Skip to main content

Advertisement

SpringerLink
Log in

Effect of Cadmium and Phosphorus Interaction on Tomato: Chlorophyll a Fluorescence, Plant Growth, and Cadmium Translocation

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

Abstract

Cadmium (Cd) is considered one of the heavy metals disturbing plant biophysiological functions. The potential role of phosphorus (P) nutrition in the attenuation of Cd effects on photosynthetic efficiency, plant growth, and cadmium uptake has been investigated in hydroponically grown tomato. Two P nutrition regimes (P15: 15 mg l-1; P30: 30 mg l-1) were assessed in the presence or absence of Cd (Cd0: 0 μM; Cd25: 25 μM of CdCl2). The results showed a positive effect of P30 concentration on leaf chlorophyll content and chlorophyll a fluorescence compared to P15 treatment under Cd stress (Cd25). The disturbance of electron transfer caused by Cd at K and I-steps of OJIP transient was attenuated with sufficient P supply. P30 enhanced the performance index of photosystem II and the efficiency of electron transfer to electron acceptor at PSI acceptor side. Besides, increased P concentration improved root growth parameters and biomass accumulation in the presence of Cd. It was found that root tissues accumulated more Cd than shoots and Cd translocation was reduced with increasing P concentration. Our results reveal that Cd-P interaction induced a cascade of physiological and chemical changes in plants. An optimal P nutrition can attenuate Cd stress on plant by the promotion of nitrogen and potassium uptake, which in return improved photosynthesis efficiency, enhanced biomass accumulation and distribution, and minimized Cd accumulation and translocation in plant tissues.

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

References

  • Andresen, E., & Küpper, H. (2013). Cadmium toxicity in plants. Metal Ions in Life Sciences, 11, 395. https://doi.org/10.1007/978-94-007-5179-8_13.

  • Armas, T., Pinto, A.P., de Varennes, A., Mourato, M.P., Martins, L.L., Gonçalves, M.L.S., Mota, A.M. (2015). Comparison of cadmium-induced oxidative stress in Brassica juncea in soil and hydroponic cultures. Plant Soil, 388, 297–305. https://doi.org/10.1007/s11104-014-2330-3.

  • Ashraf, M., Harris, P.J.C. (2004). Potential biochemical indicators of salinity tolerance in plants. Plant Science, 166, 3–16. https://doi.org/10.1016/j.plantsci.2003.10.024.

  • Bruno, L., Pacenza, M., Forgione, I., Lamerton, L. R., Greco, M., Chiappetta, A., & Bitonti, M. B. (2017). In arabidopsis thaliana cadmium impact on the growth of primary root by altering SCR expression and auxin-cytokinin cross-talk. Frontiers in Plant Science, 8, 1323. https://doi.org/10.3389/fpls.2017.01323.

  • Carstensen, A., Herdean, A., Schmidt, S. B., Sharma, A., Spetea, C., Pribil, M., & Husted, S. (2018). The impacts of phosphorus deficiency on the photosynthetic electron transport chain1. Plant Physiology, 177(1), 271–284. https://doi.org/10.1104/PP.17.01624.

  • Carvalho Bertoli, A., Gabriel Cannata, M., Carvalho, R., Ribeiro Bastos, A.R., Puggina Freitas, M., dos Santos Augusto, A. (2012). Lycopersicon esculentum submitted to Cd-stressful conditions in nutrition solution: Nutrient contents and translocation. Ecotoxicology and Environmental Safety. 86, 176–181. https://doi.org/10.1016/j.ecoenv.2012.09.011.

  • Cetner, M. D., Kalaji, H. M., Borucki, W., & Kowalczyk, K. (2020). Phosphorus deficiency affects the i-step of chlorophyll a fluorescence induction curve of radish. Photosynthetica, 58(SI), 671–681. https://doi.org/10.32615/ps.2020.015.

  • Da˛Browski, P., Baczewska-Dąbrowska, A. H., Kalaji, H. M., Goltsev, V., Paunov, M., Rapacz, M., et al. (2019). Exploration of chlorophyll a fluorescence and plant gas exchange parameters as indicators of drought tolerance in perennial ryegrass. Sensors (Switzerland), 19(12), 2736. https://doi.org/10.3390/s19122736.

  • Dąbrowski, P., Pawluśkiewicz, B., Baczewska, A. H., Oglęcki, P., & Kalaji, H. (2015). Chlorophyll a fluorescence of perennial ryegrass (Lolium perenne L.) varieties under long term exposure to shade. Zemdirbyste-Agriculture, 102, 305. https://doi.org/10.13080/z-a.2015.102.039.

  • Dai, M., Lu, H., Liu, W., Jia, H., Hong, H., Liu, J., Yan, C. (2017). Phosphorus mediation of cadmium stress in two mangrove seedlings Avicennia marina and Kandelia obovata differing in cadmium accumulation. Ecotoxicology and Environmental Safety, 139, 272–279. https://doi.org/10.1016/j.ecoenv.2017.01.017.

  • Das, M., & Maiti, S. K. (2007). Metal accumulation in A. baccifera growing naturally on abandoned copper tailings pond. Environmental Monitoring and Assessment, 127(1–3), 119–125. https://doi.org/10.1007/s10661-006-9265-y.

  • Dias, M.C., Monteiro, C., Moutinho-Pereira, J., Correia, C., Gonçalves, B., Santos, C. (2013). Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta Physiologiae Plantarum, 35, 1281–1289. https://doi.org/10.1007/s11738-012-1167-8.

  • Dong, J., Wu, F.B., Zhang, G.P. (2005). Effect of cadmium on growth and photosynthesis of tomato seedlings. Journal of Zhejiang University. Science, 6, 974–980. https://doi.org/10.1631/jzus.2005.B0974.

  • Dos Santos Utmazian, M. N., & Wenzel, W. W. (2007). Cadmium and zinc accumulation in willow and poplar species grown on polluted soils. Journal of Plant Nutrition and Soil Science, 170(2), 265–272. https://doi.org/10.1002/jpln.200622073.

  • Hasan, S. A., Fariduddin, Q., Ali, B., Hayat, S., & Ahmad, A. (2009). Cadmium: toxicity and tolerance in plants. Journal of Environmental Biology, 30(2), 165–174.https://doi.org/10.1016/c2017-0-02050-5.

  • He, S., Yang, X., He, Z., & Vc, B. (2017). Morphological and physiological responses of plants to cadmium toxicity: a review. Pedosphere, 3, 53–60. https://doi.org/10.1016/S1002-0160(17)60339-4.

  • Hoagland, D R; Arnon, D. I. (1938). Agricultural Experiment Station the Water-Culture Method for Growing Plants Without Soil. California Experiment Station, C347, 1–39.

  • Huang, X. D., Mcconkey, B. J., Babu, T. S., & Greenberg, B. M. (1997). Mechanisms of photoinduced toxicity of photomodified anthracene to plants: Inhibition of photosynthesis in the aquatic higher plant Lemna gibba (duckweed). Environmental Toxicology and Chemistry, 16(8), 1707–1715. https://doi.org/10.1002/etc.5620160819.

  • Huang, B., Xin, J., Dai, H., Liu, A., Zhou, W., Yi, Y., & Liao, K. (2014). Root morphological responses of three hot pepper cultivars to Cd exposure and their correlations with Cd accumulation. Environmental Science and Pollution Research, 22(2), 1151–1159. https://doi.org/10.1007/s11356-014-3405-7.

  • Jiang, H. M., Yang, J. C., & Zhang, J. F. (2007). Effects of external phosphorus on the cell ultrastructure and the chlorophyll content of maize under cadmium and zinc stress. Environmental Pollution, 147(3), 750–756. https://doi.org/10.1016/j.envpol.2006.09.006.

  • Jinadasa, N., Collins, D., Holford, P., Milham, P. J., & Conroy, J. P. (2016). Reactions to cadmium stress in a cadmium-tolerant variety of cabbage (Brassica oleracea L.): is cadmium tolerance necessarily desirable in food crops? Environmental Science and Pollution Research, 23(6), 5296–5306. https://doi.org/10.1007/s11356-015-5779-6.

  • Kalaji, H. M., & Loboda, T. (2007). Photosystem II of Barley seedlings under cadmium and lead stress. Plant, Soil and Environment, 53(12), 511–516. https://doi.org/10.17221/2191-pse.

  • Kalaji, H.M., Jajoo, A., Oukarroum, A., Brestic, M., Zivcak, M., Samborska, I.A., Cetner, M.D., Łukasik, I., Goltsev, V., Ladle, R.J., et al. (2014). The use of chlorophyll fluorescence kinetics analysis to study the performance of photosynthetic machinery in plants. In Emerging Technologies Managing Crop Stress Tolererance, 2, 347–384. https://doi.org/10.1016/B978-0-12-800875-1.00015-6.

  • Kalaji, H. M., Dąbrowski, P., Cetner, M. D., Samborska, I. A., Łukasik, I., Brestic, M., et al. (2017). A comparison between different chlorophyll content meters under nutrient deficiency conditions. Journal of Plant Nutrition, 40(7), 1024–1034. https://doi.org/10.1080/01904167.2016.1263323.

  • Khan, A., Khan, S., Alam, M., Khan, M. A., Aamir, M., Qamar, Z., Rehman, Z. U., & Perveen, S. (2016). Toxic metal interactions affect the bioaccumulation and dietary intake of macro- and micro-nutrients. Chemosphere, 146, 121–128.https://doi.org/10.1016/j.chemosphere.2015.12.014.

  • Loudari, A., Benadis, C., Naciri, R., Soulaimani, A., Zeroual, Y., El Gharous, M., et al. (2020). Salt stress affects mineral nutrition in shoots and roots and chlorophyll a fluorescence of tomato plants grown in hydroponic culture. Journal of Plant Interactions, 15(1), 398–405. https://doi.org/10.1080/17429145.2020.1841842.

  • Malhotra, H., Vandana Sharma, S., Pandey, R. (2018). Phosphorus nutrition: plant growth in response to deficiency and excess. In Plant Nutrients and Abiotic Stress Tolerance, 171–190. https://doi.org/10.1007/978-981-10-9044-8_7.

  • Manikandan, R., Ezhili, N., & Venkatachalam, P. (2016).  Phosphorus Supplementation Alleviation of the Cadmium-Induced Toxicity by Modulating Oxidative Stress Mechanisms in Vetiver Grass [ Chrysopogon zizanioides (L.) Roberty]. Journal of Environmental Engineering, 142(9). https://doi.org/10.1061/(asce)ee.1943-7870.0001112.

  • Nazarian, H., Amouzgar, D., Sedghianzadeh, H. (2016). Effects of different concentrations of cadmium on growth and morphological changes in basil (Ocimum Basilicum L.). Pakistan Journal of Botany, 48(3), 945–952. 

  • Oukarroum, A., Schansker, G., & Strasser, R. J. (2009). Drought stress effects on photosystem i content and photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance. Physiologia Plantarum, 137(2), 188–199. https://doi.org/10.1111/j.1399-3054.2009.01273.x.

  • Pagliano, C., Raviolo, M., Dalla Vecchia, F., Gabbrielli, R., Gonnelli, C., Rascio, N., et al. (2006). Evidence for PSII donor-side damage and photoinhibition induced by cadmium treatment on rice (Oryza sativa L.). Journal of Photochemistry and Photobiology B: Biology, 84(1), 70–78. https://doi.org/10.1016/j.jphotobiol.2006.01.012.

  • Paunov, M., Koleva, L., Vassilev, A., Vangronsveld, J., & Goltsev, V. (2018). Effects of different metals on photosynthesis: cadmium and zinc affect chlorophyll fluorescence in durum wheat. International Journal of Molecular Sciences, 19(3), 787. https://doi.org/10.3390/ijms19030787.

  • Peng, Q., Chen, W., Wu, L., Bai, L. (2017). The uptake, accumulation, and toxic effects of cadmium in barnyardgrass (Echinochloa crus-galli). Polish Journal of Environmental Studies, 26, 779–784. https://doi.org/10.15244/pjoes/65780.

  • Per, T. S., Masood, A., & Khan, N. A. (2017). Nitric oxide improves S-assimilation and GSH production to prevent inhibitory effects of cadmium stress on photosynthesis in mustard (Brassica juncea L.). Nitric Oxide - Biology and Chemistry, 68, 111–124. https://doi.org/10.1016/j.niox.2016.12.012.

  • Przedpelska-Wasowicz, E., Polatajko, A., & Wierzbicka, M. (2012). The influence of cadmium stress on the content of mineral nutrients and metal-binding proteins in arabidopsis halleri. Water, Air, and Soil Pollution, 223, 5445–5458. https://doi.org/10.1007/s11270-012-1292-4.

  • Puła, J., Barabasz-Krasny, B., Lepiarczyk, A., Zandi, P., & Mozdzeń, K. (2019). Activity of the photosynthetic apparatus in Phaseolus vulgaris L. leaves under the cadmium stress. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 47(2), 405–411. https://doi.org/10.15835/nbha47111328.

  • Qiu, Q., Wang, Y., Yang, Z., & Yuan, J. (2011). Effects of phosphorus supplied in soil on subcellular distribution and chemical forms of cadmium in two Chinese flowering cabbage (Brassica parachinensis L.) cultivars differing in cadmium accumulation. Food Chemical Toxicology, 49, 2260-2267. https://doi.org/10.1016/j.fct.2011.06.024.

  • Rizwan, M., Ali, S., Adrees, M., Ibrahim, M., Tsang, D. C. W., Zia-ur-Rehman, M., et al. (2017). A critical review on effects, tolerance mechanisms and management of cadmium in vegetables. Chemosphere, 182, 90–105. https://doi.org/10.1016/j.chemosphere.2017.05.013.

  • Rusinowski, S., Krzyżak, J., Sitko, K., Kalaji, H. M., Jensen, E., & Pogrzeba, M. (2019). Cultivation of C4 perennial energy grasses on heavy metal contaminated arable land: Impact on soil, biomass, and photosynthetic traits. Environmental Pollution, 250, 300–311. https://doi.org/10.1016/j.envpol.2019.04.048.

  • Sajwan, K. S., Paramasivam, S., Richardson, J. P., & Alva, A. K. (2002). Phosphorus alleviation of cadmium phytotoxicity. Journal of Plant Nutrition, 25, 2027–2034. https://doi.org/10.1081/PLN-120013292.

  • Shafi, M., Guoping, Z., Bakht, J., Khan, M. A., Ejaz-Ul-Islam, Khan, M. D., & Raziuddin. (2010). Effect of cadmium and salinity stresses on root morphology of wheat. Pakistan Journal of Botany, 42(4), 2747–2754.

  • Shi, G. L., Zhu, S., Bai, S. N., Xia, Y., Lou, L. Q., & Cai, Q. S. (2015). The transportation and accumulation of arsenic, cadmium, and phosphorus in 12 wheat cultivars and their relationships with each other. Journal of Hazardous Materials, 299, 94–102. https://doi.org/10.1016/j.jhazmat.2015.06.009.

  • Song, X., Yue, X., Chen, W., Jiang, H., Han, Y., & Li, X. (2019). Detection of cadmium risk to the photosynthetic performance of Hybrid pennisetum. Frontiers in Plant Science, 10. https://doi.org/10.3389/fpls.2019.00798.

  • Strasser, R. J., Tsimilli-Michael, M., & Srivastava, A. (2004). Analysis of the Chlorophyll a Fluorescence Transient. In Advances in Photosynthesis and Respiration: Chlorophyll Fluorescence, a Signature of Photosynthesis 321–362. https://doi.org/10.1007/978-1-4020-3218-9_12.

  • Tóth, S.Z., Oukarroum, A., Schansker, G. (2020). Probing the photosynthetic apparatus noninvasively in the laboratory of Reto Strasser in the countryside of Geneva between 2001 and 2009. Photosynthetica, 58(SI), 560–572. https://doi.org/10.32615/ps.2020.003.

  • Tsimilli-Michael, M., & Strasser, R. J. (2008). Experimental Resolution and Theoretical Complexity Determine the Amount of Information Extractable from the Chlorophyll Fluorescence Transient OJIP. In Photosynthesis. Energy from the Sun, 697–701. https://doi.org/10.1007/978-1-4020-6709-9_156.

  • Tsimilli-Michael M, Strasser RJ (2013) The energy flux theory 35 years later: Formulations and applications. Photosynthesis Research, 117, 289–320. https://doi.org/10.1007/s11120-013-9895-1.

  • Tuba, Z., Saxena, D.K., Srivastava, K., Singh, S., Czobel, S., Kalaji, H.M. (2010). Chlorophyll a fluorescence measurements for validating the tolerant bryophytes for heavy metal (Pb) biomapping. Current Science, 98(11), 1505–1508. Retrieved 16 Jan 2020 from http://www.jstor.org/stable/24108223.

  • Van Belleghem, F., Cuypers, A., Semane, B., Smeets, K., Vangronsveld, J., D’Haen, J., Valcke, R. (2007). Subcellular localization of cadmium in roots and leaves of Arabidopsis thaliana. New Phytologist, 173, 495–508. https://doi.org/10.1111/j.1469-8137.2006.01787.x.

  • Yu, Z., Zhou, Q. (2009). Growth responses and cadmium accumulation of Mirabilis jalapa L. under interaction between cadmium and phosphorus. Journal of Hazardous Materials, 167, 38–43. https://doi.org/10.1016/j.jhazmat.2008.12.082.

Download references

Acknowledgements

The authors would like to thank Mohammed VI Polytechnic University (UM6P), especially Plant Stress Physiology Laboratory and Agricultural Innovation and Technology Transfer Center for their valuable support.

Author information

Authors and Affiliations

  1. University Mohammed VI Polytechnic (UM6P), Lot-660 Hay Moulay Rachid, 43150, Ben Guerir, Morocco

    Mohamed Chtouki, Rachida Naciri, Aziz Soulaimani, Youssef Zeroual, Mohamed El Gharous & Abdallah Oukarroum

Authors
  1. Mohamed Chtouki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rachida Naciri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aziz Soulaimani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Youssef Zeroual
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohamed El Gharous
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Abdallah Oukarroum
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to this article, revised the text and results at different stages of the writing process, and read and approved the current manuscript.

Corresponding author

Correspondence to Abdallah Oukarroum.

Ethics declarations

Competing Interests

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

Chtouki, M., Naciri, R., Soulaimani, A. et al. Effect of Cadmium and Phosphorus Interaction on Tomato: Chlorophyll a Fluorescence, Plant Growth, and Cadmium Translocation. Water Air Soil Pollut 232, 84 (2021). https://doi.org/10.1007/s11270-021-05038-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-021-05038-x

Keywords

Search

Navigation