Efecto del cadmio en el contenido de pigmentos fotosintéticos, estructura de la raíz, y concentración de nutrientes en plantas de frijol (Phaseolus vulgaris L.)

Paulina Beatriz  Gutiérrez-Martínez; Blanca Catalina  Ramírez-Hernández; Marcela Mariel  Maldonado-Villegas

doi:10.17268/sci.agropecu.2024.035

Authors

Paulina Beatriz Gutiérrez-Martínez Universidad de Guadalajara, Centro Universitario de Ciencias Biológicas y Agropecuarias, Zapopan, Jalisco, México. https://orcid.org/0000-0002-3684-0576
Blanca Catalina Ramírez-Hernández Universidad de Guadalajara, Centro Universitario de Ciencias Biológicas y Agropecuarias, Zapopan, Jalisco, México. https://orcid.org/0000-0002-0576-8997
Marcela Mariel Maldonado-Villegas Universidad de Guadalajara, Centro Universitario de Ciencias Biológicas y Agropecuarias, Zapopan, Jalisco, México. https://orcid.org/0000-0002-0483-6951

DOI:

https://doi.org/10.17268/sci.agropecu.2024.035

Keywords:

toxicity, tissues, photosynthesis, heavy metals, synergism, antagonism

Abstract

Cadmium (Cd) is a contaminant that causes significant damage to organisms. In plants, it results in growth delay, alters photosynthetic function, and affects nutrient concentrations. This study aimed to evaluate the impact of Cd (0, 0,25, 0,50, and 1 µM) on chlorophyll content, structural damage to the root, and the absorption and translocation of nutrients (Ca, K, Mg, Mn, Fe, and Zn) in Phaseolus vulgaris var. Opus plants. An increase in chlorophyll a was observed at Cd concentrations of 0.25 and 1 µM. Chlorophyll b increased across all Cd treatments, while carotenoid content decreased in all treatments. The roots exhibited structural damage as Cd concentrations increased. For nutrients, Ca, Mg, Mn, and Zn in leaves, and K in stems, increased with higher Cd doses. Conversely, K in roots decreased with higher Cd concentrations, and Fe decreased compared to the control in all evaluated organs. Our results suggest that Cd stress at low concentrations stimulates chlorophyll synthesis and that varying Cd concentrations induce synergistic and antagonistic effects in different organs of P. vulgaris, leading to nutritional disorders. Given the global importance of this crop, studying the molecular mechanisms and membrane transporters in P. vulgaris roots exposed to Cd is crucial for enhancing its resistance to Cd.

References

An, T., Kuang, Q., Wu, Y., Gao, Y., Zhang, Y., Mickan, B. S., Xu, B., Zhang, S., Deng, X., Yu, M., & Chen, Y. (2023). Variability in cadmium stress tolerance among four maize genotypes: Impacts on plant physiology, root morphology, and chloroplast microstructure. Plant Physiology and Biochemistry, 205, 108135. https://doi.org/10.1016/j.plaphy.2023.108135

Arnon, D. I. (1949). Copper Enzymes in Isolated Chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology, 24(1), 1-15. https://doi.org/10.1104%2Fpp.24.1.1

Azizollahi, Z., Ghaderian, S. M., & Ghotbi-Ravandi, A. A. (2019). Cadmium accumulation and its effects on physiological and biochemical characters of summer savory (Satureja hortensis L.). International Journal of Phytoremediation, 21(12), 1241-1253. https://doi.org/10.1080/15226514.2019.1619163

Bankaji, I., Caçador, I., & Sleimi, N. (2015). Physiological and biochemical responses of Suaeda fruticosa to cadmium and copper stresses: growth, nutrient uptake, antioxidant enzymes, phytochelatin, and glutathione levels. Environmental Science and Pollution Research, 22, 13058-13069. https://doi.org/10.1007/s11356-015-4414-x

Baruah, N., Gogoi, N., Roy, S., Bora, P., Chetia, J., Zahra, N., Ali, N., Gogoi, P., & Farooq, M. (2023). Phytotoxic Responses and Plant Tolerance Mechanisms to Cadmium Toxicity. Journal of Soil Science and Plant Nutrition, 23, 4805-4826. https://doi.org/10.1007/s42729-023-01525-8

Bingham, F. T., Sposito, G., & Strong, J. E. (1984). The effect of chloride on the availability of cadmium. Journal of Environmental Quality, 13(1), 71-74. https://doi.org/10.2134/jeq1984.00472425001300010013x

Bora, M. S. & Sarma, K. P. (2021). Anatomical and ultrastructural alterations in Ceratopteris pteridoides under cadmium stress: A mechanism of cadmium tolerance. Ecotoxicology and Environmental Safety, 218, 112285. https://doi.org/10.1016/j.ecoenv.2021.112285

Borges, K. L. R., Hippler, F. W. R., Carvalho, M. E. A., Nalin, R. S., Matias, F. I. & Azevedo, R. A. (2019). Nutritional status and root morphology of tomato under Cd-induced stress: Comparing contrasting genotypes for metal-tolerance. Scientia Horticulturae, 246, 518-527. https://doi.org/10.1016/j.scienta.2018.11.023

Carvalho, M. E. A., Castro, P. R. C., & Azevedo, R. A. (2020). Hormesis in plants under Cd exposure: From toxic to beneficial element?. Journal of Hazardous Materials, 384, 121434. https://doi.org/10.1016/j.jhazmat.2019.121434

Chaoui, A., Ghorbal, M. H., & El Ferjani, E. (1997). Effects of cadmium-zinc interactions on hydroponically grown bean (Phaseolus vulgaris L.). Plant Science, 126, 21-28. https://doi.org/10.1016/S0168-9452(97)00090-3

Chen, F., Dong, J., Wang, F., Wu, F., Zhang, G., Li, G., Chen, Z., Chen, J., & Wei, K. (2007). Identification of barley genotypes with low grain Cd accumulation and its interaction with four microelements. Chemosphere, 67(10), 2082–2088. https://doi.org/10.1016/j.chemosphere.2006.10.014

Chen, X., Tao, H., Wu, Y., & Xu, X. (2022). Effects of Cadmium on metabolism of photosynthetic pigment and photosynthetic system in Lactuca sativa L. revealed by physiological and proteomics analysis. Scientia Horticulturae, 305, 111371. https://doi.org/10.1016/j.scienta.2022.111371

Cherif, J., Mediouni, C., Ammar, W. ben, & Jemal, F. (2011). Interactions of zinc and cadmium toxicity in their effects on growth and in antioxidative systems in tomato plants (Solarium lycopersicum). Journal of Environmental Sciences, 23(5), 837-844. https://doi.org/10.1016/S1001-0742(10)60415-9

Cocozza, C., Minnocci, A., Tognetti, R., Iori, V., Zacchini, M., Scarascia Mugnozza, G. (2008). Distribution and concentration of cadmium in root tissue of Populus alba determined by scanning electron microscopy and energy-dispersive x-ray microanalysis. iForest 1, 96-103.

Dong, Q., Hu, S., Fei, L., Liu, L., & Wang, Z. (2019). Interaction between Cd and Zn on Metal Accumulation, Translocation and Mineral Nutrition in Tall Fescue (Festuca arundinacea). International Journal of Molecular Sciences, 20(13), 3332. https://doi.org/10.3390/ijms20133332

Dražić, G., Mihailović, N., & Stojanović, Z. (2004). Cadmium Toxicity: The effect on Macro- and Micro-Nutrient Contents in Soybean Seedlings. Biologia Plantarum, 48, 605-607. https://doi.org/10.1023/B:BIOP.0000047160.79306.b7

Escalante Estrada, J. & Kohashi Shibata, J. (1993). El rendimiento y crecimiento del frijol: manual para la toma de datos. Colegio de Postgraduados. Montecillo, Texcoco. México.

Feng, D., Wang, R., Sun, X., Liu, L., Liu, P., Tang, J., Zhang, C., & Liu, H. (2023). Heavy metal stress in plants: Ways to alleviate with exogenous substances. The Science Of The Total Environment, 897, 165397. https://doi.org/10.1016/j.scitotenv.2023.165397

Franić, M., Galić, V., Mazur, M., & Šimić, D. (2018). Effects of excess cadmium in soil on JIP-test parameters, hydrogen peroxide content and antioxidant activity in two maize inbreds and their hybrid. Photosynthetica, 56(2), 660-669. https://doi.org/10.1007/s11099-017-0710-7

Gonçalvesa, J. F., Antes, F. G., Maldaner, J., Pereira, L. B., Tabaldi, L. A., Rauber, R., Rossato, L. V., Bisognin, D. A., Dressler, V. L., De Moraes Flores, É. M., & Nicoloso, F. T. (2009). Cadmium and mineral nutrient accumulation in potato plantlets grown under cadmium stress in two different experimental culture conditions. Plant Physiology and Biochemistry, 47(9), 814-821. https://doi.org/10.1016/j.plaphy.2009.04.002

Gonçalvesb, J. F., Nicoloso, F. T., Becker, A. G., Pereira, L. B., Tabaldi, L. A., Cargnelutti, D., De Pelegrin, C. M. G., Dressler, V. L., Da Rocha, J. B. T., & Schetinger, M. R. C. (2009). Photosynthetic pigments content, δ-aminolevulinic acid dehydratase and acid phosphatase activities and mineral nutrients concentration in cadmium-exposed Cucumis sativus L. Biologia, 64, 310-318. https://doi.org/10.2478/s11756-009-0034-6

Goswami, V., Deepika, S., Diwakar, S. & Kothamasi, D. (2023). Arbuscular mycorrhizas amplify the risk of heavy metal transfer to human food chain from fly ash ameliorated agricultural soils. Environmental Pollution, 329, 121733. https://doi.org/10.1016/j.envpol.2023.121733

Goyal, D., Yadav, A., Prasad, M., Singh, T. B., Shrivastav, P., Ali, A., Dantu, P. K. & Mishra, S. Naeem, M., Ansari, A., Gill, S. (Eds). (2020). Effect of Heavy Metals on Plant Growth: An Overview. En: Contaminants in Agriculture. Springer, Cham. https://doi.org/10.1007/978-3-030-41552-5_4

Haider, F. U., Liqun, C., Coulter, J. A., Cheema, S. A., Wu, J., Zhang, R., … Farroq, M. (2021). Cadmium toxicity in plants: Impacts and remediation strategies. Ecotoxicology and Environmental Safety, 211, 111887. https://doi.org/10.1016/j.ecoenv.2020.111887

Hédiji, H., Djebali, W., Belkadhi, A., Cabasson, C., Moing, A., Rolin D., … Chaïbi, W. (2015). Impact of long-term cadmium exposure on mineral content of Solanum lycopersicum plants: Consequences on fruit production. South African Journal of Botany, 97, 176-181. https://doi.org/10.1016/j.sajb.2015.01.010

Huang, X., Duan, S., Wu, Q., Yu, M. & Shabala, S. (2020). Reducing Cadmium Accumulation in Plants: Structure–Function Relations and Tissue-Specific Operation of Transporters in the Spotlight. Plants, 9(2), 223. https://doi.org/10.3390/plants9020223

Huang, Y., Chen, J., Sun, Y., Wang, H., Zhan, J., Huang, Y., Zou, J., Wang, L., Su, N., & Cui, J. (2022). Mechanisms of calcium sulfate in alleviating cadmium toxicity and accumulation in pak choi seedlings. Science of The Total Environment, 805, 150115. https://doi.org/10.1016/j.scitotenv.2021.150115

Huybrechts, M., Hendrix, S., Kyndt, T., Demeestere, K., Vandamme, D. & Cypers, A. (2021). Short-term effects of cadmium on leaf growth and nutrient transport in rice plants. Plant Science, 313, 111054. https://doi.org/10.1016/j.plantsci.2021.111054

Javad, S., Maqsood, S., Shah, A. A., Singh, A., Shah, A. N., Nawaz, M., Bashir, M. A., Nashar, E. M., Alghamdi, M. A., FEl-Kott, A., & Mosa, W. F. (2023). Iron nanoparticles mitigates cadmium toxicity in Triticum aestivum; Modulation of antioxidative defense system and physiochemical characteristics. Journal of King Saud University - Science, 35(3). https://doi.org/10.1016/j.jksus.2022.102498

Jiang, Y., Wei, C., Jiao, Q., Li, G., Alyemeni, M. N., Ahmad, P., Shah, T., Fahad, S., Zhang, J., Zhao, Y., Liu, F., Liu, S., & Liu, H. (2023). Interactive effect of silicon and zinc on cadmium toxicity alleviation in wheat plants. Journal of Hazardous Materials, 458, 131933. https://doi.org/10.1016/j.jhazmat.2023.131933

Kaleem, M., Shabir, F., Hussain, I., Hameed, M., Ahmad, M. S. A., Mehmood, A., Ashfaq, W., Riaz, S., Afzaal, Z., Maqsood, M. F., Iqbal, U., Shah, S. M. R., & Irshad, M. (2022). Alleviation of cadmium toxicity in Zea mays L. through up-regulation of growth, antioxidant defense system and organic osmolytes under calcium supplementation. PLoS ONE 17(6): e0269162. https://doi.org/10.1371/journal.pone.0269162

Kaushik, S., Ranjan, A., Sidhu, A., Singh, A. K. & Sirhindi, G. (2024). Cadmium toxicity: its’ uptake and retaliation by plant defence system and ja signaling. BioMetals, https://doi.org/10.1007/s10534-023-00569-8

Kisa, D., Öztürk, L. & Tekin, S. (2016). Gene expression analysis of metallothionein and mineral elements uptake in tomato (Solanum lycopersicum) exposed to cadmium. Journal of Plant Research, 129, 989-995. https://doi.org/10.1007/s10265-016-0847-7

Kovács, K., Kuzmann, E., Vértes, A., Lévai, L., Cseh, E. & Fodor, F. (2010). Effect of cadmium on iron uptake in cucumber roots: A Mössbauer-spectroscopic study. Plant and Soil 327, 49-56. https://doi.org/10.1007/s11104-009-0030-1

Lin, L., Wu, X., Deng, X., Lin, Z., Liu, C., Zhang, J., He, T., Yi, Y., Liu, H., Wang, Y., Sun, W., & Xu, Z. (2023). Mechanisms of low cadmium accumulation in crops: A comprehensive overview from rhizosphere soil to edible parts. Environmental Research, 245, 118054. https://doi.org/10.1016/j.envres.2023.118054

Liu, L., Shang, Y. K., Li, L., Chen, Y. H., Qin, Z. Z., Zhou, L. J., Yuan, M., Ding, C. B., Liu, J., Huang, Y., Yang, R. W., Zhou, Y. H., & Liao, J. Q. (2018). Cadmium stress in Dongying wild soybean seedlings: growth, Cd accumulation, and photosynthesis. Photosynthetica, 56(4), 1346-1352. https://doi.org/10.1007/s11099-018-0844-2

Mengel, K. & Kirkby. E. (2000). Principios de Nutrición Vegetal. Basilea: Instituto Internacional de la Potasa 1ra. Edición en español.

Mubeen, S., Ni, W., He, C. & Yang, Z. (2023). Agricultural Strategies to Reduce Cadmium Accumulation in Crops for Food Safety. Agriculture, 13(2), 471. https://doi.org/10.3390/agriculture13020471

Osmolovskaya, N. G., Dung, V. V., Kudryashova, Z. K., Kuchaeva, L. N. & Popova, N. F. (2018). Effect of Cadmium on Distribution of Potassium, Calcium, Magnesium, and Oxalate Accumulation in Amaranthus cruentus L. Plants. Russian Journal of Plant Physiology, 65, 553-562. https://doi.org/10.1134/S1021443718040076

Qin, S., Liu, H., Nie, Z., Rengel, Z., Gao, W., Li, C. & Zhao, P. (2020). Toxicity of cadmium and its competition with mineral nutrients for uptake by plants: A review. Pedosphere, 30(2), 168-180. https://doi.org/10.1016/S1002-0160(20)60002-9

Rabêlo, F.H.S., dos Santos, F.H., Lavres, J & Alleoni, L.R.F. (2022). Changes in Tillering, Nutritional Status and Biomass Yield of Panicum maximum Used for Cadmium Phytoextraction. Water Air Soil Pollution 233, 214. https://doi.org/10.1007/s11270-022-05687-6

Rivetta, A., Pesenti, M., Sacchi, G. A., Nocito, F. F. & Cocucci, M. (2023). Cadmium Transport in Maize Root Segments Using a Classical Physiological Approach: Evidence of Influx Largely Exceeding Efflux in Subapical Regions. Plants, 12(5), 992. https://doi.org/10.3390/plants12050992

Rodríguez Ortiz, J. C., Valdez Cepeda, R. D., Alcalá Jáuregui J. J. A., García Hernández, L., Rodríguez Fuentes, H., Tapia Goné, J. J., Pérez Moreno, J. A. & Woo Reza, J. L. (2009). Relaciones entre Cd, Pb y elementos esenciales en el proceso de fitoacumulación en Nicotiana tabacum L. Revista Latinoamericana de Recursos Naturales, 5(3): 205-211.

Saleem, M. H., Parveen, A., Perveen, S., Akhtar, N., Abasi, F., Ehsan, M., Ali, H., Okla, M. K., Saleh, I. A., Zomot, N., Alwasel, Y. A., Abdel-Maksoud, M. A., & Fahad, S. (2023). Alleviation of cadmium toxicity in pea (Pisum sativum L.) through Zn−Lys supplementation and its effects on growth and antioxidant defense. Environmental Science and Pollution Research, https://doi.org/10.1007/s11356-024-31874-5

Sana, S., Ramzan, M., Ejaz, S., Danish, S., Salmen, S. H., & Ansari, M. J. (2024). Differential responses of chili varieties grown under cadmium stress. BMC Plant Biology, 24(1). https://doi.org/10.1186/s12870-023-04678-x

Sardar, R., Ahmed, S., Shah, A. A., & Yasin, N. A. (2022). Selenium nanoparticles reduced cadmium uptake, regulated nutritional homeostasis and antioxidative system in Coriandrum sativum grown in cadmium toxic conditions. Chemosphere, 287. https://doi.org/10.1016/j.chemosphere.2021.132332

Sasaki, A., Yamaji, N., Yokosho, K., & Ma, J. F. (2012). Nramp5 Is a Major Transporter Responsible for Manganese and Cadmium Uptake in Rice. Plant Cell, 24(5), 2155-67. https://doi.org/10.1105/tpc.112.096925

Schmidt, É C., Scariot, L. A., Rover, T., & Bouzon, Z. L. (2009). Changes in ultrastructure and histochemistry of two red macroalgae strains of Kappaphycus alvarezii (Rhodophyta, Gigartinales), as a consequence of ultraviolet B radiation exposure. Micron, 40(8), 860-869. https://doi.org/10.1016/j.micron.2009.06.003

Shah, K., Mankad, A., Reddy, M., & Kuntal Shah, C. (2017). Cadmium accumulation and its effects on growth and biochemical parameters in Tagetes erecta L. Journal of Pharmacognosy and Phytochemistry, 6(3).

Sperdouli, I., Adamakis, I.-D., Dobrikova, A., Apostolova, E., Hanć, A., & Moustakas, M. (2022). Excess Zinc Supply Reduces Cadmium Uptake and Mitigates Cadmium Toxicity Effects on Chloroplast Structure, Oxidative Stress, and Photosystem II Photochemical Efficiency in Salvia sclarea Plants. Toxics, 10(1), 36. https://doi.org/10.3390/toxics10010036

Sun, C., Liang, X., Gong, X., Chen, H., Liu, X., Zhang, S., Li, F., Zhao, J., & Yi, J. (2022). Comparative transcriptomics provide new insights into the mechanisms by which foliar silicon alleviates the effects of cadmium exposure in rice. Journal of Environmental Sciences, 115, 294-307. https://doi.org/10.1016/j.jes.2021.07.030

Sun, H., Wang, X., Shang, Li., Zhou, Z & Wang, R. (2017). Cadmium accumulation and its effects on nutrient uptake and photosynthetic performance in cucumber (Cucumis sativus L.). https://www.researchgate.net/publication/320735530.

Swedlund, P. J., Webster, J. G. & Miskelly G. M. (2003). The effect of SO4 on the ferrihydrite adsorption of Co, Pb and Cd: ternary complexes and site heterogeneity. Applied Geochemistry, 18(11), 1617-1689. https://doi.org/10.1016/S0883-2927(03)00082-9

Taiz, L. & Zeiger, E. (2010). Fisiología vegetal. Quinta edición, Sinauer Associates Inc., Sunderland, 782 p.

Tang, L., Xiao, L., Chen, E., Lei, X., Ren, J., Yang, Y., Xiao, B., & Gong, C. (2023). Magnesium transporter CsMGT10 of tea plants plays a key role in chlorosis leaf vein greening. Plant Physiology and Biochemistry, 201, 107842. https://doi.org/10.1016/j.plaphy.2023.107842

Ukai, Y., Taoka, H., Kamada, M., Wakui, Y., Goto, F., Kitazaki, K., Abe, T., Hokura, A., Yoshihara, T., & Shimada, H. (2023). The cadmium-hypertolerant fern, Athyrium yokoscense, exhibits two cadmium stress mitigation strategies in the roots and the aerial parts. bioRxiv, 12, 06, 570362. https://doi.org/10.1101/2023.12.06.570362

Wang, K., Fu, G., Yu, Y., Wan, Y., Liu, Z., Wang, Q., Zhang, J., & Li, H. (2019). Effects of different potassium fertilizers on cadmium uptake by three crops. Environmental Science and Pollution Research, 26, 27014-27022. https://doi.org/10.1007/s11356-019-05930-4

Wang, T., Chen, X., Ju, C. & Wang, C. (2023). Calcium signaling in plant mineral nutrition: From uptake to transport. Plant Communications, 4(6), 100678. https://doi.org/10.1016/j.xplc.2023.100678

Wang, Y., Wang, X., Wang, C., Peng, F., Wang, R., Xiao, X., Zeng, J., Kang, H., Fan, X., Sha, L., Zhang, H., & Zhou, Y. (2017). Transcriptomic profiles reveal the interactions of Cd/Zn in dwarf polish wheat (Triticum polonicum L.) roots. Frontiers in Physiology, 8. https://doi.org/10.3389/fphys.2017.00168

Wu, Q., Zhu, X., Zhao, X. & Shen, R. (2020). Potassium affects cadmium resistance in Arabidopsis through facilitating root cell wall Cd retention in a nitric oxide dependent manner. Environmental and Experimental Botany, 178, 104175. https://doi.org/10.1016/j.envexpbot.2020.104175

Xu, Y., Gui, Y., Zhi, D., Pi, J., Liu, X., Xiang, J., Li, D., & Li, J. (2023). Protective effects of calcium against cadmium-induced toxicity in juvenile grass carp (Ctenopharyngodon idellus). Ecotoxicology and Environmental Safety, 258, 114972. https://doi.org/10.1016/j.ecoenv.2023.114972

Xu, Y., Tang, H., Liu, T., Li, Y., Huang, X. & Pi, J. (2018). Effects of long-term fertilization practices on heavy metal cadmium accumulation in the surface soil and rice plants of double-cropping rice system in Southern China. Environmental Science and Pollution Research, 25, 19836-19844. https://doi.org/10.1007/s11356-018-2175-z

Yang, L., Kang, Y., Li, N., Wang, Y., Mou, H., Sun, H., Ao, T., Chen, L., & Chen, W. (2024). Unlocking hormesis and toxic effects induced by cadmium in Polygonatum cyrtonema Hua based on morphology, physiology and metabolomics. Journal of Hazardous Materials, 465, 133447. https://doi.org/10.1016/j.jhazmat.2024.133447

Yerlikaya Anli, R., Akşahin, V., Dündar, Ş. & Ahmet, N. A. S. E. (2022). Cadmium pollution impairs maize growth and uptake of cationic essential nutrients. ISPEC Journal of Agricultural Sciences, 6(1), 144–153. https://doi.org/10.46291/ISPECJASvol6iss1pp144-153

Zaid, A., Mohammad, F. & Fariduddin, Q. (2020). Plant growth regulators improve growth, photosynthesis, mineral nutrient and antioxidant system under cadmium stress in menthol mint (Mentha arvensis L.). Physiology and Molecular Biology of Plants, 26, 25-39. https://doi.org/10.1007/s12298-019-00715-y

Zhang, Q., Wen, Q., Ma, T., Zhu, Q., Huang, D., Zhu, H., Xu, C., & Chen, H. (2023). Cadmium-induced iron deficiency is a compromise strategy to reduce Cd uptake in rice. Environmental and Experimental Botany, 206, 105155. https://doi.org/10.1016/j.envexpbot.2022.105155

Zhao, H., Guan, J., Liang, Q., Zhang, X., Hu, H. & Zhang, J. (2021). Effects of cadmium stress on growth and physiological characteristics of sassafras seedlings. Scientific Reports, 11, 9913. https://www.nature.com/articles/s41598-021-89322-0

Zhou, J., Cheng, K., Huang, G., Chen, G., Zhou, S., Huang, Y., Zhang, J., Duan, H., & Fan, H. (2020). Effects of exogenous 3-indoleacetic acid and cadmium stress on the physiological and biochemical characteristics of Cinnamomum camphora. Ecotoxicology and Environmental Safety, 191, 109998. https://doi.org/10.1016/j.ecoenv.2019.109998