Effect of Piriformospora indica symbiosis on growth and physiological indices of maize (Zea mays L.) seedlings exposed to microplastic particles and water deficit stress

Document Type : Research Paper

Authors

1 Assistant Professor, Department of Agricultural Sciences, Faculty of Technical and Engineering, Payame Noor University, Tehran, Iran

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

Abstract

Introduction
Microplastic contamination of agricultural lands is one of the major environmental problems that has recently gained attention. The decomposition of plastic mulches and equipment used in irrigation systems, the use of sludge-based fertilizers from wastewater purification, contaminated irrigation water, and the proximity of fields to busy roads are among the most important factors in the contamination of agricultural lands with plastic particles. The presence of microplastics in the soil with particle sizes from 100 nm to five mm causes abrasion of the root surface of plants, and physical damage to plant roots will increase with increasing particle size. Moreover, drought stress, as one of the most important factors limiting crop production, is increasing alarmingly, especially due to global climate change. Therefore, the present study was conducted to investigate the possibility of using the biological potential of the fungus Piriformospora indica to reduce the negative effects of stress caused by polyvinyl chloride (PVC) microplastic particles and water deficiency in maize crop.

Materials and methods
The experiment was conducted as factorial experiment in a completely randomized design with three replications in the research greenhouse of Bu-Ali Sina University, Hamadan, Iran, in 2023. The experimental factors included the addition of three concentrations of polyvinyl chloride microplastics to the soil (0, 0.1, and 1%), P. indica fungus at two levels (inoculation and non-inoculation), and water deficit stress at three levels (full irrigation, and irrigation at 75% and 50% of field capacity, as non- stress, moderate stress and severe stress, respectively). Germinated maize seeds (cv. ‘Tah’) were inoculated with P. indica, planted in pots containing three kg of soil, and placed in greenhouse conditions. Water deficit stress was applied 14 days after planting. One month after planting, photosynthetic parameters and relative leaf water content were measured. The plants were then harvested, and the roots were assessed under a microscope to determine the colonization percentage. Proline content, total chlorophyll content, and plant dry matter were also measured.

Research findings
The results showed that the presence of 1% microplastic in the soil, similar to water deficit stress, significantly reduced relative leaf water content, total chlorophyll content, photosynthetic indices, and shoot dry matter of maize seedlings. Although the percentage of root colonization of maize seedlings by P. indica fungus decreased by 16.9%, 30.9%, and 47.1% under 1% microplastic contamination and water deficit at 75% and 50% of field capacity conditions compared to the control, respectively, the beneficial effects of the fungus on plant growth and measured parameters was still evident, so that the relative leaf water content, chlorophyll content, net photosynthesis rate, and shoot dry weight of inoculated plants under the highest level of water deficit stress and in the presence of 1% microplastic were (8.2 and 9), (20.5 and 27), (17.9 and 17.8) and (43.5 and 46.8) percent higher than those of uninoculated plants, respectively. Moreover, the proline content of the plants also increased significantly in the presence of the fungus.

Conclusion
The results of this study showed that the presence of P. indica fungus improved the growth and photosynthetic parameters of maize seedlings under microplastic particles and water deficit stress conditions. Thus, utilizing the potential of this fungus can be considered to reduce the negative effects of these stresses.

Keywords

Main Subjects

References

Arnon, D. I. (1949). Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology, 24(1), 1-15. doi: 10.1104/pp.24.1.1.##Aslam, M. M., Karanja, J., & Bello, S. K. (2019). Piriformospora indica colonization reprograms plants to improved P-uptake, enhanced crop performance, and biotic/abiotic stress tolerance. Physiological & Molecular Plant Pathology, 106, 232-237. doi: 10.1016/j.pmpp.2019.02.010.##Aslani, Z., Hassani, A., Mandoulakani, B. A., Barin, M., & Maleki, R. (2023). Effect of drought stress and inoculation treatments on nutrient uptake, essential oil and expression of genes related to monoterpenes in sage (Salvia officinalis). Scientia Horticulturae, 309, 111610. doi: 10.1016/j.scienta.2022.111610.##Barrs, H. D., & Weatherley, P. E. (1962). A re-examination of the relative turgidity technique for estimating water deficits in leaves. Australian Journal of Biological Sciences, 15(3), 413-428. doi: 10.1071/BI9620413.##Bates, L. S., Waldren, R. P. A., & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant & Soil, 39, 205-207. doi: 10.1007/BF00018060.##Bosker, T., Bouwman, L. J., Brun, N. R., Behrens, P., & Vijver, M. G. (2019). Microplastics accumulate on pores in seed capsule and delay germination and root growth of the terrestrial vascular plant Lepidium sativum. Chemosphere, 226, 774-781. doi: 10.1016/j.chemosphere.2019.03.163.##Cao, L., Wu, D., Liu, P., Hu, W., Xu, L., Sun, Y., Wu, Q., Tian, K., Huang, B., Yoon, S. J., Kwon, B. O., & Khim, J. S. (2021). Occurrence, distribution and affecting factors of microplastics in agricultural soils along the lower reaches of Yangtze River, China. Science of the Total Environment, 794, 148694. doi: 10.1016/j.scitotenv.2021.148694.##Dabral, S., Varma, A., Choudhary, D. K., Bahuguna, R. N., & Nath, M. (2019). Biopriming with Piriformospora indica ameliorates cadmium stress in rice by lowering oxidative stress and cell death in root cells. Ecotoxicology & Environmental Safety, 186, 109741. doi: 10.1016/j.ecoenv.2019.109741.##de Souza Machado, A. A., Lau, C. W., Kloas, W., Bergmann, J., Bachelier, J. B., Faltin, E., Becker, R., Görlich, A. S., & Rillig, M. C. (2019). Microplastics can change soil properties and affect plant performance. Environmental Science & Technology, 53(10), 6044-6052. doi: 10.1021/acs.est.9b01339.##Dong, Y., Gao, M., Song, Z., & Qiu, W. (2020). Microplastic particles increase arsenic toxicity to rice seedlings. Environmental Pollution, 259, 113892. doi: 10.1016/j.envpol.2019.113892.##Fu, Q., Lai, J. L., Ji, X. H., Luo, Z. X., Wu, G., & Luo, X. G. (2022). Alterations of the rhizosphere soil microbial community composition and metabolite profiles of Zea mays by polyethylene-particles of different molecular weights. Journal of Hazardous Materials, 423, 127062. doi: 10.1016/j.jhazmat.2021.127062.##Gao, M., Liu, Y., & Song, Z. (2019). Effects of polyethylene microplastic on the phytotoxicity of di-n-butyl phthalate in lettuce (Lactuca sativa L. var. ramosa Hort). Chemosphere, 237, 124482. doi: 10.1016/j.chemosphere.2019.124482.##Gill, S. S., Gill, R., Trivedi, D. K., Anjum, N. A., Sharma, K. K., Ansari, M. W., Ansari, A. A., Johri, A. K., Prasad, R., Pereira, E., Varma, A., & Tuteja, N. (2016). Piriformospora indica: Potential and significance in plant stress tolerance. Frontiers in Microbiology, 7, 332. doi: 10.3389/fmicb.2016.00332.##Gong, W., Zhang, W., Jiang, M., Li, S., Liang, G., Bu, Q., Xu, L., Zhy, H., & Lu, A. (2021). Species-dependent response of food crops to polystyrene nanoplastics and microplastics. Science of the Total Environment, 796, 148750. doi: 10.1016/j.scitotenv.2021.148750.##He, D., Zhang, Y., & Gao, W. (2021). Micro (nano) plastic contaminations from soils to plants: Human food risks. Current Opinion in Food Science, 41, 116-121. doi: 10.1016/j.cofs.2021.04.001.##Harman, G. E. (2011). Multifunctional fungal plant symbionts: new tools to enhance plant growth and productivity. New Phytologist, 189(3), 647-649. doi: 10.1111/j.1469-8137.2010.03614.x.##Hartmann, G. F., Ricachenevsky, F. K., Silveira, N. M., & Pita-Barbosa, A. (2022). Phytotoxic effects of plastic pollution in crops: what is the size of the problem?. Environmental Pollution, 292, 118420. doi: 10.1016/j.envpol.2021.118420.##Huang, Z., Zou, Z. R., Huang, H. H., He, C. X., Zhang, Z. B., Wang, H. S., & Li, J. M. (2010). Cloning, analysis and expression of a drought-related gene MeP5CS from melon. Acta Horticulturae Sinica, 37(8), 1279-1286.##Hussin, S., Khalifa, W., Geissler, N., & Koyro, H. W. (2017). Influence of the root endophyte Piriformospora indica on the plant water relations, gas exchange and growth of Chenopodium quinoa at limited water availability. Journal of Agronomy & Crop Science, 203(5), 373-384. doi: 10.1111/jac.12199.##Jangir, P., Shekhawat, P. K., Bishnoi, A., Ram, H., & Soni, P. (2021). Role of Serendipita indica in enhancing drought tolerance in crops. Physiological & Molecular Plant Pathology, 116, 101691. doi: 10.1016/j.pmpp.2021.101691.##Jia, L., Liu, L., Zhang, Y., Fu, W., Liu, X., Wang, Q., Tanveer, M., & Huang, L. (2023). Microplastic stress in plants: Effects on plant growth and their remediations. Frontiers in Plant Science, 14, 1226484. doi: 10.3389/fpls.2023.1226484.##Jyothymol, C. P., Kutty, M. S., Pradeepkumar, T., Parvathi, M. S., & Rashmi, C. R. (2024). Piriformospora indica improves water stress tolerance in watermelon (Citrullus lanatus (Thunb.) Matsum & Nakai). Plant Physiology Reports, 29(3), 638-650. doi: 10.1007/s40502-024-00797-1.##Khalid, M., Ur-Rahman, S., Tan, H., Su, L., Zhou, P., & Hui, N. (2022). Mutualistic fungus Piriformospora indica modulates cadmium phytoremediation properties of host plant via concerted action of enzymatic and non-enzymatic biochemicals. Pedosphere, 32(2), 256-267. doi: 10.1016/S1002-0160(21)60014-0.##Lian, J., Liu, W., Meng, L., Wu, J., Zeb, A., Cheng, L., Lian, Y., & Sun, H. (2021). Effects of microplastics derived from polymer-coated fertilizer on maize growth, rhizosphere, and soil properties. Journal of Cleaner Production, 318, 128571. doi: 10.1016/j.jclepro.2021.128571.##Ma, J., Aqeel, M., Khalid, N., Nazir, A., Alzuaibr, F. M., Al-Mushhin, A. A., 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. doi: 10.1016/j.chemosphere.2022.135749.##Mohd, S., Shukla, J., Kushwaha, A. S., Mandrah, K., Shankar, J., Arjaria, N., Saxena, P. N., Narayan, R., Roy, S. K., & Kumar, M. (2017). Endophytic fungi Piriformospora indica mediated protection of host from arsenic toxicity. Frontiers in Microbiology, 8, 754. doi: 10.3389/fmicb.2017.00754.##Pehlivan, N., & Gedik, K. (2021). Particle size-dependent biomolecular footprints of interactive microplastics in maize. Environmental Pollution, 277, 116772. doi: 10.1016/j.envpol.2021.116772.##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(1), 158-161. doi: 10.1016/S0007-1536(70)80110-3.##Pignattelli, S., Broccoli, A., & Renzi, M. (2020). Physiological responses of garden cress (L. sativum) to different types of microplastics. Science of the Total Environment, 727, 138609. doi: 10.1016/j.scitotenv.2020.138609.##Rai, M., Acharya, D., Singh, A., & Varma, A. (2001). Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza, 11, 123-128. doi: 10.1007/s005720100115.##Swetha, S., & Padmavathi, T. (2020). Mitigation of drought stress by Piriformospora indica in Solanum melongena L. cultivars. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 90(3), 585-593. doi: https://doi.org/10.1007/s40011-019-01128-3.##Tyagi, J., Mishra, A., Kumari, S., Singh, S., Agarwal, H., Pudake, R. N., Varma, A., & Joshi, N. C. (2023). Deploying a microbial consortium of Serendipita indica, Rhizophagus intraradices, and Azotobacter chroococcum to boost drought tolerance in maize. Environmental & Experimental Botany, 206, 105142. doi: 10.1016/j.envexpbot.2022.105142.##Tyagi, J., Varma, A., & Pudake, R. N. (2017). Evaluation of comparative effects of arbuscular mycorrhiza (Rhizophagus intraradices) and endophyte (Piriformospora indica) association with finger millet (Eleusine coracana) under drought stress. European Journal of Soil Biology, 81, 1-10. doi: 10.1016/j.ejsobi.2017.05.007.##Xu, J., Guo, L., & Liu, L. (2022). Exogenous silicon alleviates drought stress in maize by improving growth, photosynthetic and antioxidant metabolism. Environmental & Experimental Botany, 201, 104974. doi: 10.1016/j.envexpbot.2022.104974.##Zia, R., Nawaz, M. S., Siddique, M. J., Hakim, S., & Imran, A. (2021). Plant survival under drought stress: Implications, adaptive responses, and integrated rhizosphere management strategy for stress mitigation. Microbiological Research, 242, 126626. doi: 10.1016/j.micres.2020.126626.##

Files

Share

How to cite

Statistics