With increasing plastic production and consumption, large amounts of polystyrene nanoplastics are accumulated in soil due to improper disposal causing pollution and deleterious effects to environment. However, little information is available about how to alleviate the adverse impacts of nanoplastics on crops. In this study, the involvement of melatonin in modulating nanoplastic uptake, translocation, and toxicity in wheat plant was investigated. The results demonstrated that exogenous melatonin application reduced the nanoplastic uptake by roots and their translocation to shoots via regulating the expression of genes associated with aquaporin, including the upregulation of the TIP2-9, PIP2, PIP3, and PIP1.2 in leaves and TIP2-9, PIP1-5, PIP2, and PIP1.2 in roots. Melatonin activated the ROS scavenging system to maintain a better redox homeostasis and ameliorated the negative effects of nanoplastics on carbohydrate metabolism, hence ameliorated the plant growth and enhanced the tolerance to nanoplastics toxicity. This process was closely related to the exogenous melatonin application induced melatonin accumulation in leave. These results suggest that melatonin could alleviate the adverse effects of nanoplastics on wheat, and exogenous melatonin application might be used as a promising management strategy to sustain crop production in the nanoplastic-polluted soils.

College of Advanced Agricultural Sciences University of Chinese Academy of Sciences Beijing China

Department of Botany and Plant Physiology Czech University of Life Sciences Prague Prague Czech Republic

Department of Plant Physiology Slovak Agricultural University Nitra Slovak Republic

Faculty of Science Department of Plant and Environmental Sciences University of Copenhagen Tåstrup Denmark

Key Laboratory of Molecular Epigenetics of the Ministry of Education Northeast Normal University Changchun China

Northeast Institute of Geography and Agroecology Chinese Academy of Sciences Changchun China

Zobrazit více v PubMed

Boots B, Russell CW, Green DS. Effects of microplastics in soil ecosystems: above and below ground. Environ Sci Technol. 2019;53:11496-11506.

Nizzetto L, Futter M, Langaas S. Are agricultural soils dumps for microplastics of urban origin? Environ Sci Technol. 2016;50:10777-10779.

Li L, Luo Y, Li R, et al. Effective uptake of submicrometre plastics by crop plants via a crack-entry mode. Nat Sustain. 2020;3(11):929-937.

Zhou C, Chen H, Mai L, Bao L, Liu L, Zeng E. Response of rice (Oryza sativa L.) roots to nanoplastic treatment at seedling stage. J Hazard Mater. 2021;401:123412.

Taylor SE, Pearce CI, Sanguinet KA, et al. Polystyrene nano- and microplastic accumulation at Arabidopsis and wheat root cap cells, but no evidence for uptake into roots. Environ Sci Nano. 2020;7:1942-1953.

Van Weert S, Redondo-Hasselerharm PE, Diepens NJ, Koelmans AA. Effects of nanoplastics and microplastics on the growth of sediment-rooted macrophytes. Sci Total Environ. 2019;654:1040-1047.

Lian J, Wu J, Xiong H, et al. Impact of polystyrene nanoplastics (PSNPs) on seed germination and seedling growth of wheat (Triticum aestivum L.). J Hazard Mater. 2020;385:121620.

Jia J, Liang Y, Gou T, et al. The expression response of plasma membrane aquaporins to salt stress in tomato plants. Environ Exp Bot. 2020;178:104190.

Clarkson DT, Carvajal M, Henzler T, et al. Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. J Exp Bot. 2000;51:61-70.

Kaldenhoff R, Fischer M. Functional aquaporin diversity in plants. Biochim Biophy Acta. 2006;1758:1134-1141.

Locke AM, Ort DR. Diurnal depression in leaf hydraulic conductance at ambient and elevated [CO2] reveals anisohydric water management in field-grown soybean and possible involvement of aquaporins. Environ Exp Bot. 2015;116:39-46.

Sun X, Yuan X, Jia Y, et al. Differentially charged nanoplastics demonstrate distinct accumulation in Arabidopsis thaliana. Nat Nanotechnol. 2020;15:755-760.

Browne MA, Dissanayake A, Galloway TS, Lowe DM, Thompson RC. Ingested microscopic plastic translocates to the circulatory system of the Mussel, Mytilus edulis (L.). Environ Sci Technol. 2008;42:5026-5031.

Qi Y, Yang X, Pelaez AM, et al. Macro- and micro- plastics in soil-plant system: effects of plastic mulch film residues on wheat (Triticum aestivum) growth. Sci Total Environ. 2018;645:1048-1056.

Li Z, Li R, Li Q, Zhou J, Wang G. Physiological response of cucumber (Cucumis sativus L.) leaves to polystyrene nanoplastics pollution. Chemosphere. 2020;255:127041.

Giorgetti L, Spano C, Muccifora S, et al. Exploring the interaction between polystyrene nanoplastics and Allium cepa during germination: internalization in root cells, induction of toxicity and oxidative stress. Plant Physiol Bioch. 2020;149:170-177.

Lian J, Wu J, Zeb A, et al. Do polystyrene nanoplastics affect the toxicity of cadmium to wheat (Triticum aestivum L.)? Environ Pollut. 2020;263:114498.

Dong Y, Gao M, Song Z, Qiu W. Microplastic particles increase arsenic toxicity to rice seedlings. Environ Pollut. 2020;259:113892.

Wei Y, Chang Y, Zeng H, Liu G, He C, Shi H. RAV transcription factors are essential for disease resistance against cassava bacterial blight via activation of melatonin biosynthesis genes. J Pineal Res. 2018;64(1):e12454.

Shi H, Qian Y, Tan DX, Reiter RJ, He C. Melatonin induces the transcripts of CBF/DREB1s and their involvement in both abiotic and biotic stresses in Arabidopsis. J Pineal Res. 2015;59:334-342.

Shi H, Chen Y, Tan DX, Reiter RJ, Chan Z, He C. Melatonin induces nitric oxide and the potential mechanisms relate to innate immunity against bacterial pathogen infection in Arabidopsis. J Pineal Res. 2015;59:102-108.

Zhang R, Sun Y, Liu Z, Jin W, Sun Y. Effects of melatonin on seedling growth, mineral nutrition, and nitrogen metabolism in cucumber under nitrate stress. J Pineal Res. 2017;62:e12403.

Li X, Tan DX, Jiang D, Liu F. Melatonin enhances cold tolerance in drought-primed wild type and abscisic acid-deficient mutant barley. J Pineal Res. 2016;61:328-339.

Manchester LC, Coto-Montes A, Boga JA, et al. Melatonin: an ancient molecule that makes oxygen metabolically tolerable. J Pineal Res. 2015;59:403-419.

Kanwar MK, Yu J, Zhou J. Phytomelatonin: recent advances and future prospects. J Pineal Res. 2018;65:e12526.

Zuo Z, Sun L, Wang T, et al. Melatonin improves the photosynthetic carbon assimilation and antioxidant capacity in wheat exposed to Nano-ZnO stress. Molecules. 2017;22:1727.

Jammer A, Gasperl A, Luschin-Ebengreuth N, et al. Simple and robust determination of the activity signature of key carbohydrate metabolism enzymes for physiological phenotyping in model and crop plants. J Exp Bot. 2015;66:5531-5542.

Gasperl A, Morvan-Bertrand A, Prud'homme MP, van der Graaff E, Roitsch T. Exogenous classic phytohormones have limited regulatory effects on fructan and primary carbohydrate metabolism in perennial ryegrass (Lolium perenne L.). Front Plant Sci. 2015;6:1251.

Gasperl A, Morvan-Bertrand A, Prud'homme MP, van der Graaff E, Roitsch T. A simple and fast kinetic assay for the determination of fructan exohydrolase activity in perennial ryegrass (Lolium perenne L.). Front. Plant Sci. 2015;6:1154.

Fimognari L, Dölker R, Kaselyte G, et al. Simple semi-high throughput determination of activity signatures of key antioxidant enzymes for physiological phenotyping. Plant Methods. 2020;16:42.

Li X, Brestic M, Tan DX, et al. Melatonin alleviates low PS I-limited carbon assimilation under elevated CO2 and enhances the cold tolerance of offspring in chlorophyll b-deficient mutant wheat. J Pineal Res. 2018;64:e12453.

Deng X, Zhou S, Hu W, et al. Ectopic expression of wheat TaCIPK14, encoding a calcineurin B-like protein-interacting protein kinase, confers salinity and cold tolerance in tobacco. Physiol Plant. 2013;149:367-377.

Wang C, Zhao J, Xing B. Environmental source, fate, and toxicity of microplastics. J Hazard Mater. 2021;407:124357.

Maity S, Chatterjee A, Guchhait R, De S, Pramanick K. Cytogenotoxic potential of a hazardous material, polystyrene microparticles on Allium cepa L. J Hazard Mater. 2020;385:121560.

Li C, Gao Y, He S, et al. Quantification of nanoplastic uptake in cucumber plants by pyrolysis gas chromatography/mass spectrometry. Environ Sci Tech Let. 2021;8:633-638.

Zhou Q, Hu X. Systemic stress and recovery patterns of rice roots in response to graphene oxide nanosheets. Environ Sci Technol. 2017;51:2022-2030.

Wang P, Lombi E, Sun SK, et al. Characterizing the uptake, accumulation and toxicity of silver sulfide nanoparticles in plants. Environ Sci Nano. 2017;4:448-460.

Qiao Y, Ren J, Yin L, et al. Exogenous melatonin alleviates PEG-induced short-term water deficiency in maize by increasing hydraulic conductance. Bmc Plant Biol. 2020;20:218.

Tiwari R, Lal M, Kumar R, et al. Mechanistic insights on melatonin-mediated drought stress mitigation in plants. Physiol Plant. 2021;172:1-15.

Mandal MK, Suren H, Ward B, Boroujerdi A, Kousik C. Differential roles of melatonin in plant-host resistance and pathogen suppression in cucurbits. J Pineal Res. 2018;65:e12505.

Wei Y, Hu W, Wang Q, et al. Identification, transcriptional and functional analysis of heat-shock protein 90s in banana (Musa acuminata L.) highlight their novel role in melatonin-mediated plant response to Fusarium wilt. J Pineal Res. 2016;62:e12367.

Shi H, Jiang C, Ye T, et al. Comparative physiological, metabolomic, and transcriptomic analyses reveal mechanisms of improved abiotic stress resistance in bermudagrass [Cynodon dactylon (L). Pers.] by exogenous melatonin. J Exp Bot. 2015;66:681-694.

Lee K, Lee HY, Back K. Rice histone deacetylase 10 and Arabidopsis histone deacetylase 14 genes encode N-acetylserotonin deacetylase, which catalyzes conversion of N-acetylserotonin into serotonin, a reverse reaction for melatonin biosynthesis in plants. J Pineal Res. 2017;64:e12460.

Liu N, Gong B, Jin Z, et al. Sodic alkaline stress mitigation by exogenous melatonin in tomato needs nitric oxide as a downstream signal. J Plant Physiol. 2015;186-187:68-77.

Vafadar F, Amooaghaie R, Ehsanzadeh P, Ghanati F, Sajedi RH. Crosstalk between melatonin and Ca2+/CaM evokes systemic salt tolerance in Dracocephalum kotschyi. J Plant Physiol. 2020;252:153237.

Reiter RJ, Mayo JC, Tan DX, Sainz RM, Alatorre-Jimenez M, Qin L. Melatonin as an antioxidant: under promises but over delivers. J Pineal Res. 2016;61:253-278.

Antoniou C, Chatzimichail G, Xenofontos R, et al. Melatonin systemically ameliorates drought stress-induced damage in Medicago sativa plants by modulating nitro-oxidative homeostasis and proline metabolism. J Pineal Res. 2017;62:e12401.

Shi H, Chen K, Wei Y, He C. Fundamental issues of melatonin-mediated stress signaling in plants. Front Plant Sci. 2016;7:1124.

Keunen E, Peshev D, Vangronsveld J, Van Den Ende W, Cuypers A. Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ. 2013;36:1242-1255.

Asada K. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol. 1999;50:601-639.

Li X, Ulfat A, Shokat S, Liu S, Zhu X, Liu F. Responses of carbohydrate metabolism enzymes in leaf and spike to CO2 elevation and nitrogen fertilization and their relations to grain yield in wheat. Environ Exp Bot. 2019;164:149-156.

Roitsch T, González MC. Function and regulation of plant invertases: sweet sensations. Trends Plant Sci. 2004;9:606-613.

Rhizosphere melatonin application reprograms nitrogen-cycling related microorganisms to modulate low temperature response in barley