Effect of copper, nickel and lead on callus growth dynamics of Solanum lycopersicum
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Abstract
Solanum lycopersicum cv. (Punjab Kesar Cherry) (Tomato) belonging to family Solanaceae has been priced for the presence of lycopene, low sugar content and curative properties. However, the productivity of tomatoes has been observed to be low due to both biotic as well as abiotic stress. Considering the toxicity of copper (Cu), lead (Pb) and nickel (Ni) as environmental contamination and the economic importance of S. lycopersicum, the present study was undertaken to investigate the effects of these heavy metals on various growth parameters of callus cultures and plantlet regeneration. Callus induced through nodal segments was inoculated on Murashige and Skoog medium containing different concentrations (0 µM, 50 µM, 100 µM, 200 µM, 300 µM, 400 µM and 500 µM) of copper, lead and nickel. Decrease in different growth parameters was observed as 91.66-16.66 %, 76.38-11.11 %, 81.94-13.88 % for percent callus survival, 90.90-25 %, 72.72-37.50 %, 79.66-20 % for percent callus multiplication, 79.54-0 %, 82.75-33 %, 63.8-50 % for percent root regeneration and 73.33-33 %, 72.50-33 %, 79.6- 20 % for percent shoot generation with increasing concentrations of Cu, Pb and Ni, respectively. Decrease in the average fresh and dry weight of callus was observed for all the metals. The order of toxicity was observed as Pb > Ni > Cu at the highest concentrations used for treating S. lycopersicum. The present study revealed that all three metals induced stress in the studied plant and need attention to developing methods to mitigate the consequences of metal toxicity in crop plants.
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Keywords
Environmental pollution, Heavy metals, Soil pollution, Tomato, Toxicity
References
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Ameen, N., Amjad, M., Murtaza, B., Abbas, G., Shahid, M., Imran, M. & Niazi, N. K. (2019). Biogeochemical behavior of nickel under different abiotic stresses: toxicity and detoxification mechanisms in plants. Environ. Sci. Pollut. Res., 26, 10496-10514. https://doi.org/10.1007/s11356-019-04540-4.
Anjum, NA., Sofo, A., Scopa, A., Roychoudhury, A., Gill, S.S., Iqbal, M., Lukatkin, A.S., Pereira, E., Duarte, A.C. & Ahmad, I. (2015). Lipids and proteins - Major targets of oxidative modifications in abiotic stressed plants. Env. Sci. Pollut. Res., 22, 4099- 4121. https://doi.org/10.1007/s11356-014-3917-1.
Ashrafzadeh, S. & Leung, D.M.W. (2015). In vitro breeding of heavy metal resistant plants: a review. Hortic. Environ. And Biotechnol., 56, 131-136. https://doi.org/10.1007/s13580-015-0128-8.
Barcelos, J. P. Q., Reis, H. P. G., Godoy, C. V., Gratao, P. L., Furlani Junior, E., Putti, F. F. & Reis, A. R. (2018). Impact of foliar nickel application on urease activity, antioxidant metabolism and control of powdery mildew (Microsphaera diffusa) in soybean plants. Plant Pathol., 67, 1502-1513. https://doi.org/10.1111/ppa.12 871.
Chaitanya, G., Pavani, C. & Shasthree, T. (2022). Effect of heavy metals on in vitro growth and development of the Momordica cymbalariaFenzl. Int. J. Environ. Sci. Technol. https://doi.org/10.1007/s13762-022-04437-9. https://doi.or g/10.1007/s13762-022-04437-9.
Chandra, I., Singh, P., Bhattacharya, A., Singh, P., Javed, S. & Singhmahapatra, A. (2013). In vitro callus induction, regeneration and micropropagation of Solanum lycopersicum. Int. J. Curr. Microbiol. Appl. Sci., 2, 192–197.
Chojnacka, K., Chojnacki, A.H., Gorecka, H., Gorecki, H. (2005). Bioavailability of heavy metals from polluted soils to plants. Sci.Total Environ., 337, 175-182. https://doi.org/10.1016/j.scitotenv.2004.06.009.
Dalilah, D., Chong, C.S., Samad,A. A.,Manan, F.A.(2022). Effects of Copper on Total Phenolics, Flavonoids and Mitochondrial Properties of Orthosiphon stamineus Callus Culture. Int. J. Agric. Biol., 6, 1243-1248. DOI: 10.17957/IJAB/15.0038.
Das, A., & Das, B. (2019). Nanotechnology a potential tool to mitigate abiotic stress in crop plants. Abiotic and biotic stress in plants, pp 1-18, DOI:10.5772/intechopen.83562
Dubey, D. & Pandey, A. (2011). Effect of nickel (Ni) on chlorophyll, lipid peroxidation and antioxidative enzyme activities in black gram (Vigna mungo) leaves. Int. J. Sci. Nat., 2, 395-401.
Eskew, D.L., Welch, R.M. & Norwell, W.A. (1984). Nickel in Higher Plants: Further evidence for an essential role. Plant Physiol., 76, 691-693.DOI: 10.1104/pp.76.3.691
Faiyga, A.O., Ma, L.Q., Cao, x., Rathinasabapathi, B. (2004). Effects of heavy metals on growth and arsenic accumulation in the arsenic hyperaccumulator Pteris vittata L. Environ. Pollut., 132, 289-296.https://doi.org/10.1 016/j.envpol.2004.04.020.
Fathalla, Kareem, M., Kawy, A.M. & Taha, H.S. (2011). Effect of Heavy Metal (HgCl2) on Accumulation and Production of Total Indole Alkaloids, Vinblastine and/or Vincristine from Egyptian Catharanthus Roseus (L.) G. Don. Calli Culture. Res J. Appl. Sci., 7, 542-549. DOI: http://doi.org/10.23851/mjs.v28i3.60.
Ghanavatifard, F., Mohtadi, A. & Masoumiasl, A. (2018). Investigation of tolerance to different nickel concentrations in two species Matricaria chamomilla and Matricaria aurea. International J. Environ. Sci. Technol., 15, 949-956.https://doi.org/10.1007/s13762-017-1435-7
Guo, G., Zhou, Q., Ma, L.Q. (2006). Availability and assessment of fixing additives for the in situ remediation of heavy metal contaminated soils: a review. Environ. Monit. Asses., 116, 513-528. https://doi.org/10.1007/s10661-006-7668-4.
Hanus, E. (2006). Variation in tomato plants regenerated from Cucumber Mosaic Viruses infected tissue. ISHS Acta Hort 789: XV Meeting of the EUCARPIA Tomato working group. Doi.10.17660/ActaHortic.2008.789.40
Horsfall, M., & Spiff, AI. (2004). Studies on the Effect of pH on the Sorption of Pb2+ and Cd 2+ ions from aqueous Solutions by Caladium bicolor (Wild cocoyam) Biomass. Electron. J. Biotechnol., 7, 313-323.
Husain, N. & Mahmood, R. (2019). Copper (II) generates ROS and RNS, impairs antioxidant system and damages membrane and DNA in human blood cells. Environ. Sci. Pollut. Res., 26, 20654-20668. DOI: 10.1007/s11356-019-05345-1.
Hussain, A., Qarshi, I.A., Nazir, H., & Ullah, I. (2012). Plant tissue culture: current status and opportunities. Intech., 28, 50568.
Katare, j., Pichhode, M. & Nikhil, K. (2015). Effect of Different Mining Dust on the Vegetation of District Balaghat, M.P - A Critical Review. Int. J. Sci. Res., 4, 603-607.
Khater, M.A., Soliman, S.S.A., Abdel-Hady, M.S. & Fayed, A.H. (2013). Tropane Alkaloid Production via New Promising Atropa belladonna L. Lines by In Vivo and In Vitro. J. Nat. Sci., 11, 49-57.
Kim, J.Y., Paik, J.K., Kim, O.Y., Park, H.W., Lee, J.H., Jang, Y. & Lee, J.H. (2011). Effects of lycopene supplementation on oxidative stress and markers of endothelial function in healthy men. Atherosclerosis., 215, 189-195. https://doi.org/10.1016/j.atherosclerosis.2010.11.036
Kristina, K., Hendry Henderson, A., Djohan, D., Ehrich Lister, I. N., Girsang, E., & Fachrial, E. (2019). Antioxidant and Anticollagenase Activity of Tomato (Solanum lycopersicum L.) and Lycopene. ASRJETS., 52, 57–66.
Kumar, A., Kumar, A., MMS, C. P., Chaturvedi, A. K., Shabnam, A. A., Subrahmanyam, G. & Yadav, K. K. (2020). Lead toxicity: health hazards, influence on food chain, and sustainable remediation approaches. Int. J. Environ. Res. Public Health., 17, 2179. https://doi.org/10.3390/ijerph17072179.
Kumar, V., Pandita, S., Sidhu, G. P. S., Sharma, A., Khanna, K., Kaur, P. & Setia, R. (2021). Copper bioavailability, uptake, toxicity and tolerance in plants: a comprehensive review. Chemosphere., 262, 127810. DOI: 10.1016/j.chemosphere.2020.127810.
Maroti, M. & Bognar, J. (1988). Effect of heavy metals on the growth of tissue cultures (II). Acta Biol Hung., 39, 75-85.
Miroshnichenko, D., Klementyeva, A. & Dolgov, S. (2021). The Effect of Daminozide, Dark/Light Schedule and Copper Sulphate in Tissue Culture of Triticum timopheevii. Plants., 10, 1-15. https://doi.org/10.3390/plants10122620.
Murashige, T., & Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. plant.,15, 473-497.
Nalini, P & Sharma, C.P. (2003). Effect of heavy metals Co, Ni and Cd on growth and metabolism of tomato plants. Plant Physiol., 35, 112-117.
Namitha, K. K., & Negi, P. S. (2013). Enhancement of Natural Antioxidants in Plants by Biosynthetic Pathway Modulation. Chemistry and Pharmacology of Naturally Occurring Bioactive Compounds., 505-550. CRC Press.
Okereafor, U., Makhatha, M., Mekuto, L., Uche-Okereafor, N., Sebola, T., & Mavumengwana, V. (2020). Toxic metal implications on agricultural soils, plants, animals, aquatic life and human health. Int. J. Environ. Res. Public Health., 17, 2204. https://doi.org/10.3390/ijerph17072204.
Pandey, N., & Sharma, C.P. (2002). Effect of heavy metals Co+2, Ni+2 and Cd+2 on growth and metabolism of cabbage. J.Plant. Sci., 163, 753-758. https://doi.org/10.1016/S0168-9452(02)00210-8.
Pichhode, M. & Nikhil, K. (2015). Effect of Copper Dust on Photosynthesis Pigments Concentration in Plants Species. IJERM., 2, 63-66.
Pompeu, G.B., Gratao, P.L., Vitorello, V.A., Azevedo, R.A. (2008). Antioxidant isoenzyme responses to Nickel- induced stress in Tobacco cell suspension culture. Sci. Agric., 65, 548-552.https://doi.org/10.1590/S0103-90162 008000500015.
Rahmatullh, U.Z., Zaman, M., Salim, & Hussin, K. (2001). Influences of Ni supply on tomato growth and N uptake. Int. J. Agric. Biol., 3, 320-323.
Rehman, A. U., Nazir, S., Irshad, R., Tahir, K., Rehman, K., Islam, R. U., & Wahab, Z. (2021). Toxicity of heavy metals in plants and animals and their uptake by magnetic iron oxide nanoparticles. J. Mol. Liq., 321, 114455. https://doi.org/10.1016/j.molliq.2020.114455.
Rehman, W., Shibli, R. A. A., P, Younes , L. S., Mallouh, S. A. and Qudah, T. S. A. (2020). Responses of Lantana Camara Linn. Callus Cultures to Heavy Metals Added to the Culture Media. Jordan J. Biol. Sci., 551-557.
Sharma, P. & Dubey, R. (2005). Lead toxicity in plants. Braz. J. Plant Physiol., 17, 35-52. https://doi.org/10.1590/S1677-04202005000100004.
Shimada, N. & Watanab, Y (2004). Effect of nickel on the plant growth and urea assimilation in higher plants. Int. J. Soil Sci., 4, 164–171.
Taddei, S., Bernardi, R., Salvini, M., Pugliesi, C., Durante, M. (2007) Effect of copper on callus growth and gene expression of in vitro-cultured pith explants of Nicotiana glauca. Plant Biosyst., 141, 194–203. https://doi.org/10.1080/11263500701401521.
Vijayaraghavan, K., Jegan, J., Palanivelu, K., & Velan, M. (2004). Copper removal from aqueous solution by marine green alga Ulva reticulate. Electron. J. Biotechnol., 7, 62- 67.
Yan, R., Gao, S., Yang, W., Cao, M., Wang, S. & Chen, F. (2008). Nickel toxicity induced antioxidant enzyme and phenylalanine ammonia-lyase activities in Jatropha curcas L. cotyledons. Plant soil environ., 54, 294–300.
Yarra, R., He, S.J., Abbagani, S., Ma, B., Bulle, M., Zhang, W.K. (2012). Overexpression of wheat Na+/H+antiporter gene (TaNHX2) enhances tolerance to salt stress in transgenic tomato plants (Solanum lycopersicum L.). Plant Cell Tissue Organ Cult., 111, 49–57. https://doi.org/10.1007/s11240-012-0169-y.
Abdulhameed, A. N. & AlSalihi, A. A. (2019). Effect of heavy metals on some growth parameters in callus of Iraqi Cynodon Dactylon L. Plant cultivation in vitro. Plant Arch., 19, 3811-3816.
Ameen, N., Amjad, M., Murtaza, B., Abbas, G., Shahid, M., Imran, M. & Niazi, N. K. (2019). Biogeochemical behavior of nickel under different abiotic stresses: toxicity and detoxification mechanisms in plants. Environ. Sci. Pollut. Res., 26, 10496-10514. https://doi.org/10.1007/s11356-019-04540-4.
Anjum, NA., Sofo, A., Scopa, A., Roychoudhury, A., Gill, S.S., Iqbal, M., Lukatkin, A.S., Pereira, E., Duarte, A.C. & Ahmad, I. (2015). Lipids and proteins - Major targets of oxidative modifications in abiotic stressed plants. Env. Sci. Pollut. Res., 22, 4099- 4121. https://doi.org/10.1007/s11356-014-3917-1.
Ashrafzadeh, S. & Leung, D.M.W. (2015). In vitro breeding of heavy metal resistant plants: a review. Hortic. Environ. And Biotechnol., 56, 131-136. https://doi.org/10.1007/s13580-015-0128-8.
Barcelos, J. P. Q., Reis, H. P. G., Godoy, C. V., Gratao, P. L., Furlani Junior, E., Putti, F. F. & Reis, A. R. (2018). Impact of foliar nickel application on urease activity, antioxidant metabolism and control of powdery mildew (Microsphaera diffusa) in soybean plants. Plant Pathol., 67, 1502-1513. https://doi.org/10.1111/ppa.12 871.
Chaitanya, G., Pavani, C. & Shasthree, T. (2022). Effect of heavy metals on in vitro growth and development of the Momordica cymbalariaFenzl. Int. J. Environ. Sci. Technol. https://doi.org/10.1007/s13762-022-04437-9. https://doi.or g/10.1007/s13762-022-04437-9.
Chandra, I., Singh, P., Bhattacharya, A., Singh, P., Javed, S. & Singhmahapatra, A. (2013). In vitro callus induction, regeneration and micropropagation of Solanum lycopersicum. Int. J. Curr. Microbiol. Appl. Sci., 2, 192–197.
Chojnacka, K., Chojnacki, A.H., Gorecka, H., Gorecki, H. (2005). Bioavailability of heavy metals from polluted soils to plants. Sci.Total Environ., 337, 175-182. https://doi.org/10.1016/j.scitotenv.2004.06.009.
Dalilah, D., Chong, C.S., Samad,A. A.,Manan, F.A.(2022). Effects of Copper on Total Phenolics, Flavonoids and Mitochondrial Properties of Orthosiphon stamineus Callus Culture. Int. J. Agric. Biol., 6, 1243-1248. DOI: 10.17957/IJAB/15.0038.
Das, A., & Das, B. (2019). Nanotechnology a potential tool to mitigate abiotic stress in crop plants. Abiotic and biotic stress in plants, pp 1-18, DOI:10.5772/intechopen.83562
Dubey, D. & Pandey, A. (2011). Effect of nickel (Ni) on chlorophyll, lipid peroxidation and antioxidative enzyme activities in black gram (Vigna mungo) leaves. Int. J. Sci. Nat., 2, 395-401.
Eskew, D.L., Welch, R.M. & Norwell, W.A. (1984). Nickel in Higher Plants: Further evidence for an essential role. Plant Physiol., 76, 691-693.DOI: 10.1104/pp.76.3.691
Faiyga, A.O., Ma, L.Q., Cao, x., Rathinasabapathi, B. (2004). Effects of heavy metals on growth and arsenic accumulation in the arsenic hyperaccumulator Pteris vittata L. Environ. Pollut., 132, 289-296.https://doi.org/10.1 016/j.envpol.2004.04.020.
Fathalla, Kareem, M., Kawy, A.M. & Taha, H.S. (2011). Effect of Heavy Metal (HgCl2) on Accumulation and Production of Total Indole Alkaloids, Vinblastine and/or Vincristine from Egyptian Catharanthus Roseus (L.) G. Don. Calli Culture. Res J. Appl. Sci., 7, 542-549. DOI: http://doi.org/10.23851/mjs.v28i3.60.
Ghanavatifard, F., Mohtadi, A. & Masoumiasl, A. (2018). Investigation of tolerance to different nickel concentrations in two species Matricaria chamomilla and Matricaria aurea. International J. Environ. Sci. Technol., 15, 949-956.https://doi.org/10.1007/s13762-017-1435-7
Guo, G., Zhou, Q., Ma, L.Q. (2006). Availability and assessment of fixing additives for the in situ remediation of heavy metal contaminated soils: a review. Environ. Monit. Asses., 116, 513-528. https://doi.org/10.1007/s10661-006-7668-4.
Hanus, E. (2006). Variation in tomato plants regenerated from Cucumber Mosaic Viruses infected tissue. ISHS Acta Hort 789: XV Meeting of the EUCARPIA Tomato working group. Doi.10.17660/ActaHortic.2008.789.40
Horsfall, M., & Spiff, AI. (2004). Studies on the Effect of pH on the Sorption of Pb2+ and Cd 2+ ions from aqueous Solutions by Caladium bicolor (Wild cocoyam) Biomass. Electron. J. Biotechnol., 7, 313-323.
Husain, N. & Mahmood, R. (2019). Copper (II) generates ROS and RNS, impairs antioxidant system and damages membrane and DNA in human blood cells. Environ. Sci. Pollut. Res., 26, 20654-20668. DOI: 10.1007/s11356-019-05345-1.
Hussain, A., Qarshi, I.A., Nazir, H., & Ullah, I. (2012). Plant tissue culture: current status and opportunities. Intech., 28, 50568.
Katare, j., Pichhode, M. & Nikhil, K. (2015). Effect of Different Mining Dust on the Vegetation of District Balaghat, M.P - A Critical Review. Int. J. Sci. Res., 4, 603-607.
Khater, M.A., Soliman, S.S.A., Abdel-Hady, M.S. & Fayed, A.H. (2013). Tropane Alkaloid Production via New Promising Atropa belladonna L. Lines by In Vivo and In Vitro. J. Nat. Sci., 11, 49-57.
Kim, J.Y., Paik, J.K., Kim, O.Y., Park, H.W., Lee, J.H., Jang, Y. & Lee, J.H. (2011). Effects of lycopene supplementation on oxidative stress and markers of endothelial function in healthy men. Atherosclerosis., 215, 189-195. https://doi.org/10.1016/j.atherosclerosis.2010.11.036
Kristina, K., Hendry Henderson, A., Djohan, D., Ehrich Lister, I. N., Girsang, E., & Fachrial, E. (2019). Antioxidant and Anticollagenase Activity of Tomato (Solanum lycopersicum L.) and Lycopene. ASRJETS., 52, 57–66.
Kumar, A., Kumar, A., MMS, C. P., Chaturvedi, A. K., Shabnam, A. A., Subrahmanyam, G. & Yadav, K. K. (2020). Lead toxicity: health hazards, influence on food chain, and sustainable remediation approaches. Int. J. Environ. Res. Public Health., 17, 2179. https://doi.org/10.3390/ijerph17072179.
Kumar, V., Pandita, S., Sidhu, G. P. S., Sharma, A., Khanna, K., Kaur, P. & Setia, R. (2021). Copper bioavailability, uptake, toxicity and tolerance in plants: a comprehensive review. Chemosphere., 262, 127810. DOI: 10.1016/j.chemosphere.2020.127810.
Maroti, M. & Bognar, J. (1988). Effect of heavy metals on the growth of tissue cultures (II). Acta Biol Hung., 39, 75-85.
Miroshnichenko, D., Klementyeva, A. & Dolgov, S. (2021). The Effect of Daminozide, Dark/Light Schedule and Copper Sulphate in Tissue Culture of Triticum timopheevii. Plants., 10, 1-15. https://doi.org/10.3390/plants10122620.
Murashige, T., & Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. plant.,15, 473-497.
Nalini, P & Sharma, C.P. (2003). Effect of heavy metals Co, Ni and Cd on growth and metabolism of tomato plants. Plant Physiol., 35, 112-117.
Namitha, K. K., & Negi, P. S. (2013). Enhancement of Natural Antioxidants in Plants by Biosynthetic Pathway Modulation. Chemistry and Pharmacology of Naturally Occurring Bioactive Compounds., 505-550. CRC Press.
Okereafor, U., Makhatha, M., Mekuto, L., Uche-Okereafor, N., Sebola, T., & Mavumengwana, V. (2020). Toxic metal implications on agricultural soils, plants, animals, aquatic life and human health. Int. J. Environ. Res. Public Health., 17, 2204. https://doi.org/10.3390/ijerph17072204.
Pandey, N., & Sharma, C.P. (2002). Effect of heavy metals Co+2, Ni+2 and Cd+2 on growth and metabolism of cabbage. J.Plant. Sci., 163, 753-758. https://doi.org/10.1016/S0168-9452(02)00210-8.
Pichhode, M. & Nikhil, K. (2015). Effect of Copper Dust on Photosynthesis Pigments Concentration in Plants Species. IJERM., 2, 63-66.
Pompeu, G.B., Gratao, P.L., Vitorello, V.A., Azevedo, R.A. (2008). Antioxidant isoenzyme responses to Nickel- induced stress in Tobacco cell suspension culture. Sci. Agric., 65, 548-552.https://doi.org/10.1590/S0103-90162 008000500015.
Rahmatullh, U.Z., Zaman, M., Salim, & Hussin, K. (2001). Influences of Ni supply on tomato growth and N uptake. Int. J. Agric. Biol., 3, 320-323.
Rehman, A. U., Nazir, S., Irshad, R., Tahir, K., Rehman, K., Islam, R. U., & Wahab, Z. (2021). Toxicity of heavy metals in plants and animals and their uptake by magnetic iron oxide nanoparticles. J. Mol. Liq., 321, 114455. https://doi.org/10.1016/j.molliq.2020.114455.
Rehman, W., Shibli, R. A. A., P, Younes , L. S., Mallouh, S. A. and Qudah, T. S. A. (2020). Responses of Lantana Camara Linn. Callus Cultures to Heavy Metals Added to the Culture Media. Jordan J. Biol. Sci., 551-557.
Sharma, P. & Dubey, R. (2005). Lead toxicity in plants. Braz. J. Plant Physiol., 17, 35-52. https://doi.org/10.1590/S1677-04202005000100004.
Shimada, N. & Watanab, Y (2004). Effect of nickel on the plant growth and urea assimilation in higher plants. Int. J. Soil Sci., 4, 164–171.
Taddei, S., Bernardi, R., Salvini, M., Pugliesi, C., Durante, M. (2007) Effect of copper on callus growth and gene expression of in vitro-cultured pith explants of Nicotiana glauca. Plant Biosyst., 141, 194–203. https://doi.org/10.1080/11263500701401521.
Vijayaraghavan, K., Jegan, J., Palanivelu, K., & Velan, M. (2004). Copper removal from aqueous solution by marine green alga Ulva reticulate. Electron. J. Biotechnol., 7, 62- 67.
Yan, R., Gao, S., Yang, W., Cao, M., Wang, S. & Chen, F. (2008). Nickel toxicity induced antioxidant enzyme and phenylalanine ammonia-lyase activities in Jatropha curcas L. cotyledons. Plant soil environ., 54, 294–300.
Yarra, R., He, S.J., Abbagani, S., Ma, B., Bulle, M., Zhang, W.K. (2012). Overexpression of wheat Na+/H+antiporter gene (TaNHX2) enhances tolerance to salt stress in transgenic tomato plants (Solanum lycopersicum L.). Plant Cell Tissue Organ Cult., 111, 49–57. https://doi.org/10.1007/s11240-012-0169-y.
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Effect of copper, nickel and lead on callus growth dynamics of Solanum lycopersicum. (2022). Journal of Applied and Natural Science, 14(4), 1449-1455. https://doi.org/10.31018/jans.v14i4.3913
