Research Advances in Cadmium Uptake, Transport and Resistance in Rice (Oryza sativa L.)

Yang, 2013, Distribution and speciation of metals (Cu, Zn, Cd, and Pb) in agricultural and non-agricultural soils near a stream upriver from the Pearl River, China, Environ. Pollut., 177, 64, 10.1016/j.envpol.2013.01.044

Zhang, 2013, Molecular mechanism of rice responses to cadmium stress, Chin. J. Rice Sci., 27, 539

Zhai, 2008, Regional assessment of cadmium pollution in agricultural lands and the potential health risk related to intensive mining activities: A case study in Chenzhou City, China, J. Environ. Sci., 20, 696, 10.1016/S1001-0742(08)62115-4

Song, Y., Wang, Y., Mao, W., Sui, H., Yang, L., Yang, D., Jiang, D., Zhang, L., and Gong, Y. (2017). Dietary cadmium exposure assessment among the Chinese population. PLoS ONE, 12.

Tang, 2017, Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield, Sci. Rep. UK, 7, 14438, 10.1038/s41598-017-14832-9

Seregin, 2008, Roles of root and shoot tissues in transport and accumulation of cadmium, lead, nickel, and strontium, Russ. J. Plant Physiol., 55, 1, 10.1134/S1021443708010019

Belleghem, 2007, Subcellular localization of cadmium in roots and leaves of Arabidopsis thaliana, New Phytol., 173, 495, 10.1111/j.1469-8137.2006.01940.x

Wang, 2015, Transport pathways of cadmium (Cd) and its regulatory mechanisms in plant, Acta Ecol. Sin., 35, 7921

Sasaki, 2012, Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice, Plant Cell, 24, 2155, 10.1105/tpc.112.096925

Ishikawa, 2012, Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice, Proc. Natl. Acad. Sci. USA, 109, 19166, 10.1073/pnas.1211132109

Chang, 2020, Overexpression of the manganese/cadmium transporter OsNRAMP5 reduces cadmium accumulation in rice grain, J. Exp. Bot., 71, 5705, 10.1093/jxb/eraa287

Takahashi, 2011, The OsNRAMP1 iron transporter is involved in Cd accumulation in rice, J. Exp. Bot., 62, 4843, 10.1093/jxb/err136

Chang, 2020, OsNRAMP1 contributes to cadmium and manganese uptake in rice, Plant Cell Environ., 43, 2476, 10.1111/pce.13843

Takahashi, 2011, Role of the iron transporter OsNRAMP1 in cadmium uptake and accumulation in rice, Plant Signal. Behav., 6, 1813, 10.4161/psb.6.11.17587

Lee, 2009, Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice, Plant Cell Environ., 32, 408, 10.1111/j.1365-3040.2009.01935.x

Nakanishi, 2006, Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice, Soil Sci. Plant Nutr., 52, 464, 10.1111/j.1747-0765.2006.00055.x

Ishimaru, 2006, Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+, Plant J., 45, 335, 10.1111/j.1365-313X.2005.02624.x

Ishimaru, 2011, A rice phenolic efflux transporter is essential for solubilizing precipitated apoplasmic iron in the plant stele, J. Biol. Chem., 286, 24649, 10.1074/jbc.M111.221168

Ondrasek, G., Rengel, Z., Maurovic, N., Kondres, N., Filipovic, V., Savic, R., Blagojevic, B., Tanaskovik, V., Gergichevich, C.M., and Romic, D. (2021). Growth and element uptake by salt-sensitive crops under combined NaCl and Cd stresses. Plants, 10.

Nosek, M., Kaczmarczyk, A., Jedrzejczyk, R.J., Supel, P., Kaszycki, P., and Miszalski, Z. (2020). Expression of genes involved in heavy metal trafficking in plants exposed to salinity stress and elevated Cd concentrations. Plants, 9.

Yan, 2019, Variation of a major facilitator superfamily gene contributes to differential cadmium accumulation between rice subspecies, Nat. Commun., 10, 2562, 10.1038/s41467-019-10544-y

Ramesh, 2003, Differential metal selectivity and gene expression of two zinc transporters from rice, Plant Physiol., 133, 126, 10.1104/pp.103.026815

Lim, 2014, Positive regulation of rice RING E3 ligase OsHIR1 in arsenic and cadmium uptakes, Plant Mol. Biol., 85, 365, 10.1007/s11103-014-0190-0

Kavitha, 2015, Functional characterization of a transition metal ion transporter, OsZIP6 from rice (Oryza sativa L.), Plant Physiol. Bioch., 97, 165, 10.1016/j.plaphy.2015.10.005

Shimo, 2011, Low cadmium (LCD), a novel gene related to cadmium tolerance and accumulation in rice, J. Exp. Bot., 62, 5727, 10.1093/jxb/err300

Takahashi, 2012, The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice, Plant Cell Environ., 35, 1948, 10.1111/j.1365-3040.2012.02527.x

Mori, 2012, Mutations in rice (Oryza sativa) Heavy Metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium, Plant Cell Physiol., 53, 213, 10.1093/pcp/pcr166

Yamaji, 2013, Preferential delivery of zinc to developing tissues in rice is mediated by P-Type Heavy Metal ATPase OsHMA2, Plant Physiol., 162, 927, 10.1104/pp.113.216564

Luo, 2018, A defensin-like protein drives cadmium efflux and allocation in rice, Nat. Commun., 9, 645, 10.1038/s41467-018-03088-0

Yuan, 2012, Molecular characterization of a rice metal tolerance protein, OsMTP1, Plant Cell Rep., 31, 67, 10.1007/s00299-011-1140-9

Tan, 2019, OsZIP7 functions in xylem loading in roots and inter-vascular transfer in nodes to deliver Zn/Cd to grain in rice, Biochem. Bioph. Res Co., 512, 112, 10.1016/j.bbrc.2019.03.024

Hao, 2018, A node-expressed transporter OsCCX2 is involved in grain cadmium accumulation of rice, Front. Plant Sci., 9, 476, 10.3389/fpls.2018.00476

Uraguchi, 2011, Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains, Proc. Natl. Acad. Sci. USA, 108, 20959, 10.1073/pnas.1116531109

Liu, 2014, Variations among rice cultivars in subcellular distribution of Cd: The relationship between translocation and grain accumulation, Environ. Exp. Bot., 107, 25, 10.1016/j.envexpbot.2014.05.004

Miyadate, 2011, OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles, New Phytol., 189, 190, 10.1111/j.1469-8137.2010.03459.x

Ueno, 2010, Gene limiting cadmium accumulation in rice, Proc. Natl. Acad. Sci. USA, 107, 16500, 10.1073/pnas.1005396107

Yan, 2016, A loss-of-function allele of OsHMA3 associated with high cadmium accumulation in shoots and grain of Japonica rice cultivars, Plant Cell Environ., 39, 1941, 10.1111/pce.12747

Oda, 2011, Rice ABCG43 is Cd inducible and confers Cd tolerance on yeast, Biosci. Biotech. Bioch., 75, 1211, 10.1271/bbb.110193

Shim, 2009, Orthologs of the Class A4 Heat Shock Transcription Factor HsfA4a confer cadmium tolerance in wheat and rice, Plant Cell, 21, 4031, 10.1105/tpc.109.066902

Harada, 2001, Transgenic tobacco plants expressing a rice cysteine synthase gene are tolerant to toxic levels of cadmium, J. Plant Physiol., 158, 655, 10.1078/0176-1617-00314

Park, 2019, Functional characterisation of two phytochelatin synthases in rice (Oryza sativa cv. Milyang 117) that respond to cadmium stress, Plant Biol., 21, 854, 10.1111/plb.12991

Jin, 2006, A metallothionein-like protein of rice (rgMT) functions in E. coli and its gene expression is induced by abiotic stresses, Biotechnol. Lett., 28, 1749, 10.1007/s10529-006-9152-1

Yang, 2016, OsCLT1, a CRT-like transporter 1, is required for glutathione homeostasis and arsenic tolerance in rice, New Phytol., 211, 658, 10.1111/nph.13908

Agrawal, 2003, Novel rice MAP kinases OsMSRMK3 and OsWJUMK1 involved in encountering diverse environmental stresses and developmental regulation, Biochem. Biophys. Res. Commun., 300, 775, 10.1016/S0006-291X(02)02868-1

Yu, 2015, 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., 83, 818, 10.1111/tpj.12929

Lee, 2007, Rice P1B-Type Heavy-Metal ATPase, OsHMA9, is a metal efflux protein, Plant Physiol., 145, 831, 10.1104/pp.107.102236

Liu, X.S., Feng, S.J., Zhang, B.Q., Wang, M.Q., Cao, H.W., Rono, J.K., Chen, X., and Yang, Z.M. (2019). OsZIP1 functions as a metal efflux transporter limiting excess zinc, copper and cadmium accumulation in rice. BMC Plant Biol., 19.

Fu, 2019, The ABC transporter OsABCG36 is required for Cd tolerance in rice, J. Exp. Bot., 70, 5909, 10.1093/jxb/erz335

Zhou, 2016, Changes in cadmium concentration in rice plants under different cadmium levels and expression analysis of genes retated to cadmium regulation, Chin. J. Rice Sci., 30, 380

Wang, 2021, Manganese facilitates cadmium stabilization through physicochemical dynamics and amino acid accumulation in rice rhizosphere under flood-associated low pe+pH, J. Hazard. Mater., 416, 126079, 10.1016/j.jhazmat.2021.126079

Li, 2017, Effects of calcium magnesium phosphate fertilizer on Cd bioavailability in soil and Cd contents in rice, Acta Sci. Circumst., 37, 2322

Chaney, 2015, How does contamination of rice soils with Cd and Zn cause high incidence of human Cd disease in subsistence rice farmers, Curr. Pollut. Rep., 1, 13, 10.1007/s40726-015-0002-4

Guo, 2010, Significant acidification in major Chinese croplands, Science, 327, 1008, 10.1126/science.1182570

Chen, 2020, Spectroscopic response of soil organic matter in mining area to Pb/Cd heavy metal interaction: A mirror of coherent structural variation, J. Hazard. Mater., 393, 122425, 10.1016/j.jhazmat.2020.122425

Sheng, 2008, Effects of inoculation of biosurfactant-producing Bacillus sp. J119 on plant growth and cadmium uptake in a cadmium-amended soil, J. Hazard. Mater., 155, 17, 10.1016/j.jhazmat.2007.10.107

Chai, 2013, Effect of NaCl on growth and Cd accumulation of halophyte Spartina alterniflora under CdCl2 stress, S. Afr. J. Bot., 85, 63, 10.1016/j.sajb.2012.12.004

Manousaki, 2008, Phytoextraction and phytoexcretion of Cd by the leaves of Tamarix smyrnensis growing on contaminated non-saline and saline soils, Environ. Res., 106, 326, 10.1016/j.envres.2007.04.004

Shao, 2017, Silicon reduces cadmium accumulation by suppressing expression of transporter genes involved in cadmium uptake and translocation in rice, J. Exp. Bot., 68, 5641, 10.1093/jxb/erx364

Zhu, 2016, Effects of soil acidification and liming on the phytoavailability of cadmium in paddy soils of central subtropical China, Environ. Pollut., 219, 99, 10.1016/j.envpol.2016.10.043

Jalloh, 2009, Effect of different N fertilizer forms on antioxidant capacity and grain yield of rice growing under Cd stress, J. Hazard. Mater., 162, 1081, 10.1016/j.jhazmat.2008.05.146

Wei, 2010, Effect of fertilizer amendments on phytoremediation of Cd-contaminated soil by a newly discovered hyperaccumulator Solanum nigrum L., J. Hazard. Mater., 176, 269, 10.1016/j.jhazmat.2009.11.023

Houben, 2013, Mobility, bioavailability and pH-dependent leaching of cadmium, zinc and lead in a contaminated soil amended with biochar, Chemosphere, 92, 1450, 10.1016/j.chemosphere.2013.03.055

Ondrasek, 2020, Interactions of humates and chlorides with cadmium drive soil cadmium chemistry and uptake by radish cultivars, Sci. Total Environ., 702, 134887, 10.1016/j.scitotenv.2019.134887

Nosek, 2019, The response of a model C3/CAM intermediate semi-halophyte Mesembryanthemum crystallinum L. to elevated cadmium concentrations, J. Plant Physiol., 240, 153005, 10.1016/j.jplph.2019.153005

Fujimaki, 2010, 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., 152, 1796, 10.1104/pp.109.151035

Rodda, 2011, 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, 347, 105, 10.1007/s11104-011-0829-4

Tanaka, 2007, Quantitative estimation of the contribution of the phloem in cadmium transport to grains in rice plants (Oryza sativa L.), Front. Plant Sci., 53, 72

Zhou, 2017, The difference of cadmium accumulation between the indica and japonica subspecies and the mechanism of it, Plant Growth Regul., 81, 523, 10.1007/s10725-016-0229-0

Lin, 2012, The molecular mechanism of zinc and cadmium stress response in plants, Cell. Mol. Life Sci., 69, 3187, 10.1007/s00018-012-1089-z

Weber, 2010, Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+ hypertolerant facultative metallophyte Arabidopsis halleri, Plant Cell Environ., 29, 950, 10.1111/j.1365-3040.2005.01479.x

Hall, 2002, Cellular mechanisms for heavy metal detoxification and tolerance, J. Exp. Bot., 53, 1, 10.1093/jexbot/53.366.1

Yu, 2020, Characteristics of cadmium immobilization in the cell wall of root in a cadmium-safe rice line (Oryza sativa L.), Chemosphere, 241, 125095, 10.1016/j.chemosphere.2019.125095

Ondrasek, 2019, Zinc and cadmium mapping by NanoSIMS within the root apex after short-term exposure to metal contamination, Ecotox. Environ. Safe., 171, 571, 10.1016/j.ecoenv.2019.01.021

Kuramata, 2009, Novel Cysteine-Rich Peptides from Digitaria ciliaris and Oryza sativa enhance tolerance to cadmium by limiting its cellular accumulation, Plant Cell Physiol., 50, 106, 10.1093/pcp/pcn175

Yu, 2020, The predominant role of pectin in binding Cd in the root cell wall of a high Cd accumulating rice line (Oryza sativa L.), Ecotox. Environ. Safe., 206, 111210, 10.1016/j.ecoenv.2020.111210

Zhu, 2018, Ammonium mitigates Cd toxicity in rice (Oryza sativa) via putrescine-dependent alterations of cell wall composition, Plant Physiol. Bioch., 132, 189, 10.1016/j.plaphy.2018.09.005

Han, 2014, Overexpression of Populus euphratica xyloglucan endotransglucosylase/hydrolase gene confers enhanced cadmium tolerance by the restriction of root cadmium uptake in transgenic tobacco, Environ. Exp. Bot., 100, 74, 10.1016/j.envexpbot.2013.12.021

Liu, 2020, Natural variation in the promoter of OsHMA3 contributes to differential grain cadmium accumulation between Indica and Japonica rice, J. Integr. Plant Biol., 62, 60, 10.1111/jipb.12794

Morel, 2009, AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis, Plant Physiol., 149, 894, 10.1104/pp.108.130294

Liu, 2017, Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola, New Phytol., 215, 687, 10.1111/nph.14622

Gayet, 2009, A common highly conserved cadmium detoxification mechanism from bacteria to humans: Heavy metal tolerance conferred by the ATP-binding cassette (ABC) transporter SpHMT1 requires glutathione but not metal-chelating phytochelatin peptides, J. Biol. Chem., 284, 4936, 10.1074/jbc.M808130200

Park, 2012, The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury, Plant J., 69, 278, 10.1111/j.1365-313X.2011.04789.x

Brunetti, 2015, Cadmium-inducible expression of the ABC-type transporter AtABCC3 increases phytochelatin-mediated cadmium tolerance in Arabidopsis, J. Exp. Bot., 66, 3815, 10.1093/jxb/erv185

Grill, 1989, Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase), Proc. Natl. Acad. Sci. USA, 86, 6838, 10.1073/pnas.86.18.6838

Li, 1997, A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato) cadmium, Proc. Natl. Acad. Sci. USA, 94, 42, 10.1073/pnas.94.1.42

Wang, 2017, Differential effects of citric acid on cadmium uptake and accumulation between tall fescue and Kentucky bluegrass, Ecotox. Environ. Safe., 145, 200, 10.1016/j.ecoenv.2017.07.034

Howden, 1995, Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient, Plant Physiol., 107, 1059, 10.1104/pp.107.4.1059

Heiss, 1999, Cadmium exposure in Brassica juncea causes a decline in transpiration rate and leaf expansion without effect on photosynthesis, J. Exp. Bot., 50, 1827, 10.1093/jxb/50.341.1827

Venkataramaiah, 2011, Overexpression of phytochelatin synthase (AtPCS) in rice for tolerance to cadmium stress, Biologia, 66, 1060, 10.2478/s11756-011-0135-x

Gisbert, 2003, A plant genetically modified that accumulates Pb is especially promising for phytoremediation, Biochem. Biophys. Res. Commun., 303, 440, 10.1016/S0006-291X(03)00349-8

Gasic, 2007, Transgenic Indian mustard (Brassica juncea) plants expressing an Arabidopsis phytochelatin synthase (AtPCS1) exhibit enhanced As and Cd tolerance, Plant Mol. Biol., 64, 361, 10.1007/s11103-007-9158-7

Wojas, 2008, Overexpression of phytochelatin synthase in tobacco: Distinctive effects of AtPCS1 and CePCS genes on plant response to cadmium, J. Exp. Bot., 59, 2205, 10.1093/jxb/ern092

Wang, 2012, Heteroexpression of the wheat phytochelatin synthase gene (TaPCS1) in rice enhances cadmium sensitivity, Acta Bioch. Bioph. Sin., 44, 886, 10.1093/abbs/gms073

Pomponi, 2006, Overexpression of Arabidopsis phytochelatin synthase in tobacco plants enhances Cd2+ tolerance and accumulation but not translocation to the shoot, Planta, 223, 180, 10.1007/s00425-005-0073-3

Li, 2014, Enhanced efficiency of cadmium removal by Boehmeria nivea (L.) Gaud. in the presence of exogenous citric and oxalic acids, J. Environ. Sci., 26, 2508, 10.1016/j.jes.2014.05.031

Ehsan, 2015, Citric acid assisted phytoremediation of copper by Brassica napus L., Ecotox. Environ. Safe., 120, 310, 10.1016/j.ecoenv.2015.06.020

Ondrasek, G., Clode, P.L., Kilburn, M.R., Guagliardo, P., Romić, D., and Rengel, Z. (2019). Zinc and cadmium mapping in the apical shoot and hypocotyl tissues of radish by high-resolution Secondary Ion Mass Spectrometry (NanoSIMS) after short-term exposure to metal contamination. Int. J. Environ. Res. Public Health, 16.

Ondrasek, 2018, Humic acids decrease uptake and distribution of trace metals, but not the growth of radish exposed to cadmium toxicity, Ecotox. Environ. Safe., 151, 55, 10.1016/j.ecoenv.2017.12.055

Panda, 2011, Cadmium stress-induced oxidative stress and role of nitric oxide in rice (Oryza sativa L.), Acta Physiol. Plant., 33, 1737, 10.1007/s11738-011-0710-3

Zhu, 1999, Overexpression of Glutathione Synthetase in Indian mustard enhances cadmium accumulation and tolerance, Plant Physiol., 119, 73, 10.1104/pp.119.1.73

Zhu, 1999, Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-Glutamylcysteine Synthetase, Plant Physiol., 121, 1169, 10.1104/pp.121.4.1169

Li, 2005, Arsenic and mercury tolerance and cadmium sensitivity in Arabidopsis plants expressing bacterial γ-glutamylcysteine synthetase, Environ. Toxicol. Chem., 24, 1376, 10.1897/04-340R.1

Zhang, 2013, 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., 176, 626, 10.1002/jpln.201100276

Vivancos, 2010, Recruitment of glutathione into the nucleus during cell proliferation adjusts whole-cell redox homeostasis in Arabidopsis thaliana and lowers the oxidative defence shield, Plant J., 64, 825, 10.1111/j.1365-313X.2010.04371.x

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Zhang, 2013, Sodium chloride enhances cadmium tolerance through reducing cadmium accumulation and increasing anti-oxidative enzyme activity in tobacco, Environ. Toxicol. Chem., 32, 1420, 10.1002/etc.2183

Dhakarey, 2017, Physiological and proteomic analysis of the rice mutant cpm2 suggests a negative regulatory role of Jasmonic acid in drought tolerance, Front. Plant Sci., 8, 1903, 10.3389/fpls.2017.01903

Singh, 2014, Exogenous application of methyl jasmonate lowers the effect of cadmium-induced oxidative injury in rice seedlings, Phytochemistry, 108, 57, 10.1016/j.phytochem.2014.09.007

Ondrasek, 2019, Biogeochemistry of soil organic matter in agroecosystems & environmental implications, Sci. Total Environ., 658, 1559, 10.1016/j.scitotenv.2018.12.243