Ge, Y.; Cheng, W. Non-protein thiols and glutathione S-transferase alleviate Cd stress and reduce root-to-shoot translocation of Cd in rice. J. Plant Nutr Soil Sci. 2013, 176, 626–633. [Google Scholar] [CrossRef]
  33. Choppala, G.; Saifullah, M.F.; Bolan, N.; Bibi, S.; Iqbal, M.; Rengel, Z.; Kunhikrishnan, A.; Ashwath, N.; Ok, Y.S. Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit. Rev. Plant Sci. 2014, 33, 374–391. [Google Scholar] [CrossRef]
  34. Yu, C.; Sun, C.; Shen, C.; Wang, S.; Liu, F.; Liu, Y.; Chen, Y.; Li, C.; Qian, Q.; Aryal, B.; et al. The auxin transporter, OsAUX1, is involved in primary root and root hair elongation and in Cd stress responses in rice (Oryza sativa L.). Plant J. 2015, 83, 818–830. [Google Scholar] [CrossRef] [PubMed]
  35. Zhang, X.; Wu, H.; Chen, L.; Liu, L.; Wan, X. Maintenance of mesophyll potassium and regulation of plasma membrane H+-ATPase are associated with physiological responses of tea plants to drought and subsequent rehydration. Crop. J. 2018, 6, 611–620. [Google Scholar] [CrossRef]
  36. Parrotta, L.; Guerriero, G.; Sergeant, K.; Cai, G.; Hausman, J.F. Target or barrier? The cell wall of early- and later-diverging plants vs cadmium toxicity: Differences in the response mechanisms. Front. Plant Sci. 2015, 6, 133. [Google Scholar] [CrossRef] [PubMed]
  37. Loix, C.; Huybrechts, M.; Vangronsveld, J.; Gielen, M.; Keunen, E.; Cuypers, A. Reciprocal Interactions between Cadmium-Induced Cell Wall Responses and Oxidative Stress in Plants. Front. Plant Sci. 2017, 8, 1867. [Google Scholar] [CrossRef] [PubMed]
  38. Hall, J.L. Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot. 2002, 53, 1–11. [Google Scholar] [CrossRef] [PubMed]
  39. Qiu, Q.; Wang, Y.T.; Yang, Z.Y.; Yuan, J.G. Effects of phosphorus supplied in soil on subcellular distribution and chemical forms of cadmium in two Chinese flowering cabbage (Brassica parachinensis L.) cultivars differing in cadmium accumulation. Food Chem. Toxicol. 2011, 49, 2260–2267. [Google Scholar] [CrossRef] [PubMed]
  40. Wang, X.; Liu, Y.O.; Zeng, G.M.; Chai, L.Y.; Song, X.C.; Min, Z.Y.; Xiao, X. Subcellular distribution and chemical forms of cadmium in Bechmeria nivea (L.). Gaud. Environ. Exp. Bot. 2008, 62, 389–395. [Google Scholar] [CrossRef]
  41. Zhang, J.; Sun, W.; Li, Z.; Liang, Y.; Song, A. Cadmium fate and tolerance in rice cultivars. Agron. Sustain. Dev. 2009, 29, 483–490. [Google Scholar] [CrossRef]
  42. Fu, X.P.; Dou, C.M.; Chen, Y.X.; Chen, X.C.; Shi, J.Y.; Yu, M.G.; Xu, J. Subcellular distribution and chemical forms of cadmium in Phytolacca americana L. J. Hazard. Mater. 2011, 186, 103–107. [Google Scholar] [CrossRef] [PubMed]
  43. Kim, D.Y.; Bovet, L.; Maeshima, M.; Martinoia, E.; Lee, Y.S. The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J. 2007, 50, 207–218. [Google Scholar] [CrossRef] [PubMed]
  44. Park, J.; Song, W.Y.; Ko, D.; Eom, Y.; Hansen, T.H.; Schiller, M.; Lee, T.G.; Martinoia, E.; Lee, Y.S. The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J. 2012, 69, 278–288. [Google Scholar] [CrossRef] [PubMed]
  45. Oda, K.; Otani, M.; Uraguchi, S.; Akihiro, T.; Fujiwara, T. Rice ABCG43 is Cd inducible and confers Cd tolerance on yeast. Biosci. Biotech. Biochem. 2011, 75, 1211–1213. [Google Scholar] [CrossRef] [PubMed]
  46. Sasaki, A.; Yamaji, N.; Ma, J.F. Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice. J. Exp. Bot. 2014, 65, 6013–6021. [Google Scholar] [CrossRef] [PubMed]
  47. Ueno, D.; Koyama, E.; Yamaji, N.; Ma, J.F. Physiological, genetic, molecular characterization of a high-Cd-accumulating rice cultivar, Jarjan. J. Exp. Bot. 2011, 22, 2265–2272. [Google Scholar] [CrossRef] [PubMed]
  48. Dong, J.; Mao, W.H.; Zhang, G.P.; Wu, F.B.; Cai, Y. Root excretion and plant tolerance to cadmium toxicity—a review. Plant Soil Environ. 2007, 53, 193–200. [Google Scholar] [CrossRef]
  49. Haydon, M.J.; Cobbett, C.S. Transporters of ligands for essential metal ions in plants. New Phytol. 2007, 174, 499–506. [Google Scholar] [CrossRef] [PubMed]
  50. Jabeen, R.; Ahmad, A.; Iqbal, M. Phytoremediation of heavy metals: Physiological and molecular mechanisms. Bot. Rev. 2009, 75, 339–364. [Google Scholar] [CrossRef]
  51. Verbruggen, N.; Hermans, C.; Schat, H. Molecular mechanisms of metal hyperaccumulation in plants. New Phytol. 2009, 181, 759–776. [Google Scholar] [CrossRef] [PubMed]
  52. Nocito, F.F.; Lancilli, C.; Dendena, B.; Lucchini, G.; Sacchi, G.A. Cadmium retention in rice roots is influenced by cadmium availability, chelation and translocation. Plant Cell Environ. 2011, 34, 994–1008. [Google Scholar] [CrossRef] [PubMed]
  53. Hassan, M.J.; Shao, G.; Zhang, G. Influence of cadmium toxicity on growth and antioxidant enzyme activity in rice cultivars with different grain cadmium accumulation. J. Plant Nutr. 2005, 28, 1259–1270. [Google Scholar] [CrossRef]
  54. Hsu, Y.T.; Kao, C.H. Cadmium-induced oxidative damage in rice leaves is reduced by polyamines. Plant Soil. 2007, 291, 27–37. [Google Scholar] [CrossRef]
  55. Lin, R.; Wang, X.; Luo, Y.; Du, W.; Guo, H.; Yin, D. Effects of soil cadmium on growth, oxidative stress and antioxidant system in wheat seedlings Triticum aestivum L. Chemosphere 2007, 69, 89–98. [Google Scholar] [CrossRef]
  56. Roychoudhury, A.; Basu, S.; Sengupta, D.N. Antioxidants and stressrelated metabolites in the seedlings of two indica rice varieties exposed to cadmium chloride toxicity. Acta Physiol. Plant 2012, 34, 835–847. [Google Scholar] [CrossRef]
  57. Shen, G.M.; Zhu, C.; Du, Q.Z.; Shangguan, L.N. Ascorbate-glutathione cycle alteration in cadmium sensitive rice mutant cadB1. Rice Sci. 2012, 19, 185–192. [Google Scholar] [CrossRef]
  58. Srivastava, R.K.; Pandey, P.; Rajpoot, R.; Rani, A.; Dubey, R.S. Cadmium and lead interactive effects on oxidative stress and antioxidative responses in rice seedlings. Protoplasma 2014, 251, 1047–1065. [Google Scholar] [CrossRef]
  59. Asgher, M.; Khan, M.I.; Anjum, N.A.; Khan, N.A. Minimising toxicity of cadmium in plants--role of plant growth regulators. Protoplasma 2015, 252, 399–413. [Google Scholar] [CrossRef]
  60. Aina, R.; Labra, M.; Fumagalli, P.; Vannini, C.; Marsoni, M.; Cucchi, U.; Bracale, M.; Sgorbati, S.; Citterio, S. Thiol-peptide level and proteomic changes in response to cadmium toxicity in Oryza sativa L. roots. Environ. Exp. Bot. 2007, 59, 381–392. [Google Scholar] [CrossRef]
  61. Chao, Y.Y.; Chen, C.Y.; Huang, W.D.; Kao, C.H. Salicylic acidmediated hydrogen peroxide accumulation and protection against Cd toxicity in rice leaves. Plant Soil. 2010, 329, 327–337. [Google Scholar] [CrossRef]
  62. Zhang, C.H.; Ying, G.E. Response of glutathione and glutathione Stransferase in rice seedlings exposed to cadmium stress. Rice Sci. 2008, 15, 73–76. [Google Scholar] [CrossRef]
  63. Lee, K.; Bae, D.W.; Kim, S.H.; Han, H.J.; Liu, X.; Park, H.C.; Lim, C.O.; Lee, X.Y.; Chung, W.S. Comparative proteomic analysis of the shortterm responses of rice roots and leaves to cadmium. J. Plant Physiol. 2010, 167, 161–168. [Google Scholar] [CrossRef] [PubMed]
  64. Khavari-Nejad, R.A.; Najafi, F.; Rezaei, M. The influence of cadmium toxicity on some physiological parameters as affected by iron in rice (Oryza Sativa L.) plant. J. Plant Nutr. 2014, 37, 1202–1213. [Google Scholar] [CrossRef]
  65. Wang, M.Y.; Chen, A.K.; Wong, M.H.; Qiu, R.L.; Cheng, H.; Ye, Z.H. Cadmium accumulation in and tolerance of rice Oryza sativa L. varieties with different rates of radial oxygen loss. Environ. Pollut. 2011, 159, 1730–1736. [Google Scholar] [CrossRef] [PubMed]
  66. Agrawal, G.K.; Rakwal, R.; Yonekura, M.; Kubo, A.; Saji, H. Rapid induction of defense/stress-related proteins in leaves of rice (Oryza sativa) seedlings exposed to ozone is preceded by newly phosphorylated proteins and changes in a 66-kDA ERK-typeMAPK. J. Plant Physiol. 2002, 159, 361–369. [Google Scholar] [CrossRef]
  67. Agrawal, G.K.; Rakwal, R.; Iwahashi, H. Isolation of novel rice (Oryza sativa L.) multiple stress responsive MAP kinase gene, OsMSRMK2, whose mRNA accumulates rapidly in response to environmental cues. Biochem. Biophys. Res. Commun. 2002, 294, 1009–1016. [Google Scholar] [CrossRef]
  68. Yeh, C.M.; Hsiao, L.J.H.; Hsiao, H.J. Cadmium activates a mitogenactivated protein kinase gene and MBP kinases in rice. Plant Cell Physiol. 2004, 45, 1306–1312. [Google Scholar] [CrossRef]
  69. Zhao, F.Y.; Hu, F.; Zhang, S.Y.; Wang, K.; Zhang, C.R.; Liu, T. MAPKs regulate root growth by influencing auxin signaling and cell cyclerelated gene expression in cadmium-stressed rice. Environ. Sci. Pollut. Res. 2013, 20, 5449–5460. [Google Scholar] [CrossRef]
  70. Wang, X.; Yao, H.; Wong, M.H.; Ye, Z. Dynamic changes in radial oxygen loss and iron plaque formation and their effects on Cd and As accumulation in rice (Oryza sativa L.). Environ. Geochem. Health 2013, 35, 779–788. [Google Scholar] [CrossRef]
  71. Cheng, H.; Wang, M.; Wong, M.H.; Ye, Z. Does radial oxygen loss and iron plaque formation on roots alter Cd and Pb uptake and distribution in rice plant tissues? Plant Soil. 2014, 375, 137–148. [Google Scholar] [CrossRef]
  72. Shao, J.F.; Che, J.; Yamaji, N.; Shen, R.F.; Ma, J.F. Silicon reduces cadmium accumulation by suppressing expression of transporter genes involved in cadmium uptake and translocation in rice. J. Exp. Bot. 2017, 68, 5641–5651. [Google Scholar] [CrossRef] [Green Version]
  73. Chen, Z.; Tang, Y.T.; Yao, A.J.; Cao, J.; Wu, Z.H.; Peng, Z.R.; Wang, S.Z.; Xiao, S.; Baker, A.J.M.; Qiu, R.L. Mitigation of Cd accumulation in paddy rice (Oryza sativa L.) by Fe fertilization. Environ. Pollut. 2017, 231, 549–559. [Google Scholar] [CrossRef] [PubMed]
  74. Huang, G.; Ding, C.; Zhou, Z.; Zhang, T.; Wang, X. A tillering application of zinc fertilizer based on basal stabilization reduces Cd accumulation in rice (Oryza sativa L.). Ecotoxicol. Environ. Saf. 2019, 167, 338–344. [Google Scholar] [CrossRef] [PubMed]
  75. Chen, D.; Chen, D.; Xue, R.; Long, J.; Lin, X.; Lin, Y.; Jia, L.; Zeng, R.; Song, Y. Effects of boron, silicon and their interactions on cadmium accumulation and toxicity in rice plants. J. Hazard. Mater. 2019, 367, 447–455. [Google Scholar] [CrossRef]
  76. Hermans, C.; Conn, S.J.; Chen, J.; Xiao, Q.; Verbruggen, N. An update on magnesium homeostasis mechanisms in plants. Metallomics 2013, 5, 1170–1183. [Google Scholar] [CrossRef] [PubMed]
  77. Lee, S.; Kim, Y.Y.; Lee, Y.; An, G. Rice P1B-type heavy-metal ATPase, OsHMA9, is a metal efflux protein. Plant Physiol. 2007, 145, 831–842. [Google Scholar] [CrossRef]
  78. Shimo, H.; Ishimaru, Y.; An, G.; Yamakawa, T.; Nakanishi, H.; Nishizawa, N.K. Low cadmium (LCD), a novel gene related to cadmium tolerance and accumulation in rice. J. Exp Bot. 2011, 62, 5727–5734. [Google Scholar] [CrossRef]
  79. Kuramata, M.; Masuya, S.; Takahashi, Y.; Kitagawa, E.; Inoue, C.; Ishikawa, S.; Youssefian, S.; Kusano, T. Novel cysteine-rich peptides from Digitaria ciliaris and Oryza sativa enhance tolerance to cadmium by limiting its cellular accumulation. Plant Cell Physiol. 2009, 50, 106–117. [Google Scholar] [CrossRef]
  80. Yang, J.; Gao, M.X.; Hu, H.; Ding, X.M.; Lin, H.W.; Wang, L.; Xu, J.M.; Mao, C.Z.; Zhao, F.J.; Wu, Z.C. OsCLT1, a CRT-like transporter 1, is required for glutathione homeostasis and arsenic tolerance in rice. New Phytol. 2016, 211, 658–670. [Google Scholar] [CrossRef]
  81. Moons, A. Ospdr9, which encodes a PDR-type ABC transporter, is induced by heavy metals, hypoxic stress and redox perturbations in rice roots. FEBS Lett. 2003, 553, 370–376. [Google Scholar] [CrossRef]
  82. Agrawal, G.K.; Agrawal, S.K.; Shibato, J.; Iwahashi, H.; Rakwal, R. Novel rice MAP kinases OsMSRMK3 and OsWJUMK1 involved in encountering diverse environmental stresses and developmental regulation. Biochem. Biophys. Res. Commun. 2003, 300, 775–783. [Google Scholar] [CrossRef]
  83. Shim, D.; Jae-Ung, H.; Lee, J.; Lee, S.; Choi, Y.; An, G.; Martinoia, E.; Lee, Y. Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. Plant Cell. 2009, 21, 4031–4043. [Google Scholar] [CrossRef] [PubMed]
  84. Ramesh, S.A.; Shin, R.; Eide, D.J.; Schachtman, D.P. Differential metal selectivity and gene expression of two zinc transporters from rice. Plant Physiol. 2003, 133, 126–134. [Google Scholar] [CrossRef] [PubMed]
  85. Chou, T.S.; Chao, Y.Y.; Huang, W.D.; Hong, C.Y.; Kao, C.H. Effect of magnesium deficiency on antioxidant status and cadmium toxicity in rice seedlings. J. Plant Physiol. 2011, 168, 1021–1030. [Google Scholar] [CrossRef] [PubMed]
  86. Yu, L.H.; Umeda, M.; Liu, J.Y.; Zhao, N.M.; Uchimiya, H. A novel MT gene of rice plants is strongly expressed in the node portion of the stem. Gene 1998, 206, 29–35. [Google Scholar] [CrossRef]
  87. Cheng, L.; Wang, F.; Shou, H.; Huang, F.; Zheng, L.; He, F.; Li, J.; Zhao, F.J.; Ueno, D.; Ma, J.F.; et al. Mutation in nicotianamine aminotransferase stimulated the Fe(II) acquisition system and led to iron accumulation in rice. Plant Physiol. 2007, 145, 1647–1657. [Google Scholar] [CrossRef]
  88. Luo, J.S.; Huang, J.; Zeng, D.L.; Peng, J.S.; Zhang, G.B.; Ma, H.L.; Guan, Y.; Yi, H.Y.; Fu, Y.L.; Han, B.; et al. A defensin-like protein drives cadmium efflux and allocation in rice. Nat. Commun. 2018, 9, 645. [Google Scholar] [CrossRef]
  89. Masuda, H.; Ishimaru, Y.; Aung, M.S.; Kobayashi, T.; Kakei, Y.; Takahashi, M.; Higuchi, K.; Nakanishi, H.; Nishizawa, N.K. Iron biofortification in rice by the introduction of multiple genes involved in iron nutrition. Sci. Rep. 2012, 2, 543. [Google Scholar] [CrossRef] [Green Version]
  90. Yan, H.; Xu, W.; Xie, J.; Gao, Y.; Wu, L.; Sun, L.; Feng, L.; Chen, X.; Zhang, T.; Dai, C.; et al. Variation of a major facilitator superfamily gene contributes to differential cadmium accumulation between rice subspecies. Nat. Commun. 2019, 10, 2562. [Google Scholar] [CrossRef]
  91. Zhao, J.; Yang, W.; Zhang, S.; Yang, T.; Liu, Q.; Dong, J.; Fu, H.; Mao, X.; Liu, B. Genome-wide association study and candidate gene analysis of rice cadmium accumulation in grain in a diverse rice collection. Rice 2018, 11, 61. [Google Scholar] [CrossRef] [PubMed]
  92. Ansarypour, Z.; Shahpiri, A. Heterologous expression of a rice metallothionein isoform (OsMTI-1b) in Saccharomyces cerevisiae enhances cadmium, hydrogen peroxide and ethanol tolerance. Braz. J. Microbiol. 2017, 48, 537–543. [Google Scholar] [CrossRef] [PubMed]
  93. Ishimaru, Y.; Kakei, Y.; Shimo, H.; Bashir, K.; Sato, Y.; Sato, Y.; Uozumi, N.; Nakanishi, H.; Nishizawa, N.K. A rice phenolic efflux transporter is essential for solubilizing precipitated apoplasmic iron in the plant stele. J. Biol. Chem. 2011, 286, 24649–24655. [Google Scholar] [CrossRef] [PubMed]
  94. Hao, X.; Zeng, M.; Wang, J.; Zeng, Z.; Dai, J.; Xie, Z.; Yang, Y.; Tian, L.; Chen, L.; Li, D. A Node-Expressed Transporter OsCCX2 Is Involved in Grain Cadmium Accumulation of Rice. Front. Plant Sci. 2018, 9, 476. [Google Scholar] [CrossRef] [PubMed]
  95. Nakanishi, H.; Ogawa, I.; Ishimaru, Y.; Mori, S.; Nishizawa, N.K. Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci. Plant Nutr. 2006, 52, 464–469. [Google Scholar] [CrossRef]
  96. Lee, S.; An, G. Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant Cell Environ. 2009, 32, 408–416. [Google Scholar] [CrossRef]
  97. Yuan, L.; Yang, S.; Liu, B.; Zhang, M.; Wu, K. Molecular characterization of a rice metal tolerance protein, OsMTP1. Plant Cell Rep. 2012, 31, 67–79. [Google Scholar] [CrossRef]
  98. Kavitha, P.G.; Kuruvilla, S.; Mathew, M.K. Functional characterization of a transition metal ion transporter, OsZIP6 from rice (Oryza sativa L.). Plant Physiol. Biochem. 2015, 97, 165–174. [Google Scholar]
  99. Tan, L.; Zhu, Y.; Fan, T.; Peng, C.; Wang, J.; Sun, L.; Chen, C. 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. 2019, 512, 112–118. [Google Scholar] [CrossRef]
  100. Das, N.; Bhattacharya, S.; Bhattacharyya, S.; Maiti, M. Identification of alternatively spliced transcripts of rice phytochelatin synthase 2 gene OsPCS2 involved in mitigation of cadmium and arsenic stresses. Plant Mol. Biol. 2017, 94, 167–183. [Google Scholar] [CrossRef]
  101. Uraguchi, S.; Kamiya, T.; Sakamoto, T.; Kasai, K.; Sato, Y.; Nagamura, Y.; Yoshida, A.; Kyozuka, J.; Ishikawa, S.; Fujiwara, T. Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proc. Natl. Acad Sci. 2011, 108, 20959–20964. [Google Scholar] [CrossRef] [PubMed]
  102. Uraguchi, S.; Kamiya, T.; Clemens, S.; Fujiwara, T. Characterization of OsLCT1, a cadmium transporter from indica rice Oryza sativa. Physiol. Plant 2014, 151, 339–347. [Google Scholar] [CrossRef] [PubMed]
  103. Takahashi, R.; Ishimaru, Y.; Shimo, H.; Ogo, Y.; Senoura, T.; Nishizawa, N.K.; Nakanishi, H. The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ. 2012, 35, 1948–1957. [Google Scholar] [CrossRef] [PubMed]
  104. Yamaji, N.; Xia, J.; Mitani-Ueno, N.; Yokosho, K.; Ma, J.F. Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiol. 2013, 162, 927–939. [Google Scholar] [CrossRef] [PubMed]
  105. Ueno, D.; Yamaji, N.; Kono, I.; Huang, C.F.T.; Yano, M.; Ma, J.F. Gene limiting cadmium accumulation in rice. Proc. Natl. Acad Sci. USA 2010, 107, 16500–16505. [Google Scholar] [CrossRef] [Green Version]
  106. Ishimaru, Y.; Takahashi, R.; Bashir, K.; Shimo, H.; Senoura, T.; Sugimoto, K.; Ono, K.; Yano, M.; Ishikawa, S.; Arao, T.; et al. Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Sci. Rep. 2012, 2, 286. [Google Scholar] [CrossRef] [PubMed]
  107. Sasaki, A.; Yamaji, N.; Yokosho, K.; Ma, J.F. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell. 2012, 24, 2155–2167. [Google Scholar] [CrossRef]
  108. Yang, M.; Zhang, Y.Y.; Zhang, L.; Hu, J.; Zhang, X.; Lu, K.; Dong, H.; Wang, D.; Zhao, F.J.; Huang, C.F.; et al. OsNRAMP5 contributes to manganese translocation and distribution in rice shoots. J. Exp. Bot. 2014, 65, 4849–4861. [Google Scholar] [CrossRef] [Green Version]
  109. Takahashi, R.; Ishimaru, Y.; Shimo, H.; Bashir, K.; Senoura, T.; Sugimoto, K.; Ono, K.; Suzui, N.; Kawachi, N.; Ishii, S.; et al. From laboratory to field: OsNRAMP5-knockdown rice is a promising candidate for Cd phytoremediation in paddy fields. PLoS ONE 2014, 9, e98816. [Google Scholar] [CrossRef]
  110. Tang, L.; Mao, B.; Li, Y.; Lv, Q.; Zhang, L.; Chen, C.; He, H.; Wang, W.; Zeng, X.; Shao, Y.; et al. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci. Rep. 2017, 7, 14438. [Google Scholar] [CrossRef]
  111. Takahashi, R.; Ishimaru, Y.; Nakanishi, H.; Nishizawa, N.K. Role of the iron transporter OsNRAMP1 in cadmium uptake and accumulation in rice. Plant Signal. Behav. 2011, 6, 1813–1816. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  112. Takahashi, R.; Ishimaru, Y.; Senoura, T.; Shimo, H.; Ishikawa, S.; Arao, T.; Nakanishi, H.; Nishizawa, N.K. The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J. Exp. Bot. 2011, 62, 4843–4850. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  113. Tiwari, M.; Sharma, D.; Dwivedi, S.; Singh, M.; Tripathi, R.D.; Trivedi, P.K. Expression in Arabidopsis and cellular localization reveal involvement of rice NRAMP, OsNRAMP1, in arsenic transport and tolerance. Plant Cell Environ. 2014, 37, 140–152. [Google Scholar] [CrossRef] [PubMed]
  114. Lim, S.D.; Hwang, J.G.; Han, A.R.; Park, Y.C.; Lee, C.; Ok, Y.S.; Jang, C.S. Positive regulation of rice RING E3 ligase OsHIR1 in arsenic and cadmium uptakes. Plant Mol. Biol. 2014, 85, 365–379. [Google Scholar] [CrossRef] [PubMed]
  115. 125Mukhopadhyay, A.; Vij, S.; Tyagi, A.K. Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc. Natl. Acad. Sci. USA 2004, 101, 6309–6314. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  116. Wang, F.J.; Wang, M.; Liu, Z.P.; Shi, Y.; Han, T.Q.; Ye, Y.Y.; Gong, N.; Sun, J.W.; Zhu, C. Different responses of low grain-Cd-accumulating and high grain-Cd-accumulating rice cultivars to Cd stress. Plant Mol. Biol. 2015, 96, 261–269. [Google Scholar]
  117. Jin, S.; Cheng, Y.; Guan, Q.; Liu, D.; Takano, T.; Liu, S. A metallothionein-like protein of rice (rgMT) functions in E. coli and its gene expression is induced by abiotic stresses. Biotechnol. Lett. 2006, 28, 1749–1753. [Google Scholar]
  118. Harada, E.; Choi, Y.E.; Tsuchisaka, A.; Obata, H.; Sano, H. Transgenic tobacco plants expressing a rice cysteine synthase gene are tolerant to toxic levels of cadmium. J. Plant Physiol. 2001, 158, 655–661. [Google Scholar] [CrossRef]
  119. Lu, L.L.; Tian, S.K.; Yang, X.E.; Li, T.Q.; He, Z.L. Cadmium uptake and xylem loading are active processes in the hyperaccumulator Sedum alfredii. J. Plant Physiol. 2009, 166, 579–587. [Google Scholar] [CrossRef]
  120. Ishimaru, Y.; Suzuki, M.; Tsukamoto, T.; Suzuki, K.; Nakazono, M.; Kobayashi, T.; Wada, Y.; Watanabe, S.; Matsuhashi, S.; Takahashi, M.; et al. Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J. 2006, 45, 335–346. [Google Scholar] [CrossRef]
  121. Liu, C.; Chen, G.; Li, Y.; Peng, Y.; Zhang, A.; Hong, K.; Jiang, H.; Ruan, B.; Zhang, B.; Yang, S.; et al. Characterization of a major QTL for manganese accumulation in rice grain. Sci. Rep. 2017, 7, 17704. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  122. Uraguchi, S.; Fujiwara, T. Cadmium transport and tolerance in rice: Perspectives for reducing grain cadmium accumulation. Rice 2012, 5, 1–8. [Google Scholar] [CrossRef] [PubMed]
  123. Satoh-Nagasawa, N.; Mori, M.; Nakazawa, N.; Kawamoto, T.; Nagato, Y.; Sakurai, K.; Takahashi, H.; Watanabe, A.; Akagi, H. Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol. 2012, 53, 213–224. [Google Scholar] [CrossRef] [PubMed]
  124. Satoh-Nagasawa, N.; Mori, M.; Sakurai, K.; Takahashi, H.; Watanabe, A.; Akagi, H. Functional relationship heavy metal P-type ATPases (OsHMA2 and OsHMA3) of rice (Oryza sativa) using RNAi. Plant Biotechnol. 2013, 30, 511–515. [Google Scholar] [CrossRef]
  125. Miyadate, H.; Adachi, S.; Hiraizumi, A.; Tezuka, K.; Nakazawa, N.; Kawamoto, T.; Katou, K.; Kodama, I.; Sakurai, K.; Takahashi, H.; et al. OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol. 2011, 189, 190–199. [Google Scholar] [CrossRef] [PubMed]
  126. Tanaka, K.; Fujimaki, S.; Fujiwara, T.; Yoneyama, T.; Hayashi, H. Quantitative estimation of the contribution of the phloem in cadmium transport to grains in rice plants (Oryza sativa L.). Soil Sci. Plant Nutr. 2007, 53, 72–77. [Google Scholar] [CrossRef]
  127. Wu, Z.C.; Zhao, X.H.; Sun, X.C.; Tan, Q.L.; Tang, Y.F.; Nie, Z.J.; Hu, C.X. Xylem transport and gene expression play decisive roles in cadmium accumulation in shoots of two oilseed rape cultivars (Brassica napus). Chemosphere 2015, 119, 1217–1223. [Google Scholar] [CrossRef]
  128. Fujimaki, S.; Suzui, N.; Ishioka, N.S.; Kawachi, N.; Ito, S.; Chino, M.; Nakamura, S. Tracing cadmium from culture to spikelet: Noninvasive imaging and quantitative characterization of absorption, transport, and accumulation of cadmium in an intact rice plant. Plant Physiol. 2010, 152, 1796–1806. [Google Scholar] [CrossRef]
  129. Yan, J.; Wang, P.; Wang, P.; Yang, M.; Lian, X.; Tang, Z.; Huang, C.F.; Salt, D.E.; Zhao, F.J. A loss-of-function allele of OsHMA3 associated with high cadmium accumulation in shoots and grain of Japonica rice cultivars. Plant Cell Environ. 2016, 39, 1941–1954. [Google Scholar] [CrossRef]
  130. Ishikawa, S.; Abe, T.; Kuramata, M.; Yamaguchi, M.; Ando, T.; Yamamoto, T.; Yano, M. 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. 2010, 61, 923–934. [Google Scholar] [CrossRef]
  131. Kashiwagi, T.; Shindoh, K.; Hirotsu, N.; Ishimaru, K. Evidence for separate translocation pathways in determining cadmium accumulation in grain and aerial plant parts in rice. BMC Plant Biol. 2009, 9, 8. [Google Scholar] [CrossRef] [PubMed]
  132. Sato, H.; Shirasawa, S.; Maeda, H.; Nakagomi, K.; Kaji, R.; Ohta, H.; Yamaguchi, M.; Takeshi, N. Analysis of QTL for lowering cadmium concentration in rice grains from ‘LAC- 23′. Breed. Sci. 2011, 61, 196–200. [Google Scholar]
  133. Yan, Y.F.; Lestari, P.; Lee, K.J.; Kim, M.Y.; Lee, S.H.; Lee, B.W. Identification of quantitative trait loci for cadmi um accumulation and distribution in rice (Oryza sativa). Genome 2013, 56, 227–232. [Google Scholar] [CrossRef] [PubMed]
  134. Abe, T.; Nonoue, Y.; Ono, N.; Omoteno, M.; Kuramata, M.; Fukuoka, S.; Yamamoto, T.; Yano, M.; Ishikawa, S. Detection of QTLs to reduce cadmium content in rice grains using LAC23/Koshihikari chromosome segment substitution lines. Breed. Sci. 2013, 63, 284–291. [Google Scholar] [Green Version]
  135. Liu, W.; Pan, X.; Li, Y.; Duan, Y.; Min, J.; Liu, S.; Liu, L.; Sheng, X.; Li, X. Identification of QTLs and Validation of qCd-2 Associated with Grain Cadmium Concentrations in Rice. Rice Sci. 2019, 26, 42–49. [Google Scholar] [CrossRef]
  136. Liu, X.; Chen, S.; Chen, M.; Zheng, G.; Peng, Y.; Shi, X.; Qin, P.; Xu, X.; Teng, S. Association Study Reveals Genetic Loci Responsible for Arsenic, Cadmium and Lead Accumulation in Rice Grain in Contaminated Farmlands. Front. Plant Sci. 2019, 10, 61. [Google Scholar] [CrossRef] [PubMed]
  137. Ueno, D.; Koyama, E.; Kono, I.; Ando, T.; Yano, M.; Ma, J.F. Identification of a novel major quantitative trait locus controlling distribution of Cd between roots and shoots in rice. Plant Cell Physiol. 2009, 50, 2223–2233. [Google Scholar] [CrossRef] [PubMed]
  138. Ueno, D.; Kono, I.; Yokosho, K.; Ando, T.; Yano, M.; Ma, J.F. A major quantitative trait locus controlling cadmium translocation in rice (Oryza sativa). New Phytol. 2009, 182, 644–653. [Google Scholar] [CrossRef]
  139. Xue, D.; Chen, M.; Zhang, G. Mapping of QTLs associated with cadmium tolerance and accumulation during seedling stage in rice (Oryza sativa L.). Euphytica 2009, 165, 587. [Google Scholar] [CrossRef]
  140. Norton, G.J.; Deacon, C.M.; Xiong, L.Z.; Huang, S.Y.; Meharg, A.A.; Price, A.H. Genetic mapping of the rice ionome in leaves and grain: Identification of QTLs for 17 elements including arsenic, cadmium, iron and selenium. Plant Soil 2010, 329, 139–153. [Google Scholar] [CrossRef]
  141. Ishikawa, S.; Ae, N.; Yano, M. Chromosomal regions with quantitative trait loci controlling cadmium concentration in brown rice (Oryza sativa). New Phytol. 2005, 168, 345–350. [Google Scholar] [CrossRef] [PubMed]
  142. Abe, T.; Taguchi-Shiobara, F.; Kojima, Y.; Ebitani, T.; Kuramata, M.; Yamamoto, T.; Yano, M.; Ishikawa, S. Detection of a QTL for accumulating Cd in rice that enables efficient Cd phytoextraction from soil. Breed. Sci. 2011, 61, 43–51. [Google Scholar] [CrossRef] [Green Version]
  143. Zhang, X.Q.; Zhang, G.P.; Guo, L.B.; Wang, H.Z.; Zeng, D.L.; Dong, G.J.; Qian, Q.; Xue, D.W. Identification of quantitative trait loci for Cd and Zn concentrations of brown rice grown in Cd-polluted soils. Euphytica 2011, 180, 173–179. [Google Scholar] [CrossRef]
  144. Huang, Y.; Sun, C.; Min, J.; Chen, Y.; Tong, C.; Bao, J. Association Mapping of Quantitative Trait Loci for Mineral Element Contents in Whole Grain Rice (Oryza sativa L.). J. Agric. Food Chem. 2015, 63, 10885–10892. [Google Scholar] [CrossRef] [PubMed]
  145. Guo, G.; Zhou, Q.; Ma, L.Q. Availability and assessment of fixing additives for the in-situ remediation of heavy metal contaminated soils: A review. Environ. Monit. Assess. 2006, 116, 513–528. [Google Scholar] [CrossRef] [PubMed]
  146. Madejón, E.; de Mora, A.P.; Felipe, E.; Burgos, P.; Cabrera, F. Soil amendments reduce trace element solubility in a contaminated soil and allow regrowth of natural vegetation. Environ. Pollut. 2006, 139, 40–52. [Google Scholar] [CrossRef]
  147. Yan, Y.; Zhou, Y.Q.; Liang, C.H. Evaluation of phosphate fertilizers for the immobilization of Cd in contaminated soils. PLoS ONE 2015, 10, e0124022. [Google Scholar] [CrossRef] [PubMed]
  148. Hu, P.J.; Ouyang, Y.N.; Wu, L.H.; Shen, L.B.; Luo, Y.M.; Christie, P. Effects of water management on arsenic and cadmium speciation and accumulation in an upland rice cultivar. J. Environ. Sci. 2015, 27, 225–231. [Google Scholar] [CrossRef]
  149. Honma, T.; Ohba, H.; Kaneko-Kadokura, A.; Makino, T.; Nakamura, K.; Katou, H. Optimal soil Eh, pH, and water management for simultaneously minimizing arsenic and cadmium concentrations in rice grains. Environ. Sci. Technol. 2016, 50, 4178–4185. [Google Scholar] [CrossRef]
  150. Yu, L.L.; Zhu, J.Y.; Huang, Q.Q.; Su, D.C.; Jiang, R.F.; Li, H.F. Application of a rotation system to oilseed rape and rice fields in Cd-contaminated agricultural land to ensure food safety. Ecotox. Environ. Safe. 2014, 108, 287–293. [Google Scholar] [CrossRef]
  151. Ishikawa, S.; Ishimaru, Y.; Igura, M.; Kuramata, M.; Abe, T.; Senoura, T.; Hase, Y.; Arao, T.; Nishizawa, N.K.; Nakanishi, H. Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc. Natl. Acad. Sci. USA 2012, 109, 19166–19171. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  152. Lu, C.; Zhang, L.; Tang, Z.; Huang, X.Y.; Ma, J.F.; Zhao, F.J. Producing cadmium-free Indica rice by overexpressing OsHMA3. Environ. Int. 2019, 126, 619–626. [Google Scholar] [CrossRef] [PubMed]
Ijms 20 03417 g001 550
Figure 1. A schematic of cadmium transport from the soil to grains in rice. Cadmium is absorbed from the soil by the roots, and OsNramp1, OsNramp5, and OsCd1 mediate this process. OsHMA3 plays a key role in cadmium segregation to vacuoles in root cells and thus negatively regulates cadmium xylem loading. OsHMA2, OsCCX2, and CAL1 regulate cadmium transport to the xylem. OsLCT1 contributes to cadmium remobilization from leaf blades via the phloem and is likely to play a part in intervascular cadmium transfer at nodes.
Figure 1. A schematic of cadmium transport from the soil to grains in rice. Cadmium is absorbed from the soil by the roots, and OsNramp1, OsNramp5, and OsCd1 mediate this process. OsHMA3 plays a key role in cadmium segregation to vacuoles in root cells and thus negatively regulates cadmium xylem loading. OsHMA2, OsCCX2, and CAL1 regulate cadmium transport to the xylem. OsLCT1 contributes to cadmium remobilization from leaf blades via the phloem and is likely to play a part in intervascular cadmium transfer at nodes.
Ijms 20 03417 g001
Ijms 20 03417 g002 550
Figure 2. Positions of cloned cadmium stress-related genes in rice chromosomes.
Figure 2. Positions of cloned cadmium stress-related genes in rice chromosomes.
Ijms 20 03417 g002
Table
Table 1. Genes of Rice Reported to be Regulated During Cadmium (Cd)-Exposure.
Table 1. Genes of Rice Reported to be Regulated During Cadmium (Cd)-Exposure.
GeneChr.Physical Location (bp)Gene NameFunctionReference
OsCDT314066623–4067218Encoding a Cys-rich peptideCd uptake inhibitor[79]
Ospdr9124075065–24082181 Multidrug resistance ABC transporterRedox protection in Cd stress[81]
OsWJUMK1129398191–29402466Mitogen-activated protein kinaseCd signal[82]
OsHsfA4a131370413–31372729Heat shock transcription factor geneCd tolerance[83]
OsAUX1136998334–37004685Auxin transport proteinRoot development and Cd stress response[34]
OsCLT1142086484–42095424 CRT-like transporter 1Cd tolerance[80]
OsLCD142162592–42166462 Low cadmiumCd tolerance and accumulation[78]
OsZIP1142905566–42907474 Zinc- and iron-regulated transporterCd and Zn transport[84,85]
ricMT143047164–43047861Metallothionein geneCd tolerance[86]
OsCDT426078179–6079111 Encoding a Cys-rich peptideCd uptake inhibitor[79]
OsNAAT1211997094–12002633Nicotinamide aminotransferase geneCd accumulation[87]
CAL1225190487–25191188defensin-like proteinCd accumulation in leaf[88]
OsYSL2226170387–26174970Metal-nicotinamide transporterCd translocation[89]
OsCd13842577–846408Major facilitator superfamilyCd uptake[90]
OsNramp235655157–5659147Natural resistance-associated macrophage proteinCd transporter, Cd accumulation[91]
OsMSRMK239847700–9850473 Mitogen-activated protein kinaseCd signal[67]
OsMTI-1b39957335–9958362Metallothionein-like protein 1BCd tolerance[92]
PEZ1320793053–20799805Phenol efflux proteinCd accumulation[93]
OsCDT1/OsCCX2325613825–25616179Cation/calcium (Ca) exchanger 2Cd tolerance and translocation[79,94]
OsIRT2326276301–26277206Iron-regulated transporterCd and Fe transporter[95]
OsIRT1326286156–26292023 Iron-regulated transporterCd and Fe transporter[95,96]
OsZIP3431078200–31080734Zinc- and iron-regulated transporterCd accumulation[84]
OsMTP151675488–1679056 Metal tolerance protein geneCd translocation[97]
OsZIP653807974–3810752Zinc- and iron-regulated transporterCd transport[98]
OsCDT554665325–4667853Encoding a Cys-rich peptideCd uptake inhibitor[79]
OsZIP756090801–6094068Zinc- and iron-regulated transporterCd and Zn accumulation[99]
OsPCS26167367–174319Plant chelatase synthase 2Cd tolerance[100]
OsCDT262261681–2263972 Encoding a Cys-rich peptideCd uptake inhibitor[79]
OsLCT1622566775–22571982Low affinity cation transporterCd transporter in phloem[101,102]
OsHMA9627517100–27523604P-Type Heavy Metal ATPaseCd efflux[77]
OsMSRMK3629398191–29402466Mitogen-activated protein kinaseCd signal[82]
OsHMA2629477949–29480905P-Type Heavy Metal ATPaseCd and Zn translocation[103,104]
OsHMA377405745–7409553P-Type Heavy Metal ATPaseSequestration of Cd in root[46,47,105]
OsNramp578871436–8878905Natural resistance-associated macrophage proteinCd, Mn, and Fe transporters[106,107,108,109,110]
OsNramp178966025–8970882Natural resistance-associated macrophage proteinCd and Fe transporters[111,112,113]
OsABCG43720214025–20218702ATP-binding cassette transporterCd compartmentalization[45]
OsMAPK283307520–3310590Mitogen-activated protein kinaseCd signal[68]
OsHIR1819011814–19015998Heavy metal-induced RING E3 ligase 1Cd uptake[114]
SISAP1918760704–18761836Subspecies indica stress-associated protein geneCd tolerance[115]
OsPCR110826309–824623Plant cadmium resistance 1 Cd tolerance[116]
rgMT1128827746–28828439Metallothionein-like proteinCd tolerance[117]
RCS11226698650–26703087Cytosolic cysteine synthase geneCd complexation via sulfur[118]
Table
Table 2. Quantitative Trait Loci (QTLs) of Rice Reported to be Regulated during Cadmium (Cd)-Exposure.
Table 2. Quantitative Trait Loci (QTLs) of Rice Reported to be Regulated during Cadmium (Cd)-Exposure.
StageParent SourcesPopulationMarkerTraitChr.QTLReference
Seedling stageTainan1/Chunjiang06119 DH, 3651 BC3F3RFLPCd accumulation in leaves2CAL1[88]
Seedling stageNipponbare/Anjana Dhan 965 F2SSRCd concentration in shoots7OsHMA3[105]
Seedling stageSNU-SG1/Suwon49091 RIL124 SSRCd concentration in shoots10scc10[133]
Seedling stage Koshihikari/LAC2346 CSSLs345 SNPCd concentration in shoots3glGCd3[134]
Seedling stageAnjana Dhan/Nipponbare177 F2SSRRoot-to-shoot Cd translocation7qCdT7[137]
Seedling stageBadari Dhan/Shwe War184 F2141 SSRCd concentration in shoots2,5,11—[138]
Seedling stageJX17/ZYQ8127 DH160 RFLP,83 SSRShoot/root rate of Cd concentration3qSRR3[139]
Seedling stageJX17/ZYQ8127 DH160 RFLP,83 SSRCd concentration in roots and shoots6,7qCDS7, qCDR6.1, qCDR6.2[139]
Seedling stageAzucena/Bala79 RIL164 SSRCd concentration in leaves1,3,6qCd1, qCd3, qCd6,[140]
Bfore heading Kasalath/Nipponbare 98 BILsRFLP and SSR Cd concentration in leaves and culms4,11qcd4–1, qcd4–2, qcd11[131]
Mature periodSasanishiki/Habataki85 BILSSRCd accumulation in grains2,7qGCd7[130]
Mature periodFukuhibiki/LAC23126 RIL454 SNPCd accumulation in grains3,11gLCdG3, gLCdG11[132]
Mature periodSNU-SG1/Suwon490 91 RIL124 SSRCd accumulation in grains3,5,9,11gcc3, sgr5, gcc9, gcc11[133]
Mature periodXiang 743/Katy115 RIL, SSRCd accumulation in grains2,7qCd-2, qCd-7[135]
Mature periodKasalath/Koshihikari39CSSL129 RFLPCd accumulation in grains3,6,8—[141]
Mature periodKoshihikari/Jarjan103 BIL169 SSRCd accumulation in grains7—[142]
Mature periodJX17/ZYQ8127 DH160 RFLP,83 SSRCd accumulation in grains3,6gCdc3, gCdc6[143]
Mature period127 rice cultivarsGWASCd accumulation in grains3OsCd1[90]
Mature period378 rice cultivarsGWASCd accumulation in grains3, 5qCd3, qCd5.1, qCd5.2[144]

Share and Cite

MDPI and ACS Style

Chen, J.; Zou, W.; Meng, L.; Fan, X.; Xu, G.; Ye, G. Advances in the Uptake and Transport Mechanisms and QTLs Mapping of Cadmium in Rice. Int. J. Mol. Sci. 2019, 20, 3417. https://doi.org/10.3390/ijms20143417

AMA Style

Chen J, Zou W, Meng L, Fan X, Xu G, Ye G. Advances in the Uptake and Transport Mechanisms and QTLs Mapping of Cadmium in Rice. International Journal of Molecular Sciences. 2019; 20(14):3417. https://doi.org/10.3390/ijms20143417

Chicago/Turabian Style

Chen, Jingguang, Wenli Zou, Lijun Meng, Xiaorong Fan, Guohua Xu, and Guoyou Ye. 2019. "Advances in the Uptake and Transport Mechanisms and QTLs Mapping of Cadmium in Rice" International Journal of Molecular Sciences 20, no. 14: 3417. https://doi.org/10.3390/ijms20143417

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop