Inhibition Roles of Calcium in Cadmium Uptake and Translocation in Rice: A Review
Abstract
:1. Introduction
2. Pathways of Cadmium in Soil–Plant System
2.1. Cadmium Source and Fate in Environment
2.2. Migration Pathways of Cadmium in Plants
2.2.1. Cd in Rhizosphere
2.2.2. Root Morphology
2.2.3. Cell Wall
2.2.4. Transporters
2.2.5. Translocation
2.2.6. Cd Redistribution
2.3. Cadmium Toxicity to Plants
2.3.1. Hormesis of Cd on Plant Growth
2.3.2. Ionomics of Cd with Elements
2.3.3. Detoxication of Cd by Glutathione
3. Mechanisms of Ca-Mediated Restriction in Cd Translocation in Rice
3.1. Liming
3.2. Iron Plaque
3.3. Cell-Wall Synthesis
3.4. Calcium Carrier Proteins (CAXs) Family
3.5. Transpiration
4. Conclusion and Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
ABA | Abscisic acid |
ABC | ATP-Binding Cassette |
Al | Aluminium |
AQPs | Aquaporins |
B | Boron |
Ca | Calcium |
CAX | H+/cation-antiporters Exchanger |
Cd | Cadmium |
CEC | Cation exchange capacity |
Co | Cobalt |
CS | Casparian strip |
Cu | Copper |
DASH | Dihydrazone |
DOC | Dissolved organic carbon |
EDX | Energy-dispersive X-ray micro-analysis |
Fe | Iron |
GR | Glutathione reductase |
GR1 | Glutathione reductase1 |
GST | Glutathione-S-transferase |
HMA | Heavy Metal-transporting ATPases |
JA | Jasmonic acid |
K | Potassium |
Mg | Magnesium |
Mn | Manganese |
MTs | Metallothioneins |
N | Nitrogen |
NO | Nitric oxide |
NRAMP | Natural Resistance-Associated Macrophage Protein |
P | Phosphorus |
PCs | Phytochelatins |
PM | Plasma membrane |
PME | Pectin methylesterase gene |
QTL | Quantitative Trait Loci |
ROS | Reactive oxygen species |
S | Sulfur |
SA | Salicylic acid |
SAT | Serine acetyltransferase |
Se | Selenium |
Si | Silicon |
-SH | Sulfhydryl |
SOM | Soil organic matter |
ZIP | Zinc and Iron regulated transporter |
Zn | Zinc |
References
- Zou, M.; Zhou, S.; Zhou, Y.; Jia, Z.; Guo, T.; Wang, J. Cadmium pollution of soil-rice ecosystems in rice cultivation dominated regions in China: A review. Environ. Pollut. 2021, 280, 116965. [Google Scholar] [CrossRef] [PubMed]
- Qin, G.; Niu, Z.; Yu, J.; Li, Z.; Ma, J.; Xiang, P. Soil heavy metal pollution and food safety in China: Effects, sources and removing technology. Chemosphere 2021, 267, 129205. [Google Scholar] [CrossRef]
- Wei, R.; Chen, C.; Kou, M.; Liu, Z.; Wang, Z.; Cai, J.; Tan, W. Heavy metal concentrations in rice that meet safety standards can still pose a risk to human health. Commun. Earth Environ. 2023, 4, 84. [Google Scholar] [CrossRef]
- Inkham, R.; Kijjanapanich, V.; Huttagosol, P.; Kijjanapanich, P. Low-cost alkaline substances for the chemical stabilization of cadmium-contaminated soils. J. Environ. Manag. 2019, 250, 109395. [Google Scholar] [CrossRef]
- White, P.J. Calcium in Plants. Ann. Bot. 2003, 92, 487–511. [Google Scholar] [CrossRef] [PubMed]
- Nriagu, J.O.; Pacyna, J.M. Quantitative assessment of worldwide contamination of air, water and soils by trace metals. Nature 1988, 333, 134–139. [Google Scholar] [CrossRef]
- Williams, P.N.; Lei, M.; Sun, G.; Huang, Q.; Lu, Y.; Deacon, C.; Meharg, A.A.; Zhu, Y.-G. Occurrence and Partitioning of Cadmium, Arsenic and Lead in Mine Impacted Paddy Rice: Hunan, China. Environ. Sci. Technol. 2009, 43, 637–642. [Google Scholar] [CrossRef]
- Hu, Y.; Liu, X.; Bai, J.; Shih, K.; Zeng, E.Y.; Cheng, H. Assessing heavy metal pollution in the surface soils of a region that had undergone three decades of intense industrialization and urbanization. Environ. Sci. Pollut. Res. 2013, 20, 6150–6159. [Google Scholar] [CrossRef]
- Parvin, A.; Moniruzzaman, M.; Hossain, M.K.; Saha, B.; Parvin, A.; Suchi, P.D.; Hoque, S. Chemical Speciation and Potential Mobility of Heavy Metals in Organic Matter Amended Soil. Appl. Environ. Soil Sci. 2022, 2022, 2028860. [Google Scholar] [CrossRef]
- Salati, S.; Quadri, G.; Tambone, F.; Adani, F. Fresh organic matter of municipal solid waste enhances phytoextraction of heavy metals from contaminated soil. Environ. Pollut. 2010, 158, 1899–1906. [Google Scholar] [CrossRef]
- Antonkiewicz, J.; Para, A. The use of dialdehyde starch derivatives in the phytoremediation of soils contaminated with heavy metals. Int. J. Phytorem. 2016, 18, 245–250. [Google Scholar] [CrossRef] [PubMed]
- Bolan, N.; Kunhikrishnan, A.; Thangarajan, R.; Kumpiene, J.; Park, J.; Makino, T.; Kirkham, M.B.; Scheckel, K. Remediation of heavy metal(loid)s contaminated soils–To mobilize or to immobilize? J. Hazard. Mater. 2014, 266, 141–166. [Google Scholar] [CrossRef] [PubMed]
- Wielgusz, K.; Praczyk, M.; Irzykowska, L.; Świerk, D. Fertilization and soil pH affect seed and biomass yield, plant morphology, and cadmium uptake in hemp (Cannabis sativa L.). Ind. Crops Prod. 2022, 175, 114245. [Google Scholar] [CrossRef]
- Argüello, D.; Chavez, E.; Gutierrez, E.; Pittomvils, M.; Dekeyrel, J.; Blommaert, H.; Smolders, E. Soil amendments to reduce cadmium in cacao (Theobroma cacao L.): A comprehensive field study in Ecuador. Chemosphere 2023, 324, 138318. [Google Scholar] [CrossRef] [PubMed]
- Ubeynarayana, N.; Jeyakumar, P.; Bishop, P.; Pereira, R.C.; Anderson, C.W.N. Effect of soil cadmium on root organic acid secretion by forage crops. Environ. Pollut. 2021, 268, 115839. [Google Scholar] [CrossRef]
- Zia-ur-Rehman, M.; Bani Mfarrej, M.F.; Usman, M.; Azhar, M.; Rizwan, M.; Alharby, H.F.; Bamagoos, A.A.; Alshamrani, R.; Ahmad, Z. Exogenous application of low and high molecular weight organic acids differentially affected the uptake of cadmium in wheat-rice cropping system in alkaline calcareous soil. Environ. Pollut. 2023, 329, 121682. [Google Scholar] [CrossRef]
- Zhu, X.F.; Zheng, C.; Hu, Y.T.; Jiang, T.; Liu, Y.; Dong, N.Y.; Yang, J.L.; Zheng, S.J. Cadmium-induced oxalate secretion from root apex is associated with cadmium exclusion and resistance in Lycopersicon esulentum: Oxalate secretion and cadmium exclusion. Plant Cell Environ. 2011, 34, 1055–1064. [Google Scholar] [CrossRef]
- Tao, Q.; Hou, D.; Yang, X.; Li, T. Oxalate secretion from the root apex of Sedum alfredii contributes to hyperaccumulation of Cd. Plant Soil 2016, 398, 139–152. [Google Scholar] [CrossRef]
- Sakouhi, L.; Kharbech, O.; Ben Massoud, M.; Munemasa, S.; Murata, Y.; Chaoui, A. Exogenous Oxalic Acid Protects Germinating Chickpea Seeds Against Cadmium Injury. J. Soil Sci. Plant Nutr. 2022, 22, 647–659. [Google Scholar] [CrossRef]
- Hill, K.A.; Lion, L.W.; Ahner, B.A. Reduced Cd Accumulation in Zea mays: A Protective Role for Phytosiderophores? Environ. Sci. Technol. 2002, 36, 5363–5368. [Google Scholar] [CrossRef]
- Meda, A.R.; Scheuermann, E.B.; Prechsl, U.E.; Erenoglu, B.; Schaaf, G.; Hayen, H.; Weber, G.; Von Wirén, N. Iron Acquisition by Phytosiderophores Contributes to Cadmium Tolerance. Plant Physiol. 2007, 143, 1761–1773. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Redjala, T.; Zelko, I.; Sterckeman, T.; Legué, V.; Lux, A. Relationship between root structure and root cadmium uptake in maize. Environ. Exp. Bot. 2011, 71, 241–248. [Google Scholar] [CrossRef]
- Thakur, S.; Singh, L.; Wahid, Z.A.; Siddiqui, M.F.; Atnaw, S.M.; Din, M.F.M. Plant-driven removal of heavy metals from soil: Uptake, translocation, tolerance mechanism, challenges, and future perspectives. Environ. Monit Assess 2016, 188, 206. [Google Scholar] [CrossRef] [PubMed]
- Gupta, N.; Yadav, K.K.; Kumar, V.; Kumar, S.; Chadd, R.P.; Kumar, A. Trace elements in soil-vegetables interface: Translocation, bioaccumulation, toxicity and amelioration—A review. Sci. Total Environ. 2019, 651, 2927–2942. [Google Scholar] [CrossRef] [PubMed]
- Manousaki, E.; Kalogerakis, N. Phytoextraction of Pb and Cd by the Mediterranean saltbush (Atriplex halimus L.): Metal uptake in relation to salinity. Environ. Sci Pollut. Res 2009, 16, 844–854. [Google Scholar] [CrossRef]
- Maksimović, I.; Kastori, R.; Krstić, L.; Luković, J. Steady presence of cadmium and nickel affects root anatomy, accumulation and distribution of essential ions in maize seedlings. Biol. Plant. 2007, 51, 589–592. [Google Scholar] [CrossRef]
- Farrell, R.E.; McArthur, D.F.E.; Van Rees, K.C.J. Net Cd2+ flux at the root surface of durum wheat (Triticum turgidum L. var. durum) cultivars in relation to cultivar differences in Cd accumulation. Can. J. Plant Sci. 2005, 85, 103–107. [Google Scholar] [CrossRef]
- Piñeros, M.A.; Shaff, J.E.; Kochian, L.V. Development, Characterization, and Application of a Cadmium-Selective Microelectrode for the Measurement of Cadmium Fluxes in Roots of Thlaspi Species and Wheat1. Plant Physiol. 1998, 116, 1393–1401. [Google Scholar] [CrossRef] [Green Version]
- Chen, X.; Ouyang, Y.; Fan, Y.; Qiu, B.; Zhang, G.; Zeng, F. The pathway of transmembrane cadmium influx via calcium-permeable channels and its spatial characteristics along rice root. J. Exp. Bot. 2018, 69, 5279–5291. [Google Scholar] [CrossRef] [Green Version]
- Huang, L.; Hansen, H.C.B.; Wang, H.; Mu, J.; Xie, Z.; Zheng, L.; Hu, Z. Effects of sulfate on cadmium uptake in wheat grown in paddy soil-pot experiment. Plant Soil Environ. 2019, 65, 602–608. [Google Scholar] [CrossRef] [Green Version]
- Anwen, X.; Danting, C.; Chin, L.W.; Zhihong, Y. Root Morphology and Anatomy Affect Cadmium Translocation and Accumulation in Rice. Rice Sci. 2021, 28, 594–604. [Google Scholar] [CrossRef]
- Laporte, M.A.; Denaix, L.; Pagès, L.; Sterckeman, T.; Flénet, F.; Dauguet, S.; Nguyen, C. Longitudinal variation in cadmium influx in intact first order lateral roots of sunflower (Helianthus annuus. L). Plant Soil 2013, 372, 581–595. [Google Scholar] [CrossRef]
- Van Belleghem, F.; Cuypers, A.; Semane, B.; Smeets, K.; Vangronsveld, J.; d’Haen, J.; Valcke, R. Subcellular localization of cadmium in roots and leaves of Arabidopsis thaliana. New Phytol. 2007, 173, 495–508. [Google Scholar] [CrossRef] [PubMed]
- Carrier, P.; Baryla, A.; Havaux, M. Cadmium distribution and microlocalization in oilseed rape (Brassica napus) after long-term growth on cadmium-contaminated soil. Planta 2003, 216, 939–950. [Google Scholar] [CrossRef]
- Li, T.; Tao, Q.; Shohag, M.J.I.; Yang, X.; Sparks, D.L.; Liang, Y. Root cell wall polysaccharides are involved in cadmium hyperaccumulation in Sedum alfredii. Plant Soil 2015, 389, 387–399. [Google Scholar] [CrossRef]
- Riaz, M.; Kamran, M.; Fahad, S.; Wang, X. Nano-silicon mediated alleviation of Cd toxicity by cell wall adsorption and antioxidant defense system in rice seedlings. Plant Soil 2023, 486, 103–117. [Google Scholar] [CrossRef]
- Wang, K.; Yu, H.; Zhang, X.; Ye, D.; Huang, H.; Wang, Y.; Zheng, Z.; Li, T. Hydrogen peroxide contributes to cadmium binding on root cell wall pectin of cadmium-safe rice line (Oryza sativa L.). Ecotoxicol. Environ. Saf. 2022, 237, 113526. [Google Scholar] [CrossRef]
- Yu, M.; Zhuo, R.; Lu, Z.; Li, S.; Chen, J.; Wang, Y.; Li, J.; Han, X. Molecular insights into lignin biosynthesis on cadmium tolerance: Morphology, transcriptome and proteome profiling in Salix matsudana. J. Hazard. Mater. 2023, 441, 129909. [Google Scholar] [CrossRef]
- Delgado, L.; Martínez, G.; López-Iglesias, C.; Mercadé, E. Cryo-electron tomography of plunge-frozen whole bacteria and vitreous sections to analyze the recently described bacterial cytoplasmic structure, the Stack. J. Struct. Biol. 2015, 189, 220–229. [Google Scholar] [CrossRef]
- Serova, T.A.; Tikhonovich, I.A.; Tsyganov, V.E. Analysis of nodule senescence in pea (Pisum sativum L.) using laser microdissection, real-time PCR, and ACC immunolocalization. J. Plant Physiol. 2017, 212, 29–44. [Google Scholar] [CrossRef]
- 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: OsNRAMP1 in arsenic transport and tolerance. Plant Cell Environ. 2014, 37, 140–152. [Google Scholar] [CrossRef] [PubMed]
- 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]
- Chang, J.; Huang, S.; Yamaji, N.; Zhang, W.; Ma, J.F.; Zhao, F. OsNRAMP1 transporter contributes to cadmium and manganese uptake in rice. Plant Cell Environ. 2020, 43, 2476–2491. [Google Scholar] [CrossRef] [PubMed]
- 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, 476, 79–95. [Google Scholar] [CrossRef]
- 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] [PubMed] [Green Version]
- 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. [Google Scholar] [CrossRef] [Green Version]
- 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. [Google Scholar] [CrossRef]
- 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]
- 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. [Google Scholar] [CrossRef] [Green Version]
- Wiggenhauser, M.; Aucour, A.-M.; Bureau, S.; Campillo, S.; Telouk, P.; Romani, M.; Ma, J.F.; Landrot, G.; Sarret, G. Cadmium transfer in contaminated soil-rice systems: Insights from solid-state speciation analysis and stable isotope fractionation. Environ. Pollut. 2021, 269, 115934. [Google Scholar] [CrossRef]
- 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] [PubMed] [Green Version]
- 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. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [Green Version]
- White, P.J. The pathways of calcium movement to the xylem. J. Exp. Bot. 2001, 52, 891–899. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Salt, D.E.; Prince, R.C.; Pickering, I.J.; Raskin, I. Mechanisms of Cadmium Mobility and Accumulation in Indian Mustard. Plant Physiol. 1995, 109, 1427–1433. [Google Scholar] [CrossRef] [Green Version]
- Van Der Vliet, L.; Peterson, C.; Hale, B. Cd accumulation in roots and shoots of durum wheat: The roles of transpiration rate and apoplastic bypass. J. Exp. Bot. 2007, 58, 2939–2947. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Uraguchi, S.; Mori, S.; Kuramata, M.; Kawasaki, A.; Arao, T.; Ishikawa, S. Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J. Exp. Bot. 2009, 60, 2677–2688. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mishra, S.; Mishra, A.; Küpper, H. Protein Biochemistry and Expression Regulation of Cadmium/Zinc Pumping ATPases in the Hyperaccumulator Plants Arabidopsis halleri and Noccaea caerulescens. Front. Plant Sci. 2017, 8, 835. [Google Scholar] [CrossRef] [Green Version]
- 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] [Green Version]
- Kato, M.; Ishikawa, S.; Inagaki, K.; Chiba, K.; Hayashi, H.; Yanagisawa, S.; Yoneyama, T. Possible chemical forms of cadmium and varietal differences in cadmium concentrations in the phloem sap of rice plants (Oryza sativa L.). Soil Sci. Plant Nutr. 2010, 56, 839–847. [Google Scholar] [CrossRef] [Green Version]
- Liñero, O.; Cornu, J.-Y.; De Diego, A.; Bussière, S.; Coriou, C.; Thunot, S.; Robert, T.; Nguyen, C. Source of Ca, Cd, Cu, Fe, K, Mg, Mn, Mo and Zn in grains of sunflower (Helianthus annuus) grown in nutrient solution: Root uptake or remobilization from vegetative organs? Plant Soil 2018, 424, 435–450. [Google Scholar] [CrossRef]
- Yan, B.-F.; Nguyen, C.; Pokrovsky, O.S.; Candaudap, F.; Coriou, C.; Bussière, S.; Robert, T.; Cornu, J.Y. Contribution of remobilization to the loading of cadmium in durum wheat grains: Impact of post-anthesis nitrogen supply. Plant Soil 2018, 424, 591–606. [Google Scholar] [CrossRef]
- Kobayashi, N.I.; Tanoi, K.; Hirose, A.; Nakanishi, T.M. Characterization of rapid intervascular transport of cadmium in rice stem by radioisotope imaging. J. Exp. Bot. 2013, 64, 507–517. [Google Scholar] [CrossRef] [Green Version]
- Yamaji, N.; Ma, J.F. Node-controlled allocation of mineral elements in Poaceae. Curr. Opin. Plant Biol. 2017, 39, 18–24. [Google Scholar] [CrossRef] [PubMed]
- Hasan, S.A.; Hayat, S.; Ahmad, A. Screening of tomato (Lycopersicon esculentum) cultivars against cadmium through shotgun approach. J. Plant Interact. 2009, 4, 187–201. [Google Scholar] [CrossRef]
- Lysenko, E.A.; Klaus, A.A.; Pshybytko, N.L.; Kusnetsov, V.V. Cadmium accumulation in chloroplasts and its impact on chloroplastic processes in barley and maize. Photosynth. Res. 2015, 125, 291–303. [Google Scholar] [CrossRef] [PubMed]
- Potters, G.; Pasternak, T.P.; Guisez, Y.; Palme, K.J.; Jansen, M.A.K. Stress-induced morphogenic responses: Growing out of trouble? Trends Plant Sci. 2007, 12, 98–105. [Google Scholar] [CrossRef]
- Anjum, S.A.; Tanveer, M.; Hussain, S.; Bao, M.; Wang, L.; Khan, I.; Ullah, E.; Tung, S.A.; Samad, R.A.; Shahzad, B. Cadmium toxicity in Maize (Zea mays L.): Consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environ. Sci. Pollut. Res. 2015, 22, 17022–17030. [Google Scholar] [CrossRef]
- DalCorso, G.; Farinati, S.; Furini, A. Regulatory networks of cadmium stress in plants. Plant Signal. Behav. 2010, 5, 663–667. [Google Scholar] [CrossRef]
- Sanità Di Toppi, L.; Gabbrielli, R. Response to cadmium in higher plants. Environ. Exp. Bot. 1999, 41, 105–130. [Google Scholar] [CrossRef]
- Haider, F.U.; Liqun, C.; Coulter, J.A.; Cheema, S.A.; Wu, J.; Zhang, R.; Wenjun, M.; Farooq, M. Cadmium toxicity in plants: Impacts and remediation strategies. Ecotoxicol. Environ. Saf. 2021, 211, 111887. [Google Scholar] [CrossRef] [PubMed]
- El Rasafi, T.; Oukarroum, A.; Haddioui, A.; Song, H.; Kwon, E.E.; Bolan, N.; Tack, F.M.G.; Sebastian, A.; Prasad, M.N.V.; Rinklebe, J. Cadmium stress in plants: A critical review of the effects, mechanisms, and tolerance strategies. Crit. Rev. Environ. Sci. Technol. 2022, 52, 675–726. [Google Scholar] [CrossRef]
- Rashid, A.; Schutte, B.J.; Ulery, A.; Deyholos, M.K.; Sanogo, S.; Lehnhoff, E.A.; Beck, L. Heavy Metal Contamination in Agricultural Soil: Environmental Pollutants Affecting Crop Health. Agronomy 2023, 13, 1521. [Google Scholar] [CrossRef]
- Riaz, M.; Kamran, M.; Rizwan, M.; Ali, S.; Zhou, Y.; Núñez-Delgado, A.; Wang, X. Boron application mitigates Cd toxicity in leaves of rice by subcellular distribution, cell wall adsorption and antioxidant system. Ecotoxicol. Environ. Saf. 2021, 222, 112540. [Google Scholar] [CrossRef]
- 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]
- Mostofa, M.G.; Rahman, A.; Ansary, M.d.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] [Green Version]
- Domínguez, M.T.; Marañón, T.; Murillo, J.M.; Redondo-Gómez, S. Response of Holm oak (Quercus ilex subsp. ballota) and mastic shrub (Pistacia lentiscus L.) seedlings to high concentrations of Cd and Tl in the rhizosphere. Chemosphere 2011, 83, 1166–1174. [Google Scholar] [CrossRef]
- Gapper, C.; Dolan, L. Control of Plant Development by Reactive Oxygen Species. Plant Physiol. 2006, 141, 341–345. [Google Scholar] [CrossRef] [Green Version]
- Xie, M.; Gao, X.; Zhang, S.; Fu, X.; Le, Y.; Wang, L. Cadmium stimulated cooperation between bacterial endophytes and plant intrinsic detoxification mechanism in Lonicera japonica thunb. Chemosphere 2023, 325, 138411. [Google Scholar] [CrossRef]
- Mengdi, X.; Wenqing, C.; Haibo, D.; Xiaoqing, W.; Li, Y.; Yuchen, K.; Hui, S.; Lei, W. Cadmium-induced hormesis effect in medicinal herbs improves the efficiency of safe utilization for low cadmium-contaminated farmland soil. Ecotoxicol. Environ. Saf. 2021, 225, 112724. [Google Scholar] [CrossRef]
- Nogueira, M.L.; Carvalho, M.E.A.; Ferreira, J.M.M.; Bressanin, L.A.; Piotto, K.D.B.; Piotto, F.A.; Marques, D.N.; Barbosa, S.; Azevedo, R.A. Cadmium-induced transgenerational effects on tomato plants: A gift from parents to progenies. Sci. Total Environ. 2021, 789, 147885. [Google Scholar] [CrossRef] [PubMed]
- Erofeeva, E.A. Hormesis in plants: Its common occurrence across stresses. Curr. Opin. Toxicol. 2022, 30, 100333. [Google Scholar] [CrossRef]
- He, S.; Yang, X.; He, Z.; Baligar, V.C. Morphological and Physiological Responses of Plants to Cadmium Toxicity: A Review. Pedosphere 2017, 27, 421–438. [Google Scholar] [CrossRef]
- Rizwan, M.; Ali, S.; Adrees, M.; Rizvi, H.; Zia-ur-Rehman, M.; Hannan, F.; Qayyum, M.F.; Hafeez, F.; Ok, Y.S. Cadmium stress in rice: Toxic effects, tolerance mechanisms, and management: A critical review. Environ. Sci. Pollut. Res. 2016, 23, 17859–17879. [Google Scholar] [CrossRef] [PubMed]
- Siddique, A.B.; Rahman, M.M.; Islam, M.d.R.; Naidu, R. Influences of soil pH, iron application and rice variety on cadmium distribution in rice plant tissues. Sci. Total Environ. 2022, 810, 152296. [Google Scholar] [CrossRef] [PubMed]
- Dundar, E.; Sonmez, G.D.; Unver, T. Isolation, molecular characterization and functional analysis of OeMT2, an olive metallothionein with a bioremediation potential. Mol. Genet. Genom. 2015, 290, 187–199. [Google Scholar] [CrossRef] [PubMed]
- Adrees, M.; Ali, S.; Rizwan, M.; Zia-ur-Rehman, M.; Ibrahim, M.; Abbas, F.; Farid, M.; Qayyum, M.F.; Irshad, M.K. Mechanisms of silicon-mediated alleviation of heavy metal toxicity in plants: A review. Ecotoxicol. Environ. Saf. 2015, 119, 186–197. [Google Scholar] [CrossRef]
- Riaz, M.; Kamran, M.; Fang, Y.; Yang, G.; Rizwan, M.; Ali, S.; Zhou, Y.; Wang, Q.; Deng, L.; Wang, Y.; et al. Boron supply alleviates cadmium toxicity in rice (Oryza sativa L.) by enhancing cadmium adsorption on cell wall and triggering antioxidant defense system in roots. Chemosphere 2021, 266, 128938. [Google Scholar] [CrossRef]
- Bano, K.; Kumar, B.; Alyemeni, M.N.; Ahmad, P. Protective mechanisms of sulfur against arsenic phytotoxicity in Brassica napus by regulating thiol biosynthesis, sulfur-assimilation, photosynthesis, and antioxidant response. Plant Physiol. Biochem. 2022, 188, 1–11. [Google Scholar] [CrossRef]
- Rajendran, M.; Shi, L.; Wu, C.; Li, W.; An, W.; Liu, Z.; Xue, S. Effect of sulfur and sulfur-iron modified biochar on cadmium availability and transfer in the soil–rice system. Chemosphere 2019, 222, 314–322. [Google Scholar] [CrossRef]
- Anjum, S.A.; Tanveer, M.; Hussain, S.; Shahzad, B.; Ashraf, U.; Fahad, S.; Hassan, W.; Jan, S.; Khan, I.; Saleem, M.F.; et al. Osmoregulation and antioxidant production in maize under combined cadmium and arsenic stress. Environ. Sci. Pollut. Res. 2016, 23, 11864–11875. [Google Scholar] [CrossRef] [PubMed]
- Seth, C.S.; Remans, T.; Keunen, E.; Jozefczak, M.; Gielen, H.; Opdenakker, K.; Weyens, N.; Vangronsveld, J.; Cuypers, A. Phytoextraction of toxic metals: A central role for glutathione: Metal phytoextraction and glutathione. Plant Cell Environ. 2012, 35, 334–346. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schützendübel, A.; Schwanz, P.; Teichmann, T.; Gross, K.; Langenfeld-Heyser, R.; Godbold, D.L.; Polle, A. Cadmium-Induced Changes in Antioxidative Systems, Hydrogen Peroxide Content, and Differentiation in Scots Pine Roots. Plant Physiol. 2001, 127, 887–898. [Google Scholar] [CrossRef] [PubMed]
- Chaouch, S.; Queval, G.; Vanderauwera, S.; Mhamdi, A.; Vandorpe, M.; Langlois-Meurinne, M.; Van Breusegem, F.; Saindrenan, P.; Noctor, G. Peroxisomal Hydrogen Peroxide Is Coupled to Biotic Defense Responses by ISOCHORISMATE SYNTHASE1 in a Daylength-Related Manner. Plant Physiol. 2010, 153, 1692–1705. [Google Scholar] [CrossRef] [Green Version]
- Guo, B.; Liu, C.; Li, H.; Yi, K.; Ding, N.; Li, N.; Lin, Y.; Fu, Q. Endogenous salicylic acid is required for promoting cadmium tolerance of Arabidopsis by modulating glutathione metabolisms. J. Hazard. Mater. 2016, 316, 77–86. [Google Scholar] [CrossRef]
- Deckers, J.; Hendrix, S.; Prinsen, E.; Vangronsveld, J.; Cuypers, A. Identifying the Pressure Points of Acute Cadmium Stress Prior to Acclimation in Arabidopsis thaliana. Int. J. Mol. Sci. 2020, 21, 6232. [Google Scholar] [CrossRef]
- Ma, Z.; An, T.; Zhu, X.; Ji, J.; Wang, G.; Guan, C.; Jin, C.; Yi, L. GR1-like gene expression in Lycium chinense was regulated by cadmium-induced endogenous jasmonic acids accumulation. Plant Cell Rep. 2017, 36, 1457–1476. [Google Scholar] [CrossRef]
- Bočová, B.; Huttová, J.; Mistrík, I.; Tamás, L. Auxin signalling is involved in cadmium-induced glutathione-S-transferase activity in barley root. Acta Physiol. Plant. 2013, 35, 2685–2690. [Google Scholar] [CrossRef]
- Dodd, A.N.; Kudla, J.; Sanders, D. The Language of Calcium Signaling. Annu. Rev. Plant Biol. 2010, 61, 593–620. [Google Scholar] [CrossRef]
- Bolat, I.; Kaya, C.; Almaca, A.; Timucin, S. Calcium Sulfate Improves Salinity Tolerance in Rootstocks of Plum. J. Plant Nutr. 2006, 29, 553–564. [Google Scholar] [CrossRef]
- Rentel, M.C.; Knight, M.R. Oxidative Stress-Induced Calcium Signaling in Arabidopsis. Plant Physiol. 2004, 135, 1471–1479. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sanyal, S.K.; Sharma, K.; Bisht, D.; Sharma, S.; Sushmita, K.; Kateriya, S.; Pandey, G.K. Role of calcium sensor protein module CBL-CIPK in abiotic stress and light signaling responses in green algae. Int. J. Biol. Macromol. 2023, 237, 124163. [Google Scholar] [CrossRef]
- Zhu, H.; Chen, C.; Xu, C.; Zhu, Q.; Huang, D. Effects of soil acidification and liming on the phytoavailability of cadmium in paddy soils of central subtropical China. Environ. Pollut. 2016, 219, 99–106. [Google Scholar] [CrossRef]
- Wang, M.; Yang, Y.; Chen, W. Manganese, Zinc, and pH Affect Cadmium Accumulation in Rice Grain under Field Conditions in Southern China. J. Environ. Qual. 2018, 47, 306–311. [Google Scholar] [CrossRef] [PubMed]
- He, L.-L.; Huang, D.-Y.; Zhang, Q.; Zhu, H.-H.; Xu, C.; Li, B.; Zhu, Q.-H. Meta-analysis of the effects of liming on soil pH and cadmium accumulation in crops. Ecotoxicol. Environ. Saf. 2021, 223, 112621. [Google Scholar] [CrossRef] [PubMed]
- Hong, C.O.; Kim, S.Y.; Gutierrez, J.; Owens, V.N.; Kim, P.J. Comparison of oyster shell and calcium hydroxide as liming materials for immobilizing cadmium in upland soil. Biol. Fertil. Soils 2010, 46, 491–498. [Google Scholar] [CrossRef]
- Cao, X.; Hu, P.; Tan, C.; Wu, L.; Peng, B.; Christie, P.; Luo, Y. Effects of a natural sepiolite bearing material and lime on the immobilization and persistence of cadmium in a contaminated acid agricultural soil. Environ. Sci. Pollut. Res. 2018, 25, 22075–22084. [Google Scholar] [CrossRef]
- Antoniadis, V.; Levizou, E.; Shaheen, S.M.; Ok, Y.S.; Sebastian, A.; Baum, C.; Prasad, M.N.V.; Wenzel, W.W.; Rinklebe, J. Trace elements in the soil-plant interface: Phytoavailability, translocation, and phytoremediation—A review. Earth-Sci. Rev. 2017, 171, 621–645. [Google Scholar] [CrossRef]
- Siddique, A.B.; Rahman, M.M.; Islam, M.d.R.; Naidu, R. Varietal variation and formation of iron plaques on cadmium accumulation in rice seedling. Environ. Adv. 2021, 5, 100075. [Google Scholar] [CrossRef]
- Fu, Y.; Yang, X.; Shen, H. Root iron plaque alleviates cadmium toxicity to rice (Oryza sativa) seedlings. Ecotoxicol. Environ. Saf. 2018, 161, 534–541. [Google Scholar] [CrossRef]
- Sebastian, A.; Prasad, M.N.V. Iron plaque decreases cadmium accumulation in Oryza sativa L. and serves as a source of iron. Plant Biol. J. 2016, 18, 1008–1015. [Google Scholar] [CrossRef] [PubMed]
- Guo, B.; Liu, J.; Liu, C.; Lin, Y.; Li, H.; Zhu, D.; Zhang, Q.; Chen, X.; Qiu, G.; Fu, Q.; et al. Shade and iron plaque of Sesbania affect cadmium accumulation in rice: A new strategy for safe production in contaminated soil. Environ. Technol. Innov. 2023, 29, 102964. [Google Scholar] [CrossRef]
- Zandi, P.; Yang, J.; Darma, A.; Bloem, E.; Xia, X.; Wang, Y.; Li, Q.; Schnug, E. Iron plaque formation, characteristics, and its role as a barrier and/or facilitator to heavy metal uptake in hydrophyte rice (Oryza sativa L.). Environ. Geochem Health 2023, 45, 525–559. [Google Scholar] [CrossRef]
- Rivera, M.B.; Giráldez, M.I.; Fernández-Caliani, J.C. Assessing the environmental availability of heavy metals in geogenically contaminated soils of the Sierra de Aracena Natural Park (SW Spain). Is there a health risk? Sci. Total Environ. 2016, 560–561, 254–265. [Google Scholar] [CrossRef] [PubMed]
- Buckley, W.T.; Buckley, K.E.; Huang, J.J. Root cadmium desorption methods and their evaluation with compartmental modeling. New Phytol. 2010, 188, 280–290. [Google Scholar] [CrossRef]
- Zhang, H.; Xie, S.; Wan, N.; Feng, B.; Wang, Q.; Huang, K.; Fang, Y.; Bao, Z.; Xu, F. Iron plaque effects on selenium and cadmium stabilization in Cd-contaminated seleniferous rice seedlings. Environ. Sci. Pollut. Res. 2022, 30, 22772–22786. [Google Scholar] [CrossRef]
- Liu, J.; Ma, J.; He, C.; Li, X.; Zhang, W.; Xu, F.; Lin, Y.; Wang, L. Inhibition of cadmium ion uptake in rice (Oryza sativa) cells by a wall-bound form of silicon. New Phytol. 2013, 200, 691–699. [Google Scholar] [CrossRef]
- Liu, P.; Jin, Z.; Dai, C.; Guo, L.; Cui, X.; Yang, Y. Potassium enhances cadmium resistance ability of Panax notoginseng by brassinolide signaling pathway-regulated cell wall pectin metabolism. Ecotoxicol. Environ. Saf. 2021, 227, 112906. [Google Scholar] [CrossRef]
- Huang, Y.; Huang, B.; Shen, C.; Zhou, W.; Liao, Q.; Chen, Y.; Xin, J. Boron supplying alters cadmium retention in root cell walls and glutathione content in Capsicum annuum. J. Hazard. Mater. 2022, 432, 128713. [Google Scholar] [CrossRef]
- Hocking, B.; Tyerman, S.D.; Burton, R.A.; Gilliham, M. Fruit Calcium: Transport and Physiology. Front. Plant Sci. 2016, 7, 569. [Google Scholar] [CrossRef] [Green Version]
- Martins, V.; Garcia, A.; Costa, C.; Sottomayor, M.; Gerós, H. Calcium- and hormone-driven regulation of secondary metabolism and cell wall enzymes in grape berry cells. J. Plant Physiol. 2018, 231, 57–67. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marcec, M.J.; Tanaka, K. Crosstalk between Calcium and ROS Signaling during Flg22-Triggered Immune Response in Arabidopsis Leaves. Plants 2021, 11, 14. [Google Scholar] [CrossRef] [PubMed]
- Rodríguez-Serrano, M.; Romero-Puertas, M.C.; Pazmiño, D.M.; Testillano, P.S.; Risueño, M.C.; Del Río, L.A.; Sandalio, L.M. Cellular Response of Pea Plants to Cadmium Toxicity: Cross Talk between Reactive Oxygen Species, Nitric Oxide, and Calcium. Plant Physiol. 2009, 150, 229–243. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McAinsh, M.R.; Pittman, J.K. Shaping the calcium signature. New Phytol. 2009, 181, 275–294. [Google Scholar] [CrossRef] [PubMed]
- Choi, W.; Miller, G.; Wallace, I.; Harper, J.; Mittler, R.; Gilroy, S. Orchestrating rapid long-distance signaling in plants with Ca2+, ROS and electrical signals. Plant J. 2017, 90, 698–707. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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: Cadmium impairs ion homeostasis. Plant Cell Environ. 2012, 35, 1998–2013. [Google Scholar] [CrossRef]
- Tian, S.; Xie, R.; Wang, H.; Hu, Y.; Ge, J.; Liao, X.; Gao, X.; Brown, P.; Lin, X.; Lu, L. Calcium Deficiency Triggers Phloem Remobilization of Cadmium in a Hyperaccumulating Species1. Plant Physiol 2016, 172, 2300–2313. [Google Scholar] [CrossRef] [Green Version]
- Li, Z.; Mei, X.; Li, T.; Yang, S.; Qin, L.; Li, B.; Zu, Y. Effects of calcium application on activities of membrane transporters in Panax notoginseng under cadmium stress. Chemosphere 2021, 262, 127905. [Google Scholar] [CrossRef]
- Kamiya, T.; Maeshima, M. Residues in Internal Repeats of the Rice Cation/H+ Exchanger Are Involved in the Transport and Selection of Cations. J. Biol. Chem. 2004, 279, 812–819. [Google Scholar] [CrossRef] [Green Version]
- Korenkov, V.; Hirschi, K.; Crutchfield, J.D.; Wagner, G.J. Enhancing tonoplast Cd/H antiport activity increases Cd, Zn, and Mn tolerance, and impacts root/shoot Cd partitioning in Nicotiana tabacum L. Planta 2007, 226, 1379–1387. [Google Scholar] [CrossRef]
- Baliardini, C.; Meyer, C.-L.; Salis, P.; Saumitou-Laprade, P.; Verbruggen, N. CATION EXCHANGER1 Cosegregates with Cadmium Tolerance in the Metal Hyperaccumulator Arabidopsis halleri and Plays a Role in Limiting Oxidative Stress in Arabidopsis Spp. Plant Physiol. 2015, 169, 549–559. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zou, W.; Chen, J.; Meng, L.; Chen, D.; He, H.; Ye, G. The Rice Cation/H+ Exchanger Family Involved in Cd Tolerance and Transport. Int. J. Mol. Sci. 2021, 22, 8186. [Google Scholar] [CrossRef] [PubMed]
- Zou, W.; Zhan, J.; Meng, L.; Chen, Y.; Chen, D.; Zhang, M.; He, H.; Chen, J.; Ye, G. The Cation/H+ exchanger OsCAX2 is involved in cadmium tolerance and accumulation through vacuolar sequestration in rice. Plant Biol. 2022. [Google Scholar] [CrossRef]
- Liu, H.; Wang, H.; Ma, Y.; Wang, H.; Shi, Y. Role of transpiration and metabolism in translocation and accumulation of cadmium in tobacco plants (Nicotiana tabacum L.). Chemosphere 2016, 144, 1960–1965. [Google Scholar] [CrossRef] [PubMed]
- Gilliham, M.; Dayod, M.; Hocking, B.J.; Xu, B.; Conn, S.J.; Kaiser, B.N.; Leigh, R.A.; Tyerman, S.D. Calcium delivery and storage in plant leaves: Exploring the link with water flow. J. Exp. Bot. 2011, 62, 2233–2250. [Google Scholar] [CrossRef] [PubMed]
- Chen, H.; Zhang, W.; Yang, X.; Wang, P.; McGrath, S.P.; Zhao, F.-J. Effective methods to reduce cadmium accumulation in rice grain. Chemosphere 2018, 207, 699–707. [Google Scholar] [CrossRef]
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Liu, J.; Feng, X.; Qiu, G.; Li, H.; Wang, Y.; Chen, X.; Fu, Q.; Guo, B. Inhibition Roles of Calcium in Cadmium Uptake and Translocation in Rice: A Review. Int. J. Mol. Sci. 2023, 24, 11587. https://doi.org/10.3390/ijms241411587
Liu J, Feng X, Qiu G, Li H, Wang Y, Chen X, Fu Q, Guo B. Inhibition Roles of Calcium in Cadmium Uptake and Translocation in Rice: A Review. International Journal of Molecular Sciences. 2023; 24(14):11587. https://doi.org/10.3390/ijms241411587
Chicago/Turabian StyleLiu, Junli, Xiaoyu Feng, Gaoyang Qiu, Hua Li, Yuan Wang, Xiaodong Chen, Qinglin Fu, and Bin Guo. 2023. "Inhibition Roles of Calcium in Cadmium Uptake and Translocation in Rice: A Review" International Journal of Molecular Sciences 24, no. 14: 11587. https://doi.org/10.3390/ijms241411587
APA StyleLiu, J., Feng, X., Qiu, G., Li, H., Wang, Y., Chen, X., Fu, Q., & Guo, B. (2023). Inhibition Roles of Calcium in Cadmium Uptake and Translocation in Rice: A Review. International Journal of Molecular Sciences, 24(14), 11587. https://doi.org/10.3390/ijms241411587