Submitted Successfully!
To reward your contribution, here is a gift for you: A free trial for our video production service.
Thank you for your contribution! You can also upload a video entry or images related to this topic.
Version Summary Created by Modification Content Size Created at Operation
1
Lingli Lu
 -- 3361 2022-08-04 12:45:07 |
2 format
Jason Zhu
 Meta information modification 3361 2022-08-05 04:17:26 |

Video Upload Options

Do you have a full video?
Send video materials Upload full video

Confirm

Are you sure to Delete?
Yes No
Cite
If you have any further questions, please contact Encyclopedia Editorial Office.
Tao, J.;  Lu, L. Genes-Encoding Transporters for Cadmium Uptake, Translocation, and Accumulation. Encyclopedia. Available online: https://encyclopedia.pub/entry/25848 (accessed on 27 July 2024).
Tao J,  Lu L. Genes-Encoding Transporters for Cadmium Uptake, Translocation, and Accumulation. Encyclopedia. Available at: https://encyclopedia.pub/entry/25848. Accessed July 27, 2024.
Tao, Jingyu, Lingli Lu. "Genes-Encoding Transporters for Cadmium Uptake, Translocation, and Accumulation" Encyclopedia, https://encyclopedia.pub/entry/25848 (accessed July 27, 2024).
Tao, J., & Lu, L. (2022, August 04). Genes-Encoding Transporters for Cadmium Uptake, Translocation, and Accumulation. In Encyclopedia. https://encyclopedia.pub/entry/25848
Tao, Jingyu and Lingli Lu. "Genes-Encoding Transporters for Cadmium Uptake, Translocation, and Accumulation." Encyclopedia. Web. 04 August, 2022.
Genes-Encoding Transporters for Cadmium Uptake, Translocation, and Accumulation
Edit
This entry is adapted from the peer-reviewed paper 10.3390/toxics10080411

Cadmium (Cd) is a heavy metal that is highly toxic for plants, animals, and human beings. A better understanding of the mechanisms involved in Cd accumulation in plants is beneficial for developing strategies for either the remediation of Cd-polluted soils using hyperaccumulator plants or preventing excess Cd accumulation in the edible parts of crops and vegetables. As a ubiquitous heavy metal, the transport of Cd in plant cells is suggested to be mediated by transporters for essential elements such as Ca, Zn, K, and Mn. Identification of the genes encoding Cd transporters is important for understanding the mechanisms underlying Cd uptake, translocation, and accumulation in either crop or hyperaccumulator plants.

Cadmium transporters Nramp

1. Introduction

Cadmium (Cd) is a heavy metal that is highly toxic to animals and plants, ranking first among inorganic pollutants. Cd enters the soil–plant environment through natural processes and anthropogenic activities [1]. Natural processes include volcanic eruptions and soil erosion, and anthropogenic activities include power stations, heating systems, and urban transportation [2][3]. Soil pollution by heavy metals, including Cd, is essentially an irreversible process that may take hundreds of years to recover from. Cd accumulation in plants inhibits Fe(III) reductase activity, leading to Fe(II) deficiency that in turn affects photosynthesis [4]. Plants affected by Cd toxicity in polluted soils usually present retarded growth, chlorotic leaves, and brown root tips. Compared with other heavy metals, such as Pb, Cd is more soluble and easily absorbed by plants, and is subsequently accumulated in their edible parts, thus entering the food chain and posing a threat to humans [1]. An excessive intake of Cd in humans can damage the kidneys, leading to rhinitis, emphysema, and osteomalacia [5]. In recent years, Cd has become one of the major soil pollutants worldwide due to uncontrolled industrialization, unsustainable urbanization, and intensive agricultural practices. The itai—itai disease is the most serious chronic Cd poisoning caused by long-term oral consumption of Cd in Japan [6]. In China, Cd is the most severe pollutant in agricultural soils, with a site-level rate as high as 7.0% [7][8][9], and Cd soil pollution further shows an increasing trend from North to South China [10]. Field surveys showed that Cd concentrations in a considerable proportion of rice grains, especially in those grown in South China, exceeded the recommended food safety standard in the country [11][12][13]. One strategy to prevent Cd food contamination is to find and create more Cd low-accumulating cultivars of crops and vegetables using genetic breeding, and alleviation of Cd soil pollution can be achieved through phytoremediation utilizing high-accumulating plants. Therefore, understanding the physiological and molecular mechanisms of Cd uptake, transport, and accumulation by plants is of great significance for formulating strategies for phytoremediation of Cd-contaminated soils or prevention of Cd accumulation in crops.

2. Natural Resistance-Associated Macrophage Proteins

Nramps represent a class of metal transporters widely present in plants that are mainly involved in the absorption and transport of Fe2+, Mn2+, Cd2+, and other metal ions [14][15]. The involvement of Nramp genes in Cd transport was first reported in the model plant Arabidopsis thaliana. In recent years, research has been focused on food crops such as Oryza sativa, Triticum polonicum and Fagopyrum esculentum, and hyperaccumulator plants have also been explored. These proteins have also been identified in other plants.
In A. thaliana, four Nramp genes have been found to be related to Cd transport. Overexpression of AtNramp1 increased Cd sensitivity and accumulation in yeast [16]. AtNramp3 and AtNramp4 encode tonoplast-localized proteins, and yeast expressing the two genes showed an increased sensitivity to Cd. Overexpression of AtNramp3 in Arabidopsis conferred hypersensitivity to Cd [16][17][18][19], but overexpression of AtNramp4 in A. thaliana only conferred a slight hypersensitivity to Cd [16][20]; AtNramp3 and AtNramp4 can also mediate the transport of Cd out of the vacuoles in Arabidopsis [16][19]. AtNramp6 is a Cd transporter that can either transport Cd out of its storage compartment or into the toxic cellular compartment [21].
Nramp genes involved in the transport of Cd are mainly studied in rice among food crops. Three Nramp genes have been identified to be functionally associated with Cd. OsNramp1, a transporter localized in the plasma membrane responsible for Cd uptake and transport within plants, is mainly expressed in the roots and the leaves and is localized in all root cells except the central vasculature and in leaf mesophyll cells [22][23]. Tiwari et al. [24] observed that OsNramp1 is involved in xylem-mediated loading and that it increased the accumulation of As and Cd in plants by heterologous expression of OsNramp1 in Arabidopsis. However, Chang et al. [23] showed that OsNramp1 transported Cd and Mn when expressed in yeast but did not transport Fe or As. Overexpression of OsNramp1 in rice reduced Cd accumulation in the roots, but increased it in the leaves. Knockout of OsNramp1 resulted in decreased Cd and Mn uptake by the roots and their accumulation in the shoots and the grains [22][23].
OsNramp2 is localized in the tonoplast and mainly expressed in the embryo of germinating seeds, roots, leaf sheaths, and leaf blades [25]. The knockout of OsNramp2 significantly decreased Cd concentration in the grains, but increased it in the leaves and the straws, suggesting that it mediates Cd efflux from the vacuoles in the vegetative tissues for translocation to the grains [25][26].
OsNramp5 encodes a plasma membrane protein polarly localized at the distal side of both exodermis and endodermis cells, and responsible for the influx of Mn and Cd into root cells from external solutions [27][28]. Knockout of OsNramp5 significantly reduced Cd concentration in the roots and shoots [28][29]. In a Cd-contaminated paddy field experiment, it was found that Cd concentration in the grains of the knockout line was much lower than that of the wild-type (WT) [29]. Surprisingly, the overexpression of OsNramp5 enhanced Cd root uptake, but significantly reduced its accumulation in the shoots and grains. Xylem loading was also disturbed in OsNramp5-overexpressing plants, with a reduced translocation from the roots to the shoots [30].
In Triticum polonicum L and Triticum turgidum L, TpNramp3, TpNramp5, and TtNramp6 encode plasma membrane proteins. Overexpression of TtNramp6 increased Cd concentration and its accumulation in the whole plant of Arabidopsis [31]. Overexpression of TpNramp3 or TpNramp5 also increased the concentrations of Cd, Co, and Mn in the whole plant [32][33]. In Hordeum vulgare, HvNramp5 encodes a plasma membrane-localized transporter required for the uptake of Cd and Mn, but not Fe, that presents 84% identity with OsNramp5. HvNramp5 was mainly expressed in the roots, with higher expression levels in the root tips than in the basal region [34]. Knockout of HvNramp5 in barley resulted in reduced concentrations of Mn and Cd in the roots and shoots but did not change the concentrations of other metals [34]. In Fagopyrum esculentum Moench, the plasma membrane-localized transporter FeNramp5 is responsible for the uptake of Mn and Cd. FeNramp5 can also complement the phenotype of an AtNramp1 Arabidopsis mutant in terms of growth and accumulation of Mn and Cd [35]. BnNramp1b is localized in the plasma membrane and can transport Cd [36]. Yue et al. demonstrated that BcNramp1 plays a role in Cd influx of Arabidopsis root cells using noninvasive microelectrode ion flux measurements [37].
Studies on Nramp Cd-transporting genes in hyperaccumulator plants are mainly focused on Noccaea caerulescens (Thlaspi caerulescens) and Sedum alfredii Hance. In N. caerulescens, NcNramp1 participates in the influx of Cd across the endodermal plasma membrane and thus may play an important role in the Cd flux into the stele and its root-to-shoot translocation [38]. TcNramp3 and TcNramp4 are localized in the tonoplast. TcNramp3 or TcNramp4 expression rescued Cd and Zn hypersensitivity induced by the inactivation of AtNramp3 and AtNramp4 in Arabidopsis [39]. Additionally, in overexpression tobacco lines, the roots were found to be more sensitive to Cd [40]. In the S. alfredii Hance, the plasma membrane-localized SaNramp1 transporter is highly expressed in the young tissues of the shoots, and its overexpression in tobacco significantly increased Cd concentration at this location [41]. Ectopic expression of SaNramp3 in Brassica juncea enhanced Cd root-to-shoot translocation, thus increasing Cd accumulation in the shoots [42]. Overexpression of SaNramp6, localized in the plasma membrane, increased Cd uptake and accumulation in A. thaliana [43]. Employing site-directed mutagenesis and functional analysis of mutants in yeast and Arabidopsis, the conserved L157 site in SaNramp6h was found to be critical for metal transport [44].
Nramp genes have also been identified in other plants. MxNramp1 (localized in the plasma membrane) and MxNramp3 (localized in the tonoplast) can transport Cd in yeast [45]. In Malus hupehensis, overexpression of MhNramp1 increases Cd uptake and accumulation, thereby exacerbating cell death [46]. SpNramp1, SpNramp2, and SpNramp3 are plasma membrane-localized transporters in Spirodela polyrhiza, and overexpression of SpNramp1 or SpNramp2 increased Cd accumulation [47]. Similarly, overexpression of CjNramp1 in Arabidopsis resulted in high tolerance to Cd [48]. Furthermore, overexpression of NtNramp1 in tobacco could promote Cd uptake and Fe transportation [49], and the tonoplast-localized NtNramp3 transporter was found to be involved in the regulation of Cd transport from the vacuole to the cytoplasm using CRISPR/Cas9 technology [50].

3. Heavy Metal Transporting ATPases

HMAs play an important role in absorbing and transporting essential metal ions, such as Cu2+, Co2+ and Zn2+, by ATP hydrolysis; they can also transport Cd2+ and Pb2+. HMAs can be divided into two classes: those transporting monovalent cations (Cu, Ag) and those transporting divalent cations (Zn, Co, Cd, Pb) [51]. First described in A. thaliana, they have been studied more in food crops and hyperaccumulator plants in recent years due to their strong capacity to transport Cd; they have also been slightly less researched in other plants.
AtHMA2, AtHMA3, and AtHMA4 are reportedly associated with Cd transport in A. thaliana. AtHMA3 encodes a tonoplast-localized transporter that plays a role in Cd, Zn, Co, and Pb detoxification [52]. Overexpression of AtHMA3 enhanced Cd tolerance and increased its accumulation [52][53]. AtHMA2 and AtHMA4, localized in the plasma membrane, are responsible for the xylem loading of Zn/Cd and play a key role in their accumulation in the shoots [54][55][56]. Ceasar et al. [57] found that the di-cysteine residues at the C-terminus of HMA4 in A. thaliana were only partially required for Cd transport. Furthermore, ectopic expression of 35S::AtHMA4 reduced Cd accumulation due to the induction of the apoplastic barrier in tobacco [58].
The study of the HMA family is predominantly focused on food crops. Three Cd-transport associated HMA genes were identified in the genome of rice, one of the major food crops. The plasma membrane-localized transporter OsHMA2 is involved in the root-to-shoot translocation of Zn and Cd. OsHMA2 is mainly expressed in the mature zone of the roots at the vegetative stage, with the C-terminal region being essential for Zn/Cd translocation into the shoots [59][60]. Moreover, at the reproductive stage, OsHMA2 also showed a high expression in the nodes. Knockout of OsHMA2 resulted in reduced Zn and Cd concentrations in the upper nodes and reproductive organs compared with the WT, suggesting that OsHMA2 participates in the transport of Zn and Cd through the phloem to developing tissues [61]. OsHMA3 is localized in the tonoplast and sequestrates Cd into the root vacuoles to reduce its translocation, thereby mitigating Cd poisoning [62][63][64][65]. Silencing of OsHMA3 resulted in increased root-to-shoot Cd translocation, whereas OsHMA3 overexpression markedly decreased root-to-shoot Cd translocation and increased Cd tolerance, while greatly reducing its concentration in the grains [63][66]. The C-terminal region, and particularly the region containing the first 105 amino-acids, has an important role in the activity of OsHMA3 [67]. OsHMA9 encodes a heavy metal (Cd, Cu, Zn, and Pb) efflux protein present in the plasma membrane. Knockout of OsHMA9 results in higher Cd accumulation in the shoots compared with that of the WT, thus making the mutant sensitive to Cd [68]. Moreover, in Triticum aestivum L., overexpression of TaHMA2 improved the root-shoot Zn/Cd translocation [69]. In Glycine max (soybean), GmHAM3w restricts Cd to the endoplasmic reticulum, where it is localized, and in the roots to limit translocation to the shoots. Overexpression of GmHMA3w increased Cd concentration in the roots and decreased it in the shoots [70].
As a popular tool for the remediation of Cd-contaminated soils, there have been many studies on HMA genes with Cd transport and sequestration functions in hyperaccumulator plants in recent years. SpHMA1 is an important efflux transporter localized in the chloroplast envelope and is responsible for exporting Cd from the chloroplast, thus preventing Cd accumulation in Sedum plumbizincicola. Significantly increased Cd concentration in chloroplasts in SpHMA1 RNAi transgenic plants and CRISPR/Cas9-induced mutants compared to WT [71]. SpHMA3, localized in the tonoplast and expressed mainly in the shoots, plays an important role in Cd detoxification in young leaves by sequestering Cd into the vacuole [72]. In S. alfredii, the tonoplast-localized transporter SaHMA3 is mainly expressed in shoots. Its overexpression in tobacco significantly enhanced Cd tolerance and accumulation and greatly increased Cd sequestration in the roots [73]. Increased amounts of Cd were sequestered in the roots, but not in the leaf vacuoles, probably due to the heterologous expression. TcHMA3 is a tonoplast-localized transporter responsible for Cd sequestration into the leaf vacuoles in Thlaspi caeulescens [74]. TcHMA4 is involved in the active efflux of a large number of different heavy metals (Cd, Zn, Pb, and Cu) out of the cell, with the C-terminus of the TcHMA4 protein being essential for heavy metal binding [75]. Moreover, BjHMA4R can significantly improve Cd tolerance and accumulation at low heavy metal concentrations by specifically binding to Cd2+ in the cytosol [76]. In other plants, IlHMA2 is a plasma membrane transporter involved in Cd root-to-shoot translocation. The genes regulating Zn homeostasis were significantly down regulated in IlHMA2-silenced lines, compared with that in WT [77]. PtoHMA5 also participates in Cd root-to-shoot translocation [78].

4. ATP-Binding Cassette

This protein superfamily is one of the largest known superfamilies, with over 120 members in both A. thaliana and O. sativa. ABC transporters comprise four core domains (two nucleotide-binding and two transmembrane domains) [79] and are located in the plasma, vacuolar, and mitochondrial membranes, where they facilitate the transmembrane transport of substances via active transport [80][81][82][83]. The ABC family is further divided into 13 subfamilies, according to the size and domains of their members; the subfamilies involved in the transport of Cd and its chelates include the multidrug resistance-associated protein (MRP), pleiotropic drug resistance (PDR), and ABC transporter of the mitochondrion (ATM) subfamilies [84]. The current research on these three subfamilies is mainly focused on A. thaliana and O. sativa.
In A. thaliana, AtABCC1 and AtABCC2—two important tonoplast transporters—play an essential role in sequestering the PC–Cd(II) complexes to the vacuoles, thereby reducing the metal concentration in the root cells and its translocation to the shoots [83]. AtABCC3 is involved in the vacuolar transport of the PC–Cd complexes, with its activity being regulated by Cd and coordinated with the function of AtABCC1/AtABCC2 [85]. The expression levels of AtMRP6/AtABCC6 are significantly upregulated under Cd stress [86]. Overexpression of AtMRP7, which is localized in both the tonoplast and the plasma membrane, increased Cd concentration in the leaf vacuoles and its retention in the roots in tobacco [87]. AtPDR8, located in the plasma membrane and the root epidermal cells, is an important efflux transporter that increases Cd tolerance by effluxing Cd2+ out of the root epidermal cells. Overexpression of AtPDR8 improved Cd tolerance but did not affect its accumulation or that of Pb [82]. AtATM3 is a transporter localized in the mitochondrial membrane, and its overexpression improved Cd tolerance and accumulation by increasing the biogenesis of Fe-S clusters and exporting them from the mitochondria into the cytosol in Arabidopsis [81]. Overexpression of AtATM3 in B. juncea conferred enhanced Cd and Pb tolerance by inducing the expression of its glutathione synthetase II (BjGSHII) and phytochelatin synthase 1 (BjPCS1) enzymes [88].
In O. sativa, OsABCC9 was predominantly expressed in the root stele after Cd treatment. It mainly mediates Cd accumulation by sequestering of Cd into the root vacuoles, thereby reducing its translocation to the shoots and grains [89]. The plasma membrane-localized OsABCG36 transporter functions as a Cd extrusion pump, thus increasing Cd tolerance by exporting it or its conjugates from the root cells in rice. Compared with the WT, OsABCG36 knockout had a significantly higher Cd accumulation in the root cell sap and significantly increased sensitivity to Cd [90]. Yeast heterologous expression indicated that OsABCG43 and OsABCG48 conferred Cd tolerance; overexpression of OsABCG48 in rice reduced Cd concentration in the roots [91][92]. Similarly, in Triticum aestivum, TaABCC13 was reportedly involved in Cd uptake and transport, as Cd concentration in the roots and shoots of TaABCC13:RNAi line decreased, compared with that of the WT [93].
In other plants, some ABC genes have also been found to have a Cd-transporting role. Yeast-expressed RgABCC1, found in Rehmannia glutinosa, increased Cd tolerance [94]. Similarly, PtoABCG36 reduced Cd concentration in plants by mediating its efflux, thereby improving Cd tolerance [95].

5. Zinc- and Iron-Regulated Transporter Proteins

There are many members in the ZIP family, with all of them generally presenting eight transmembrane regions and metal ion-binding conserved domains that play a role in their transport. Not only can they transport essential metal ions such as Fe2+ and Zn2+, but also Cd2+ [96]. The first member of the ZIP family to be described was NcZNT1, found in N. caerulescens [97]. Overexpression of NcZNT1 enhanced the tolerance and accumulation of Zn and Cd in Arabidopsis, suggesting its involvement in the long-distance translocation of xylem loading from the roots to the shoots [98].
In recent years, studies on the role of the ZIP family in Cd transport have mainly focused on O. sativa. OsIRT1 and OsIRT2 are the major transporters participating in Fe and Cd uptake as observed in an heterologous expression experiment in yeast [99]. The IRT1 protein, first described in A. thaliana, mediates the absorption of a variety of metals including Fe, Zn, and Cd [100][101]. Similarly, IRT1 has also been explored in pea seedlings, mulberry (Morus L.), Triticum polonicum L., and Hordeum vulgare. Overexpression of IRTI in Arabidopsis and rice increased their sensitivity to Zn and Cd [99][102][103][104][105][106]. OsZIP1, a metal efflux transporter, is localized in the endoplasmic reticulum and the plasma membrane and is mainly expressed in the roots. Overexpression of OsZIP1 protects rice plants from an excess of Zn, Cu, and Cd by limiting metal accumulation in their tissues [107]. Plasma membrane-localized proteins OsZIP5 and OsZIP9 have influx transporter activity that functions synergistically in the Zn/Cd uptake in rice. Overexpression of OsZIP9 markedly increased the Zn/Cd levels in the aboveground tissues in brown rice. OsZIP9 is also responsible for the uptake of Zn and Co into the root cells [108][109]. Employing electrophysiological techniques, Kavitha et al. [110] demonstrated the uptake of Cd by OsZIP6. OsZIP7 encodes a plasma membrane-localized protein responsible for Cd/Zn influx and is expressed in the parenchyma cells of vascular bundles in the roots and nodes. Compared with the WT, an OsZIP7 knockout results in Zn and Cd retention in the roots and the basal ganglia, hindering their upward transmission and thus playing a role in xylem loading in the roots and inter-vascular transfer in the nodes to deliver Zn/Cd to the grains in rice [111].
ZIP genes related to Cd transport have also been reported in other plants. In Nicotiana tabacum, NtZIP4A and NtZIP4B are two copies of ZIP4, with 97.57% homology at the amino acid level. NtZIP4A/B is a plasma membrane-localized transporter that regulates Zn and Cd translocation from the roots to the shoots [112][113]. Similarly, MaZIP4 is also localized in the plasma membrane and has Cd transport activity[102].

6. Yellow Stripe-Like Proteins

The YSL family mediates the transmembrane transport of metal ions and chelates formed by metal ions and nicotinamide in plants, as well as the long-distance transport from the roots to the shoots [96]. YSL proteins were first reported to have a role in Fe transport, and then were subsequently found to participate in the transport of Cu, Zn, Cd, and Mn [114]. Members of this family involved in Cd transport include YSL1, YSL3, YSL6, and YSL7. MsYSL1 and SnYSL3 are plasma membrane-localized transporters responsible for long-distance Cd translocation from the roots to the shoots. An excess of Cd reportedly stimulated their expression. Overexpression of MsYSL1 or SnYSL3 in Arabidopsis increased the Cd translocation ratio under Cd stress [115][116]. VcYSL6 is located in the chloroplast, and its expression is up-regulated under Cd induction. Overexpression of VcYSL6 in tobacco increased Cd concentrations in the leaves [117]. BjYSL7 encodes a plasma membrane-localized metal–nicotinamide transporter. The concentrations of Cd and Ni in the shoots of BjYSL7-overexpressing transgenic tobacco plants are significantly higher than that of WT plants, suggesting a role of BjYSL7 in Cd translocation from the roots to the shoots [118].

References

  1. Sarwar, N.; Saifullah; Malhi, S.S.; Zia, M.H.; Naeem, A.; Bibi, S.; Farid, G. Role of mineral nutrition in minimizing cadmium accumulation by plants. J. Sci. Food Agric. 2010, 90, 925–937.
  2. Sanita, L.; Gabbrielli, R. Response to cadmium in higher plants. Environ. Exp. Bot. 1999, 41, 105–130.
  3. Li, Y.; Kuang, H.; Hu, C.; Ge, G. Source Apportionment of Heavy Metal Pollution in Agricultural Soils around the Poyang Lake Region Using UNMIX Model. Sustainability 2021, 13, 5272.
  4. Ghori, N.H.; Ghori, T.; Hayat, M.Q.; Imadi, S.R.; Gul, A.; Altay, V.; Ozturk, M. Heavy metal stress and responses in plants. Int. J. Environ. Sci. Technol. 2019, 16, 1807–1828.
  5. Edelstein, M.; Ben-Hur, M. Heavy metals and metalloids: Sources, risks and strategies to reduce their accumulation in horticultural crops. Sci. Hortic. 2018, 234, 431–444.
  6. Inaba, T.; Kobayashi, E.; Suwazono, Y.; Uetani, M.; Oishi, M.; Nakagawa, H.; Nogawa, K. Estimation of cumulative cadmium intake causing Itai-itai disease. Toxicol. Lett. 2005, 159, 192–201.
  7. Khan, M.A.; Khan, S.; Khan, A.; Alam, M. Soil contamination with cadmium, consequences and remediation using organic amendments. Sci. Total Environ. 2017, 601–602, 1591–1605.
  8. Yang, Q.; Li, Z.; Lu, X.; Duan, Q.; Huang, L.; Bi, J. A review of soil heavy metal pollution from industrial and agricultural regions in China: Pollution and risk assessment. Sci. Total Environ. 2018, 642, 690–700.
  9. Zhao, F.J.; Ma, Y.; Zhu, Y.G.; Tang, Z.; McGrath, S.P. Soil contamination in China: Current status and mitigation strategies. Environ. Sci. Technol. 2015, 49, 750–759.
  10. Wang, Y.; Duan, X.; Wang, L. Spatial distribution and source analysis of heavy metals in soils influenced by industrial enterprise distribution: Case study in Jiangsu Province. Sci. Total Environ. 2020, 710, 134953.
  11. Hu, Y.; Cheng, H.; Tao, S. The Challenges and Solutions for Cadmium-contaminated Rice in China: A Critical Review. Environ. Int. 2016, 92–93, 515–532.
  12. Wang, P.; Chen, H.; Kopittke, P.M.; Zhao, F.J. Cadmium contamination in agricultural soils of China and the impact on food safety. Environ. Pollut. 2019, 249, 1038–1048.
  13. Zheng, S.; Wang, Q.; Yuan, Y.; Sun, W. Human health risk assessment of heavy metals in soil and food crops in the Pearl River Delta urban agglomeration of China. Food Chem. 2020, 316, 126213.
  14. Hall, J.L.; Williams, L.E. Transition metal transporters in plants. J. Exp. Bot. 2003, 54, 2601–2613.
  15. Socha, A.L.; Guerinot, M.L. Mn-euvering manganese: The role of transporter gene family members in manganese uptake and mobilization in plants. Front. Plant Sci. 2014, 5, 106.
  16. Thomine, S.; Wang, R.; Ward, J.M.; Crawford, N.M.; Crawford, J.I. Cadmium and iron transport by members of a Plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc. Natl. Acad. Sci. USA 2000, 97, 4991–4996.
  17. Li, J.; Wang, L.; Zheng, L.; Wang, Y.; Chen, X.; Zhang, W. A Functional Study Identifying Critical Residues Involving Metal Transport Activity and Selectivity in Natural Resistance-Associated Macrophage Protein 3 in Arabidopsis thaliana. Int. J. Mol. Sci. 2018, 19, 1430.
  18. Thomine, S.; Lelievre, F.; Debarbieux, E.; Schroeder, J.I.; Barbier-Brygoo, H. AtNRAMP3, a multispecic vacuolar metal transporter involved in Plant responses to iron deciency. Plant J. 2003, 34, 685–695.
  19. Pottier, M.; Oomen, R.; Picco, C.; Giraudat, J.; Scholz-Starke, J.; Richaud, P.; Carpaneto, A.; Thomine, S. Identification of mutations allowing Natural Resistance Associated Macrophage Proteins (NRAMP) to discriminate against cadmium. Plant J. 2015, 83, 625–637.
  20. Lanquar, V.; Lelièvre, F.; Barbier-Brygoo, H.; Thomine, S. Regulation and function of AtNRAMP4 metal transporter protein. Soil Sci. Plant Nutr. 2004, 50, 1141–1150.
  21. Cailliatte, R.; Lapeyre, B.; Briat, J.F.; Mari, S.; Curie, C. The NRAMP6 metal transporter contributes to cadmium toxicity. Biochem. J. 2009, 422, 217–228.
  22. 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.
  23. Chang, J.D.; Huang, S.; Yamaji, N.; Zhang, W.; Ma, J.F.; Zhao, F.J. OsNRAMP1 transporter contributes to cadmium and manganese uptake in rice. Plant Cell Environ. 2020, 43, 2476–2491.
  24. 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.
  25. Chang, J.-D.; Xie, Y.; Zhang, H.; Zhang, S.; Zhao, F.-J. The vacuolar transporter OsNRAMP2 mediates Fe remobilization during germination and affects Cd distribution to rice grain. Plant Soil 2022, 1–17.
  26. 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.
  27. 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.
  28. 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.
  29. 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.
  30. Chang, J.D.; Huang, S.; Konishi, N.; Wang, P.; Chen, J.; Huang, X.Y.; Ma, J.F.; Zhao, F.J. Overexpression of the manganese/cadmium transporter OsNRAMP5 reduces cadmium accumulation in rice grain. J. Exp. Bot. 2020, 71, 5705–5715.
  31. Wang, C.; Chen, X.; Yao, Q.; Long, D.; Fan, X.; Kang, H.; Zeng, J.; Sha, L.; Zhang, H.; Zhou, Y.; et al. Overexpression of TtNRAMP6 enhances the accumulation of Cd in Arabidopsis. Gene 2019, 696, 225–232.
  32. Peng, F.; Wang, C.; Cheng, Y.; Kang, H.; Fan, X.; Sha, L.; Zhang, H.; Zeng, J.; Zhou, Y.; Wang, Y. Cloning and Characterization of TpNRAMP3, a Metal Transporter from Polish Wheat (Triticum polonicum L.). Front. Plant Sci. 2018, 9, 1354.
  33. Peng, F.; Wang, C.; Zhu, J.; Zeng, J.; Kang, H.; Fan, X.; Sha, L.; Zhang, H.; Zhou, Y.; Wang, Y. Expression of TpNRAMP5, a metal transporter from Polish wheat (Triticum polonicum L.), enhances the accumulation of Cd, Co and Mn in transgenic Arabidopsis plants. Planta 2018, 247, 1395–1406.
  34. Wu, D.; Yamaji, N.; Yamane, M.; Kashino-Fujii, M.; Sato, K.; Feng Ma, J. The HvNramp5 Transporter Mediates Uptake of Cadmium and Manganese, But Not Iron. Plant Physiol. 2016, 172, 1899–1910.
  35. Yokosho, K.; Yamaji, N.; Ma, J.F. Buckwheat FeNramp5 Mediates High Manganese Uptake in Roots. Plant Cell Physiol. 2021, 62, 600–609.
  36. Meng, J.G.; Zhang, X.D.; Tan, S.K.; Zhao, K.X.; Yang, Z.M. Genome-wide identification of Cd-responsive NRAMP transporter genes and analyzing expression of NRAMP 1 mediated by miR167 in Brassica napus. Biometals 2017, 30, 917–931.
  37. Yue, X.; Song, J.; Fang, B.; Wang, L.; Zou, J.; Su, N.; Cui, J. BcNRAMP1 promotes the absorption of cadmium and manganese in Arabidopsis. Chemosphere 2021, 283, 131113.
  38. Milner, M.J.; Mitani-Ueno, N.; Yamaji, N.; Yokosho, K.; Craft, E.; Fei, Z.; Ebbs, S.; Clemencia Zambrano, M.; Ma, J.F.; Kochian, L.V. Root and shoot transcriptome analysis of two ecotypes of Noccaea caerulescens uncovers the role of NcNramp1 in Cd hyperaccumulation. Plant J. 2014, 78, 398–410.
  39. Oomen, R.J.; Wu, J.; Lelievre, F.; Blanchet, S.; Richaud, P.; Barbier-Brygoo, H.; Aarts, M.G.; Thomine, S. Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytol. 2009, 181, 637–650.
  40. Wei, W.; Chai, T.; Zhang, Y.; Han, L.; Xu, J.; Guan, Z. The Thlaspi caerulescens NRAMP homologue TcNRAMP3 is capable of divalent cation transport. Mol. Biotechnol. 2009, 41, 15–21.
  41. Zhang, J.; Zhang, M.; Song, H.; Zhao, J.; Shabala, S.; Tian, S.; Yang, X. A novel plasma membrane-based NRAMP transporter contributes to Cd and Zn hyperaccumulation in Sedum alfredii Hance. Environ. Exp. Bot. 2020, 176.
  42. Feng, Y.; Wu, Y.; Zhang, J.; Meng, Q.; Wang, Q.; Ma, L.; Ma, X.; Yang, X. Ectopic expression of SaNRAMP3 from Sedum alfredii enhanced cadmium root-to-shoot transport in Brassica juncea. Ecotoxicol. Environ. Saf. 2018, 156, 279–286.
  43. Chen, S.; Han, X.; Fang, J.; Lu, Z.; Qiu, W.; Liu, M.; Sang, J.; Jiang, J.; Zhuo, R. Sedum alfredii SaNramp6 Metal Transporter Contributes to Cadmium Accumulation in Transgenic Arabidopsis thaliana. Sci. Rep. 2017, 7, 13318.
  44. Lu, Z.; Chen, S.; Han, X.; Zhang, J.; Qiao, G.; Jiang, Y.; Zhuo, R.; Qiu, W. A Single Amino Acid Change in Nramp6 from Sedum Alfredii Hance Affects Cadmium Accumulation. Int. J. Mol. Sci. 2020, 21, 3169.
  45. Zha, Q.; Xiao, Z.; Zhang, X.; Han, Z.; Wang, Y. Cloning and functional analysis of MxNRAMP1 and MxNRAMP3, two genes related to high metal tolerance of Malus xiaojinensis. S. Afr. J. Bot. 2016, 102, 75–80.
  46. Zhang, W.; Yue, S.; Song, J.; Xun, M.; Han, M.; Yang, H. MhNRAMP1 from Malus hupehensis Exacerbates Cell Death by Accelerating Cd Uptake in Tobacco and Apple Calli. Front. Plant Sci. 2020, 11, 957.
  47. Chen, Y.; Li, G.; Yang, J.; Zhao, X.; Sun, Z.; Hou, H. Role of Nramp transporter genes of Spirodela polyrhiza in cadmium accumulation. Ecotoxicol. Environ. Saf. 2021, 227, 112907.
  48. Nakanishi-Masuno, T.; Shitan, N.; Sugiyama, A.; Takanashi, K.; Inaba, S.; Kaneko, S.; Yazaki, K. The Crotalaria juncea metal transporter CjNRAMP1 has a high Fe uptake activity, even in an environment with high Cd contamination. Int. J. Phytoremediat. 2018, 20, 1427–1437.
  49. Liu, W.; Huo, C.; He, L.; Ji, X.; Yu, T.; Yuan, J.; Zhou, Z.; Song, L.; Yu, Q.; Chen, J.; et al. The NtNRAMP1 transporter is involved in cadmium and iron transport in tobacco (Nicotiana tabacum). Plant Physiol. Biochem. 2022, 173, 59–67.
  50. Jia, H.; Yin, Z.; Xuan, D.; Lian, W.; Han, D.; Zhu, Z.; Li, C.; Li, C.; Song, Z. Mutation of NtNRAMP3 improves cadmium tolerance and its accumulation in tobacco leaves by regulating the subcellular distribution of cadmium. J. Hazard. Mater. 2022, 432, 128701.
  51. Takahashi, R.; Bashir, K.; Ishimaru, Y.; Nishizawa, N.K.; Nakanishi, H. The role of heavy-metal ATPases, HMAs, in zinc and cadmium transport in rice. Plant Signal Behav. 2012, 7, 1605–1607.
  52. Morel, M.; Crouzet, J.; Gravot, A.; Auroy, P.; Leonhardt, N.; Vavasseur, A.; Richaud, P. AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol. 2009, 149, 894–904.
  53. Gravot, A.; Lieutaud, A.; Verret, F.; Auroy, P.; Vavasseur, A.; Richaud, P. AtHMA3, a Plant P1B-ATPase, functions as a Cd/Pb transporter in yeast. FEBS Lett. 2004, 561, 22–28.
  54. Wong, C.K.E.; Cobbett, C.S. HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol. 2009, 181, 71–78.
  55. Wong, C.K.E.; Jarvis, R.S.; Sherson, S.M.; Cobbett, C.S. Functional analysis of the heavy metal binding domains of the Zn/Cd-transporting ATPase, HMA2, in Arabidopsis thaliana. New Phytol. 2009, 181, 79–88.
  56. Verret, F.; Gravot, A.; Auroy, P.; Leonhardt, N.; David, P.; Nussaume, L.; Vavasseur, A.; Richaud, P. Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and Plant metal tolerance. FEBS Lett. 2004, 576, 306–312.
  57. Ceasar, S.A.; Lekeux, G.; Motte, P.; Xiao, Z.; Galleni, M.; Hanikenne, M. di-Cysteine Residues of the Arabidopsis thaliana HMA4 C-Terminus Are Only Partially Required for Cadmium Transport. Front. Plant Sci. 2020, 11, 560.
  58. Siemianowski, O.; Barabasz, A.; Kendziorek, M.; Ruszczynska, A.; Bulska, E.; Williams, L.E.; Antosiewicz, D.M. HMA4 expression in tobacco reduces Cd accumulation due to the induction of the apoplastic barrier. J. Exp. Bot. 2014, 65, 1125–1139.
  59. 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.
  60. 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.
  61. Yamaji, N.; Xia, J.; Mitani-Ueno, N.; Yokosho, K.; Feng Ma, J. Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiol. 2013, 162, 927–939.
  62. 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.
  63. 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.
  64. Ueno, D.; Yamaji, N.; Kono, I.; Huang, C.F.; Ando, T.; Yano, M.; Ma, J.F. Gene limiting cadmium accumulation in rice. Proc. Natl. Acad. Sci. USA 2010, 107, 16500–16505.
  65. Wang, H.Q.; Xuan, W.; Huang, X.Y.; Mao, C.; Zhao, F.J. Cadmium Inhibits Lateral Root Emergence in Rice by Disrupting OsPIN-Mediated Auxin Distribution and the Protective Effect of OsHMA3. Plant Cell Physiol. 2021, 62, 166–177.
  66. 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.
  67. Kumagai, S.; Suzuki, T.; Tezuka, K.; Satoh-Nagasawa, N.; Takahashi, H.; Sakurai, K.; Watanabe, A.; Fujimura, T.; Akagi, H. Functional analysis of the C-terminal region of the vacuolar cadmium-transporting rice OsHMA3. FEBS Lett. 2014, 588, 789–794.
  68. 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.
  69. Tan, J.; Wang, J.; Chai, T.; Zhang, Y.; Feng, S.; Li, Y.; Zhao, H.; Liu, H.; Chai, X. Functional analyses of TaHMA2, a P(1B)-type ATPase in wheat. Plant Biotechnol. J. 2013, 11, 420–431.
  70. Wang, Y.; Wang, C.; Liu, Y.; Yu, K.; Zhou, Y. GmHMA3 sequesters Cd to the root endoplasmic reticulum to limit translocation to the stems in soybean. Plant Sci. 2018, 270, 23–29.
  71. Zhao, H.; Wang, L.; Zhao, F.J.; Wu, L.; Liu, A.; Xu, W. SpHMA1 is a chloroplast cadmium exporter protecting photochemical reactions in the Cd hyperaccumulator Sedum plumbizincicola. Plant Cell Environ. 2019, 42, 1112–1124.
  72. Liu, H.; Zhao, H.; Wu, L.; Liu, A.; Zhao, F.J.; Xu, W. Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola. New Phytol. 2017, 215, 687–698.
  73. Zhang, J.; Zhang, M.; Shohag, M.J.; Tian, S.; Song, H.; Feng, Y.; Yang, X. Enhanced expression of SaHMA3 plays critical roles in Cd hyperaccumulation and hypertolerance in Cd hyperaccumulator Sedum alfredii Hance. Planta 2016, 243, 577–589.
  74. Ueno, D.; Milner, M.J.; Yamaji, N.; Yokosho, K.; Koyama, E.; Clemencia Zambrano, M.; Kaskie, M.; Ebbs, S.; Kochian, L.V.; Ma, J.F. Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Plant J. 2011, 66, 852–862.
  75. Papoyan, A.; Kochian, L.V. Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol. 2004, 136, 3814–3823.
  76. Wang, J.; Liang, S.; Xiang, W.; Dai, H.; Duan, Y.; Kang, F.; Chai, T. A repeat region from the Brassica juncea HMA4 gene BjHMA4R is specifically involved in Cd(2+) binding in the cytosol under low heavy metal concentrations. BMC Plant Biol. 2019, 19, 89.
  77. Guo, Q.; Tian, X.; Mao, P.; Meng, L. Functional characterization of IlHMA2, a P1B2-ATPase in Iris lactea response to Cd. Environ. Exp. Bot. 2019, 157, 131–139.
  78. Wang, X.; Zhi, J.; Liu, X.; Zhang, H.; Liu, H.; Xu, J. Transgenic tobacco plants expressing a P1B-ATPase gene from Populus tomentosa Carr. (PtoHMA5) demonstrate improved cadmium transport. Int. J. Biol. Macromol. 2018, 113, 655–661.
  79. Grafe, K.; Schmitt, L. The ABC transporter G subfamily in Arabidopsis thaliana. J. Exp. Bot. 2021, 72, 92–106.
  80. Verrier, P.J.; Bird, D.; Burla, B.; Dassa, E.; Forestier, C.; Geisler, M.; Klein, M.; Kolukisaoglu, U.; Lee, Y.; Martinoia, E.; et al. Plant ABC proteins–a unified nomenclature and updated inventory. Trends Plant Sci. 2008, 13, 151–159.
  81. Kim, D.Y.; Bovet, L.; Kushnir, S.; Noh, E.W.; Martinoia, E.; Lee, Y. AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol. 2006, 140, 922–932.
  82. Kim, D.Y.; Bovet, L.; Maeshima, M.; Martinoia, E.; Lee, Y. The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J. 2007, 50, 207–218.
  83. Park, J.; Song, W.Y.; Ko, D.; Eom, Y.; Hansen, T.H.; Schiller, M.; Lee, T.G.; Martinoia, E.; Lee, Y. The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J. 2012, 69, 278–288.
  84. Rea, P.A. Plant ATP-binding cassette transporters. Annu. Rev. Plant Biol. 2007, 58, 347–375.
  85. Brunetti, P.; Zanella, L.; De Paolis, A.; Di Litta, D.; Cecchetti, V.; Falasca, G.; Barbieri, M.; Altamura, M.M.; Costantino, P.; Cardarelli, M. Cadmium-inducible expression of the ABC-type transporter AtABCC3 increases phytochelatin-mediated cadmium tolerance in Arabidopsis. J. Exp. Bot. 2015, 66, 3815–3829.
  86. Gaillard, S.; Jacquet, H.; Vavasseur, A.; Leonhardt, N.; Forestier, C. AtMRP6/AtABCC6, an ATP-binding cassette transporter gene expressed during early steps of seedling development and up-regulated by cadmium in Arabidopsis thaliana. BMC Plant Biol. 2008, 8, 22.
  87. Wojas, S.; Hennig, J.; Plaza, S.; Geisler, M.; Siemianowski, O.; Sklodowska, A.; Ruszczynska, A.; Bulska, E.; Antosiewicz, D.M. Ectopic expression of Arabidopsis ABC transporter MRP7 modifies cadmium root-to-shoot transport and accumulation. Environ. Pollut. 2009, 157, 2781–2789.
  88. Bhuiyan, M.S.U.; Min, S.R.; Jeong, W.J.; Sultana, S.; Choi, K.S.; Lee, Y.; Liu, J.R. Overexpression of AtATM3 in Brassica juncea confers enhanced heavy metal tolerance and accumulation. Plant Cell Tissue Organ. Cult. 2011, 107, 69–77.
  89. Yang, G.; Fu, S.; Huang, J.; Li, L.; Long, Y.; Wei, Q.; Wang, Z.; Chen, Z.; Xia, J. The tonoplast-localized transporter OsABCC9 is involved in cadmium tolerance and accumulation in rice. Plant Sci. 2021, 307, 110894.
  90. Fu, S.; Lu, Y.; Zhang, X.; Yang, G.; Chao, D.; Wang, Z.; Shi, M.; Chen, J.; Chao, D.Y.; Li, R.; et al. The ABC transporter ABCG36 is required for cadmium tolerance in rice. J. Exp. Bot. 2019, 70, 5909–5918.
  91. Oda, K.; Otani, M.; Uraguchi, S.; Akihiro, T.; Fujiwara, T. Rice ABCG43 is Cd inducible and confers Cd tolerance on yeast. Biosci. Biotechnol. Biochem. 2011, 75, 1211–1213.
  92. Cai, X.; Wang, M.; Jiang, Y.; Wang, C.; Ow, D.W. Overexpression of OsABCG48 Lowers Cadmium in Rice (Oryza sativa L.). Agronomy 2021, 11, 918.
  93. Bhati, K.K.; Alok, A.; Kumar, A.; Kaur, J.; Tiwari, S.; Pandey, A.K. Silencing of ABCC13 transporter in wheat reveals its involvement in grain development, phytic acid accumulation and lateral root formation. J. Exp. Bot. 2016, 67, 4379–4389.
  94. Yang, Y.H.; Wang, C.J.; Li, R.F.; Yi, Y.J.; Zeng, L.; Yang, H.; Zhang, C.F.; Song, K.Y.; Guo, S.J. Transcriptome-based identification and expression characterization of RgABCC transp.porters in Rehmannia glutinosa. PLoS ONE 2021, 16, e0253188.
  95. Wang, H.; Liu, Y.; Peng, Z.; Li, J.; Huang, W.; Liu, Y.; Wang, X.; Xie, S.; Sun, L.; Han, E.; et al. Ectopic Expression of Poplar ABC Transporter PtoABCG36 Confers Cd Tolerance in Arabidopsis thaliana. Int. J. Mol. Sci. 2019, 20, 3293.
  96. Verbruggen, N.; Hermans, C.; Schat, H. Molecular mechanisms of metal hyperaccumulation in plants. New Phytol. 2009, 181, 759–776.
  97. Pence, N.S.; Larsen, P.B.; Ebbs, S.D.; Letham, D.L.D.; Lasat, M.M.; Garvin, D.F.; Eide, D.; Kochian, L.V. The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc. Natl. Acad. Sci. USA 2000, 97, 4956–4960.
  98. Lin, Y.F.; Hassan, Z.; Talukdar, S.; Schat, H.; Aarts, M.G. Expression of the ZNT1 Zinc Transporter from the Metal Hyperaccumulator Noccaea caerulescens Confers Enhanced Zinc and Cadmium Tolerance and Accumulation to Arabidopsis thaliana. PLoS ONE 2016, 11, e0149750.
  99. 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.
  100. Connolly, E.L.; Fett, J.P.; Guerinot, M.L. Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 2002, 14, 1347–1357.
  101. Korshunova, Y.O.; Eide, D.; Clark, W.G.; Guerinot, M.L.; Pakrasi, H.B. The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol. Biol. 1999, 40, 37–44.
  102. Fan, W.; Liu, C.; Cao, B.; Qin, M.; Long, D.; Xiang, Z.; Zhao, A. Genome-Wide Identification and Characterization of Four Gene Families Putatively Involved in Cadmium Uptake, Translocation and Sequestration in Mulberry. Front. Plant Sci. 2018, 9, 879.
  103. Cohen, C.K.; Garvin, D.F.; Kochian, L.V. Kinetic properties of a micronutrient transporter from Pisum sativum indicate a primary function in Fe uptake from the soil. Planta 2004, 218, 784–792.
  104. Jiang, Y.; Chen, X.; Chai, S.; Sheng, H.; Sha, L.; Fan, X.; Zeng, J.; Kang, H.; Zhang, H.; Xiao, X.; et al. TpIRT1 from Polish wheat (Triticum polonicum L.) enhances the accumulation of Fe, Mn, Co, and Cd in Arabidopsis. Plant Sci. 2021, 312, 111058.
  105. Lee, S.; An, G. Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant Cell Environ. 2009, 32, 408–416.
  106. Pedas, P.; Ytting, C.K.; Fuglsang, A.T.; Jahn, T.P.; Schjoerring, J.K.; Husted, S. Manganese efficiency in barley: Identification and characterization of the metal ion transporter HvIRT1. Plant Physiol. 2008, 148, 455–466.
  107. Liu, X.S.; Feng, S.J.; Zhang, B.Q.; Wang, M.Q.; Cao, H.W.; Rono, J.K.; Chen, X.; Yang, Z.M. OsZIP1 functions as a metal efflux transporter limiting excess zinc, copper and cadmium accumulation in rice. BMC Plant Biol. 2019, 19, 283.
  108. Tan, L.; Qu, M.; Zhu, Y.; Peng, C.; Wang, J.; Gao, D.; Chen, C. ZINC TRANSPORTER5 and ZINC TRANSPORTER9 Function Synergistically in Zinc/Cadmium Uptake. Plant Physiol. 2020, 183, 1235–1249.
  109. Yang, M.; Li, Y.; Liu, Z.; Tian, J.; Liang, L.; Qiu, Y.; Wang, G.; Du, Q.; Cheng, D.; Cai, H.; et al. A high activity zinc transporter OsZIP9 mediates zinc uptake in rice. Plant J. 2020, 103, 1695–1709.
  110. 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.
  111. 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.
  112. Barabasz, A.; Palusinska, M.; Papierniak, A.; Kendziorek, M.; Kozak, K.; Williams, L.E.; Antosiewicz, D.M. Functional Analysis of NtZIP4B and Zn Status-Dependent Expression Pattern of Tobacco ZIP Genes. Front. Plant Sci. 2018, 9, 1984.
  113. Maslinska-Gromadka, K.; Barabasz, A.; Palusinska, M.; Kozak, K.; Antosiewicz, D.M. Suppression of NtZIP4A/B Changes Zn and Cd Root-to-Shoot Translocation in a Zn/Cd Status-Dependent Manner. Int. J. Mol. Sci. 2021, 22, 5355.
  114. Zang, J.; Huo, Y.; Liu, J.; Zhang, H.; Liu, J.; Chen, H. Maize YSL2 is required for iron distribution and development in kernels. J. Exp. Bot. 2020, 71, 5896–5910.
  115. Chen, H.; Zhang, C.; Guo, H.; Hu, Y.; He, Y.; Jiang, D. Overexpression of a Miscanthus sacchariflorus yellow stripe-like transporter MsYSL1 enhances resistance of Arabidopsis to cadmium by mediating metal ion reallocation. Plant Growth Regul. 2018, 85, 101–111.
  116. Feng, S.; Tan, J.; Zhang, Y.; Liang, S.; Xiang, S.; Wang, H.; Chai, T. Isolation and characterization of a novel cadmium-regulated Yellow Stripe-Like transporter (SnYSL3) in Solanum nigrum. Plant Cell Rep. 2016, 36, 281–296.
  117. Chen, S.; Liu, Y.; Deng, Y.; Liu, Y.; Dong, M.; Tian, Y.; Sun, H.; Li, Y. Cloning and functional analysis of the VcCXIP4 and VcYSL6 genes as Cd-regulating genes in blueberry. Gene 2019, 686, 104–117.
  118. Wang, J.W.; Li, Y.; Zhang, Y.X.; Chai, T.Y. Molecular cloning and characterization of a Brassica juncea yellow stripe-like gene, BjYSL7, whose overexpression increases heavy metal tolerance of tobacco. Plant Cell Rep. 2013, 32, 651–662.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
Upload a video for this entry
Information
Subjects: Environmental Sciences
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Jingyu Tao
,
Lingli Lu
View Times: 300
Revisions: 2 times (View History)
Update Date: 05 Aug 2022
Table of Contents
    1000/1000
    Hot Most Recent
    Video Production Service
    Feedback