Physiological, nutritional, and biochemical indicators of lead tolerance in sunflower genotypes
DOI:
https://doi.org/10.5433/1679-0359.2022v43n4p1517Keywords:
Mineral nutrition, Organic solutes, Pigments, Toxic metal.Abstract
This study aimed to select and classify sunflower genotypes tolerant to lead (Pb) stress and evaluate their capacity of phytoextraction based on physiological, nutritional, and biochemical responses. Two experiments were carried out under lead stress. In the first experiment, out of 21 genotypes studied three showed higher relative biomass yield and were characterized as Pb-tolerant and five showed lower relative biomass production and were considered Pb-sensitive. In the second experiment, one Pb-tolerant (BRS-G27) and two Pb-sensitive (H251 and AG963) genotypes were studied. In this experiment, Pb stress reduced the growth and contents photosynthetic pigments in all genotypes, but more pronouncedly in sensitive genotypes. There were no substantial changes in micronutrient levels in the leaves and stem, but the levels of Cu and Mn in the stressed roots of sensitive genotypes were much lower than in BRS-G27. The contents of organic solutes in the roots suggest that sensitive genotypes have higher energy costs for osmoregulation by carbohydrates and amino acids synthesis. However, the accumulation of proline may be related to a greater Pb tolerance. Considering the results of dry mass yield, transfer coefficient, translocation factor, and tolerance index, the BRS-G27 genotype can be recommended for use in phytoremediation of Pb-contaminated soils.Downloads
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References
Abreu, C. B. de, Sacramento, B. L. do, Alves, A. T., Moura, S. C., Pinelli, M. S., & Azevedo, A. D. de, Neto. (2016). Nutritional and biochemical changes induced by lead in sunflower (Helianthus annuus L.). Semina: Ciências Agrárias, 37(3), 1229. doi: 10.5433/1679-0359.2016v37n3p1229
Adam, F. I. M., & El-Ashry, Z. M. (2010). Evaluation of genotoxicity of 4-n-nonylphenol using Vicia faba L. Journal of Biological Sciences, 10(4), 368-372. doi: 10.3923/jbs.2010.368.372
Alaboudi, K. A., Ahmed, B., & Brodie, G. (2018). Phytoremediation of Pb and Cd contaminated soils by using sunflower (Helianthus annuus) plant. Annals of Agricultural Sciences, 63(1), 123-127. doi: 10.1016/j. aoas.2018.05.007
Almeida, A. A. F., Valle, R. R., Mielke, M. S., & Gomes, F. P. (2007). Tolerance and prospection of phytoremediator woody species of Cd, Pb, Cu and Cr. Brazilian Journal of Plant Physiology, 19(2), 83-98. doi: 10.1590/S1677-04202007000200001
Alvares, C. A., Stape, J. L., Sentelhas, P. C., Gonçalves, J. L. M., & Sparovek, G. (2013). Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22(6), 711-728. doi: 10.1127/0941-2948/20 13/0507
Andrade, L. F., Davide, L. C., & Gedraite, L. S. (2010). The effect of cyanide compounds, fluorides, aluminum, and inorganic oxides present in spent pot liner on germination and root tip cells of Lactuca sativa. Ecotoxicology and Environmental Safety, 73(4), 626-631. doi: 10.1016/j.ecoenv.2009.12.012
Antoniadis, V., Levizou, E., Shaheen, S. M., Ok, Y. S., Sebastian, A., Baum, C., Prasad, M. N. V., Wenzel, W. W., & Rinklebe, J. (2017). Trace elements in the soil-plant interface: Phytoavailability, translocation, and phytoremediation-A review. Earth-Science Reviews, 171(1), 621-645. doi: 10.1016/j.earscirev.2017. 06.005
Ashraf, M., & Foolad, M. R. (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany, 59(2), 206-216. doi: 10.1016/j.envexpbot.2005.12. 006
Ashraf, U., Mahmood, M. H., Hussain, S., Anjum, S. A., & Tang, X. (2020). Lead (Pb) distribution and accumulation in different plant parts and its associations with grain Pb contents in fragrant rice. Chemosphere, 248(1), 126003. doi: 10.1016/j.chemosphere.2020.126003
Aslam, R., Bhat, T. M., Choudhary, S., & Ansari, M. Y. K. (2017). An overview on genotoxicity of heavy metal in a spice crop (Capsicum annuum L.) in respect to cyto-morphological behaviour. Caryologia, 70(1), 42-47. doi: 10.1080/00087114.2016.1258884
Azad, H. M., Shiva, A. H., & Malekpour, R. (2011). Toxic effects of lead on growth and some biochemical and ionic parameters of sunflower (Helianthus annuus L.) seedlings. Current Research Journal of Biological Sciences, 3(4), 398-403. https://maxwellsci.com/print/crjbs/v3-398-403.pdf
Azevedo, A. D. de, Neto, Mota, K. N. A. B., Silva, P. C. C., Cova, A. M. W., Ribas, R. F., & Gheyi, H. R. (2020). Selection of sunflower genotypes for salt stress and mechanisms of salt tolerance in contrasting genotypes. Ciência e Agrotecnologia, 44(1), e020120. doi: 10.1590/1413-7054202044020120
Bassegio, C., Santos, R. F., Bassegio, D., & Souza, S. N. M. de. (2020). Genotypic variation in growth and lead accumulation among Brassica juncea accessions. International Journal of Phytoremediation, 22(12), 1249-1258. doi: 10.1080/15226514.2020.1759506
Bates, L. S., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39(1), 205-207. doi: 10.1007/BF00018060
Bosso, S. T., & Enzweiler, J. (2008). Ensaios para determinar a (bio)disponibilidade de chumbo em solos contaminados: Revisão. Quimica Nova, 31(2), 394-400. doi: 10.1590/S0100-40422008000200036
Bradford, M. M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248-254. doi: 10.1016/j. cj.2017.04.003
Caetano, L. C. S., Prezotti, L. C., Pacheco, B. M., & Guarçoni, R. V. (2016). Soil chemical characteristics, biomass production and levels of nutrient and heavy metals in corn plants according to doses of steel slag and limestone. Revista Ceres, 63(6), 879-886. doi: 10.1590/0034-737X201663060018
Cova, A. M. W., Azevedo, A. D., Neto, Silva, P. C. C., Menezes, R. V, Ribas, R. F., & Gheyi, H. R. (2020). Physiological and biochemical responses and fruit production of noni (Morinda citrifolia L.) plants irrigated with brackish water. Scientia Horticulturae, 260(1), 108852. doi: 10.1016/j.scienta.2019.108852
Dalyan, E., Yuzbasioglu, E., & Akpinar, I. (2020). Physiological and biochemical changes in plant growth and different plant enzymes in response to lead stress. In D. Gupta, S. Chatterjee, & C. Walther (Eds.), Lead in plants and the environment (pp. 129-147). Cham.
Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28(3), 350-356. doi: 10.1021/ac60 111a017
Fageria, N. K. (2009). The use of nutrients in crop plants. CRC Press.
Ferreira, D. F. (2019). Sisvar: a computer analysis system to fixed effects split plot type designs. Revista Brasileira de Biometria, 37(4), 529-535. doi: 10.28951/rbb.v37i4.450
Hammer, O., Harper, D. A. T., & Ryan, P. D. (2001). Paleontological statistics software package for education and analysis. Palaeontologia Electronica, 4(1), 1-9. https://www.researchgate.net/publication/2596402 26_PAST_Paleontological_Statistics_Software_Package_for_Education_and_Data_Analysis
Hoagland, D. R., & Arnon, D. I. (1950). The water-culture method for growing plants without soil. Circular. California Agricultural Experiment Station, 347(2), 1-32. https://www.researchgate.net/file.PostFile Loader.html?id=54aefd7ed4c118b6358b45db&assetKey=AS%3A273668901408776%401442259158553
Hossain, M. A., Piyatida, P., Silva, J. A. T. da, & Fujita, M. (2012). Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. Journal of Botany, 2012(1), 1-37. doi: 10.1155/2012/ 872875
Houri, T., Khairallah, Y., Al Zahab, A., Osta, B., Romanos, D., & Haddad, G. (2020). Heavy metals accumulation effects on the photosynthetic performance of geophytes in Mediterranean reserve. Journal of King Saud University Science, 32(1), 874-880. doi: 10.1016/j.jksus.2019.04.005
Hussain, A., Abbas, N., Arshad, F., Akram, M., Khan, Z. I., Ahmad, K., Mansha, M., & Mirzaei, F. (2013). Effects of diverse doses of lead (Pb) on different growth attributes of Zea-mays L. Agricultural Sciences, 4(5), 262-265. doi: 10.4236/as.2013.45037
Jones, J. B. Jr. (2001). Laboratory guide for conducting soil tests and plant analysis. CRC Press.
Kabata-Pendias, A. (2010). Trace elements in soils and plants. CRC Press.
Kim, R.-Y., Yoon, J.-K., Kim, T.-S., Yang, J. E., Owens, G., & Kim, K.-R. (2015). Bioavailability of heavy metals in soils: definitions and practical implementation—a critical review. Environmental Geochemistry and Health, 37(6), 1041-1061. doi: 10.1007/s10653-015-9695-y
Kumar, R., Mishra, R. K., Mishra, V., Qidwai, A., Pandey, A., Shukla, S. K., Pandey, M., Pathak, A., & Dikshit, A. (2016). Detoxification and tolerance of heavy metals in plants. In P. Ahmad (Ed.), Plant metal interaction (pp. 335-359). Amsterdam..
Lamhamdi, M., El Galiou, O., Bakrim, A., Nóvoa-Munoz, J. C., Arias-Estévez, M., Aarab, A., & Lafont, R. (2013). Effect of lead stress on mineral content and growth of wheat (Triticum aestivum) and spinach (Spinacia oleracea) seedlings. Saudi Journal of Biological Sciences, 20(1), 29-36. doi: 10.1016/j.sjbs. 2012.09.001
Lichtenthaler, H. K., & Buschmann, C. (2001). Chlorophylls and carotenoids: measurement and characterization by UV-VIS Spectroscopy. Current Protocols in Food Analytical Chemistry, 1(1), F4.3.1-F4.3.8. doi: 10.1002/0471142913.faf0403s01
Liu, T., Liu, S., Guan, H., Ma, L., Chen, Z., Gu, H., & Qu, L.-J. (2009). Transcriptional profiling of Arabidopsis seedlings in response to heavy metal lead (Pb). Environmental and Experimental Botany, 67(2), 377-386. doi: 10.1016/j.envexpbot.2009.03.016
Malar, S., Manikandan, R., Favas, P. J. C., Sahi, S. V., & Venkatachalam, P. (2014). Effect of lead on phytotoxicity, growth, biochemical alterations, and its role on genomic template stability in Sesbania grandiflora: a potential plant for phytoremediation. Ecotoxicology and Environmental Safety, 108(1), 249-257. doi: 10.1016/j.ecoenv.2014.05.018
Malkowski, E., Kurtyka, R., Kita, A., & Karcz, W. (2005). Accumulation of Pb and Cd and its effect on Ca distribution in maize seedlings (Zea Mays L.). Polish Journal of Environmental Studies, 14(2), 203-207. http://www.pjoes.com/pdf-87749-21608?filename=Accumulation+of+Pb+and+Cd.pdf
Marschner, H. (2012). Mineral nutrition of higher plants (3rd ed.). Academic Press.
Onakpa, M. M., Njan, A. A., & Kalu, O. C. (2018). A review of heavy metal contamination of food crops in Nigeria. Annals of Global Health, 84(3), 488-494. doi: 10.29024/aogh.2314
Revathi, S., & Venugopal, S. (2013). Physiological and biochemical mechanisms of heavy metal tolerance. International Journal of Environmental Sciences, 3(5), 1339-1354. doi: 10.6088/ijes.2013030500004
Rucinska-Sobkowiak, R., Nowaczyk, G., Krzeslowska, M., Rabeda, I., & Jurga, S. (2013). Water status and water diffusion transport in lupine roots exposed to lead. Environmental and Experimental Botany, 87(1), 100-109. doi: 10.1016/j.envexpbot.2012.09.012
Sardans, J., & Penuelas, J. (2021). Potassium control of plant functions: ecological and agricultural implications. Plants, 10(2), 419. doi: 10.3390/plants10020419
Sharma, P., & Dubey, S. (2005). Lead toxicity in plants. Brazilian Journal of Plant Physiology, 17(1), 491-500. doi: 10.1590/S1677-04202005000100004
Silva, P. C. C., Azevedo, A. D. de, Neto, Gheyi, H. R., Ribas, R. F., Reis Silva, C. R. dos, & Cova, A. M. W. (2020). Salt-tolerance induced by leaf spraying with H2O2 in sunflower is related to the ion homeostasis balance and reduction of oxidative damage. Heliyon, 6(9), e05008. doi: 10.1016/j.heliyon.2020.e05008
Song, X., Zhang, C., Chen, W., Zhu, Y., & Wang, Y. (2020). Growth responses and physiological and biochemical changes in five ornamental plants grown in urban lead contaminated soils. Plant Environment Interactions, 1(1), 29-47. doi: 10.1002/pei3.10013
Verbruggen, N., & Hermans, C. (2008). Proline accumulation in plants: a review. Amino Acids, 35(4), 753-759. doi: 10.1007/s00726-008-0061-6
Vissenberg, K., Claeijs, N., Balcerowicz, D., & Schoenaers, S. (2020). Hormonal regulation of root hair growth and responses to the environment in Arabidopsis. Journal of Experimental Botany, 71(8), 2412-2427. doi: 10.1093/jxb/eraa048
White, P. J., & Pongrac, P. (2017). Heavy metal toxicity in plants. In S. Shabala (Ed.), Plant stress physiology (2nd ed., pp. 300-331). Boston. doi: 10.1023/A:1020305400324.
Yang, Y., Zhang, L., Huang, X., Zhou, Y., Quan, Q., Li, Y., & Zhu, X. (2020). Response of photosynthesis to different concentrations of heavy metals in Davidia involucrata. Plos One, 15(3), e0228563. doi: 10.1371/ journal.pone.0228563
Yemm, E. W., & Cocking, E. C. (1955). The determination of amino-acids with ninhydrin. The Analyst, 80(948), 209. doi: 10.1039/an9558000209
Zhou, J., Zhang, Z., Zhang, Y., Wei, Y., & Jiang, Z. (2018). Effects of lead stress on the growth, physiology, and cellular structure of privet seedlings. Plos One, 13(3), e0191139. doi: 10.1371/journal.pone.0191139
Adam, F. I. M., & El-Ashry, Z. M. (2010). Evaluation of genotoxicity of 4-n-nonylphenol using Vicia faba L. Journal of Biological Sciences, 10(4), 368-372. doi: 10.3923/jbs.2010.368.372
Alaboudi, K. A., Ahmed, B., & Brodie, G. (2018). Phytoremediation of Pb and Cd contaminated soils by using sunflower (Helianthus annuus) plant. Annals of Agricultural Sciences, 63(1), 123-127. doi: 10.1016/j. aoas.2018.05.007
Almeida, A. A. F., Valle, R. R., Mielke, M. S., & Gomes, F. P. (2007). Tolerance and prospection of phytoremediator woody species of Cd, Pb, Cu and Cr. Brazilian Journal of Plant Physiology, 19(2), 83-98. doi: 10.1590/S1677-04202007000200001
Alvares, C. A., Stape, J. L., Sentelhas, P. C., Gonçalves, J. L. M., & Sparovek, G. (2013). Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22(6), 711-728. doi: 10.1127/0941-2948/20 13/0507
Andrade, L. F., Davide, L. C., & Gedraite, L. S. (2010). The effect of cyanide compounds, fluorides, aluminum, and inorganic oxides present in spent pot liner on germination and root tip cells of Lactuca sativa. Ecotoxicology and Environmental Safety, 73(4), 626-631. doi: 10.1016/j.ecoenv.2009.12.012
Antoniadis, V., Levizou, E., Shaheen, S. M., Ok, Y. S., Sebastian, A., Baum, C., Prasad, M. N. V., Wenzel, W. W., & Rinklebe, J. (2017). Trace elements in the soil-plant interface: Phytoavailability, translocation, and phytoremediation-A review. Earth-Science Reviews, 171(1), 621-645. doi: 10.1016/j.earscirev.2017. 06.005
Ashraf, M., & Foolad, M. R. (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany, 59(2), 206-216. doi: 10.1016/j.envexpbot.2005.12. 006
Ashraf, U., Mahmood, M. H., Hussain, S., Anjum, S. A., & Tang, X. (2020). Lead (Pb) distribution and accumulation in different plant parts and its associations with grain Pb contents in fragrant rice. Chemosphere, 248(1), 126003. doi: 10.1016/j.chemosphere.2020.126003
Aslam, R., Bhat, T. M., Choudhary, S., & Ansari, M. Y. K. (2017). An overview on genotoxicity of heavy metal in a spice crop (Capsicum annuum L.) in respect to cyto-morphological behaviour. Caryologia, 70(1), 42-47. doi: 10.1080/00087114.2016.1258884
Azad, H. M., Shiva, A. H., & Malekpour, R. (2011). Toxic effects of lead on growth and some biochemical and ionic parameters of sunflower (Helianthus annuus L.) seedlings. Current Research Journal of Biological Sciences, 3(4), 398-403. https://maxwellsci.com/print/crjbs/v3-398-403.pdf
Azevedo, A. D. de, Neto, Mota, K. N. A. B., Silva, P. C. C., Cova, A. M. W., Ribas, R. F., & Gheyi, H. R. (2020). Selection of sunflower genotypes for salt stress and mechanisms of salt tolerance in contrasting genotypes. Ciência e Agrotecnologia, 44(1), e020120. doi: 10.1590/1413-7054202044020120
Bassegio, C., Santos, R. F., Bassegio, D., & Souza, S. N. M. de. (2020). Genotypic variation in growth and lead accumulation among Brassica juncea accessions. International Journal of Phytoremediation, 22(12), 1249-1258. doi: 10.1080/15226514.2020.1759506
Bates, L. S., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39(1), 205-207. doi: 10.1007/BF00018060
Bosso, S. T., & Enzweiler, J. (2008). Ensaios para determinar a (bio)disponibilidade de chumbo em solos contaminados: Revisão. Quimica Nova, 31(2), 394-400. doi: 10.1590/S0100-40422008000200036
Bradford, M. M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248-254. doi: 10.1016/j. cj.2017.04.003
Caetano, L. C. S., Prezotti, L. C., Pacheco, B. M., & Guarçoni, R. V. (2016). Soil chemical characteristics, biomass production and levels of nutrient and heavy metals in corn plants according to doses of steel slag and limestone. Revista Ceres, 63(6), 879-886. doi: 10.1590/0034-737X201663060018
Cova, A. M. W., Azevedo, A. D., Neto, Silva, P. C. C., Menezes, R. V, Ribas, R. F., & Gheyi, H. R. (2020). Physiological and biochemical responses and fruit production of noni (Morinda citrifolia L.) plants irrigated with brackish water. Scientia Horticulturae, 260(1), 108852. doi: 10.1016/j.scienta.2019.108852
Dalyan, E., Yuzbasioglu, E., & Akpinar, I. (2020). Physiological and biochemical changes in plant growth and different plant enzymes in response to lead stress. In D. Gupta, S. Chatterjee, & C. Walther (Eds.), Lead in plants and the environment (pp. 129-147). Cham.
Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28(3), 350-356. doi: 10.1021/ac60 111a017
Fageria, N. K. (2009). The use of nutrients in crop plants. CRC Press.
Ferreira, D. F. (2019). Sisvar: a computer analysis system to fixed effects split plot type designs. Revista Brasileira de Biometria, 37(4), 529-535. doi: 10.28951/rbb.v37i4.450
Hammer, O., Harper, D. A. T., & Ryan, P. D. (2001). Paleontological statistics software package for education and analysis. Palaeontologia Electronica, 4(1), 1-9. https://www.researchgate.net/publication/2596402 26_PAST_Paleontological_Statistics_Software_Package_for_Education_and_Data_Analysis
Hoagland, D. R., & Arnon, D. I. (1950). The water-culture method for growing plants without soil. Circular. California Agricultural Experiment Station, 347(2), 1-32. https://www.researchgate.net/file.PostFile Loader.html?id=54aefd7ed4c118b6358b45db&assetKey=AS%3A273668901408776%401442259158553
Hossain, M. A., Piyatida, P., Silva, J. A. T. da, & Fujita, M. (2012). Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. Journal of Botany, 2012(1), 1-37. doi: 10.1155/2012/ 872875
Houri, T., Khairallah, Y., Al Zahab, A., Osta, B., Romanos, D., & Haddad, G. (2020). Heavy metals accumulation effects on the photosynthetic performance of geophytes in Mediterranean reserve. Journal of King Saud University Science, 32(1), 874-880. doi: 10.1016/j.jksus.2019.04.005
Hussain, A., Abbas, N., Arshad, F., Akram, M., Khan, Z. I., Ahmad, K., Mansha, M., & Mirzaei, F. (2013). Effects of diverse doses of lead (Pb) on different growth attributes of Zea-mays L. Agricultural Sciences, 4(5), 262-265. doi: 10.4236/as.2013.45037
Jones, J. B. Jr. (2001). Laboratory guide for conducting soil tests and plant analysis. CRC Press.
Kabata-Pendias, A. (2010). Trace elements in soils and plants. CRC Press.
Kim, R.-Y., Yoon, J.-K., Kim, T.-S., Yang, J. E., Owens, G., & Kim, K.-R. (2015). Bioavailability of heavy metals in soils: definitions and practical implementation—a critical review. Environmental Geochemistry and Health, 37(6), 1041-1061. doi: 10.1007/s10653-015-9695-y
Kumar, R., Mishra, R. K., Mishra, V., Qidwai, A., Pandey, A., Shukla, S. K., Pandey, M., Pathak, A., & Dikshit, A. (2016). Detoxification and tolerance of heavy metals in plants. In P. Ahmad (Ed.), Plant metal interaction (pp. 335-359). Amsterdam..
Lamhamdi, M., El Galiou, O., Bakrim, A., Nóvoa-Munoz, J. C., Arias-Estévez, M., Aarab, A., & Lafont, R. (2013). Effect of lead stress on mineral content and growth of wheat (Triticum aestivum) and spinach (Spinacia oleracea) seedlings. Saudi Journal of Biological Sciences, 20(1), 29-36. doi: 10.1016/j.sjbs. 2012.09.001
Lichtenthaler, H. K., & Buschmann, C. (2001). Chlorophylls and carotenoids: measurement and characterization by UV-VIS Spectroscopy. Current Protocols in Food Analytical Chemistry, 1(1), F4.3.1-F4.3.8. doi: 10.1002/0471142913.faf0403s01
Liu, T., Liu, S., Guan, H., Ma, L., Chen, Z., Gu, H., & Qu, L.-J. (2009). Transcriptional profiling of Arabidopsis seedlings in response to heavy metal lead (Pb). Environmental and Experimental Botany, 67(2), 377-386. doi: 10.1016/j.envexpbot.2009.03.016
Malar, S., Manikandan, R., Favas, P. J. C., Sahi, S. V., & Venkatachalam, P. (2014). Effect of lead on phytotoxicity, growth, biochemical alterations, and its role on genomic template stability in Sesbania grandiflora: a potential plant for phytoremediation. Ecotoxicology and Environmental Safety, 108(1), 249-257. doi: 10.1016/j.ecoenv.2014.05.018
Malkowski, E., Kurtyka, R., Kita, A., & Karcz, W. (2005). Accumulation of Pb and Cd and its effect on Ca distribution in maize seedlings (Zea Mays L.). Polish Journal of Environmental Studies, 14(2), 203-207. http://www.pjoes.com/pdf-87749-21608?filename=Accumulation+of+Pb+and+Cd.pdf
Marschner, H. (2012). Mineral nutrition of higher plants (3rd ed.). Academic Press.
Onakpa, M. M., Njan, A. A., & Kalu, O. C. (2018). A review of heavy metal contamination of food crops in Nigeria. Annals of Global Health, 84(3), 488-494. doi: 10.29024/aogh.2314
Revathi, S., & Venugopal, S. (2013). Physiological and biochemical mechanisms of heavy metal tolerance. International Journal of Environmental Sciences, 3(5), 1339-1354. doi: 10.6088/ijes.2013030500004
Rucinska-Sobkowiak, R., Nowaczyk, G., Krzeslowska, M., Rabeda, I., & Jurga, S. (2013). Water status and water diffusion transport in lupine roots exposed to lead. Environmental and Experimental Botany, 87(1), 100-109. doi: 10.1016/j.envexpbot.2012.09.012
Sardans, J., & Penuelas, J. (2021). Potassium control of plant functions: ecological and agricultural implications. Plants, 10(2), 419. doi: 10.3390/plants10020419
Sharma, P., & Dubey, S. (2005). Lead toxicity in plants. Brazilian Journal of Plant Physiology, 17(1), 491-500. doi: 10.1590/S1677-04202005000100004
Silva, P. C. C., Azevedo, A. D. de, Neto, Gheyi, H. R., Ribas, R. F., Reis Silva, C. R. dos, & Cova, A. M. W. (2020). Salt-tolerance induced by leaf spraying with H2O2 in sunflower is related to the ion homeostasis balance and reduction of oxidative damage. Heliyon, 6(9), e05008. doi: 10.1016/j.heliyon.2020.e05008
Song, X., Zhang, C., Chen, W., Zhu, Y., & Wang, Y. (2020). Growth responses and physiological and biochemical changes in five ornamental plants grown in urban lead contaminated soils. Plant Environment Interactions, 1(1), 29-47. doi: 10.1002/pei3.10013
Verbruggen, N., & Hermans, C. (2008). Proline accumulation in plants: a review. Amino Acids, 35(4), 753-759. doi: 10.1007/s00726-008-0061-6
Vissenberg, K., Claeijs, N., Balcerowicz, D., & Schoenaers, S. (2020). Hormonal regulation of root hair growth and responses to the environment in Arabidopsis. Journal of Experimental Botany, 71(8), 2412-2427. doi: 10.1093/jxb/eraa048
White, P. J., & Pongrac, P. (2017). Heavy metal toxicity in plants. In S. Shabala (Ed.), Plant stress physiology (2nd ed., pp. 300-331). Boston. doi: 10.1023/A:1020305400324.
Yang, Y., Zhang, L., Huang, X., Zhou, Y., Quan, Q., Li, Y., & Zhu, X. (2020). Response of photosynthesis to different concentrations of heavy metals in Davidia involucrata. Plos One, 15(3), e0228563. doi: 10.1371/ journal.pone.0228563
Yemm, E. W., & Cocking, E. C. (1955). The determination of amino-acids with ninhydrin. The Analyst, 80(948), 209. doi: 10.1039/an9558000209
Zhou, J., Zhang, Z., Zhang, Y., Wei, Y., & Jiang, Z. (2018). Effects of lead stress on the growth, physiology, and cellular structure of privet seedlings. Plos One, 13(3), e0191139. doi: 10.1371/journal.pone.0191139
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2022-05-05
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Ribeiro, M. de O., Azevedo Neto, A. D. de, Cova, A. M. W., Ribeiro, L. de O., Menezes, R. V., Abreu, C. B. de, … Gheyi, H. R. (2022). Physiological, nutritional, and biochemical indicators of lead tolerance in sunflower genotypes. Semina: Ciências Agrárias, 43(4), 1517–1540. https://doi.org/10.5433/1679-0359.2022v43n4p1517
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