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Cadmium toxicity in plants and alleviation through seed priming approach

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Abstract

Heavy metals (Cd) contamination of soil and water due to anthropogenic activity, causing toxicity/stress, has potential to turn down the crop productivity and quality globally. Cd affects the fundamental and crucial processes of plants from seed germination to grain maturity, among them antioxidant defense and photosynthesis are prime one. Recent development in various disciplines of agricultural and biological sciences such as molecular breeding, integrative multiomics, and advance agronomical technology involved in heavy metal tolerance, although they are limited to lab conditions or less popular among farmers fields. Therefore, seed priming is promising and versatile approach to heavy metal stress tolerance. Seed priming with various organic and inorganic salts (CaCl2, Mg (NO3)2, proline), plant growth regulators (auxin, gibberellins, salicylic acid), showed the promising results in counteracts the effect of Cd. Seed priming involve in improvements of seed germination, seedling establishment, antioxidant defense, water and mineral nutrition, and carrying stress memory in progenies. To consider the above points, this review summarizes the effect of Cd toxicity on plant system and mineral nutrition. We also provide a glance of seed priming technology in respect to Cd stress tolerance at physiological, biochemical and molecular levels at different plant growth stages.

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References

  • Abedi, S., Alireza, I., Zahra, O. A., & Mostafa, E. (2020). Seed priming with cold plasma improved early growth, flowering, and protection of Cichorium intybus against selenium nanoparticle. Journal of Theoretical and Applied Physics, 14, 113–119.

    Google Scholar 

  • Adhikari, B., Adhikari, M., Ghimire, B., Adhikari, B. C., Park, G., & Choi, E. H. (2020). Cold plasma seed priming modulates growth, redox homeostasis and stress response by inducing reactive species in tomato (Solanum lycopersicum). Free Radical Biology and Medicine, 156, 57–69.

    CAS  PubMed  Google Scholar 

  • Agami, R. A., & Mohamed, G. F. (2013). Exogenous treatment with indole-3-acetic acid and salicylic acid alleviates cadmium toxicity in wheat seedlings. Ecotoxicology and Environmental Safety, 94, 164–171.

    CAS  PubMed  Google Scholar 

  • Agency for Toxic Substances and Disease Registry. (1999). Toxicological profile for cadmium. Atlanta: US Department of Health and Human Services. NTIS Report No. PB/89/194476/AS.

  • Akar, M., & Atis, I. (2018). The effects of priming pretreatments on germination and seedling growth in perennial ryegrass exposed to heavy metal stress. Feb-Fresenius Environmental Bulletin, 6677.

  • Anjum, S. A., Tanveer, M., Hussain, S., Bao, M., Wang, L., Khan, I., Ullah, E., Tung, S. A., Samad, R. A., & Shahzad, B. (2015). Cadmium toxicity in Maize (Zea mays L.): Consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environmental Science and Pollution Research, 22, 17022–17030.

    CAS  PubMed  Google Scholar 

  • Araújo, S. D. S., Paparella, S., Dondi, D., Bentivoglio, A., Carbonera, D., & Balestrazzi, A. (2016). Physical methods for seed invigoration: Advantages and challenges in seed technology. Frontiers in Plant Science, 7, 646.

    PubMed Central  Google Scholar 

  • Belkadhi, A., De Haro, A., Obregon, S., Chaïbi, W., & Djebali, W. (2015). Positive effects of salicylic acid pretreatment on the composition of flax plastidial membrane lipids under cadmium stress. Environmental Science and Pollution Research, 22, 1457–1467.

    CAS  PubMed  Google Scholar 

  • Belkhadi, A., Hediji, H., Abbes, Z., Nouairi, I., Barhoumi, Z., Zarrouk, M., & Djebali, W. (2010). Effects of exogenous salicylic acid pre-treatment on cadmium toxicity and leaf lipid content in Linum usitatissimum L. Ecotoxicology and Environmental Safety, 73, 1004–1011.

    CAS  PubMed  Google Scholar 

  • Benavides, M. P., Gallego, S. M., & Tomaro, M. L. (2005). Cadmium toxicity in plants. Brazilian Journal of Plant Physiology, 17, 21–34.

    CAS  Google Scholar 

  • Bhaduri, A. M., & Fulekar, M. H. (2012). Antioxidant enzyme responses of plants to heavy metal stress. Reviews in Environmental Science and Bio/technology, 11, 55–69.

    CAS  Google Scholar 

  • Bose, B., Kumar, M., Singhal, R. K., & Mondal, S. (2018). Impact of seed priming on the modulation of physico-chemical and molecular processes during germination, growth, and development of crops. In Advances in Seed Priming. Springer, Singapore, (pp. 23–40).

  • Cailliatte, R., Lapeyre, B., Briat, J. F., Mari, S., & Curie, C. (2009). The NRAMP6 metal transporter contributes to cadmium toxicity. Biochemical Journal, 422, 217–228.

    CAS  Google Scholar 

  • Chandra, R., & Kang, H. (2016). Mixed heavy metal stress on photosynthesis, transpiration rate, and chlorophyll content in poplar hybrids. Forest Science and Technology, 12, 55–61.

    Google Scholar 

  • Chang, J. D., Huang, S., Yamaji, N., Zhang, W., Ma, J. F., & Zhao, F. J. (2020). OsNRAMP1 transporter contributes to cadmium and manganese uptake in rice. Plant, Cell & Environment, 43, 2476–2491.

    CAS  Google Scholar 

  • Chao, D. Y., Silva, A., Baxter, I., Huang, Y. S., Nordborg, M., Danku, J., & Salt, D. E. (2012). Genome-wide association studies identify heavy metal ATPase3 as the primary determinant of natural variation in leaf cadmium in Arabidopsis thaliana. PLOS Genetics. https://doi.org/10.1371/journal.pgen.1002923

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen, K., & Arora, R. (2013). Priming memory invokes seed stress-tolerance. Environmental and Experimental Botany, 94, 33–45.

    CAS  Google Scholar 

  • Cheng, S., Ren, F., Grosse, W., & Wu, Z. (2002). Effects of cadmium on chlorophyll content, photochemical efficiency, and photosynthetic intensity of Canna indica Linn. International Journal of Phytoremediation, 4, 239–246.

    CAS  Google Scholar 

  • Chen, H. C., Zhang, S. L., Wu, K. J., Li, R., He, X. R., He, D. N., Huang, C., & Wei, H. (2020). The effects of exogenous organic acids on the growth, photosynthesis and cellular ultrastructure of Salix variegata Franch under Cd stress. Ecotoxicology and Environmental Safety, 187, 109790.

    CAS  PubMed  Google Scholar 

  • Dheri, G. S., Singh Brar, M., & Malhi, S. S. (2007). Influence of phosphorus application on growth and cadmium uptake of spinach in two cadmium-contaminated soils. Journal of Plant Nutrition and Soil Science, 170, 495–499.

    CAS  Google Scholar 

  • do Espirito Santo Pereira, A., Caixeta Oliveira, H., Fernandes Fraceto, L., & Santaella, C. (2021). Nanotechnology potential in seed priming for sustainable agriculture. Nanomaterials, 11, 267.

  • EL Sabagh, A., Islam, M.S., Hossain, A., Iqbal, M., Mbarki, S., Raza, A., Llanes, A., Reginato, M., Rahman, M.A., Mahboob, W., & Singhal, R. (2021) Plant growth regulators (PGRs) influence physiological modifications in plants under abiotic stresses. Frontiers in Agronomy, 77.

  • Emamverdian, A., Ding, Y., Mokhberdoran, F., & Xie, Y. (2015). Heavy metal stress and some mechanisms of plant defense response. The Scientific World Journal.

  • Espanany, A., Fallah, S., & Tadayyon, A. (2016). Seed priming improves seed germination and reduces oxidative stress in black cumin (Nigella sativa) in presence of cadmium. Industrial Crops and Products, 79, 195–204.

    CAS  Google Scholar 

  • Feng, G., Xie, T., Wang, X., Bai, J., Tang, L., Zhao, H., Wei, W., Wang, M., & Zhao, Y. (2018). Metagenomic analysis of microbial community and function involved in cd-contaminated soil. BMC Microbiology, 18, 1–13.

    Google Scholar 

  • Figlioli, F., Sorrentino, M. C., Memoli, V., Arena, C., Maisto, G., Giordano, S., Capozzi, F., & Spagnuolo, V. (2019). Overall plant responses to Cd and Pb metal stress in maize: Growth pattern, ultrastructure, and photosynthetic activity. Environmental Science and Pollution Research, 26, 1781–1790.

    CAS  PubMed  Google Scholar 

  • Galhaut, L., de Lespinay, A., Walker, D. J., Bernal, M. P., Correal, E., & Lutts, S. (2014). Seed priming of Trifolium repens L. improved germination and early seedling growth on heavy metal-contaminated soil. Water, Air, & Soil Pollution, 225, 1905.

    Google Scholar 

  • Gul, F., Arfan, M., Shahbaz, M., & Basra, S. (2020). Salicylic acid seed priming modulates morphology, nutrient relations and photosynthetic attributes of wheat grown under cadmium stress. International Journal of Agriculture Biology, 23, 197–204.

    CAS  Google Scholar 

  • Hafsi, C., Romero-Puertas, M. C., Gupta, D. K., Luis, A., Sandalio, L. M., & Abdelly, C. (2010). Moderate salinity enhances the antioxidative response in the halophyte Hordeum maritimum L. under potassium deficiency. Environmental and Experimental Botany, 69, 129–136.

    CAS  Google Scholar 

  • Haider, F. U., Liqun, C., Coulter, J. A., Cheema, S. A., Wu, J., Zhang, R., Wenjun, M., & Farooq, M. (2021). Cadmium toxicity in plants: Impacts and remediation strategies. Ecotoxicology and Environmental Safety, 211, 111887.

    CAS  PubMed  Google Scholar 

  • Hameed, A., Farooq, T., Hameed, A., & Sheikh, M. A. (2021). Sodium nitroprusside mediated priming memory invokes water-deficit stress acclimation in wheat plants through physio-biochemical alterations. Plant Physiology and Biochemistry, 160, 329–340.

    CAS  PubMed  Google Scholar 

  • Hasanuzzaman, M., Hossain, M. A., & Fujita, M. (2012). Exogenous selenium pretreatment protects rapeseed seedlings from cadmium-induced oxidative stress by upregulating antioxidant defense and methylglyoxal detoxification systems. Biological Trace Element Research, 149, 248–261.

    CAS  PubMed  Google Scholar 

  • Hermans, C., Chen, J., Coppens, F., Inzé, D., & Verbruggen, N. (2011). Low magnesium status in plants enhances tolerance to cadmium exposure. New Phytologist, 192, 428–436.

    CAS  Google Scholar 

  • Hocoglu-Özyigit, A., & Genc, B. N. (2020). Cadmium in plants, humans and the environment. Frontiers in Life Sciences and Related Technologies, 1, 12–21.

    Google Scholar 

  • Hossain, Z., Makino, T., & Komatsu, S. (2012). Proteomic study of β-aminobutyric acid-mediated cadmium stress alleviation in soybean. Journal of Proteomics, 75, 4151–4164.

    CAS  PubMed  Google Scholar 

  • Howladar, S. M., Al-Robai, S. A., Al-Zahrani, F. S., Howladar, M. M., & Aldhebiani, A. Y. (2018). Silicon and its application method effects on modulation of cadmium stress responses in Triticum aestivum (L.) through improving the antioxidative defense system and polyamine gene expression. Ecotoxicology and Environmental Safety, 159, 143–152.

    CAS  PubMed  Google Scholar 

  • Hu, Y., Ge, Y., Zhang, C., Ju, T., & Cheng, W. (2009). Cadmium toxicity and translocation in rice seedlings are reduced by hydrogen peroxide pretreatment. Plant Growth Regulation, 59, 51.

    CAS  Google Scholar 

  • Huang, D., Gong, X., Liu, Y., Zeng, G., Lai, C., Bashir, H., Zhou, L., Wang, D., Xu, P., Cheng, M., & Wan, J. (2017a). Effects of calcium at toxic concentrations of cadmium in plants. Planta, 245, 863–873.

    CAS  PubMed  Google Scholar 

  • Huang, Q. N., An, H., Yang, Y. J., Liang, Y., & Shao, G. S. (2017b). Effects of Mn-Cd antagonistic interaction on Cd accumulation and major agronomic traits in rice genotypes by different Mn forms. Plant Growth Regulation, 82, 317.

    CAS  Google Scholar 

  • Hussain, S., Khaliq, A., Noor, M. A., Tanveer, M., Hussain, H. A., Hussain, S., Shah, T., & Mehmood, T. (2020). Metal toxicity and nitrogen metabolism in plants: an overview. Carbon and Nitrogen Cycling in Soil, 221–248.

  • Indu, Lal, D., Dadrwal, B. K., Saha, D., Chand, S., Chauhan, J., Dey, P., Kumar, V., Mishra, U. N., Hidangmayum, A., Singh, A., & Singhal, R. K. (2021). Molecular advances in plant root system architecture response and redesigning for improved performance under unfavorable environments. Frontiers in Plant-Soil Interaction, Academic Press. https://doi.org/10.1016/B978-0-323-90943-3.00013-4.

  • International Agency for Research on Cancer. IARC (1993). Evaluation of carcinogenic risks of chemical to humans. In Some naturally-occurring substances: Food items and constituents. Heterocyclic Aromatic Amines and Mycotoxins. IARC monographs, Lyon, France, (pp. 359–362).

  • Ishikawa, S., Ishimaru, Y., Igura, M., Kuramata, M., Abe, T., Senoura, T., & Nakanishi, H. (2012). Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proceedings of the National Academy of Sciences, 109(47), 19166–19171.

    CAS  Google Scholar 

  • Islam, M. M., Hoque, M. A., Okuma, E., Banu, M. N. A., Shimoishi, Y., Nakamura, Y., & Murata, Y. (2009). Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. Journal of Plant Physiology, 166, 1587–1597.

    CAS  PubMed  Google Scholar 

  • Ismael, M. A., Elyamine, A. M., Moussa, M. G., Cai, M., Zhao, X., & Hu, C. (2019). Cadmium in plants: Uptake, toxicity, and its interactions with selenium fertilizers. Metallomics, 11, 255–277.

    CAS  PubMed  Google Scholar 

  • Issam, N., Kawther, M., Haythem, M., & Moez, J. (2012). Effects of CaCl 2 pretreatment on antioxidant enzyme and leaf lipid content of faba bean (Vicia faba L.) seedlings under cadmium stress. Plant Growth Regulation, 68, 37–47.

    CAS  Google Scholar 

  • Jan, S., & Parray, J. A. (2016). Approaches to heavy metal tolerance in plants (pp. 1–18). Springer.

    Google Scholar 

  • Jawad Hassan, M., Ali Raza, M., Ur Rehman, S., Ansar, M., Gitari, H., Khan, I., Wajid, M., Ahmed, M., Abbas Shah, G., Peng, Y., & Li, Z. (2020). Effect of cadmium toxicity on growth, oxidative damage, antioxidant defense system and cadmium accumulation in two sorghum cultivars. Plants, 9, 1575.

    PubMed Central  Google Scholar 

  • Júnior, C. A. L., Mazzafera, P., & Arruda, M. A. Z. (2014). A comparative ionomic approach focusing on cadmium effects in sunflowers (Helianthus annuus L.). Environmental and Experimental Botany, 107, 180–186.

    Google Scholar 

  • Kabała, K., Zboińska, M., Głowiak, D., Reda, M., Jakubowska, D., & Janicka, M. (2019). Interaction between the signaling molecules hydrogen sulfide and hydrogen peroxide and their role in vacuolar H+-ATPase regulation in cadmium-stressed cucumber roots. Physiologia Plantarum, 166, 688–704.

    PubMed  Google Scholar 

  • Kadioglu, A., Terzi, R., Saruhan, N., & Saglam, A. (2012). Current advances in the investigation of leaf rolling caused by biotic and abiotic stress factors. Plant Science, 182, 42–48.

    CAS  PubMed  Google Scholar 

  • Karalija, E., & Selović, A. (2018). The effect of hydro and proline seed priming on growth, proline and sugar content, and antioxidant activity of maize under cadmium stress. Environmental Science and Pollution Research, 25, 33370–33380.

    CAS  PubMed  Google Scholar 

  • Khan, A., Khan, S., Alam, M., Khan, M. A., Aamir, M., Qamar, Z., Rehman, Z. U., & Perveen, S. (2016a). Toxic metal interactions affect the bioaccumulation and dietary intake of macro-and micro-nutrients. Chemosphere, 146, 121–128.

    CAS  PubMed  Google Scholar 

  • Khan, K. Y., Ali, B., Stoffella, P. J., Cui, X., Yang, X., & Guo, Y. (2020). Study amino acid contents, plant growth variables and cell ultrastructural changes induced by cadmium stress between two contrasting cadmium accumulating cultivars of Brassica rapa ssp. chinensis L. (pak choi). Ecotoxicology and Environmental Safety, 200, 110748.

    CAS  PubMed  Google Scholar 

  • Khan, M. I. R., Iqbal, N., Masood, A., Mobin, M., Anjum, N. A., & Khan, N. A. (2016b). Modulation and significance of nitrogen and sulfur metabolism in cadmium challenged plants. Plant Growth Regulation, 78, 1–11.

    CAS  Google Scholar 

  • Korenkov, V., King, B., Hirschi, K., & Wagner, G. J. (2009). Root-selective expression of AtCAX4 and AtCAX2 results in reduced lamina cadmium in field-grown Nicotiana tabacum L. Plant Biotechnology Journal, 7(3), 219–226.

    CAS  PubMed  Google Scholar 

  • Krämer, U., Talke, I. N., & Hanikenne, M. (2007). Transition metal transport. FEBS Letters, 581, 2263–2272.

    PubMed  Google Scholar 

  • Kranner, I., & Colville, L. (2011). Metals and seeds: Biochemical and molecular implications and their significance for seed germination. Environmental and Experimental Botany, 72, 93–105.

    CAS  Google Scholar 

  • Krantev, A., Yordanova, R., Janda, T., Szalai, G., & Popova, L. (2008). Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. Journal of Plant Physiology, 165(9), 920–931.

    CAS  PubMed  Google Scholar 

  • Kubier, A., Wilkin, R. T., & Pichler, T. (2019). Cadmium in soils and groundwater: a review. Applied Geochemistry, 108, 104388.

    CAS  Google Scholar 

  • Kubier, A., Hamer, K., & Pichler, T. (2020). Cadmium background levels in groundwater in an area dominated by agriculture. Integrated Environmental Assessment and Management, 16, 103–113.

    CAS  PubMed  Google Scholar 

  • Kumar, V., Singhal, R.K., Kumar, N., & Bose, B. (2020). Micro-nutrient seed priming: A pragmatic approach towards abiotic. New Frontiers in Stress Management for Durable Agriculture, 231.

  • Kumar, M., Singhal, R. K., & Bose, B. (2018). Effect of hydro and hormonal priming on growth and development of rice under timely and late sown conditions. International Journal of Current Microbiology and Applied Science, 7, 2970–2976.

    Google Scholar 

  • Lanquar, V., Lelièvre, F., Bolte, S., Hamès, C., Alcon, C., Neumann, D., & Thomine, S. (2005). Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. The EMBO Journal, 24(23), 4041–4051.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li, L. Z., Tu, C., Peijnenburg, W. J., & Luo, Y. M. (2017). Characteristics of cadmium uptake and membrane transport in roots of intact wheat (Triticum aestivum L.) seedlings. Environmental Pollution, 221, 351–358.

    CAS  PubMed  Google Scholar 

  • Li, W., Khan, M. A., Yamaguchi, S., & Kamiya, Y. (2005). Effects of heavy metals on seed germination and early seedling growth of Arabidopsis thaliana. Plant Growth Regulation, 46, 45–50.

    CAS  Google Scholar 

  • Li, L., Wang, Y., & Shen, W. (2012). Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. BioMetals, 25, 617–631.

    CAS  PubMed  Google Scholar 

  • Lu, J., & Lu, H. (2019). Enhanced Cd transport in the soil-plant-atmosphere continuum (SPAC) system by tobacco (Nicotiana tabacum L.). Chemosphere, 225, 395–405.

    CAS  PubMed  Google Scholar 

  • Matusik, J., Bajda, T., & Manecki, M. (2008). Immobilization of aqueous cadmium by addition of phosphates. Journal of Hazardous Materials, 152, 1332–1339.

    CAS  PubMed  Google Scholar 

  • Méndez, A. A., Pena, L. B., Benavides, M. P., & Gallego, S. M. (2016). Priming with NO controls redox state and prevents cadmium-induced general up-regulation of methionine sulfoxide reductase gene family in Arabidopsis. Biochimie, 131, 128–136.

    PubMed  Google Scholar 

  • Miyadate, H., Adachi, S., Hiraizumi, A., Tezuka, K., Nakazawa, N., Kawamoto, T., & Akagi, H. (2011). OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytologist, 189(1), 190–199.

    CAS  Google Scholar 

  • Mohsin, S. M., Hasanuzzaman, M., Parvin, K., Hossain, M. S., & Fujita, M. (2021). Protective role of tebuconazole and trifloxystrobin in wheat (Triticum aestivum L.) under cadmium stress via enhancement of antioxidant defense and glyoxalase systems. Physiology and Molecular Biology of Plants, 27, 1043–1057.

    CAS  PubMed  Google Scholar 

  • Mondal, S., & Bose, B. (2019). Impact of micronutrient seed priming on germination, growth, development, nutritional status and yield aspects of plants. Journal of Plant Nutrition, 42, 2577–2599.

    CAS  Google Scholar 

  • Mourato, M., Pinto, F., Moreira, I., Sales, J., Leitão, I., & Martins, L. L. (2019). The effect of Cd stress in mineral nutrient uptake in plants. In Cadmium toxicity and tolerance in plants. Academic Press, (pp. 327–348).

  • Naciri, R., Lahrir, M., Benadis, C., Chtouki, M., & Oukarroum, A. (2021). Interactive effect of potassium and cadmium on growth, root morphology and chlorophyll a fluorescence in tomato plant. Scientific Reports, 11, 1–10.

    Google Scholar 

  • Nada, E., Ferjani, B. A., Ali, R., Bechir, B. R., Imed, M., & Makki, B. (2007). Cadmium-induced growth inhibition and alteration of biochemical parameters in almond seedlings grown in solution culture. Acta Physiologiae Plantarum, 29, 57–62.

    CAS  Google Scholar 

  • Nakanishi, H., Ogawa, I., Ishimaru, Y., Mori, S., & Nishizawa, N. K. (2006). Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Science and Plant Nutrition, 52(4), 464–469.

    CAS  Google Scholar 

  • Nawaz, A., Amjad, M., Jahangir, M. M., Khan, S. M., Cui, H., & Hu, J. (2012). Induction of salt tolerance in tomato (‘Lycopersicon esculentum’ Mill.) seeds through sand priming. Australian Journal of Crop Science, 6(7), 1199.

    CAS  Google Scholar 

  • Nocito, F. F., Lancilli, C., Crema, B., Fourcroy, P., Davidian, J. C., & Sacchi, G. A. (2006). Heavy metal stress and sulfate uptake in maize roots. Plant Physiology, 141(3), 1138–1148.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nouairi, I., Jalali, K., Essid, S., Zribi, K., & Mhadhbi, H. (2019a). Alleviation of cadmium-induced genotoxicity and cytotoxicity by calcium chloride in faba bean (Vicia faba L. var. minor) roots. Physiology and Molecular Biology of Plants, 25, 921–931.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nouairi, I., Jalali, K., Zribi, F., Barhoumi, F., Zribi, K., & Mhadhbi, H. (2019b). Seed priming with calcium chloride improves the photosynthesis performance of faba bean plants subjected to cadmium stress. Photosynthetica, 57, 438–445.

    CAS  Google Scholar 

  • Panković, D., Plesničar, M., Arsenijević-Maksimović, I., Petrović, N., Sakač, Z., & Kastori, R. (2000). Effects of nitrogen nutrition on photosynthesis in Cd-treated sunflower plants. Annals of Botany, 86, 841–847.

    Google Scholar 

  • Park, J., Song, W. Y., Ko, D., Eom, Y., Hansen, T. H., Schiller, M., & Lee, Y. (2012). The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. The Plant Journal, 69(2), 278–288.

    CAS  PubMed  Google Scholar 

  • Popova, L. P., Maslenkova, L. T., Yordanova, R. Y., Ivanova, A. P., Krantev, A. P., Szalai, G., & Janda, T. (2009). Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiology and Biochemistry, 47, 224–231.

    CAS  PubMed  Google Scholar 

  • Qureshi, M. I., D’Amici, G. M., Fagioni, M., Rinalducci, S., & Zolla, L. (2010). Iron stabilizes thylakoid protein–pigment complexes in Indian mustard during Cd-phytoremediation as revealed by BN-SDS-PAGE and ESI-MS/MS. Journal of Plant Physiology, 167(10), 761–770.

    CAS  PubMed  Google Scholar 

  • Rady, M. M., & Hemida, K. A. (2015). Modulation of cadmium toxicity and enhancing cadmium-tolerance in wheat seedlings by exogenous application of polyamines. Ecotoxicology and Environmental Safety, 119, 178–185.

    CAS  PubMed  Google Scholar 

  • Rai, P. K., Lee, S. S., Zhang, M., Tsang, Y. F., & Kim, K. H. (2019). Heavy metals in food crops: Health risks, fate, mechanisms, and management. Environment International, 125, 365–385.

    CAS  PubMed  Google Scholar 

  • Rasheed, R., Ashraf, M. A., Arshad, A., Iqbal, M., & Hussain, I. (2020). Interactive effects of chitosan and cadmium on growth, secondary metabolism, oxidative defense, and element uptake in pea (Pisum sativum L.). Arabian Journal of Geosciences, 13, 1–14.

    Google Scholar 

  • Rathod, G. R., & Anand, A. (2016). Effect of seed magneto-priming on growth, yield and Na/K ratio in wheat (Triticum aestivum L.) under salt stress. Indian Journal of Plant Physiology, 21, 15–22.

    Google Scholar 

  • Rivetta, A., Negrini, N., & Cocucci, M. (1997). Involvement of Ca2+-calmodulin in Cd2+ toxicity during the early phases of radish (Raphanus sativus L.) seed germination. Plant, Cell & Environment, 20, 600–608.

    CAS  Google Scholar 

  • Rizwan, M., Ali, S., ur Rehman, M. Z., & Maqbool, A. (2019). A critical review on the effects of zinc at toxic levels of cadmium in plants. Environmental Science and Pollution Research, 26, 6279–6289.

  • Rizwan, M., Ali, S., Ali, B., Adrees, M., Arshad, M., Hussain, A., ur Rehman, M. Z., & Waris, A. A. (2019). Zinc and iron oxide nanoparticles improved the plant growth and reduced the oxidative stress and cadmium concentration in wheat. Chemosphere, 214, 269–277.

  • Roychoudhury, A., Ghosh, S., Paul, S., Mazumdar, S., Das, G., & Das, S. (2016). Pre-treatment of seeds with salicylic acid attenuates cadmium chloride-induced oxidative damages in the seedlings of mungbean (Vigna radiata L. Wilczek). Acta Physiologiae Plantarum, 38, 1–18.

    CAS  Google Scholar 

  • Shafi, M., Zhang, G., Bakht, J., Khan, M. A., Islam, U. E., Khan, M. D., & Raziuddin, G. Z. (2010). Effect of cadmium and salinity stresses on root morphology of wheat. Pakistan Journal of Botany, 42, 2747–2754.

    CAS  Google Scholar 

  • Shah, A. A., Ahmed, S., & Yasin, N. A. (2020a). 2-Hydroxymelatonin induced nutritional orchestration in Cucumis sativus under cadmium toxicity: Modulation of non-enzymatic antioxidants and gene expression. International Journal of Phytoremediation, 22(5), 497–507.

    CAS  PubMed  Google Scholar 

  • Shah, A. A., Ahmed, S., Abbas, M., & Yasin, N. A. (2020). Seed priming with 3-epibrassinolide alleviates cadmium stress in Cucumis sativus through modulation of antioxidative system and gene expression. Scientia Horticulturae, 265, 109203.

    CAS  Google Scholar 

  • Shah, T., Latif, S., Saeed, F., Ali, I., Ullah, S., Alsahli, A. A., Jan, S., & Ahmad, P. (2021). Seed priming with titanium dioxide nanoparticles enhances seed vigor, leaf water status, and antioxidant enzyme activities in maize (Zea mays L.) under salinity stress. Journal of King Saud University-Science, 33, 101207.

    Google Scholar 

  • Shakirova, F. M., Allagulova, C. R., Maslennikova, D. R., Klyuchnikova, E. O., Avalbaev, A. M., & Bezrukova, M. V. (2016). Salicylic acid-induced protection against cadmium toxicity in wheat plants. Environmental and Experimental Botany, 122, 19–28.

    CAS  Google Scholar 

  • Shanying, H. E., Xiaoe, Y. A. N. G., Zhenli, H. E., & Baligar, V. C. (2017). Morphological and physiological responses of plants to cadmium toxicity: A review. Pedosphere, 27(3), 421–438.

    Google Scholar 

  • Sharma, S. S., & Dietz, K. J. (2006). The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. Journal of Experimental Botany, 57, 711–726.

    CAS  PubMed  Google Scholar 

  • Sharma, S. S., Kaul, S., Metwally, A., Goyal, K. C., Finkemeier, I., & Dietz, K. J. (2004). Cadmium toxicity to barley (Hordeum vulgare) as affected by varying Fe nutritional status. Plant Science, 166, 1287–1295.

    CAS  Google Scholar 

  • Shehzad, M. A., Nawaz, F., Ahmad, F., Ahmad, N., & Masood, S. (2020). Protective effect of potassium and chitosan supply on growth, physiological processes and antioxidative machinery in sunflower (Helianthus annuus L) under drought stress. Ecotoxicology and Environmental Safety, 187, 109841.

    CAS  PubMed  Google Scholar 

  • Singhal, R. K., Jatav, H. S., Aftab, T., Pandey, S., Mishra, U. N., Chauhan, J., Chand, S., Saha, D., Dadarwal, B. K., Chandra, K., Khan, M. A. (2021). Roles of nitric oxide in conferring multiple abiotic stress tolerance in plants and crosstalk with other plant growth regulators. Journal of Plant Growth Regulation, 1–26.

  • Singhal, R. K., & Bose, B. (2020). Wheat seedlings as affected by Mg (NO3)2 and ZnSO4 priming treatments. World Scientific News, 144, 13–29.

    CAS  Google Scholar 

  • Singhal, R. K., Kumar, V., & Bose, B. (2019). Improving the yield and yield attributes in wheat crop using seed priming under drought stress. Journal of Pharmacognosy and Phytochemistry, 8, 214–220.

    CAS  Google Scholar 

  • Sneideris, L. C., Gavassi, M. A., Campos, M. L., D’Amico-Damiao, V., & Carvalho, R. F. (2015). Effects of hormonal priming on seed germination of pigeon pea under cadmium stress. Anais Da Academia Brasileira De Ciências, 87, 1847–1852.

    CAS  PubMed  Google Scholar 

  • Song, A., Li, Z., Zhang, J., Xue, G., Fan, F., & Liang, Y. (2009). Silicon-enhanced resistance to cadmium toxicity in Brassica chinensis L. is attributed to Si-suppressed cadmium uptake and transport and Si-enhanced antioxidant defense capacity. Journal of Hazardous Materials, 172, 74–83.

    CAS  PubMed  Google Scholar 

  • Song, Y., Jin, L., & Wang, X. (2017). Cadmium absorption and transportation pathways in plants. International Journal of Phytoremediation, 19, 133–141.

    CAS  PubMed  Google Scholar 

  • Spielmann, J., Ahmadi, H., Scheepers, M., Weber, M., Nitsche, S., Carnol, M., Bosman, B., Kroymann, J., Motte, P., Clemens, S., & Hanikenne, M. (2020). The two copies of the zinc and cadmium ZIP6 transporter of Arabidopsis halleri have distinct effects on cadmium tolerance. Plant, Cell & Environment, 43, 2143–2157.

    CAS  Google Scholar 

  • Srivastava, A. K., Suresh Kumar, J., & Suprasanna, P. (2021). Seed ‘primeomics’: Plants memorize their germination under stress. Biological Reviews.

  • Street, R. A., Kulkarni, M. G., Stirk, W. A., Southway, C., & Van Staden, J. (2010). Effect of cadmium on growth and micronutrient distribution in wild garlic (Tulbaghia violacea). South African Journal of Botany, 76, 332–336.

    CAS  Google Scholar 

  • Sun, J., Wang, R., Zhang, X., Yu, Y., Zhao, R., Li, Z., & Chen, S. (2013). Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiology and Biochemistry, 65, 67–74.

    CAS  PubMed  Google Scholar 

  • Taie, H. A., El-Yazal, M. A. S., Ahmed, S. M., & Rady, M. M. (2019). Polyamines modulate growth, antioxidant activity, and genomic DNA in heavy metal–stressed wheat plant. Environmental Science and Pollution Research, 26, 22338–22350.

    CAS  PubMed  Google Scholar 

  • Tang, L., Mao, B., Li, Y., Lv, Q., Zhang, L., Chen, C., & Zhao, B. (2017). Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Scientific Reports, 7(1), 1–12.

    Google Scholar 

  • Tlustos, P., Száková, J., Korinek, K., Pavlíková, D., Hanc, A., & Balík, J. (2006). The effect of liming on cadmium, lead, and zinc uptake reduction by spring wheat grown in contaminated soil. Plant Soil and Environment, 52, 16.

    CAS  Google Scholar 

  • Tondey, M., Kalia, A., Singh, A., Dheri, G. S., Taggar, M. S., Nepovimova, E., Krejcar, O., & Kuca, K. (2021). Seed priming and coating by nano-scale zinc oxide particles improved vegetative growth, yield and quality of fodder maize (Zea mays). Agronomy, 11, 729.

    CAS  Google Scholar 

  • Tran, T. A., & Popova, L. P. (2013). Functions and toxicity of cadmium in plants: Recent advances and future prospects. Turkish Journal of Botany, 37(1), 1–13.

    CAS  Google Scholar 

  • Ueno, D., Yamaji, N., Kono, I., Huang, C. F., Ando, T., Yano, M., & Ma, J. F. (2010). Gene limiting cadmium accumulation in rice. Proceedings of the National Academy of Sciences, 107(38), 16500–16505.

    CAS  Google Scholar 

  • Uraguchi, S., Kamiya, T., Clemens, S., & Fujiwara, T. (2014). Characterization of OsLCT1, a cadmium transporter from indica rice (Oryza sativa). Physiologia Plantarum, 151(3), 339–347.

    CAS  PubMed  Google Scholar 

  • Uraguchi, S., Kamiya, T., Sakamoto, T., Kasai, K., Sato, Y., Nagamura, Y., & Fujiwara, T. (2011). Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proceedings of the National Academy of Sciences, 108(52), 20959–20964.

    CAS  Google Scholar 

  • Valivand, M., Amooaghaie, R., & Ahadi, A. (2019). Seed priming with H2S and Ca2+ trigger signal memory that induces cross-adaptation against nickel stress in zucchini seedlings. Plant Physiology and Biochemistry, 143, 286–298.

    CAS  PubMed  Google Scholar 

  • Wan, Y., Wang, K., Liu, Z., Yu, Y., Wang, Q., & Li, H. (2019). Effect of selenium on the subcellular distribution of cadmium and oxidative stress induced by cadmium in rice (Oryza sativa L.). Environmental Science and Pollution Research, 26, 16220–16228.

    CAS  PubMed  Google Scholar 

  • Wang, C. Q., & Song, H. (2009). Calcium protects Trifolium repens L. seedlings against cadmium stress. Plant Cell Reports, 28, 1341–1349.

    CAS  PubMed  Google Scholar 

  • Wang, H., Wang, P. F., & Zhang, H. (2009). Use of phosphorus to alleviate stress induced by cadmium and zinc in two submerged macrophytes. African Journal of Biotechnology, 8.

  • Wang, Y. M., Tang, D. D., Yuan, X. Y., Uchimiya, M., Li, J. Z., Li, Z. Y., Luo, Z. C., Xu, Z. W., & Sun, S. G. (2020). Effect of amendments on soil Cd sorption and trophic transfer of Cd and mineral nutrition along the food chain. Ecotoxicology and Environmental Safety, 189, 110045.

    CAS  PubMed  Google Scholar 

  • Wangeline, A. L., Burkhead, J. L., Hale, K. L., Lindblom, S. D., Terry, N., Pilon, M., & Pilon-Smits, E. A. (2004). Overexpression of ATP sulfurylase in indian mustard. Journal of Environmental Quality, 33(1), 54–60.

    CAS  PubMed  Google Scholar 

  • Yamaji, N., Sasaki, A., Xia, J. X., Yokosho, K., & Ma, J. F. (2013). A node-based switch for preferential distribution of manganese in rice. Nature Communications, 4(1), 1–11.

    Google Scholar 

  • Yang, M., Zhang, Y., Zhang, L., Hu, J., Zhang, X., Lu, K., & Lian, X. (2014). OsNRAMP5 contributes to manganese translocation and distribution in rice shoots. Journal of Experimental Botany, 65(17), 4849–4861.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, L., Ji, J., Harris-Shultz, K. R., Wang, H., Wang, H., Abd-Allah, E. F., Luo, Y., & Hu, X. (2016). The dynamic changes of the plasma membrane proteins and the protective roles of nitric oxide in rice subjected to heavy metal cadmium stress. Frontiers in Plant Science, 7, 190.

    PubMed  PubMed Central  Google Scholar 

  • Yang, L. P., Zhu, J., Wang, P., Zeng, J., Tan, R., Yang, Y. Z., & Liu, Z. M. (2018). Effect of Cd on growth, physiological response, Cd subcellular distribution and chemical forms of Koelreuteria paniculata. Ecotoxicology and Environmental Safety, 160, 10–18.

    CAS  PubMed  Google Scholar 

  • Yoneyama, T., Ishikawa, S., & Fujimaki, S. (2015). Route and regulation of zinc, cadmium, and iron transport in rice plants (Oryza sativa L.) during vegetative growth and grain filling: Metal transporters, metal speciation, grain Cd reduction and Zn and Fe biofortification. International Journal of Molecular Sciences, 16, 19111–19129.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan, Z., Luo, T., Liu, X., Hua, H., Zhuang, Y., Zhang, X., Zhang, L., Zhang, Y., Xu, W., & Ren, J. (2019). Tracing anthropogenic cadmium emissions: From sources to pollution. Science of the Total Environment, 676, 87–96.

    CAS  Google Scholar 

  • Zhang, C., Wang, L., Nie, Q., Zhang, W., & Zhang, F. (2008). Long-term effects of exogenous silicon on cadmium translocation and toxicity in rice (Oryza sativa L.). Environmental and Experimental Botany, 62, 300–307.

    CAS  Google Scholar 

  • Zhang, H., Tan, Z. Q., Hu, L. Y., Wang, S. H., Luo, J. P., & Jones, R. L. (2010). Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings. Journal of Integrative Plant Biology, 52, 556–567.

    CAS  PubMed  Google Scholar 

  • Zhang, J., Martinoia, E., & Lee, Y. (2018). Vacuolar transporters for cadmium and arsenic in plants and their applications in phytoremediation and crop development. Plant and Cell Physiology, 59, 1317–1325.

    CAS  PubMed  Google Scholar 

  • Zhu, G., Xiao, H., Guo, Q., Zhang, Z., Zhao, J., & Yang, D. (2018). Effects of cadmium stress on growth and amino acid metabolism in two Compositae plants. Ecotoxicology and Environmental Safety, 158, 300–308.

    CAS  PubMed  Google Scholar 

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Kumar, N., Kumar, V., Bose, B. et al. Cadmium toxicity in plants and alleviation through seed priming approach. Plant Physiol. Rep. 26, 647–660 (2021). https://doi.org/10.1007/s40502-021-00619-8

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