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Cinnamaldehyde Facilitates Cadmium Tolerance by Modulating Ca2+ in Brassica rapa

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Abstract

Exogenous regulation of plant physiology is a kind of effective approach to help plant grow under Cd (cadmium)-contaminated environment. CA (cinnamaldehyde) is an environmental friendly natural compound with medicinal properties and antimicrobial activities. In this work, we found that CA was able to confer plant Cd tolerance by priming defense in the root of B. rapa. Pretreatment with CA attenuated the phytotoxicity induced by subsequent Cd stress, such as root growth inhibition, ROS accumulation, oxidative injury, and cell death in root tip. Cd stress decreased the intracellular Ca2+ level in roots, which could be enhanced by pretreatment with CA. Pretreatment with a Ca2+ chelator or a Ca2+ channel blocker blocked all the beneficial effects of CA on the increase in the intracellular Ca2+ level and the amelioration of physiological injury in roots under Cd stress. Correlation analysis combined with cluster analysis suggested that CA was able to prime plant defense by regulating endogenous Ca2+ in order to facilitate Cd tolerance. These results shed a new light on the novel role of CA in modulating plant resistant physiology against metal stress, which may extend our knowledge on both CA and plant Cd tolerance.

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References

  • Ahmad, P., Sarwat, M., Bhat, N. A., Wani, M. R., Kazi, A. G., & Tran, L.-S. P. (2015). Alleviation of cadmium toxicity in Brassica juncea L. (Czern. & Coss.) by calcium application involves various physiological and biochemical strategies. PLoS One, 10(1), e0114571.

    Google Scholar 

  • Ali, S. M., Khan, A. A., Ahmed, I., Musaddiq, M., Ahmed, K. S., Polasa, H., et al. (2005). Antimicrobial activities of Eugenol and Cinnamaldehyde against the human gastric pathogen Helicobacter pylori. Annals of Clinical Microbiology and Antimicrobials, 4(1), 1–7.

    Google Scholar 

  • Aranega-Bou, P., de la O Leyva, M., Finiti, I., García-Agustín, P., & González-Bosch, C. (2014). Priming of plant resistance by natural compounds. Hexanoic acid as a model. Frontiers in Plant Science, 5, 488.

    Google Scholar 

  • Chmielowska-Bąk, J., Gzyl, J., Rucińska-Sobkowiak, R., Arasimowicz-Jelonek, M., & Deckert, J. (2014). The new insights into cadmium sensing. Frontiers in Plant Science, 5, 245.

    Google Scholar 

  • DalCorso, G., Farinati, S., & Furini, A. (2010). Regulatory networks of cadmium stress in plants. Plant Signaling & Behavior, 5(6), 663–667.

    CAS  Google Scholar 

  • de Hoon, M. J. L., Imoto, S., Nolan, J., & Miyano, S. (2004). Open source clustering software. Bioinformatics, 20(9), 1453–1454.

    Google Scholar 

  • Demidchik, V., Shabala, S., Isayenkov, S., Cuin, T. A., & Pottosin, I. (2018). Calcium transport across plant membranes: Mechanisms and functions. The New Phytologist, 220(1), 49–69.

    CAS  Google Scholar 

  • Dunand, C., Crèvecoeur, M., & Penel, C. (2007). Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: Possible interaction with peroxidases. The New Phytologist, 174(2), 332–341.

    CAS  Google Scholar 

  • Fasani, E., DalCorso, G., Costa, A., Zenoni, S., & Furini, A. (2019). The Arabidopsis thaliana transcription factor MYB59 regulates calcium signalling during plant growth and stress response. Plant Molecular Biology, 99(6), 517–534.

    CAS  Google Scholar 

  • Foreman, J., Demidchik, V., Bothwell, J. H., Mylona, P., Miedema, H., Torres, M. A., et al. (2003). Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature, 422(6930), 442–446.

    CAS  Google Scholar 

  • Fu, S., Li, L., Kang, H., Yang, X., Men, S., & Shen, Y. (2017). Chronic mitochondrial calcium elevation suppresses leaf senescence. Biochemical and Biophysical Research Communications, 487(3), 672–677.

    CAS  Google Scholar 

  • Han, Y., Zhang, J., Chen, X., Gao, Z., Xuan, W., Xu, S., et al. (2008). Carbon monoxide alleviates cadmium-induced oxidative damage by modulating glutathione metabolism in the roots of Medicago sativa. The New Phytologist, 177(1), 155–166.

    CAS  Google Scholar 

  • Hu, L., Li, H., Huang, S., Wang, C., Sun, W. J., Mo, H. Z., et al. (2018). Eugenol confers cadmium tolerance via intensifying endogenous hydrogen sulfide signaling in Brassica rapa. Journal of Agricultural and Food Chemistry, 66(38), 9914–9922.

    CAS  Google Scholar 

  • Hu, L., Wang, D., Liu, L., Chen, J., Xue, Y., & Shi, Z. (2013). Ca2+ efflux is involved in cinnamaldehyde-induced growth inhibition of Phytophthora capsici. PLoS One, 8(10), e76264.

    CAS  Google Scholar 

  • Huang, D., Gong, X., Liu, Y., Zeng, G., Lai, C., Bashir, H., et al. (2017). Effects of calcium at toxic concentrations of cadmium in plants. Planta, 245(5), 863–873.

    CAS  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(2), 255–277.

    CAS  Google Scholar 

  • Kang, L.-L., Zhang, D.-M., Ma, C.-H., Zhang, J.-H., Jia, K.-K., Liu, J.-H., et al. (2016). Cinnamaldehyde and allopurinol reduce fructose-induced cardiac inflammation and fibrosis by attenuating CD36-mediated TLR4/6-IRAK4/1 signaling to suppress NLRP3 inflammasome activation. Scientific Reports, 6, 27460. https://doi.org/10.21038/srep27460.

    Article  CAS  Google Scholar 

  • Leitão, N., Dangeville, P., Carter, R., & Charpentier, M. (2019). Nuclear calcium signatures are associated with root development. Nature Communications, 10(1), 4865.

    Google Scholar 

  • Li, P., Zhao, C., Zhang, Y., Wang, X., Wang, J., Wang, F., et al. (2016). Calcium alleviates cadmium-induced inhibition on root growth by maintaining auxin homeostasis in Arabidopsis seedlings. Protoplasma, 253(1), 185–200.

    CAS  Google Scholar 

  • Li, Y. J., Chen, J., Xian, M., Zhou, L. G., Han, F. X., Gan, L. J., et al. (2014). In site bioimaging of hydrogen sulfide uncovers its pivotal role in regulating nitric oxide-induced lateral root formation. PLoS One, 9(2), e90340.

    Google Scholar 

  • Liu, Y. Y., Wang, R. L., Zhang, P., Sun, L. L., & Xu, J. (2016). Involvement of reactive oxygen species in lanthanum-induced inhibition of primary root growth. Journal of Experimental Botany, 67(21), 6149–6159.

    CAS  Google Scholar 

  • Lv, C., Yuan, X., Zeng, H. W., Liu, R. H., & Zhang, W. D. (2017). Protective effect of cinnamaldehyde against glutamate-induced oxidative stress and apoptosis in PC12 cells. European Journal of Pharmacology, 815, 487–494.

    CAS  Google Scholar 

  • Mathavarajah, S., Salsman, J., & Dellaire, G. (2019). An emerging role for calcium signalling in innate and autoimmunity via the cGAS-STING axis. Cytokine & Growth Factor Reviews, 50, 43–51.

    CAS  Google Scholar 

  • Meena, V., Sree, S. N., Surya, P. D. V., & Sumanjali, A. (2012). A review on pharmacological activities and clinical effects of Cinnamon species. Research Journal of Pharmaceutical, Biological and Chemical Sciences, 3, 653–663.

    Google Scholar 

  • Mostofa, M. G., Rahman, A., Ansary, M. M. U., Watanabe, A., Fujita, M., & Tran, L.-S. P. (2015). Hydrogen sulfide modulates cadmium-induced physiological and biochemical responses to alleviate cadmium toxicity in rice. Scientific Reports, 5, 14078.

    Google Scholar 

  • Pérez-Chaca, M. V., RodrÍGuez-Serrano, M., Molina, A. S., Pedranzani, H. E., Zirulnik, F., Sandalio, L. M., et al. (2014). Cadmium induces two waves of reactive oxygen species in Glycine max (L.) roots. Plant, Cell & Environment, 37(7), 1672–1687.

    Google Scholar 

  • Perilli, S., Di Mambro, R., & Sabatini, S. (2012). Growth and development of the root apical meristem. Current Opinion in Plant Biology, 15(1), 17–23.

    CAS  Google Scholar 

  • Pires, P. W., & Earley, S. (2018). Neuroprotective effects of TRPA1 channels in the cerebral endothelium following ischemic stroke. eLife, 7, e35316.

    Google Scholar 

  • Qadir, S., Jamshieed, S., Rasool, S., Ashraf, M., Akram, N. A., & Ahmad, P. (2014). Modulation of plant growth and metabolism in cadmium-enriched environments. Reviews of Environmental Contamination and Toxicology, 229, 51–88.

    CAS  Google Scholar 

  • Raffai, G., Kim, B., Park, S., Khang, G., Lee, D., & Vanhoutte, P. M. (2014). Cinnamaldehyde and cinnamaldehyde-containing micelles induce relaxation of isolated porcine coronary arteries: Role of nitric oxide and calcium. International Journal of Nanomedicine, 9, 2557–2566.

    Google Scholar 

  • Ranasinghe, P., Pigera, S., Premakumara, G. S., Galappaththy, P., Constantine, G. R., & Katulanda, P. (2013). Medicinal properties of ‘true’ cinnamon (Cinnamomum zeylanicum): A systematic review. BMC Complementary and Alternative Medicine, 13, 275. https://doi.org/10.1186/1472-6882-1113-1275.

    Article  Google Scholar 

  • Rodríguez-Serrano, M., Romero-Puertas, M. C., Pazmiño, D. M., Testillano, P. S., Risueño, M. C., Del Río, L. A., et al. (2009). Cellular response of pea plants to cadmium toxicity: Cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiology, 150, 229–243.

    Google Scholar 

  • Saijo, Y., & Loo, E. P. (2020). Plant immunity in signal integration between biotic and abiotic stress responses. The New Phytologist, 225(1), 87–104.

    Google Scholar 

  • Shi, H., Ye, T., & Chan, Z. (2014). Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiology and Biochemistry, 74, 99–107.

    CAS  Google Scholar 

  • Siddiqui, M. H., Al-Whaibi, M. H., Sakran, A. M., Basalah, M. O., & Ali, H. M. (2012). Effect of calcium and potassium on antioxidant system of Vicia faba L. under cadmium stress. International Journal of Molecular Sciences, 13(6), 6604–6619.

    CAS  Google Scholar 

  • Subash-Babu, P., Alshatwi, A. A., & Ignacimuthu, S. (2014). Beneficial antioxidative and antiperoxidative effect of cinnamaldehyde protect streptozotocin-induced pancreatic β-cells damage in wistar rats. Biomolecules & Therapeutics, 22(1), 47–54.

    CAS  Google Scholar 

  • Thor, K. (2019). Calcium-nutrient and messenger. Frontiers in Plant Science, 10, 440.

    Google Scholar 

  • Wang, D., Hou, J., Yang, Y., Zhou, P., Liu, S., Wan, J., et al. (2019). Cinnamaldehyde ameliorates high-glucose-induced oxidative stress and cardiomyocyte injury through transient receptor potential ankyrin 1. Journal of Cardiovascular Pharmacology, 74(1), 30–37.

    CAS  Google Scholar 

  • Wang, Y. S., & Yang, Z. M. (2005). Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant & Cell Physiology, 46(12), 1915–1923.

    CAS  Google Scholar 

  • Wen, J., Deng, M., & Gong, M. (2012). Cd2+ stress induces two waves of H2O2 accumulation associated with ROS-generating system and ROS-scavenging system in cultured tobacco cells. Australian Journal of Crop Science, 6, 846–853.

    CAS  Google Scholar 

  • Wu, Z., Weng, S., Yan, D., Xie, Z., Zhou, Q., Li, H., et al. (2018). Administration of cinnamaldehyde promotes osteogenesis in ovariectomized rats and differentiation of osteoblast in vitro. Journal of Pharmacological Sciences, 138(1), 63–70.

    CAS  Google Scholar 

  • Xu, J., Zhu, Y., Ge, Q., Li, Y., Sun, J., Zhang, Y., et al. (2012). Comparative physiological responses of Solanum nigrum and Solanum torvum to cadmium stress. The New Phytologist, 196(1), 125–138.

    CAS  Google Scholar 

  • Xue, Y. F., Zhang, M., Qi, Z. Q., Li, Y. Q., Shi, Z., & Chen, J. (2015). Cinnamaldehyde promotes root branching by regulating endogenous hydrogen sulfide. Journal of the Science of Food and Agriculture, 96(3), 909–914.

    Google Scholar 

  • Yamamoto, Y., Kobayashi, Y., Devi, S. R., Rikiishi, S., & Matsumoto, H. (2002). Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiology, 128(1), 63–72.

    CAS  Google Scholar 

  • Yamamoto, Y., Kobayashi, Y., & Matsumoto, H. (2001). Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiology, 125(1), 199–208.

    CAS  Google Scholar 

  • Yang, C.-M., & Juang, K.-W. (2015). Alleviation effects of calcium and potassium on cadmium rhizotoxicity and absorption by soybean and wheat roots. Journal of Plant Nutrition and Soil Science, 178(5), 748–754.

    CAS  Google Scholar 

  • Ye, X., Ling, T., Xue, Y., Xu, C., Zhou, W., Hu, L., et al. (2016). Thymol mitigates cadmium stress by regulating glutathione levels and reactive oxygen species homeostasis in tobacco seedlings. Molecules, 21(10), 1339.

    Google Scholar 

  • Youn, H. S., Lee, J. K., Choi, Y. J., Saitoh, S. I., Miyake, K., Hwang, D. H., et al. (2008). Cinnamaldehyde suppresses toll-like receptor 4 activation mediated through the inhibition of receptor oligomerization. Biochemical Pharmacology, 75(2), 494–502.

    CAS  Google Scholar 

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Acknowledgments

We thank Mr. Cunfa Xu from Central Laboratory, Jiangsu Academy of Agricultural Sciences, for his technical support during stereoscopic microscope study.

Funding

This study was supported by the National Natural Science Foundation of China (31771705), Jiangsu Agricultural Science and Technology Innovation Fund (CX(20)1011), and Program for Tackling Key Problems in Science and Technology of Henan Province (202102110046).

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Author notes

  1. Yanwei Cheng and Ning Wang contributed equally to this work.

Authors and Affiliations

  1. College of Life Science, Luoyang Normal University, Luoyang, 471934, China

    Yanwei Cheng

  2. Central Laboratory, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China

    Ning Wang

  3. Institute of Industrial Crops, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China

    Ruixian Liu

  4. Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, 50 Zhongling Street, Nanjing, 210014, China

    Hongwu Bai, Jian Chen & Zhiqi Shi

  5. Grain and Oil Monitor Institute of Huaian, Huaian, 223001, China

    Weichun Tao

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  1. Yanwei Cheng
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Cheng, Y., Wang, N., Liu, R. et al. Cinnamaldehyde Facilitates Cadmium Tolerance by Modulating Ca2+ in Brassica rapa. Water Air Soil Pollut 232, 19 (2021). https://doi.org/10.1007/s11270-020-04952-w

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