Toxicity mechanisms of photodegraded polyvinyl chloride nanoplastics on pea seedlings

Highlights

● Photodegraded polyvinyl chloride nanoplastics (PVC-NPs) inhibited pea seedlings’ growth.

● Photodegraded PVC-NPs resulted in damage of leaf stomata and roots.

● Photodegraded PVC-NPs influenced protein processing in endoplasmic reticulum.

● Photodegraded PVC-NPs influenced phenylpropanoid biosynthesis.

Abstract

Nanoplasctics (NPs), which are very small in particle size, exert toxic effect to organisms. Additionally, compared to original NPs, photodegraded NPs would pose higher toxicity. This is because their relatively higher specific surface areas and the presence of additives which can more easily leach. How original NPs and aged NPs affect plant growth has not been widely investigated. This work chose polyvinyl chloride NPs (PVC-NPs) that were subjected to up to 1000 h UV light radiation to explore the impact of PVC-NPs on the growth of pea seedlings (Pisum Sativum L.). The results indicated the existence of PVC-NPs with longer UV light radiation time and higher concentrations had more negative influences on pea seedlings’ growth such as germination rate (decreased by 10.6%–22.5%), stem length (decreased by 2.8%–8.1%), dry weight (decreased by 6.3%–7.1%) and fresh weight (decreased by 6.7%–14.8%). It was also noted that photodegraded PVC-NPs resulted in damage to leaf stomata and roots, hindering photosynthesis and absorption of nutrients and hence the decrease in chlorophyll and soluble sugar contents. According to transcriptomic investigation results, the presence of aged PVC-NPs primarily influenced protein processing in endoplasmic reticulum (upregulated metabolic pathway) and phenylpropanoid biosynthesis (downregulated metabolic pathway) of pea seedlings. These results provide an in-depth understanding of how NPs influence the growth of plants.

Graphical abstract

Keywords

Nanoplasctics / Polyvinyl chloride / Toxicity mechanisms / Plant growth

References

[1] AbdElgawad H , Farfan-Vignolo E R , Vos D D , Asard H . (2015). Elevated CO₂ mitigates drought and temperature-induced oxidative stress differently in grasses and legumes. Plant Science, 231: 1–10

[2] Anthony B M , Chaparro J M , Prenni J E , Minas I S . (2023). Carbon sufficiency boosts phenylpropanoid biosynthesis early in peach fruit development priming superior fruit quality. Plant Physiology and Biochemistry, 196: 1019–1031

[3] Arp H P H , Kuhnel D , Rummel C , Macleod M , Potthoff A , Reichelt S , Rojo-Nieto E , Schmitt-Jansen M , Sonnenberg J , Toorman E . . (2021). Weathering plastics as a planetary boundary threat: exposure, fate, and hazards. Environmental Science & Technology, 55(11): 7246–7255

[4] Bandow N , Will V , Wachtendorf V , Simon F G . (2017). Contaminant release from aged microplastic. Environmental Chemistry, 14(6): 394–405

[5] Besseling E , Redondo-Hasselerharm P , Foekema E M , Koelmans A A . (2019). Quantifying ecological risks of aquatic micro- and nanoplastic. Critical Reviews in Environmental Science and Technology, 49(1): 32–80

[6] Çelen Erdem İ , Ünek C , Akkuş Süt P , Karabıyık Acar Ö , Yurtsever M , Şahin F . (2023). Combined approaches for detecting polypropylene microplastics in crop plants. Journal of Environmental Management, 347: 119258

[7] Chen Y , Qi H , Yang L , Xu L , Wang J , Guo J , Zhang L , Tan Y , Pan R , Shu Q , Qian Q , Song S . (2023). The OsbHLH002/OsICE1–OSH1 module orchestrates secondary cell wall formation in rice. Cell Reports, 42(7): 112702

[8] Choo C Y L , Wu P C , Yago J I , Chung K R . (2023). The Pex3-mediated peroxisome biogenesis plays a critical role in metabolic biosynthesis, stress response, and pathogenicity in Alternaria alternata. Microbiological Research, 266: 127236

[9] Daraei H , Toolabian K , Thompson G . (2021). Biotoxicity evaluation of zinc oxide nanoparticles on bacterial performance of activated sludge at COD, nitrogen, and phosphorus reduction. Frontiers of Environmental Science & Engineering, 16(2): 19

[10] Ding L , Ouyang Z Z , Liu P , Wang T C , Jia H Z , Guo X T . (2022a). Photodegradation of microplastics mediated by different types of soil: the effect of soil components. Science of the Total Environment, 802: 149840

[11] Ding L , Yu X Q , Guo X T , Zhang Y P , Ouyang Z Z , Liu P , Zhang C , Wang T C , Jia H Z , Zhu L Y . (2022b). The photodegradation processes and mechanisms of polyvinyl chloride and polyethylene terephthalate microplastic in aquatic environments: important role of clay minerals. Water Research, 208: 117879

[12] Domínguez-Jaimes L P , Cedillo-González E I , Luévano-Hipólito E , Acuña-Bedoya J D , Hernández-López J M . (2021). Degradation of primary nanoplastics by photocatalysis using different anodized TiO₂ structures. Journal of Hazardous Materials, 413: 125452

[13] Dong Y , Gao M , Qiu W , Song Z . (2021). Uptake of microplastics by carrots in presence of As (III): combined toxic effects. Journal of Hazardous Materials, 411: 125055

[14] Du T T , Yu X , Shao S , Li T , Xu S M , Wu L J . (2023). Aging of nanoplastics significantly affects protein corona composition thus enhancing macrophage uptake. Environmental Science & Technology, 57(8): 3206–3217

[15] Gao Z , Yao L , Pan L . (2022). Gene expression and functional analysis of different heat shock protein (HSPs) in Ruditapes philippinarum under BaP stress. Comparative Biochemistry and Physiology. Toxicology & Pharmacology: CBP, 251: 109194

[16] Gong W , Xing Y , Han L , Lu A , Qu H , Xu L . (2022). Occurrence and distribution of micro- and mesoplastics in the high-latitude nature reserve, northern China. Frontiers of Environmental Science & Engineering, 16(9): 2095–2201

[17] Guan X , Li Q , Maimaiti T , Lan S , Ouyang P , Ouyang B , Wu X , Yang S T . (2021). Toxicity and photosynthetic inhibition of metal-organic framework MOF-199 to pea seedlings. Journal of Hazardous Materials, 409: 124521

[18] Guo Q C , Bandala E R , Goonetilleke A , Hong N , Li Y Q , Liu A . (2021). Application of Chlorella pyrenoidosa embedded biochar beads for water treatment. Journal of Water Process Engineering, 40: 101892

[19] Hahladakis J N , Velis C A , Weber R , Iacovidou E , Purnell P . (2018). An overview of chemical additives present in plastics: migration, release, fate and environmental impact during their use, disposal and recycling. Journal of Hazardous Materials, 344: 179–199

[20] He B B , Liu A , Duan H B , Wijesiri B , Goonetilleke A . (2022). Risk associated with microplastics in urban aquatic environments: a critical review. Journal of Hazardous Materials, 439: 129587

[21] He B B , Liu A , Duodu G O , Wijesiri B , Ayoko G A , Goonetilleke A . (2023). Distribution and variation of metals in urban river sediments in response to microplastics presence, catchment characteristics and sediment properties. Science of the Total Environment, 856: 159139

[22] Hua Z D , Ma S R , Ouyang Z Z , Liu P , Qiang H , Guo X T . (2023). The review of nanoplastics in plants: detection, analysis, uptake, migration and risk. Trends in Analytical Chemistry, 158: 116889

[23] Huo Y X , Dijkstra F A , Possell M , Singh B . (2022). Ecotoxicological effects of plastics on plants, soil fauna and microorganisms: a meta-analysis. Environmental Pollution, 310: 119892

[24] Juneja S , Saini R , Adhikary A , Yadav R , Khan S A , Nayyar H , Kumar S . (2023). Drought priming evokes essential regulation of Hsp gene families, Hsfs and their related miRNAs and induces heat stress tolerance in chickpea. Plant Stress, 10: 100189

[25] Li C J , Gao Y , He S , Chi H Y , Li Z C , Zhou X X , Yan B . (2021). Quantification of nanoplastic uptake in cucumber plants by pyrolysis gas chromatography/mass spectrometry. Environmental Science & Technology Letters, 8(8): 633–638

[26] Li L Z , Luo Y M , Li R J , Zhou Q , Peijnenburg W J G M , Yin N , Yang J , Tu C , Zhang Y C . (2020a). Effective uptake of submicrometre plactics by crop plants via a crack-entry mode. Nature Sustainability, 3(11): 929–937

[27] Li M Y , Kong J , Chen Y R , Li Y T , Xuan H Z , Liu M , Zhang Q , Liu J . (2023). Comparative interaction study of soy protein isolate and three flavonoids (Chrysin, Apigenin and Luteolin) and their potential as natural preservatives. Food Chemistry, 414: 135738

[28] Li Q , Hu R , Chen Z , Chen L , Zhang J , Wu X , Li J B , Gao Y , Yang S T , Wang H . (2022). Phytotoxicity of VO₂ nanoparticles with different sizes to pea seedlings. Ecotoxicology and Environmental Safety, 242: 113885

[29] Li Z X , Li R J , Li Q F , Zhou J G , Wang G Y . (2020b). Physiological response of cucumber (Cucumis sativus L.) leaves to polystyrene nanoplastics pollution. Chemosphere, 255: 127041

[30] Lima J Z , Cassaro R , Ogura A P , Vianna M M G R . (2023). A systematic review of the effects of microplastics and nanoplastics on the soil-plant system. Sustainable Production and Consumption, 38: 266–282

[31] Liu Y , Zhou C , Li F , Liu H , Yang J . (2020). Stocks and flows of polyvinyl chloride (PVC) in China: 1980–2050. Resources, Conservation and Recycling, 154: 104584

[32] Liu Y Y , Guo R , Zhang S W , Sun Y H , Wang F Y . (2022). Uptake and translocation of nano/microplastics by rice seedlings: evidence from a hydroponic experiment. Journal of Hazardous Materials, 421: 126700

[33] Lu S H , Zhu K R , Song W C , Song G , Chen D Y , Hayat T , Alharbi N S , Chen C L , Sun Y B . (2018). Impact of water chemistry on surface charge and aggregation of polystyrene microspheres suspensions. Science of the Total Environment, 630: 951–959

[34] Luo H W , Li Y , Zhao Y Y , Xiang Y H , He D Q , Pan X L . (2020). Effects of accelerated aging on characteristics, leaching, and toxicity of commercial lead chromate pigmented microplastics. Environmental Pollution, 257: 113475

[35] Maity S , Pramanick K . (2020). Perspectives and challenges of micro/nanoplastics-induced toxicity with special reference to phytotoxicity. Global Change Biology, 26(6): 3241–3250

[36] Mao Y , Ai H , Chen Y , Zhang Z , Zeng P , Kang L , Li W , Gu W , He Q , Li H . (2018). Phytoplankton response to polystyrene microplastics: perspective from an entire growth period. Chemosphere, 208: 59–68

[37] Mattsson K , Johnson E V , Malmendal A , Linse S , Hansson L A , Cedervall T . (2017). Brain damage and behavioural disorders in fish induced by plastic nanoparticles delivered through the food chain. Scientific Reports, 7(1): 11452

[38] McCue P , Zheng Z , Pinkham J L , Shetty K . (2000). A model for enhanced pea seedling vigour following low pH and salicylic acid treatments. Process Biochemistry, 35(6): 603–613

[39] Meng J , Xu B , Liu F , Li W , Sy N , Zhou X , Yan B . (2021). Effects of chemical and natural ageing on the release of potentially toxic metal additives in commercial PVC microplastics. Chemosphere, 283: 131274

[40] Mondal S , Karmakar S , Panda D , Pramanik K , Bose B , Singhal R K . (2023). Crucial plant processes under heat stress and tolerance through heat shock proteins. Plant Stress, 10: 100227

[41] Nayak L , Lal M K , Tiwari R K , Kumar R , Lal P , Das R , Behera B , Thakur P , Altaf M A , Kumar A . (2023). A balancing act: exploring the interplay between HSPs and osmoprotectants in temperature stress responses. South African Journal of Botany, 162: 64–71

[42] O’Brien S , Rauert C , Ribeiro F , Okoffo E D , Burrows S D , O’Brien J W , Wang X Y , Wright S L , Thomas K V . (2023). There’s something in the air: a review of sources, prevalence and behaviour of microplastics in the atmosphere. Science of the Total Environment, 874: 162193

[43] Pfohl P , Bahl D , Ruckel M , Wagner M , Meyer L , Bolduan P , Battagliarin G , Huffer T , Zumstein M , Hofmann T . . (2022). Effect of polymer properties on the biodegradation of polyurethane microplastics. Environmental Science & Technology, 56(23): 16873–16884

[44] Pitt J A , Kozal J S , Jayasundara N , Massarsky A , Trevisan R , Geitner N , Wiesner M , Levin E D , Di Giulio R T . (2018). Uptake, tissue distribution, and toxicity of polystyrene nanoparticles in developing zebrafish (Danio rerio). Aquatic Toxicology, 194: 185–194

[45] Qiao M M , Xia G Y , Cui T , Xu Y , Gao X J , Su Y , Li Y B , Fan H F . (2022). Effect of moisture, protein, starch, soluble sugar contents and microstructure on mechanical properties of maize kernels. Food Chemistry, 379: 132147

[46] Ren X , Han Y , Zhao H R , Zhang Z Q , Tsui T H , Wang Q . (2023). Elucidating the characteristic of leachates released from microplastics under different aging conditions: perspectives of dissolved organic carbon fingerprints and nano-plastics. Water Research, 233: 119786

[47] Rencoret J , del Río J C , Nierop K G J , Gutiérrez A , Ralph J . (2016). Rapid Py-GC/MS assessment of the structural alterations of lignins in genetically modified plants. Journal of Analytical and Applied Pyrolysis, 121: 155–164

[48] Rist S , Baun A , Hartmann N B . (2017). Ingestion of micro- and nanoplastics in Daphnia magna: quantification of body burdens and assessment of feeding rates and reproduction. Environmental Pollution, 228: 398–407

[49] Schwarz A E , Lensen S M C , Langeveld E , Parker L A , Urbanus J H . (2023). Plastics in the global environment assessed through material flow analysis, degradation and environmental transportation. Science of the Total Environment, 875: 162644

[50] Shekhawat K , Almeida-Trapp M , García-Ramírez G X , Hirt H . (2022). Beat the heat: plant- and microbe-mediated strategies for crop thermotolerance. Trends in Plant Science, 27(8): 802–813

[51] Shi C , Liu Z , Yu B , Zhang Y , Yang H , Han Y , Wang B , Liu Z , Zhang H . (2024). Emergence of nanoplastics in the aquatic environment and possible impacts on aquatic organisms. Science of the Total Environment, 906: 167404

[52] Sun H F , Lei C L , Xu J H , Li R L . (2021). Foliar uptake and leaf-to-root translocation of nanoplastics with different coating charge in maize plants. Journal of Hazardous Materials, 416: 125854

[53] Sun X D , Yuan X Z , Jia Y , Feng L J , Zhu F P , Dong S S , Liu J , Kong X , Tian H , Duan J L . . (2020). Differentially charged nanoplastics demonstrate distinct accumulation in Arabidopsis thaliana. Nature Nanotechnology, 15(9): 755–760

[54] Surendran U , Jayakumar M , Raja P , Gopinath G , Chellam P V . (2023). Microplastics in terrestrial ecosystem: sources and migration in soil environment. Chemosphere, 318: 137946

[55] Tallec K , Huvet A , Di Poi C D , González-Fernández C , Lambert C , Petton B , Le Goïc N L , Berchel M , Soudant P , Paul-Pont I . (2018). Nanoplastics impaired oyster free living stages, gametes and embryos. Environmental Pollution, 242: 1226–1235

[56] Tang Y , Ren J , Liu C X , Jiang J B , Yang H H , Li J F . (2021). Genetic characteristics and QTL analysis of the soluble sugar content in ripe tomato fruits. Scientia Horticulturae, 276: 109785

[57] Tong H Y , Zhong X C , Duan Z H , Yi X L , Cheng F Q , Xu W Q , Yang X J . (2022a). Micro- and nanoplastics released from biodegradable and conventional plastics during degradation: formation, aging factors, and toxicity. Science of the Total Environment, 833: 155275

[58] Tong Y , Yi S C , Liu S Y , Xu L , Qiu Z X , Zeng D Q , Tang W W . (2022b). Bruceine D may affect the phenylpropanoid biosynthesis by acting on ADTs thus inhibiting Bidens pilosa L. seed germination. Ecotoxicology and Environmental Safety, 242: 113943

[59] Vidal A , Cantabella D , Bernal-Vicente A , Díaz-Vivancos P , Hernández J A . (2018). Nitrate- and nitric oxide-induced plant growth in pea seedlings is linked to antioxidative metabolism and the ABA/GA balance. Journal of Plant Physiology, 230: 13–20

[60] Wang F Y , Feng X Y , Liu Y Y , Adams C A , Sun Y H , Zhang S W . (2022). Micro(nano)plastics and terrestrial plants: up-to-date knowledge on uptake, translocation, and phytotoxicity. Resources, Conservation and Recycling, 185: 106503

[61] Wang H Q , Zhu J H , He Y , Wang J W , Zeng N D , Zhan X H . (2023). Photoaging process and mechanism of four commonly commercial microplastics. Journal of Hazardous Materials, 451: 131151

[62] Wang Q , Wangjin X , Zhang Y , Wang N , Wang Y , Meng G , Chen Y . (2020). The toxicity of virgin and UV-aged PVC microplastics on the growth of freshwater algae Chlamydomonas reinhardtii. Science of the Total Environment, 749: 141603

[63] Wu H , He B B , Chen B C , Liu A . (2023). Toxicity of polyvinyl chloride microplastics on Brassica rapa. Environmental Pollution, 336: 122435

[64] Wu X , Liu Y , Yin S S , Xiao K K , Xiong Q , Bian S J , Liang S , Hou H J , Hu J P , Yang J K . (2020). Metabolomics revealing the response of rice (Oryza sativa L.) exposed to polystyrene microplastics. Environmental Pollution, 266: 115159

[65] Xia X H , Guo W W , Ma X Y , Liang N , Duan X Y , Zhang P H , Zhang Y , Chang Z J , Zhang X W . (2023). Reproductive toxicity and cross-generational effect of polyethylene microplastics in Paramisgurnus dabryanus. Chemosphere, 313: 137440

[66] Yan X Y , Yang X Y , Tang Z , Fu J J , Chen F M , Zhao Y , Ruan L L , Yang Y S . (2020). Downward transport of naturally-aged light microplastics in natural loamy sand and the implication to the dissemination of antibiotic resistance genes. Environmental Pollution, 262: 114270

[67] Yang H R , Tang K , Liu H T , Huang W D . (2011). Effect of salicylic acid on jasmonic acid-related defense response of pea seedlings to wounding. Scientia Horticulturae, 128(3): 166–173

[68] Yang J , Monnot M , Sun Y , Asia L , Wong-Wah-Chung P W W , Doumenq P , Moulin P . (2023). Microplastics in different water samples (seawater, freshwater, and wastewater): removal efficiency of membrane treatment processes. Water Research, 232: 119673

[69] Yang X , He Q , Guo F , Liu X , Chen Y . (2021). Translocation and biotoxicity of metal (oxide) nanoparticles in the wetland-plant system. Frontiers of Environmental Science & Engineering, 15(6): 138

[70] Yin L S , Wen X F , Huang D L , Du C Y , Deng R , Zhou Z Y , Tao J X , Li R J , Zhou W , Wang Z Y . . (2021). Interactions between microplastics/nanoplastics and vascular plants. Environmental Pollution, 290: 117999

[71] Yu Y , Li J . (2024). Biochar-derived dissolved and particulate matter effects on the phytotoxicity of polyvinyl chloride nanoplastics. Science of the Total Environment, 906: 167258

[72] Yue Z , Chen Y , Chen C , Ma K , Tian E , Wang Y , Liu H , Sun Z . (2021). Endophytic Bacillus altitudinis WR10 alleviates Cu toxicity in wheat by augmenting reactive oxygen species scavenging and phenylpropanoid biosynthesis. Journal of Hazardous Materials, 405: 124272

[73] Zhang D , Li J , Niu X , Deng C , Song X , Li W , Cheng Z , Xu Q , Zhang B , Guo W . (2021). GhANN1 modulates the salinity tolerance by regulating ABA biosynthesis, ion homeostasis and phenylpropanoid pathway in cotton. Environmental and Experimental Botany, 185: 104427

[74] Zhang X S , Su H , Gao P , Li B H , Feng L , Liu Y Z , Du Z W , Zhang L Q . (2022). Effects and mechanisms of aged polystyrene microplastics on the photodegradation of sulfamethoxazole in water under simulated sunlight. Journal of Hazardous Materials, 433: 128813

[75] Zhao X , Tang B , Xu J , Wang N , Zhou Z , Zhang J . (2020). A SET domain-containing protein involved in cell wall integrity signaling and peroxisome biogenesis is essential for appressorium formation and pathogenicity of Colletotrichum gloeosporioides. Fungal Genetics and Biology, 145: 103474

[76] Zheng X , Liu X , Zhang L , Wang Z , Yuan Y , Li J , Li Y , Huang H , Cao X , Fan Z . (2022). Toxicity mechanism of nylon microplastics on Microcystis aeruginosa through three pathways: photosynthesis, oxidative stress and energy metabolism. Journal of Hazardous Materials, 426: 128094

[77] Zhou C Q , Lu C H , Mai L , Bao L J , Liu L Y , Zeng E Y . (2021a). Response of rice (Oryza sativa L.) roots to nanoplastic treatment at seedling stage. Journal of Hazardous Materials, 401: 123412

[78] Zhou X X , He S , Gao Y , Chi H Y , Wang D J , Li Z C , Yan B . (2021b). Quantitative analysis of polystyrene and poly(methyl methacrylate) nanoplastics in tissues of aquatic animals. Environmental Science & Technology, 55(5): 3032–3040

[79] Zhu K C , Jia H Z , Zhao S , Xia T J , Guo X T , Wang T C , Zhu L Y . (2019). Formation of environmentally persistent free radicals on microplastics under light irradiation. Environmental Science & Technology, 53(14): 8177–8186

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 52170100 and U21A2036), the Guangdong Basic and Applied Basic Research Foundation (No. 2022A1515110257), the Shenzhen Science and Innovation Commission (No. JCYJ20200109113006046).

Conflict of Interests

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-024-1809-2 and is accessible for authorized users.

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