Skip to main content
SpringerLink
Log in

Thallium Differentially Affects Macronutrients Concentration and Stoichiometric Ratios with Nitrogen in the Leaves of Chili Pepper Varieties

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

This study aimed to assess the effects of thallium (Tl) on the leaf concentration of macronutrients (N, P, K, Ca, Mg, and S) and the stoichiometric relationships of P, K, Ca, Mg, and S with N in three varieties of chili pepper (Capsicum annuum): Jalapeño, Poblano, and Serrano. Sixty-day-old seedlings of the three varieties were treated with Tl, in doses of 0, 5.5, and 11 nM in the nutrient solution. After 80 days of exposure to Tl treatments, the nutrient concentration in leaf tissue was determined. With the data obtained, an analysis of variance and comparison of means with Tukey’s test (\(\alpha =0.05\)) were carried out, and through a meta-analysis, the size and direction of the effect of the evaluated Tl doses were determined, in the leaf concentrations of macronutrients. The 5.5 and 11 nM Tl doses increased the leaf concentration of P in Serrano and that of N in Poblano, respectively. Applying 5.5 nM Tl significantly reduced the leaf concentration of K in Jalapeño and Serrano, that of Ca in Poblano, and that of Mg in Serrano. In Jalapeño, both Tl doses tested reduced the leaf Ca concentration. Low Tl doses (5.5 nM) caused significant and positive effects on the leaf K concentration in all three varieties. High Tl doses (11 nM) caused significant negative effects on the leaf concentration of Mg. In the three varieties evaluated, the addition of Tl increased the leaf N:K ratio, that of N:Mg in Poblano and Serrano, the N:Mg ratio in Jalapeño, the P:K ratio in Serrano, and the N:Ca ratio in Jalapeño and Poblano. There was no effect of Tl on shoot dry biomass in any variety evaluated. In Tl-treated plants, foliar concentration of this element varied from12.0 to 26.6 mg kg−1 on a dry basis. The sum of principal component 1 and principal component 2 represented 80.8, 72.3, and 79.6% of the total variance of macronutrient concentration in leaves of the Jalapeño, Poblano, and Serrano varieties, respectively. We conclude that Tl had differential effects on the nutrient status among varieties of chili pepper, with Jalapeño being the most affected and Poblano the least.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Alcántar, G. G., & Sandoval, V. M. (1999). Manual de Análisis Químico de Tejido Vegetal. Publicación especial No. 10. Sociedad Mexicana de la Ciencia del Suelo A. C.

  • Alcántar, G. G., Trejo-Téllez, L. I., & Gómez-Merino, F. C. (2016). Nutrición de cultivos. Segunda edición. Biblioteca Básica de Agricultura, Colegio de Postgraduados.

  • Arif, N., Yadav, V., Singh, S., Singh, S., Ahmad, P., Mishra, R. K., Sharma, S., Tripathi, D. K., Dubey, N. K., & Chauhan, D. K. (2016). Influence of high and low levels of plant-beneficial heavy metal ions on plant growth and development. Frontiers in Environmental Science, 4(69), 1–11. https://doi.org/10.3389/fenvs.2016.00069

    Article  Google Scholar 

  • Azofeifa, A., & Moreira, M. A. (2008). Absorción y distribución de nutrimentos en plantas de chile jalapeño (Capsicum annuum L. cv. Hot) en Alajuela, Costa Rica. Agronomía Costarricense, 32(1), 19–29.

  • Barker, A. V., & Pilbeam, D. J. (2007). Handbook of plant nutrition. CRC Press.

    Google Scholar 

  • Buendía-Valverde, M. L., Trejo-Téllez, L. I., Corona-Torres, T., & Aguilar-Rincón, V. H. (2018). Cadmio, talio y vanadio afectan diferencialmente la germinación y crecimiento inicial de tres variedades de chile. Revista Internacional de Contaminación Ambiental, 34(4), 737–749. https://doi.org/10.20937/RICA.2018.34.04.14

  • Carballar-Hernández, S., Hernández-Cuevas, L. V., Montaño, N. M., Ferrera-Cerrato, R., & Alarcón, A. (2018). Species composition of native arbuscular mycorrhizal fungal consortia influences growth and nutrition of poblano pepper plants (Capsicum annuum L.). Applied Soil Ecology, 130, 50–58. https://doi.org/10.1016/j.apsoil.2018.05.022

    Article  Google Scholar 

  • Cruz-Crespo, E., Can-Chulim, Á., Bugarín-Montoya, R., Pineda-Pineda, J., Flores-Canales, R., Juárez-López, P., & Alejo-Santiago, G. (2014). Concentración nutrimental foliar y crecimiento de chile serrano en función de la solución nutritiva y el sustrato. Revista Fitotecnia Mexicana, 37(3), 289–295.

    Article  Google Scholar 

  • Cvjetko, P., Cvjetko, I., & Pavlica, M. (2010). Thallium toxicity in humans. Arhiv Za Higijenu Rada i Toksikologiju, 61(1), 111–119.

    Article  CAS  Google Scholar 

  • D’Orazio, M., Camapella, B., Bramanti, E., Ghezzi, L., Onor, M., Vianello, G., Vittori-Antisari, L., & Petrini, R. (2020). Thallium pollution in water, soils and plants from a past-mining site of Tuscany: Sources, transfer processes and toxicity. Journal of Geochemical Exploration, 209, 106434. https://doi.org/10.1016/j.gexplo.2019.106434

    Article  CAS  Google Scholar 

  • DalCorso, G., Manara, A., Piasentin, S., & Furini, A. (2014). Nutrient Metal Elements in Plants. Metallomics, 6(10), 1770–1788. https://doi.org/10.1039/c4mt00173g

    Article  CAS  Google Scholar 

  • FAO (Food and Agriculture Organization of the United Nations). 2022. FAOSTATS. Food and agriculture data. Crops. Chillies and peppers. Retrieved April 20, 2022, from https://www.fao.org/faostat/en/#data/QCL

  • Fernández, G. (2022). Mexico, the world’s leading exporter of fresh pepper. AMQueretaro 13–02–2022. Retrieved April 20, 2022, from https://amqueretaro.com/negocios/2022/02/13/mexico-principal-exportador-mundial-de-pimiento-fresco/

  • Frattini, P. (2005). Thallium properties and behavior - A literature study. Retrieved November 1, 2021, from http://tupa.gtk.fi/raportti/arkisto/s41_0000_2005_2.pdf

  • Galván-Arzate, S., & Santamarı́a, A. (1998). Thallium toxicity. Toxicology Letters, 99(1), 1–13.

  • Hasanuzzaman, M., Bhuyan, B. M. H. M., Nahar, K., Hossain, M. S., Al Mahmud, J., Hossen, M. S., Masud, A. A. C., & Moumita & Fujita, M. (2018). Potassium: A vital regulator of plant responses and tolerance to abiotic stresses. Agronomy, 8, 31. https://doi.org/10.3390/agronomy8030031

    Article  CAS  Google Scholar 

  • Hauer-Jákli, M., & Tränkner, M. (2019). Critical leaf magnesium thresholds and the impact of magnesium on plant growth and photo-oxidative defense: A systematic review and meta-analysis from 70 years of research. Frontiers in Plant Science, 10, 766. https://doi.org/10.3389/fpls.2019.00766

    Article  Google Scholar 

  • Health Council of the Netherlands. (2002). Committee on Updating of Occupational Exposure Limits. Thallium and water-soluble thallium compounds; Health-based Reassessment of Administrative Occupational Exposure Limits. The Hague: Health Council of the Netherlands, 2000/15OSH/057

  • Hedges, L. V., Gurevitch, J., & Curtis, P. S. (1999). The meta-analysis of response ratios in experimental ecology. Ecology, 80(4), 1150–1156.

    Article  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(2), 428–436. https://doi.org/10.1111/j.1469-8137.2011.03814.x

    Article  CAS  Google Scholar 

  • Holubík, O., Vaněk, A., Mihaljevic, M., & Vejvodová, K. (2021). Thallium uptake/tolerance in a model (hyper)accumulating plant: Effect of extreme contaminant loads. Soil & Water Research, 16, 129−135. https://doi.org/10.17221/167/2020-SWR

  • Jiang, F., Ren, B., Hursthouse, A., & Deng, R. (2020). Evaluating health risk indicators for PTE exposure in the food chain: Evidence from a thallium mine area. Environmental Science and Pollution Research, 27, 23686–23694. https://doi.org/10.1007/s11356-020-08733-0

    Article  CAS  Google Scholar 

  • Johnson, C. D., & Decotearu, D. R. (1996). Nitrogen and potassium fertility affects Jalapeño pepper plant growth, pod yield, and pungency. HortScience, 31(7), 1119–1123.

    Article  CAS  Google Scholar 

  • Kam, O. R., Bakouan, C., Zongo, I., & Guel, B. (2019). Assessing the source of thallium contamination in ground and surface waters in the locality of Yamtenga (Burkina-Faso): Correlation with some heavy metal ions. International Research Journal of Pure and Applied Chemistry, 19(4), 1–14. https://doi.org/10.9734/IRJPAC/2019/v19i430122

    Article  Google Scholar 

  • Kapusta, P., & Godzik, B. (2013). Does heavy metal deposition affect nutrient uptake by moss Pleurozium schreberi? In E3S Web of Conferences (Vol. 1, p. 29005). EDP Sciences.

  • Karbowska, B. (2016). Presence of thallium in the environment: Sources of contaminations, distribution and monitoring methods. Environmental Monitoring and Assessment, 188(11), 640.

    Article  Google Scholar 

  • Kazantzis, G. (2000). Thallium in the environment and health effects. Environmental Geochemistry and Health, 22, 275–280.

    Article  CAS  Google Scholar 

  • Khan, S., & Khan, N. N. (1983). Influence of lead and cadmium on the growth and nutrient concentration of tomato (Lycopersicum esculentum) and eggplant (Solanum melongena). Plant and Soil, 74(3), 387–394.

    Article  CAS  Google Scholar 

  • Kim, D. J., Park, B. C., Ahn, B. K., & Lee, J. H. (2016). Thallium uptake and translocation in barley and sunflower grown in hydroponic conditions. International Journal of Environmental Research, 10(4), 575–582. https://doi.org/10.22059/IJER.2016.59686

  • Kwan, K. H. M., & Smith, S. (1991). Some aspects of the kinetics of cadmium and thallium uptake by fronds of Lemna minor L. New Phytologist, 117, 91–102. https://doi.org/10.1111/j.1469-8137.1991.tb00948.x

    Article  CAS  Google Scholar 

  • Léonard, A., & Gerber, G. B. (1997). Mutagenicity, carcinogenicity and teratogenicity of thallium compounds. Mutation Research, 387(1), 47–53.

    Article  Google Scholar 

  • Madejón, P., Murillo, J. M., Marañon, T., & Lepp, N. W. (2007). Factors affecting accumulation of thallium and other trace elements in two wild Brassicaceae spontaneously growing on soils contaminated by tailings dam waste. Chemosphere, 67, 20–28.

    Article  Google Scholar 

  • Marchetti, C. (2013). Role of calcium channels in heavy metal toxicity. ISRN Toxicology, 1, 1–9. https://doi.org/10.1155/2013/184360

    Article  CAS  Google Scholar 

  • Marschner, P. (2012). Marschner’s mineral nutrition of higher plants. Third edition. Academic Press.

  • Mazur, R., Sadowska, M., Kowalewska, Ł., Abratowska, A., Kalaji, H. M., Mostowska, A., Garstka, M., & Krasnodębska-Ostręga, B. (2016). Overlapping toxic effect of long term thallium exposure on white mustard (Sinapis alba L.) photosynthetic activity. BMC Plant Biology, 16(1), 191. https://doi.org/10.1186/s12870-016-0883-4

  • De Mello, P. R., & Caione, G. (2012). Plant analysis. In R. N. Issaka (Ed.), Soil Fertility (1st ed., pp. 115–134). IntechOpen. https://doi.org/10.5772/53388

  • Mills, H. A., & Jones, J. B. (1996). Plant analysis handbook II. A practical sampling, preparation, analysis, and interpretation guide. Ed. Micro-Macropublishing.

  • Nazar, R., Iqbal, N., Masood, A., Khan, M. I. R., Syeed, S., & Khan, N. A. (2012). Cadmium toxicity in plants and role of mineral nutrients in its alleviation. American Journal of Plant Sciences, 3(10), 1476–1489. https://doi.org/10.4236/ajps.2012.310178

    Article  CAS  Google Scholar 

  • Nguyen, N. T., McInturf, S. A., & Mendoza-Cózatl, D. G. (2016). Hydroponics: A versatile system to study nutrient allocation and plant responses to nutrient availability and exposure to toxic elements. Journal of Visualized Experiments, 113, e54317.

    Google Scholar 

  • Ning, Z., He, L., Xiao, T., & László, M. (2015). High accumulation and subcellular distribution of thallium in green cabbage (Brassica oleracea L. var. capitata L.). International Journal of Phytoremediation, 17(11), 1097–1104. https://doi.org/10.1080/15226514.2015.1045133

  • Pavoni, E., Petranich, E., Adami, G., Baracchini, E., Crosera, M., Emili, A., Lenaz, D., Higueras, P., & Covelli, S. (2016). Bioaccumulation of thallium and other trace metals in Biscutella laevigata nearby a decommissioned zinc-lead mine (Northeastern Italian Alps). Journal of Environmental Management, 186(2), 214–224. https://doi.org/10.1016/j.jenvman.2016.07.022

    Article  CAS  Google Scholar 

  • Queirolo, F., Stegen, S., Contreras-Ortega, C., Ostapczuk, P., Queirolo, A., & Paredes, B. (2009). Thallium levels and bioaccumulation in environmental samples of Northern Chile: Human health risks. Journal of the Chilean Chemical Society, 54(4), 464–469.

    Article  CAS  Google Scholar 

  • R Core Team. (2018). A language and environment for statistical computing. R Foundation for Statistical Computing. Retrieved April 18, 2022, from http://www.r-project.org/

  • Rader, S. T., Maier, R. M., Barton, M. D., & Mazdab, F. K. (2019). Uptake and fractionation of thallium by Brassica juncea in geogenic thallium-amended substrate. Environmental Science & Technology, 53(5), 2441–2449. https://doi.org/10.1021/acs.est.8b06222

    Article  CAS  Google Scholar 

  • Rengel, Z., Bose, J., Chen, Q., & Tripathi, B. N. (2015). Magnesium alleviates plant toxicity of aluminium and heavy metals. Crop and Pasture Science, 66(12), 1298–1307. https://doi.org/10.1071/CP15284

    Article  CAS  Google Scholar 

  • Rezaeian, M., Moghadam, T. M., Kiaei, M. M., & Zadeh, M. H. (2019). The effect of heavy metals on the nutritional value of alfalfa: Comparison of nutrients and heavy metals of alfalfa (Medicago sativa) in industrial and non-industrial areas. Toxicological Research, 36(2), 183–193. https://doi.org/10.1007/s43188-019-00012-6

    Article  CAS  Google Scholar 

  • Riga, P., & Anza, M. (2003). Effect of magnesium deficiency on pepper growth parameters: Implications for determination of magnesium critical value. Journal of Plant Nutrition, 26(8), 1581–1593. https://doi.org/10.1081/PLN-120022367

    Article  CAS  Google Scholar 

  • Rodríguez-Mercado, J. J., & Altamirano-Lozano, M. A. (2013). Genetic toxicology of thallium: A review. Drug and Chemical Toxicology, 36(3), 369–383.

    Article  Google Scholar 

  • Sardans, J., Grau, O., Chen, H. Y. H., Janssens, I. A., Ciais, P., Piao, S., & Peñuelas, J. (2017). Changes in nutrient concentrations of leaves and roots in response to global change factors. Global Change Biology, 23(9), 3849–3856. https://doi.org/10.1111/gcb.13721

    Article  Google Scholar 

  • SAS Institute Inc. (2011). SAS/STAT Users Guide. Version 9.3. SAS Institute Inc.

  • Sasmaz, M., Akgul, B., Yıldırım, D., & Sasmaz, A. (2016). Bioaccumulation of thallium by the wild plants grown in soils of mining area. International Journal of Phytoremediation, 18(11), 1164–1170. https://doi.org/10.1080/15226514.2016.1183582

    Article  CAS  Google Scholar 

  • Sinclair, A. G., Morrison, J. D., Smith, L. C., & Dodds, K. G. (1997). Determination of optimum nutrient element ratios in plant tissue. Journal of Plant Nutrition, 20(9), 1069–1083. https://doi.org/10.1080/01904169709365319

    Article  CAS  Google Scholar 

  • Smical, A. I., Hotea, V., Oros, V., Juhasz, J., & Pop, E. (2008). Studies on transfer and bioaccumulation of heavy metals from soil into lettuce. Environmental Engineering and Management Journal, 7(5), 609–615.

    Article  CAS  Google Scholar 

  • Steiner, A. A. (1984). The universal nutrient solution. 6th international congress on soilless culture. Wageningen, The Netherlands. pp. 633–650

  • Tanoi, K., & Kobayashi, N. (2015). Leaf Senescence by Magnesium Deficiency. Plants, 4, 756–772. https://doi.org/10.3390/plants4040756

    Article  CAS  Google Scholar 

  • Thévenod, F. (2009). Cadmium and cellular signaling cascades: To be or not to be? Toxicology and Applied Pharmacology, 238(3), 221–239. https://doi.org/10.1016/j.taap.2009.01.013

    Article  CAS  Google Scholar 

  • Uchida, R. (2000). Recommended plant tissue nutrient levels for some vegetable, fruit, and ornamental foliage and flowering plants in Hawaii. In J. A. Silva & R. Uchida (Eds.), Plant nutrient management in Hawaii’s soils (pp. 57–64). University of Hawaii at Manoa.

    Google Scholar 

  • USEPA. (2021). National Primary Drinking Water Regulations. Retrieved November 2, 2021, from https://www.epa.gov/ground-water-and-drinking-water/national-primary-drinking-water-regulations

  • Viraraghavan, T., & Srinivasan, A. (2011). Thallium: Environmental pollution and health effects. Encyclopedia of Environmental Health, 6, 39–47. https://doi.org/10.1016/B978-0-444-63951-6.00643-4

    Article  Google Scholar 

  • Wawrzynska, A., Moniuszko, G., & Sirko, A. (2015). Links between ethylene and sulfur nutrition—A regulatory interplay or just metabolite association? Frontiers in Plant Science, 6, 1053. https://doi.org/10.3389/fpls.2015.01053

    Article  Google Scholar 

  • Yu, M. H., & Tsunoda, H. (2016). Environmental toxicology: Biological and health effects of pollutants. Third Edition. CRC Press.

  • Zhang, G., Fukami, M., & Sekimoto, H. (2002). Influence of cadmium on mineral concentrations and yield components in wheat genotypes differing in Cd tolerance at seedling stage. Field Crops Research, 77(2–3), 93–98. https://doi.org/10.1016/S0378-4290(02)00061-8

    Article  Google Scholar 

  • Zhang, F., Wan, X., & Zhong, Y. (2014). Nitrogen as an important detoxification factor to cadmium stress in poplar plants. Journal of Plant Interactions, 9(1), 249–258. https://doi.org/10.1080/17429145.2013.819944

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Colegio de Postgraduados, Campus Montecillo, Carretera México-Texcoco km 36.5, 56230, Montecillo, Mexico

    María de la Luz Buendía-Valverde, Fernando C. Gómez-Merino, Tarsicio Corona-Torres, Serafín Cruz-Izquierdo & Libia I. Trejo-Téllez

  2. Unidad de Investigación en Genética y Toxicología Ambiental (UNIGEN), Laboratorio 5, primer piso, Unidad Multidisciplinaria de Investigación Experimental (UMIEZ-Z), Facultad de Estudios Superiores-Zaragoza, Campus II, Universidad Nacional Autónoma de México, 15000, Mexico City, Mexico

    Rodrigo A. Mateos-Nava

Authors
  1. María de la Luz Buendía-Valverde
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fernando C. Gómez-Merino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tarsicio Corona-Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Serafín Cruz-Izquierdo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rodrigo A. Mateos-Nava
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Libia I. Trejo-Téllez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Libia I. Trejo-Téllez.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Buendía-Valverde, M., Gómez-Merino, F.C., Corona-Torres, T. et al. Thallium Differentially Affects Macronutrients Concentration and Stoichiometric Ratios with Nitrogen in the Leaves of Chili Pepper Varieties. Water Air Soil Pollut 233, 201 (2022). https://doi.org/10.1007/s11270-022-05671-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-022-05671-0

Keywords

Search

Navigation