Climate change-induced stressors such as extreme temperatures negatively affect plant growth and development. Therefore, methods are needed to improve plant tolerance to abiotic stresses. The aim of this study was to evaluate whether the foliar application of putrescine (Put) and a chitosan-putrescine nanocomposite (Ch-Put) can modulate the antioxidant response and membrane properties of lettuce under chilling stress. In this study, Put and Ch-Put were applied via foliar spraying at two concentrations (1 mM and 2.5 mM), and after treatment, the plants were placed in a phytotron at 4 °C and 20 °C. Changes in the properties of the cell membranes were assessed in the seedlings. Additionally, the antioxidant enzymatic activity and content of nonenzymatic bioactive compounds were evaluated. The results indicated that the use of Put and Ch-Put influenced the permeability and fluidity of the lipid membranes, which also depended on the treatment temperature. An increase in Alim (all treatments) and a decrease in Cs⁻1 values (Put and Ch-Put at a concentration of 2.5 mM) were observed at 4 °C, suggesting looser packing and increased elasticity of cell membranes, facilitating the metabolic and physiological adaptation of plants to stress. The treatment of chilled plants with Put and Ch-Put resulted in increased contents of proline, carbohydrates, glutathione, phenolics and L-ascorbic acid, as well as increased activity of several antioxidant enzymes, such as catalase (CAT) and ascorbate peroxidase (APX), which could contribute to increased tolerance to stress. The strongest effects were observed for Put at concentrations of 1 mM and 2.5 mM and Ch-Put at the 2.5 mM concentration, suggesting the potential use of these substances in strategies to increase plant tolerance to chilling stress.

Department of Agricultural Sciences Biotechnology and Food Science Cyprus University of Technology 3036 Limassol Cyprus

Department of Chemistry and Biochemistry Faculty of AgriSciences Mendel University in Brno Zemedelska 1 61300 Brno Czech Republic

Department of Herbal and Animal Production Vocational School of Technical Sciences Igdir University 76000 Igdir Turkey

Department of Horticultural Sciences Faculty of Agriculture University of Maragheh Maragheh 551877684 Iran

Department of Horticulture Faculty of Biotechnology and Horticulture University of Agriculture in Krakow 29 Listopada 54 31 425 Kraków Poland

Institute of Biology and Earth Sciences University of the National Education Commission Podchorążych 2 30 084 Kraków Poland

Zobrazit více v PubMed

Bray, E. A., Bailey-Serres, J. & Weretilnyk, E. Responses to abiotic stresses. In

Sachdev, S., Ansari, S. A., Ansari, M. I., Fujita, M. & Hasanuzzaman, M. Abiotic stress and reactive oxygen species: Generation, signaling, and defense mechanisms. PubMed PMC

Upchurch, R. G. Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. PubMed

Henschel, J. M. et al. Lipidomics in plants under abiotic stress conditions: An overview.

Das, K. & Roychoudhury, A. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants.

Hasanuzzaman, M. et al. Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of a universal defense regulator. PubMed PMC

Gill, S. S. & Tuteja, N. Polyamines and abiotic stress tolerance in plants. PubMed PMC

Sequera-Mutiozabal, M., Antoniou, C., Tiburcio, A. F., Alcázar, R. & Fotopoulos, V. Polyamines: Emerging hubs promoting drought and salt stress tolerance in plants.

Bitrián, M., Zarza, X., Altabella, T., Tiburcio, A. F. & Alcázar, R. Polyamines under abiotic stress: Metabolic crossroads and hormonal crosstalks in plants. PubMed PMC

Walters, D. Resistance to plant pathogens: Possible roles for free polyamines and polyamine catabolism. PubMed

González-Hernández, A. I. et al. Putrescine: A key metabolite involved in plant development, tolerance and resistance responses to stress. PubMed PMC

Tyagi, A. et al. Revisiting the role of polyamines in plant growth and abiotic stress resilience: Mechanisms, crosstalk, and future perspectives.

Cuevas, J. C. et al. Putrescine as a signal to modulate the indispensable ABA increase under cold stress. PubMed PMC

Song, Y., Diao, Q. & Qi, H. Putrescine enhances chilling tolerance of tomato (

Sun, X. et al. Physiological and transcriptome changes induced by exogenous putrescine in anthurium under chilling stress. PubMed PMC

Crini, G. & Lichtfouse, E.

Ji, H. et al. Meta-analysis of chitosan-mediated effects on plant defense against oxidative stress. PubMed

Negm, N. A., Hefni, H. H. H., Abd-Elaal, A. A. A., Badr, E. A. & Abou Kana, M. T. H. Advancement on modification of chitosan biopolymer and its potential applications. PubMed

Kashyap, P. L., Xiang, X. & Heiden, P. Chitosan nanoparticle based delivery systems for sustainable agriculture. PubMed

Abdel-Aziz, H. M., Hasaneen, M. N. & Omer, A. M. Nano chitosan-NPK fertilizer enhances the growth and productivity of wheat plants grown in sandy soil.

Ghosh, A., Saha, I., Debnath, S. C., Hasanuzzaman, M. & Adak, M. K. Chitosan and putrescine modulate reactive oxygen species metabolism and physiological responses during chili fruit ripening. PubMed

Mahmoudi, R., Razavi, F., Rabiei, V., Gohari, G. & Palou, L. Application of glycine betaine coated chitosan nanoparticles alleviate chilling injury and maintain quality of plum ( PubMed

Gohari, G., Jiang, M., Manganaris, G. A., Zhou, J. & Fotopoulos, V. Next generation chemical priming: With a little help from our nanocarrier friends. PubMed

Los, D. A. & Murata, N. Membrane fluidity and its roles in the perception of environmental signals. PubMed

Murata, N. & Los, D. A. Membrane fluidity and temperature perception. PubMed PMC

Conde, A., Chaves, M. M. & Gerós, H. Membrane transport, sensing and signaling in plant adaptation to environmental stress. PubMed

Aslam, M. et al. Plant low-temperature stress: Signaling and response.

Yang, F., Hu, J., Li, J., Wu, X. & Qian, Y. Chitosan enhances leaf membrane stability and antioxidant enzyme activities in apple seedlings under drought stress.

Niu, Y. & Xiang, Y. An overview of biomembrane functions in plant responses to high-temperature stress. PubMed PMC

Rajput, V. D. et al. Recent developments in enzymatic antioxidant defence mechanism in plants with special reference to abiotic stress. PubMed PMC

Lastdrager, J., Hanson, J. & Smeekens, S. Sugar signals and the control of plant growth and development. PubMed

El-Bassiouny, H. M. S. & Bekheta, M. A. Role of putrescine on growth, regulation of stomatal aperture, ionic contents and yield by two wheat cultivars under salinity stress.

Zhong, M. et al. Effects of exogenous putrescine on glycolysis and Krebs cycle metabolism in cucumber leaves subjected to salt stress.

Thalmann, M. & Santelia, D. Starch as a determinant of plant fitness under abiotic stress. PubMed

Zhao, J., Wang, X., Pan, X., Jiang, Q. & Xi, Z. Exogenous putrescine alleviates drought stress by altering reactive oxygen species scavenging and biosynthesis of polyamines in the seedlings of Cabernet Sauvignon. PubMed PMC

Kalisz, A. et al. Foliar spraying with amino acids and their chitosan nanocomposites as promising way to alleviate abiotic stress in iceberg lettuce grown at different temperatures. PubMed PMC

Kornas, A., Kuźniak, E., Ślesak, I. & Miszalski, Z. The key role of the redox status in regulation of metabolism in photosynthesizing organisms. PubMed

Pilon, M., Ravet, K. & Tapken, W. The biogenesis and physiological function of chloroplast superoxide dismutases. PubMed

Bowler, C., van Camp, W., van Montagu, M., Inzé, D. & Asada, K. Superoxide dismutase in plants.

Kliebenstein, D. J., Monde, R.-A. & Last, R. L. Superoxide dismutase in Arabidopsis: An eclectic enzyme family with disparate regulation and protein localization. PubMed PMC

Myouga, F. et al. Heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in PubMed PMC

Armbruster, U. et al. Chloroplast proteins without cleavable transit peptides: Rare exceptions or a major constituent of the chloroplast proteome? PubMed

Dvořák, P. et al. PubMed

Melicher, P. et al. PubMed PMC

Ogawa, K., Kanematsu, S., Tabake, K. & Asada, K. Attachment of CuZn-superoxide dismutase to thylakoid membranes at the site of superoxide generation (PSI) in spinach chloroplasts: Detection by immuno-gold labeling after rapid freezing and substitution method.

Sakamoto, A., Okumura, T., Kaminaka, H. & Tanaka, K. Molecular cloning of the gene ( PubMed PMC

Verma, S. & Mishra, S. N. Putrescine alleviation of growth in salt stressed PubMed

Çakmak, T. & Atıcı, Ö. Effects of putrescine and low temperature on the apoplastic antioxidant enzymes in the leaves of two wheat cultivars.

Bahmani, R., Razavi, F., Mortazavi, S. N., Juárez-Maldonado, A. & Gohari, G. Chitosan–putrescine nanoparticle coating attenuates postharvest decay and maintains ROS scavenging system activity of strawberry cv. ‘Camarosa’ during cold storage.

Sharma, S. et al. Synergistic effect of polyamine treatment and chitosan coating on postharvest senescence and enzyme activity of bell pepper (

Bal, E. & Ürün, B. A. Effects of chitosan coating with putrescine on bioactive compounds and quality of strawberry cv. San Andreas during cold storage.

Rafique, M. et al. Mitigation of adverse effect of cadmium toxicity in lettuce ( PubMed PMC

Groppa, M. D. & Benavides, M. P. Polyamines and abiotic stress: Recent advances. PubMed

Xiao, M. et al. The multiple roles of ascorbate in the abiotic stress response of plants: Antioxidant, cofactor, and regulator. PubMed PMC

Li, M. et al. Abscisic acid and putrescine synergistically regulate the cold tolerance of melon seedlings. PubMed

Panahirad, S. et al. Foliar application of chitosan–putrescine nanoparticles (CTS-Put NPs) alleviates cadmium toxicity in grapevine ( PubMed PMC

Zhao, X., Zhang, Y., Zhang, X. & Shan, C. H. Putrescine improves salt tolerance of wheat seedlings by regulating ascorbate and glutathione metabolism, photosynthetic performance, and ion homeostasis.

Mohsin, S. M. et al. Tebuconazole and trifloxystrobin regulate the physiology, antioxidant defense and methylglyoxal detoxification systems in conferring salt stress tolerance in PubMed PMC

Lee, J.-H. & Oh, M.-M. Short-term low temperature increases phenolic antioxidant levels in kale.

Kalisz, A. et al. Chilling-induced changes in the antioxidant status of basil plants.

Strzałka, K., Kostecka-Gugała, A. & Latowski, D. Carotenoids and environmental stress in plants: Significance of carotenoid-mediated modulation of membrane physical properties.

Ljubej, V., Karalija, E., Salopek-Sondi, B. & Šamec, D. Effects of short-term exposure to low temperatures on proline, pigments, and phytochemicals level in kale (

Talaat, I. M., Bekheta, M. A. & Mahgoubi, M. H. Physiological response of periwinkle plants (

Singh, M., Kumar, J., Singh, S., Singh, V. P. & Prasad, S. M. Roles of osmoprotectants in improving salinity and drought tolerance in plants: A review.

Zhu, X., Song, F. & Liu, S. Arbuscular mycorrhiza impacts on drought stress of maize plants by lipid peroxidation, proline content and activity of antioxidant system.

Su, G. X. & Bai, L. P. Contribution of putrescine degradation to proline accumulation in soybean leaves under salinity.

Wu, J., Nadeem, M., Galagedara, L., Thomas, R. & Cheema, M. Effects of chilling stress on morphological, physiological, and biochemical attributes of silage corn genotypes during seedling establishment. PubMed PMC

Aroca, R. et al. Involvement of abscisic acid in leaf and root of maize (

Bligh, E. G. & Dyer, W. J. A rapid method of total lipid extraction and purification. PubMed

Block, M. A., Dorne, A. J., Joyard, J. & Douce, R. Preparation and characterization of membrane fraction enriched in outer and inner envelope membranes from spinach chloroplasts. II. Biochemical characterization. PubMed

Ábrahám, E., Hourton-Cabassa, C., Erdei, L. & Szabados, L. Methods for determination of proline in plants. In PubMed

Maness, N. Extraction and analysis of soluble carbohydrates. In PubMed

Aebi, H. Catalase PubMed

Nakano, Y. & Asada, K. Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts.

Zhang, Z., Pang, X., Duan, X., Ji, Z. L. & Jiang, Y. Role of peroxidase in anthocyanin degradation in litchi fruit pericarp.

Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. PubMed

Beauchamp, C. & Fridovich, I. Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. PubMed

Ślesak, I. & Miszalski, Z. Superoxide dismutase-like protein from roots of the intermediate C3-CAM plant

Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. PubMed

Ikewuchi, J. C. & Ikewuchi, C. C. Iodometric determination of the ascorbic acid (vitamin C) content of some fruits consumed in a university community in Nigeria.

Guri, A. Variation in glutathione and ascorbic acid content among selected cultivars of

Djeridane, A. et al. Antioxidant activity of some Algerian medicinal plants extracts containing phenolic compounds.

Dhindsa, R. S. & Matowe, W. Drought tolerance in two mosses: Correlated with enzymatic defense against lipid peroxidation.