Effect of polyvinyl chloride and cadmium on absorption and accumulation of nutrients under symbiotic fungi in foxtail millet (Setaria italica L.) seedling

Document Type : Original Article

Authors

1 Ph.D student, Department of Plant Production and Genetics, Faculty of Agriculture, Bu-Ali Sina University, Hamedan, Iran

2 Associate Professor, Department of Plant Production and Genetics, Faculty of Agriculture, Bu-Ali Sina University, Hamedan, Iran

Abstract

Introduction
Polyvinyl chloride is one of the dominant microplastic types used in agricultural land and is mainly concentrated in shallow soils (Yang et al., 2022). Cadmium toxicity can damage the metal absorption metabolic mechanisms and affect essential element level control (Mourato et al., 2019). Co-presence of microplastics and heavy metals can cause synergistic, antagonistic, or reinforcing effects on plants, but definitive information is still limited (Kumar et al., 2022). Using symbiotic fungi is a cost-effective and environmentally friendly method to increase plant growth and tolerance to cadmium stress (Kumar and Verma, 2018). We aimed to investigate the polyvinyl chloride effect under cadmium stress and S. indica role in modulating the combined stress on the absorption, translocation, and accumulation of important nutrients in foxtail millet root and shoot.
 
Materials and methods
A factorial, completely randomized design experiment with three replicates was conducted. The investigated factors included 0, 2.5, 5, and 10 mg cadmium kg-1 soil, 0, 0.1, and 1% polyvinyl chloride, and S. indica symbiosis (fungus absence and presence). The sterilized seeds were placed in a plastic pot containing 1.5 kg cadmium and microplastic-contaminated soil. Then fungus spore suspension was applied to the seeds. After 60 days, the plant organs were harvested and the plant organs were dried for 48 hours in an oven at 70°C and then weighed. The 0.5 g of milled dry leaves and roots were ashed at 550°C for 5 hours, after the digestion, element contents were measured by an atomic absorption device. The fungal colonization percentage, root-to-shoot ratio, heavy metal tolerance index, and content of macronutrients and micronutrients were calculated. Data were analyzed through the SAS (9.4) statistical program and means values were compared by LSD test (P < 0.05).
 
Results and discussion
The results of the data variance analysis showed that the combined effect of cadmium and polyvinyl chloride on the examined traits was significant at the 1% probability level, except for the Ca and K contents in root, Cd contents in root and shoot, which was at the 5% probability level. The presence of microplastic improved colonization percentage, metal tolerance index, root and shoot dry weight, so decreased root/shoot in cadmium-stressed plants. Microplastic reduces the negative effects of heavy metal on the dry weight of roots and shoots due to the property of maintaining heavy metal on their surface (Dong et al., 2022). Cadmium reduced contents of Na, K, Mg, Ca, Cu, Mn, and Zn in root and shoot, and the presence of a microplastic increased their contents in shoot and root only in 10 mg cadmium except Ca and Zn that was in shoot. Microplastics can bind to root surfaces (Yang et al., 2021), reduce root activity and heavy metal absorption (Dong et al., 2022), and increase nutrient absorption. Moreover, microplastics have a lower absorption capacity for metal pollutants in the soil, and due to their diluting properties; they can increase metal mobility and availability (Zhang et al., 2020). Fe content decreased in the shoot and increased in the root under cadmium toxicity. Co-treatment of cadmium and microplastic just increased Fe root content in 0.1% PVC and 2.5 mg Cd. The formation of Fe-Mn plaques on the roots increases the cadmium chelation in the rhizosphere and root surfaces, which can act as a barrier to protect the plant against cadmium toxicity (Liu et al., 2010). S. indica increased plant dry weight and macronutrient and micronutrient contents in the shoots and the roots. It is due to plant hormone production and increased absorption of micronutrients and macronutrients by the roots (Zahoor, 2017). The mentioned fungus also improves the metal tolerance index by elevating cadmium content in the root and alleviating it in the shoot. This can be related to the binding of metals to the fungal hyphae cell walls and their transfer reduction to the plant's above-ground parts (Baghaie et al., 2021).
 
Conclusion
The results showed that polyvinyl chloride can modulate cadmium's adverse effect on the foxtail millet shoot in cadmium-contaminated soil and reduce the entry of cadmium into the food chain. In addition, S. indica increases the plant's tolerance to cadmium and microplastic stress conditions by increasing water availability and nutrient absorption, increasing cadmium accumulation in the roots, and reducing its transfer to the shoots. Considering the complexity of different soil-plant systems, this conclusion needs further investigation and cannot generalized to other cases.

Keywords

Main Subjects


Abbasi, S., Moore, F., Keshavarzi, B., Hopke, P.K., Naidu, R., Rahman, M.M., Oleszczuk, P., Karimi, J., 2020. PET-microplastics as a vector for heavy metals in a simulated plant rhizosphere zone. Science of the Total Environment. 744, 140984. https://doi.org/10.1016/j.scitotenv.2020.140984
Ahmad, A., Shahzadi, I., Mubeen, S., Yasin, N.A., Akram, W., Khan, W.U., Wu, T., 2021. Karrikinolide alleviates BDE-28, heat and Cd stressors in Brassica alboglabra by correlating and modulating biochemical attributes, antioxidative machinery and osmoregulators. Ecotoxicology and Environmental Safety. 213, 112047. https://doi.org/10.1016/j.ecoenv.2021.112047
Baghaie, A.H., Aghili, F., 2021. Contribution of Piriformospora indica on improving the nutritional quality of greenhouse tomato and its resistance against cu toxicity after humic acid addition to soil. Environmental Science and Pollution Research. 28, 64572-64585. https://doi.org/10.1007/s11356-021-15599-3
Bertolazi, A.A., de Souza, S.B., Ruas, K.F., Campostrini, E., de Rezende, C.E., Cruz, C., Melo, J., Colodete, C.M., Varma, A., Ramos, A.C., 2019. Inoculation with Piriformospora indica is more efficient in wild-type rice than in transgenic rice over-expressing the vacuolar H+-PPase. Frontiers in Microbiology. https://doi.org/10. 10.3389/fmicb.2019.01087
Cornu, J.Y., Bussière, S., Coriou, C., Robert, T., Maucourt, M., Deborde, C., Moing, A., Nguyen, C., 2020. Changes in plant growth, Cd partitioning and xylem sap composition in two sunflower cultivars exposed to low Cd concentrations in hydroponics. Ecotoxicology and Environmental Safety. 205, 111145. https://doi.org/10.1016/j.ecoenv.2020.111145
de Souza Machado, A.A., Lau, C.W., Till, J., Kloas, W., Lehmann, A., Becker, R., Rillig, M.C., 2018. Impacts of microplastics on the soil biophysical environment. Environmental Science & Technology. 52, 9656-9665. https://doi.org/10.1021/acs.est.8b02212
Dong, Y., Bao, Q., Gao, M., Qiu, W., Song, Z., 2022. A novel mechanism study of microplastic and As co-contamination on indica rice (Oryza sativa L.). Journal of Hazardous Materials. 421, 126694. https://doi.org/10.1016/j.jhazmat.2021.126694
Feng, X., Wang, Q., Sun, Y., Zhang, S., Wang, F., 2022. Microplastics change soil properties, heavy metal availability and bacterial community in a Pb-Zn-contaminated soil. Journal of Hazardous Materials 424, 127364. https://doi.org/10.1016/j.jhazmat.2021.127364
Galloway, T.S., Cole, M., Lewis, C., 2017. Interactions of microplastic debris throughout the marine ecosystem. Nature Ecology and Evolution. 1, 116. https://doi.org/10.1038/s41559-017-0116
Ghabooli, M., Khatabi, B., Ahmadi, F.S., Sepehri, M., Mirzaei, M., Amirkhani, A., Jorrín-Novo, J.V., Salekdeh, G.H., 2013. Proteomics study reveals the molecular mechanisms underlying water stress tolerance induced by Piriformospora indica in barley. Journal of Proteomics. 94, 289-301. https://doi.org/10.1016/j.jprot.2013.09.017
Hédiji, H., Djebali, W., Belkadhi, A., Cabasson, C., Moing, A., Rolin, D., Brouquisse, R., Gallusci, P., 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
Hui, F., Liu, J., Gao, Q., Lou, B., 2015. Piriformospora indica confers cadmium tolerance in Nicotiana tabacum. Journal of Environmental Sciences. 37, 184-191. https://doi.org/10.1016/j.jes.2015.06.005
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, 255-277. https://doi.org/10.1039/c8mt00247a
Jackson, ML., 1967. Soil Chemical Analysis, 1st ed. Prentice Hall of India Pvt. Ltd, New Delhi, 144–197
Jia, N., Zhihui, C., Khan, A.R., Ahmad, I., 2015. Effects of temperature during seedling stage on growth and nutrient absorbance of Gerbera jamesonii growing in organic substrate. Journal of Plant Nutrition. 38, 700-711. https://doi.org/10.1080/01904167.2014.934481
Kalra, Y., (Ed.). 1997. Handbook of reference methods for plant analysis. CRC press.
Kumar, A., Verma, J.P., 2018. Does plant microbe interaction confer stress tolerance in plants: A review? Microbiological Research. 207, 41-52. https://doi.org/10.1016/j.micres.2017.11.004
Kumar, R., Ivy, N., Bhattacharya, S., Dey, A., Sharma, P., 2022. Coupled effects of microplastics and heavy metals on plants: Uptake, bioaccumulation, and environmental health perspectives. Science of the Total Environment. 836, 155619. https://doi.org/10.1016/j.scitotenv.2022.155619
Lei, C., Engeseth, N.J., 2022. Comparison of growth and quality between hydroponically grown and soil-grown lettuce under the stress of microplastics. ACS ES&T Water. 2, 1182-1194. https://doi.org/10.1021/acsestwater.1c00485
Leitão, I., Sales, J., Martins, L.L., Mourato, M.P., 2021. Response to stress induced by different potentially toxic elements (As, Cd, Cu and Na) in rapeseed leaves. Plant Physiology Reports. 26, 478-490. https://doi.org/10.1007/s40502-021-00601-4
Li, C., Zhou, K., Qin, W., Tian, C., Qi, M., Yan, X., Han, W., 2019. A review on heavy metals contamination in soil: effects, sources, and remediation techniques. Soil and Sediment Contamination: An International Journal. 28, 380-394. https://doi.org/10.1080/15320383.2019.1592108
Li, N., Xiao, H., Sun, J., Wang, S., Wang, J., Chang, P., Zhou, X., Lei, B., Lu, K., Luo, F., Shi, X., Li, J., 2018. Genome-wide analysis and expression profiling of the HMA gene family in Brassica napus under cd stress. Plant and Soil. 426, 365-381. https://doi.org/10.1007/s11104-018-3637-2
Li, S.U.N., Yu, J., Zhu, M., Zhao, F., Luan, S., 2012. Cadmium impairs ion homeostasis by altering K+ and Ca2+ channel activities in rice root hair cells. Plant, Cell & Environment. 35, 1998-2013. https://doi.org/10.1111/j.1365-3040.2012.02532.x
Liang, Y., Wu, Q.-T., Lee, C.C.C., Jiang, C.a., Wei, Z., 2022. Evaluation of manganese application after soil stabilization to effectively reduce cadmium in rice. Journal of Hazardous Materials. 424, 127296. https://doi.org/10.1016/j.jhazmat.2021.127296
Liu, B., An, C., Jiao, S., Jia, F., Liu, R., Wu, Q., Dong, Z., 2022. Impacts of the inoculation of Piriformospora indica on photosynthesis, osmoregulatory substances, and antioxidant enzymes of Alfalfa seedlings under cadmium stress. Agriculture, 12, 1928. https://doi.org/10.3390/agriculture12111928
Liu, J., Cao, C., Wong, M., Zhang, Z., Chai, Y., 2010. Variations between rice cultivars in iron and manganese plaque on roots and the relation with plant cadmium uptake. Journal of Environmental Sciences. 22, 1067-1072. https://doi.org/10.1016/S1001-0742(09)60218-7
Liu, Y., Cui, W., Li, W., Xu, S., Sun, Y., Xu, G., Wang, F., 2023a. Effects of microplastics on cadmium accumulation by rice and arbuscular mycorrhizal fungal communities in cadmium-contaminated soil. Journal of Hazardous Materials. 442, 130102. https://doi.org/10.1016/j.jhazmat.2022.130102
Liu, Y.-Q., Chen, Y., Ren, X.-M., Li, Y.-Y., Zhang, Y.-J., Zhang, H., Han, H., Chen, Z.-J., 2023b. Plant growth-promoting bacteria modulate gene expression and induce antioxidant tolerance to alleviate synergistic toxicity from combined microplastic and Cd pollution in sorghum. Ecotoxicology and Environmental Safety. 264, 115439. https://doi.org/10.1016/j.ecoenv.2023.115439
Ma, J., Aqeel, M., Khalid, N., Nazir, A., Alzuaibr, F.M., Al-Mushhin, A.A.M., Hakami, O., Iqbal, M.F., Chen, F., Alamri, S., Hashem, M., Noman, A., 2022. Effects of microplastics on growth and metabolism of rice (Oryza sativa L.). Chemosphere. 307, 135749. https://doi.org/10.1016/j.chemosphere.2022.135749
Mangal, V., Nguyen, T.Q., Fiering, Q., Guéguen, C., 2020. An untargeted metabolomic approach for the putative characterization of metabolites from Scenedesmus obliquus in response to cadmium stress. Environmental Pollution. 266, 115123. https://doi.org/10.1016/j.envpol.2020.115123
Marchiol, L., Assolari, S., Sacco, P., Zerbi, G., 2004. Phytoextraction of heavy metals by canola (Brassica napus) and radish (Raphanus sativus) grown on multicontaminated soil. Environmental Pollution. 132, 21-27. https://doi.org/10.1016/j.envpol.2004.04.001
Mohd, S., Shukla, J., Kushwaha, A. S., Mandrah, K., Shankar, J., Arjaria, N., Saxena, PN., Narayan, R., Roy, SK., Kumar, M., 2017. Endophytic fungi Piriformospora indica mediated protection of host from arsenic toxicity. Frontiers in Microbiology. 8, 754.‏ https://doi.org/10.3389/fmicb.2017.00754
Moreno-Jiménez, E., Leifheit, E.F., Plaza, C., Feng, L., Bergmann, J., Wulf, A., Lehmann, A., Rillig, M.C., 2022. Effects of microplastics on crop nutrition in fertile soils and interaction with arbuscular mycorrhizal fungi. Journal of Sustainable Agriculture and Environment. 1, 66-72. https://doi.org/10.1002/sae2.12006
Mourato, M., Pinto, F., Moreira, I., Sales, J., Leitão, I., Martins, L.L., 2019. Chapter 13 - The effect of Cd stress in mineral nutrient uptake in plants. In: Hasanuzzaman, M., Prasad, M.N.V., Fujita, M. (Eds.), Cadmium Toxicity and Tolerance in Plants. Academic Press, pp. 327-348. https://doi.org/10.1016/B978-0-12-814864-8.00013-9
Oelmüller, R., Sherameti, I., Tripathi, S., Varma, A., 2009. Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis. 49, 1-17. https://doi.org/10.1007/s13199-009-0009-y
Phillips, J.M., Hayman, D.S., 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society. 55, 158-IN118. https://doi.org/10.1016/S0007-1536(70)80110-3
Qin, S., Liu, H., Rengel, Z., Gao, W., Nie, Z., Li, C., Hou, M., Cheng, J., Zhao, P., 2020. Boron inhibits cadmium uptake in wheat (Triticum aestivum) by regulating gene expression. Plant Science. 297, 110522. https://doi.org/10.1016/j.plantsci.2020.110522
Sagonda, T., Adil, M.F., Sehar, S., Rasheed, A., Joan, H.I., Ouyang, Y., Shamsi, I.H., 2021. Physio-ultrastructural footprints and iTRAQ-based proteomic approach unravel the role of Piriformospora indica-colonization in counteracting cadmium toxicity in rice. Ecotoxicology and Environmental Safety. 220, 112390. https://doi.org/10.1016/j.ecoenv.2021.112390
Saman, M., Sepehri, A., 2021. Alleviating effects of Serendipita indica and nitric oxide in proso millet plants (Panicum miliaceum L.) exposed to copper toxicity. Journal of Soil Science and Plant Nutrition. 21, 3065-3075. https://doi.org/10.1007/s42729-021-00589-8
Saud, S., Yang, A., Jiang, Z., Ning, D., Fahad, S., 2023. New insights in to the environmental behavior and ecological toxicity of microplastics. Journal of Hazardous Materials Advances. 10, 100298. https://doi.org/10.1016/j.hazadv.2023.100298
Sepehri, M., Khatabi, B., 2021. Combination of siderophore-producing bacteria and Piriformospora indica provides an efficient approach to improve cadmium tolerance in Alfalfa. Microbial Ecology. 81, 717-730. https://doi.org/10.1007/s00248-020-01629-z
Shah, A.A., Aslam, S., Akbar, M., Ahmad, A., Khan, W.U., Yasin, N.A., Ali, B., Rizwan, M., Ali, S., 2021. Combined effect of Bacillus fortis IAGS 223 and zinc oxide nanoparticles to alleviate cadmium phytotoxicity in Cucumis melo. Plant Physiology and Biochemistry. 158, 1-12. https://doi.org/10.1016/j.plaphy.2020.11.011
Shahabivand, S., Parvaneh, A., Aliloo, A.A., 2017. Root endophytic fungus Piriformospora indica affected growth, cadmium partitioning and chlorophyll fluorescence of sunflower under cadmium toxicity. Ecotoxicology and Environmental Safety. 145, 496-502. https://doi.org/10.1016/j.ecoenv.2017.07.064
Shahabivand, S., Parvaneh, A., Aliloo, A.A., 2020. Different response of Alyssum montanum and Helianthus annuus to cadmium bioaccumulation mediated by the endophyte fungus Serendipita indica. Acta Ecologica Sinica. 40, 315-322. https://doi.org/10.1016/j.chnaes.2019.09.002
Shahid, M., Dumat, C., Khalid, S., Niazi, N.K., Antunes, P.M.C., 2017. Cadmium bioavailability, uptake, toxicity and detoxification in soil-plant system. In: de Voogt, P., Gunther, F.A. (Eds.), Reviews of Environmental Contamination and Toxicology. Volume 241. Springer International Publishing, Cham, pp. 73-137. https://doi.org/10.1007/398_2016_8
Su, Z-z., Wang, T., Shrivastava, N., Chen, Y-y., Liu, X., Sun, C., Yin, Y., Gao, Q-k., Lou, B-g., 2017. Piriformospora indica promotes growth, seed yield and quality of Brassica napus L. Microbiological Research. 199, 29-39. https://doi.org/10.1016/j.micres.2017.02.006
Thijs, S., Langill, T., Vangronsveld, J., 2017. Chapter Two - The bacterial and fungal microbiota of hyperaccumulator plants: small organisms, large influence. In: Cuypers, A., Vangronsveld, J. (Eds.), Advances in Botanical Research. Academic Press, pp. 43-86. https://doi.org/10.1016/bs.abr.2016.12.003
Wang, F., Feng, X., Liu, Y., Adams, C.A., Sun, Y., Zhang, S., 2022a. Micro(nano)plastics and terrestrial plants: up-to-date knowledge on uptake, translocation, and phytotoxicity. Resources, Conservation and Recycling. 185, 106503. https://doi.org/10.1016/j.resconrec.2022.106503
Wang, F., Zhang, X., Zhang, S., Zhang, S., Sun, Y., 2020. Interactions of microplastics and cadmium on plant growth and arbuscular mycorrhizal fungal communities in an agricultural soil. Chemosphere. 254, 126791. https://doi.org/10.1016/j.chemosphere.2020.126791
Wang, X., Fan, X., Wang, W., Song, F., 2022b. Use of Serendipita indica to improve soybean growth, physiological properties, and soil enzymatic activities under different Cd concentrations. Chemical and Biological Technologies in Agriculture. 9, 66. https://doi.org/10.1186/s40538-022-00331-1
Yang, L., Kang, S., Wang, Z., Luo, X., Guo, J., Gao, T., Chen, P., Yang, C., Zhang, Y., 2022. Microplastic characteristic in the soil across the Tibetan Plateau. Science of The Total Environment. 828, 154518. https://doi.org/10.1016/j.scitotenv.2022.154518
Yang, W., Cheng, P., Adams, C.A., Zhang, S., Sun, Y., Yu, H., Wang, F., 2021. Effects of microplastics on plant growth and arbuscular mycorrhizal fungal communities in a soil spiked with ZnO nanoparticles. Soil Biology and Biochemistry. 155, 108179. https://doi.org/10.1016/j.soilbio.2021.108179
Zahoor, M., Irshad, M., Rahman, H., Qasim, M., Afridi, S.G., Qadir, M., Hussain, A., 2017. Alleviation of heavy metal toxicity and phytostimulation of Brassica campestris L. by endophytic Mucor sp. MHR-7. Ecotoxicology and Environmental Safety. 142, 139-149. https://doi.org/10.1016/j.ecoenv.2017.04.005
Zhang, S., Han, B., Sun, Y., Wang, F., 2020. Microplastics influence the adsorption and desorption characteristics of Cd in an agricultural soil. Journal of Hazardous Materials. 388, 121775. https://doi.org/10.1016/j.jhazmat.2019.121775
Zhang, W., Wang, J., Xu, L., Wang, A., Huang, L., Du, H., Qiu, L., Oelmüller, R., 2017. Drought stress responses in maize are diminished by Piriformospora indica. Plant Signaling & Behavior. 13. https://doi.org/10.1080/15592324.2017.1414121
Zhang, Z., Cui, Q., Chen, L., Zhu, X., Zhao, S., Duan, C., Zhang, X., Song, D., Fang, L., 2022a. A critical review of microplastics in the soil-plant system: distribution, uptake, phytotoxicity and prevention. Journal of Hazardous Materials. 424(Pt D), 127750. https://doi.org/10.1016/j.jhazmat.2021.127750
Zhang, Z., Li, Y., Qiu, T., Duan, C., Chen, L., Zhao, S., Zhang, X., Fang, L., 2022b. Microplastics addition reduced the toxicity and uptake of cadmium to Brassica chinensis L. Science of the Total Environment. 852, 158353. https://doi.org/10.1016/j.scitotenv.2022.158353
Zhou, Y., Wang, J., Zou, M., Jia, Z., Zhou, S., Li, Y., 2020. Microplastics in soils: a review of methods, occurrence, fate, transport, ecological and environmental risks. Science of the Total Environment. 748, 141368. https://doi.org/10.1016/j.scitotenv.2020.141368
 

Articles in Press, Accepted Manuscript
Available Online from 29 November 2025
  • Receive Date: 08 August 2024
  • Revise Date: 27 September 2024
  • Accept Date: 07 October 2024