TSitologiya i Genetika 2022, vol. 56, no. 2, 49-67
Cytology and Genetics 2022, vol. 56, no. 2, 148–163, doi: https://www.doi.org/10.3103/S0095452722020062

Polyamines: participation in cellular signaling and plant adaptation to the action of abiotic stressors

Kolupaev Yu.E., Kokorev A.I., Dmitriev A.P.

  1. Dokuchaev Kharkiv National Agrarian University, p/o Dokuchaevske-2, 62483, Kharkiv, Ukraine
  2. Karazin Kharkiv National University, Svobody sq., 4, 61022, Kharkiv, Ukraine
  3. Institute of Cellular Biology and Genetic Engineering of NAS of Ukraine, Academic Zabolotniy St., 148, 03143, Kyiv, Ukraine

SUMMARY. Polyamines (PA) are aliphatic amines found in all cells, including plant cells. The most common PAs of higher plants are putrescine, spermidine and spermine. PAs are localized in cell walls, vacuoles, mitochondria, chloroplasts and nucleus. PA content in plant tissue significantly increases under adverse conditions. These compounds are considered as typical stress metabo-lites. They are involved in the stabilization of bio-macromolecules and membrane structures. At the same time, in recent years, PA functions under stress conditions have been considered in the context of their involvement in cellular signaling processes. The review provides up-to-date information on the synthesis and catabolism of PA. The processes of formation of hydrogen peroxide from PA, which plays the role of one of the key signaling molecules are considered. The probable synthesis of nitric oxide during oxidative degradation of PA is discussed. Information on the effect of PA on the calcium homeostasis of plant cells, the participation of PA in the regulation of ionic, including calcium, channels is presented. The gasotransmitter hydrogen sulfide is considered as one of the mediators in the implementation of the effects of PA. The paper summarizes the role of the PA in maintaining the redox balance in plant cells, their involvement in the regulation of gene expression of stress proteins, state stomatal apparatus and other processes related to adaptation to the adverse environmental factors.

Keywords: polyamines, signaling mediators, reactive oxygen species, nitric oxide, calcium, antioxidant system, stomata, stressors, resistance

TSitologiya i Genetika
2022, vol. 56, no. 2, 49-67

Current Issue
Cytology and Genetics
2022, vol. 56, no. 2, 148–163,
doi: 10.3103/S0095452722020062

Full text and supplemented materials


Abbasi, N.A., Ali, I., Hafiz, I.A., and Khan, A.S., Application of polyamines in horticulture: A review, Int. J. Biosci., 2017, vol. 10, no. 5, pp. 319–342. https://doi.org/10.12692/ijb/10.5.319-342

Acharya, B.R. and Assmann, S.M., Hormone interactions in stomatal function, Plant Mol. Biol., 2009, vol. 69, no. 4, pp. 451–462. https://doi.org/10.1007/s11103-008-9427-0

Agurla, S., Gayatri, G., and Raghavendra, A.S., Polyamines increase nitric oxide and reactive oxygen species in guard cells of Arabidopsis thaliana during stomatal closure, Protoplasma, 2018, vol. 255, no. 1, pp. 153–162. https://doi.org/10.1007/s00709-017-1139-3

Alcázar, R., Bueno, M., and Tiburcio, A.F., Polyamines: Small amines with large effects on plant abiotic stress tolerance, Cells, 2020, vol. 9, no. 11, art. ID 2373. https://doi.org/10.3390/cells9112373

An, Z., Jing, W., Liu, Y., and Zhang, W., Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba, J. Exp. Bot., 2008, vol. 59, no. 4, pp. 815–825. https://doi.org/10.1093/jxb/erm370

An, Z.F., Li, C.Y., Zhang, L.X., and Alva, A.K., Role of polyamines and phospholipase D in maize (Zea mays L.) response to drought stress, S. Afr. J. Bot., 2012, vol. 83, pp. 145–150. https://doi.org/10.1016/j.sajb.2012.08.009

Andronis, E.A., Moschou, P.N., Toumi, I., and Roubelakis-Angelakis, K.A., Peroxisomal polyamine oxidase and NADPH-oxidase cross-talk for ROS homeostasis which affects respiration rate in Arabidopsis thaliana, Front. Plant Sci., 2014, vol. 5, pp. 132. https://doi.org/10.3389/fpls.2014.00132

Angelini, R., Cona, A., Federico, R., Fincato, P., Tavladoraki, P., and Tisi, A., Plant amine oxidases “on the move”: An update, Plant Physiol. Biochem., 2010, vol. 48, no. 7, pp. 560–564. https://doi.org/10.1016/j.plaphy.2010.02.001

Aronova, E.E., Shevyakova, N.I., Stetsenko, L.A., and Kuznetsov, Vl.V., Cadaverine-induced induction of superoxide dismutase gene expression in Mesembryanthemum crystallinum L., Dokl. Biol. Sci., 2005, vol. 403, nos. 1–6, pp. 257–259.

Asgher, M., Per, T.S., Anjum, S., Khan, M.I.R., Masood, A., Verma, S., and Khan, N.A., Contribution of glutathione in heavy metal stress tolerance in plants, in Reactive Oxygen Species and Antioxidant Systems in Plants: Role and Regulation under Abiotic Stress, Khan, M.I.R. and Khan, N.A., Eds., Singapore: Springer-Verlag, 2017, pp. 297–313. https://doi.org/10.1007/978-981-10-5254-5_12


Bienert, G.P., Moller, A.L., Kristiansen, K.A., Schulz, A., Møller, I.M., Schjoerring, J.K., and Jahn, T.P., Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes, J. Biol. Chem., 2007, vol. 282, no. 2, pp. 1183– 1192. https://doi.org/10.1074/jbc.M603761200

Brosché, M., Merilo, E., Mayer, F., Pechter, P., Puzõrjova, I., Brader, G., Kangasjärvi, J., and Kollist, H., Natural variation in ozone sensitivity among Arabidopsis thaliana accessions and its relation to stomatal conductance, Plant Cell Environ., 2010, vol. 33, no. 6, pp. 914–925. https://doi.org/10.1111/j.1365-3040.2010.02116.x

Cai, Q., Zhang, J., Guo, C., and Al, E., Reviews of the physiological roles and molecular biology of polyamines in higher plants, J. Fujian Educ. Coll., 2006, vol. 7, pp. 118–124. https://doi.org/10.3969/j.issn.1673-9884.2006.10.039

Chen, X., Chen, Q., Zhang, X., Li, R., Jia, Y., Ef, A.A., Jia, A., Hu, L., and Hu, X., Hydrogen sulfide mediates nicotine biosynthesis in tobacco (Nicotiana tabacum) under high temperature conditions, Plant Physiol. Biochem., 2016, vol. 104, pp. 174–179. https://doi.org/10.1016/j.plaphy.2016.02.033

Chen, D., Shao, Q., Yin, L., Younis, A., and Zheng, B., Polyamine function in plants: Metabolism, regulation on development, and roles in abiotic stress responses, Front. Plant Sci., 2019, vol. 9, art. ID 1945. https://doi.org/10.3389/fpls.2018.01945

Corpas, F.J. and Barroso, J.B., Nitric oxide synthase-like activity in higher plants, Nitric Oxide, 2017, vol. 68, pp. 5–6. https://doi.org/10.1016/j.niox.2016.10.009

Courtois, C., Besson, A., Dehan, J., Bourque, S., Dobrowolska, G., Pugin, A., and Wendehenne, D., Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases, J. Exp. Bot., 2008, vol. 59, no. 2, pp. 155–163. https://doi.org/10.1093/jxb/erm197

De Oliveira, L.F., Navarro, B.V., Cerruti, G., et al., Polyamines and amino acid related metabolism: the roles of arginine and ornithine are associated with the embryogenic potential, Plant Cell Physiol., 2018, vol. 59, pp. 1084–1098. https://doi.org/10.1093/pcp/pcy049

Diao, Q., Song, Y., Shi, D., and Qi, H., Interaction of polyamines, abscisic acid, nitric oxide, and hydrogen peroxide under chilling stress in tomato (Lycopersicon esculentum Mill.) seedlings, Front. Plant Sci., 2017, vol. 8, art. ID 203. https://doi.org/10.3389/fpls.2017.00203

Dubovskaya, L.V., Kolesneva, E.V., Knyazev, D.M., and Volotovskii, I.D., Protective role of nitric oxide during hydrogen peroxide-induced oxidative stress in tobacco plants, Russ. J. Plant Physiol., 2007, vol. 54, no. 6, pp. 755–761. https://doi.org/10.1134/S1021443707060064

Ebeed, H.T., Hassan, N.M., and Aljarani, A.M., Exogenous applications of Polyamines modulate drought responses in wheat through osmolytes accumulation, increasing free polyamine levels and regulation of polyamine biosynthetic genes, Plant Physiol. Biochem., 2017, vol. 118, pp. 438–448. https://doi.org/10.1016/j.plaphy.2017.07.014

Echevarría-Machado, I., Muñoz-Sánchez, A., Loyola-Vargas, V.M., and Hernández-Sotomayor, S.M.T., Spermine stimulation of phospholipase C from Catharanthus roseus transformed roots, J. Plant Physiol., 2002, vol. 159, no. 11, pp. 1179–1188. https://doi.org/10.1078/0176-1617-00893

Farnese, F.S., Menezes-Silva, P.E., Gusman, G.S., and Oliveira, J.A., When bad guys become good ones: the key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress, Front. Plant Sci., 2016, vol. 7, art. ID 471. https://doi.org/10.3389/fpls.2016.00471

Fraudentali, I., Rodrigues-Pousada, R.A., Angelini, R., Ghuge, S.A., and Cona, A., Plant copper amine oxidases: Key players in hormone signaling leading to stress-induced phenotypic plasticity, Int. J. Mol. Sci., 2021, vol. 22, no. 10, art. ID 5136. https://doi.org/10.3390/ijms22105136

Gautam, V., Kaur, R., Kohli, S.K., Verma, V., Kaur, P., Singh, R., Saini, P., Arora, S., Thukral, A.K., Karpets, Yu.V., Kolupaev, Yu.E., and Bhardwaj, R., ROS compartmentalization in plant cells under abiotic stress condition, in Reactive Oxygen Species and Antioxidant Systems in Plants: Role and Regulation under Abiotic Stress, Khan, M.I.R. and Khan, N.A., Eds., Singapore: Springer-Verlag, 2017, pp. 89–114. https://doi.org/10.1007/978-981-10-5254-5_4


Ghosh, N., Das, S.P., Mandal, C., Gupta, S., Das, K., Dey, N., and Adak, M.K., Variations of antioxidative responses in two rice cultivars with polyamine treatment under salinity stress, Physiol. Mol. Biol. Plants, 2012, vol. 18, no. 4, pp. 301–313. https://doi.org/10.1007/s12298-012-0124-8

Gill, S.S. and Tuteja, N., Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants, Plant Physiol. Biochem., 2010, vol. 48, no. 12, pp. 909–930. https://doi.org/10.1016/j.plaphy.2010.08.016

Groß, F., Rudolf, E.-E., Thiele, B., Durner, J., and Astier, J., Copper amine oxidase 8 regulates arginine-dependent nitric oxide production in Arabidopsis thaliana, J. Exp. Bot., 2017, vol. 68, no. 9, pp. 2149–2162. https://doi.org/10.1093/jxb/erx105

Guo, H., Xiao, T., Zhou, H., Xie, Y., and Shen, W., Hydrogen sulfide: a versatile regulator of environmental stress in plants, Acta Physiol. Plant., 2016, vol. 38, no. 1, art. ID 16. https://doi.org/10.1007/s11738-015-2038-x

Gupta, K.J. and Kaiser, W.M., Production and scavenging of nitric oxide by barley root mitochondria, Plant Cell Physiol., 2010, vol. 51, no. 4, pp. 576–584. https://doi.org/10.1093/pcp/pcq022

Gupta, K., Dey, A., and Gupta, B., Plant polyamines in abiotic stress responses, Acta Physiol. Plant., 2013, vol. 35, pp. 2015–2036. https://doi.org/10.1007/s11738-013-1239-4

Gupta, K.J., Hancock, J.T., Petrivalsky, M., Kolbert, Z., Lindermayr, C., Durner, J., Barroso, J.B., Palma, J.M., Brouquisse, R., and Wendehenne, D., Recommendations on terminology and experimental best practice associated with plant nitric oxide research, New Phytol., 2020, vol. 225, no. 5, pp. 1828–2834. https://doi.org/10.1111/nph.16157

Hancock, J.T., Hydrogen sulfide and environmental stresses, Environ. Exp. Bot., 2019, vol. 161, pp. 50–56. https://doi.org/10.1016/j.envexpbot.2018.08.034

Hao, Y., Huang, B., Jia, D., Mann, T., Jiang, X., Qiu, Y., Niitsu, M., Berberich, T., Kusano, T., and Liu, T., Identification of seven polyamine oxidase genes in tomato (Solanum lycopersicum L.) and their expression profiles under physiological and various stress conditions, J. Plant Physiol., 2018, vol. 228, pp. 1–11. https://doi.org/10.1016/j.jplph.2018.05.004

He, H. and He, L., The role of carbon monoxide signaling in the responses of plants to abiotic stresses, Nitric Oxide, 2014, vol. 42, pp. 40–43. https://doi.org/10.1016/j.niox.2014.08.011

Jing, J., Guo, S., Li, Y., and Li, W., The alleviating effect of exogenous polyamines on heat stress susceptibility of different heat resistant wheat (Triticum aestivum L.) varieties, Sci. Rep., 2020, vol. 10, art. ID 7467. https://doi.org/10.1038/s41598-020-64468-5

Kaur-Sawhney, R., Tiburcio, A.F., Altabella, T., and Galston, A.W., Polyamines in plants: An overview, J. Cell Mol. Biol., 2003, vol. 2, pp. 1–12.

Khan, A.S., Singh, Z., Abbasi, N.A., and Swinny, E.E., Pre- or post-harvest application of putrescine and low temperature storage affect fruit ripening and quality of ‘Angelino’ plum, J. Sci. Food Agric., 2008, vol. 88, pp. 1686–1695. https://doi.org/10.1002/jsfa.3265

Kohli, S.K., Handa, N., Gautam, V., Bali, S., Sharma, A., Khanna, K., Arora, S., Thukral, K.A., Ohri, P., Karpets, Yu.V., Kolupaev, Yu.E., and Bhardwaj, R., ROS signaling in plants under heavy metal stress, in Reactive Oxygen Species and Antioxidant Systems in Plants: Role and Regulation under Abiotic Stress, Khan, M.I.R. and Khan, N.A., Eds., Singapore: Springer-Verlag, pp. 185–214. https://doi.org/10.1007/978-981-10-5254-5_8

Kokorev, A.I., Kolupaev, Yu.E., Shkliarevskyi, M.A., and Lugovaya, A.A., The effect of cadaverine on redox homeostasis of wheat seedling roots and their resistance to damage heating, Vestn. Tomsk. Gos. Univ., Biol., 2021, vol. 54, pp.116–137. https://doi.org/10.17223/19988591/54/6

Kokorev, A.I., Kolupaev, Yu.E., Yastreb, T.O., Horielova, E.I., and Dmitriev, A.P., Realization of polyamines’ effect on the state of pea stomata with the involvement of calcium and components of lipid signaling, Cytol. Genet., 2021, vol. 55, no. 2, pp. 117–124. https://doi.org/10.3103/S0095452721020079

Kokorev, A.I., Shkliarevskyi, M.A., Shvydenko, N.V., and Kolupaev, Yu.E., Possible role of hydrogen sulfide in induction of activity of antioxidative enzymes and heat resistance of wheat seedlings by putrescine, Visn. Hark. nac. agrar. univ., 2020, vol. 1, no. 49, pp. 44–53. https://doi.org/10.35550/vbio2020.01.044

Kolbert, Z., Barroso, J.B., Brouquisse, R., Corpas, F.J., Gupta, K.J., Lindermayr, C., Loake, G.J., Palma, J.M., Petřivalský, M., Wendehenne, D., and Hancock, J.T., A forty year journey: The generation and roles of NO in plants, 2019, Nitric Oxide, vol. 93, pp. 53–70. https://doi.org/10.1016/j.niox.2019.09.006

Kolupaev, Yu.E., Karpets, Yu.V., Beschasniy, S.P., abd Dmitriev, A.P., Gasotransmitters and their role in adaptive reactions of plant cells, Cytol. Genet., 2019, vol. 53, no. 5, pp. 392–406. https://doi.org/10.3103/S0095452719050098

Kolupaev, Yu.E., Karpets, Yu.V., and Kabashnikova, L.F., Antioxidative system of plants: cellular compartmentalization, protective and signaling functions, mechanisms of regulation (review), Appl. Biochem. Microbiol., 2019, vol. 55, no. 5, pp. 441–459. https://doi.org/10.1134/S0003683819050089

Kolupaev, Yu.E., Kokorev, A.I., Yastreb, T.O., and Horielova, E.I., Hydrogen peroxide as a signal mediator at inducing heat resistance in wheat seedlings by putrescine, Ukr. Biochem. J., 2019, vol. 91, no. 6, pp. 103–111.https://doi.org/10.15407/ubj91.06.103

Kolupaev, Yu.E., Kokorev, A.I., and Shkliarevskyi, M.A., Calcium-dependent changes in the activity of antioxidant enzymes and heat resistance of wheat seedlings under the influence of exogenous putrescine, Vestn. Tomsk. Gos. Univ., Biol., 2020, vol. 51, pp. 105–122. https://doi.org/10.17223/19988591/51/6

Kolupaev, Yu.E., Kokorev, A.I., Shkliarevskyi, M.A., Lugovaya, A.A., Karpets, Yu.V., and Ivanchenko, O.E., Role of NO synthesis modification in the protective effect of putrescine in wheat seedlings subjected to heat stress, Appl. Biochem. Microbiol., 2021, vol. 57, no. 3, pp. 384–391. https://doi.org/10.1134/S0003683821030066

Kozeko, L.Ye. and Kordyum, E.L., Using of heat shock proteins HSP70 for evaluation of plant state in natural phytocenoses: approaches and problems, Visn. Hark. nac. agrar. univ., 2021, vol. 2, no. 53, pp. 23–40. https://doi.org/10.35550/vbio2021.02.023

Krasylenko, Y.A., Yemets, A.I., and Blume, Y.B., Functional role of nitric oxide in plants, Russ. J. Plant Physiol., 2010, vol. 57, pp. 451–461. https://doi.org/10.1134/S1021443710040011

Kumar, N. and Mallick, S., Ameliorative mechanisms of polyamines against abiotic stress in the rice plants, in Advances in Rice Research for Abiotic Stress Tolerance, Hasanuzzaman, M., Fujita, M., Nahar, K., and Biswas, J., Eds., Elsevier, 2019. https://doi.org/10.1016/B978-0-12-814332-2.00035-6


Kuznetsov, Vl.V., Radyukina, N.L., and Shevyakova, N.I., Polyamines and stress: Biological role, metabolism, and regulation, Russ. J. Plant Physiol., 2006, vol. 53, no. 5, pp. 583–604. https://doi.org/10.1134/S1021443706050025

Kuznetsov, Vl.V. and Shevyakova, N.I., Polyamines and plant adaptation to saline environment, in Desert Plants, Biology and Biotechnology, Ramawat, K.B., Ed., Berlin: Springer-Verlag, 2011, pp. 261–297. https://doi.org/10.1007/978-3-642-02550-1_13


Kwak, J.M., Nguyen, V., and Schroeder, J.I., The role of reactive oxygen species in hormonal responses, Plant Physiol., 2006, vol. 141, no. 2, pp. 323–329. https://doi.org/10.1104/pp.106.079004

Larher, F., Aziz, A., Deleu, C., Lemesle, P., Ghaffar, A., Bouchard, F., and Plasman, M., Suppression of the osmoinduced proline response of rapeseed leaf discs by polyamines, Physiol. Plant., 1998, vol. 102, no. 1, pp. 139–147. https://doi.org/10.1034/j.1399-3054.1998.1020118.x

Li, Z.G., Hydrogen sulfide: a multifunctional gaseous molecule in plants, Russ. J. Plant Physiol., 2013, vol. 60, no. 6, pp. 733–740. https://doi.org/10.1134/S1021443713060058

Li, Z.G., Analysis of some enzymes activities of hydrogen sulfide metabolism in plants, Methods Enzymol., 2015, vol. 555, pp. 253–269. https://doi.org/10.1016/bs.mie.2014.11.035

Li, Z.G., Xie, L.R., and Li, X.J., Hydrogen sulfide acts as a downstream signal molecule in salicylic acid-induced heat tolerance in maize (Zea mays L.) seedlings, J. Plant Physiol., 2015, vol. 177, pp. 121–127. https://doi.org/10.1016/j.jplph.2014.12.018

Li, Z., Zhou, H., Peng, Y., Zhang, X., Ma, X., Huang, L., and Yan, Y., Exogenously applied spermidine improves drought tolerance in creeping bentgrass associated with changes in antioxidant defense, endogenous polyamines and phytohormones, Plant Growth Regul., 2015, vol. 76, pp. 71–82. https://doi.org/10.1007/s10725-014-9978-9

Li, Z., Cheng, B., Peng, Y., and Zhang, Y., Adaptability to abiotic stress regulated by γ-aminobutyric acid in relation to alterations of endogenous polyamines and organic metabolites in creeping bentgrass, Plant Physiol. Biochem., 2020, vol. 157, pp. 185–194. https://doi.org/10.1016/j.plaphy.2020.10.025

Li, Q., Wang, Z., Zhao, Y., Zhang, X., Zhang, S., Bo, L., Wang, Y., Ding, Y., and An, L., Putrescine protects hulless barley from damage due to UV-B stress via H2S and H2O2-mediated signaling pathways, Plant Cell Rep., 2016, vol. 35, no. 5, pp. 1155–1168. https://doi.org/10.1007/s00299-016-1952-8

Li, Q. and Lancaster, J.R., Chemical foundations of hydrogen sulfide biology, Nitric Oxide, 2013, vol. 35, pp. 21–34. https://doi.org/10.1016/j.niox.2013.07.001

Liang, X., Zhang, L., Natarajan, S.K., and Becker, D.F., Proline mechanisms of stress survival, Antioxid. Redox Signaling., 2013, vol. 19, pp. 998–1011. https://doi.org/10.1089/ars.2012.5074

Liu, K., Fu, H., Bei, Q., and Luan, S., Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements, Plant Physiol., 2000, vol. 124, no. 3, pp. 1315–1326. https://doi.org/10.1104/pp.124.3.1315

Liu, J., Hou, Z.H., Liu, G.H., Hou, L.X., and Liu, X., Hydrogen sulfide may function downstream of nitric oxide in ethylene-induced stomatal closure in Vicia faba L., J. Integr. Agric., 2012, vol. 11, no. 10, pp. 1644–1653. https://doi.org/10.1016/S2095-3119(12)60167-1

Liu, Q, Nishibori, N., Imai, I., and Hollibaugh, J.T., Response of polyamine pools in marine phytoplankton to nutrient limitation and variation in temperature and salinity, Mar. Ecol.: Prog. Ser., 2016, vol. 544, pp. 93–105. https://doi.org/10.3354/meps11583

Liu, W., Tan, M., Zhang, C., et al., Functional characterization of murB-potABCD operon for polyamine uptake and peptidoglycan synthesis in Streptococcus suis, Microbiol. Res., 2017, vol. 207, pp. 177–187. https://doi.org/10.1016/j.micres.2017.11.008

Luo, L., Li, Z., Tang, M.Y., Cheng, B.Z., Zeng, W.H., Peng, Y., Nie, G., and Zhang, X.Q., Metabolic regulation of polyamines and γ-aminobutyric acid in relation to spermidine-induced heat tolerance in white clover, Plant Biol., 2020, vol. 22, no. 5, pp. 794–804. https://doi.org/10.1111/plb.13139

Mayer, M.P. and Bukau, B., Hsp70 chaperones: cellular functions and molecular mechanism, Cell Mol. Life Sci., 2005, vol. 62, pp. 670–684. https://doi.org/10.1007/s00018-004-4464-6

Medvedev, S.S., Principles of calcium signal generation and transduction in plant cells, Russ. J. Plant Physiol., 2018, vol. 65, no. 6, pp. 771–783. https://doi.org/10.1134/S1021443718060109

Mellidou, I., Karamanoli, K., Constantinidou, H.I.A., and Roubelakis-Angelakis, K.A., Antisense-mediated S‑adenosyl-L-methionine decarboxylase silencing affects heat stress responses of tobacco plants, Funct. Plant Biol., 2020, vol. 47, no. 7, pp. 651–658. https://doi.org/10.1071/FP19350

Miller, E.W., Dickinson, B.C., and Chang, C.J., Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling, Proc. Natl. Acad. Sci. U. S. A., 2010, vol. 107, no. 36, pp. 15681–15686. https://doi.org/10.1073/pnas.1005776107

Minocha, R., Majumdar, R., and Minocha, S.C., Polyamines and abiotic stress in plants: a complex relationship, Front. Plant Sci., 2014, vol. 5, art. ID 175. https://doi.org/10.3389/fpls.2014.00175

Miura, K., Okamoto, H., Okuma, E., Shiba, H., Kamada, H., Hasegawa, P.M., and Murata, Y., SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis, Plant J., 2013, vol. 73, no. 1, pp. 91–104. https://doi.org/10.1111/tpj.12014

Montillet, J.L., Leonhardt, N., Mondy, S., Tranchimand, S., Rumeau, D., Boudsocq, M., Garcia, A.V., Douki, T., Bigear, J., Lauriere, C., Chevalier, A., Castresana, C., and Hirt, H., An abscisic acid-independent oxylipin pathway controls stomatal closure and immune defense in Arabidopsis, PLoS Biol., 2013, vol. 11, no. 3, p. e1001513. https://doi.org/10.1371/journal.pbio.1001513

Mostofa, M.G., Yoshida, N., and Fujita, M., Spermidine pretreatment enhances heat tolerance in rice seedlings through modulating antioxidative and glyoxalase systems, Plant Growth Regul., 2014, vol. 73, no. 1, pp. 31–44. https://doi.org/10.1007/s10725-013-9865-9

Munemasa, S., Mori, I.C., Murata, Y., Methyl jasmonate signaling and signal crosstalk between methyl jasmonate and abscisic acid in guard cells, Plant Signal Behav., 2011, vol. 6, no. 7, pp. 939–941. https://doi.org/10.4161/psb.6.7.15439

Nahar, K., Hasanuzzaman, M., Rahman, A., et al., Polyamines confer salt tolerance in Mung Bean (Vigna radiata L.) by reducing sodium uptake, improving nutrient homeostasis, antioxidant defense, and methylglyoxal detoxification systems, Front. Plant Sci., 2016, vol. 7, art. ID 1104. https://doi.org/10.3389/fpls.2016.01104

Nahar, K., Motiar, R., Hasanuzzaman, M., Alam, Md.M., Anisur, R., Suzuki, T., and Fujita, M., Physiological and biochemical mechanisms of spermine-induced cadmium stress tolerance in mung bean (Vigna radiata L.) seedlings, Environ. Sci. Pollut. Res., 2016, vol. 23, pp. 21206–21218. https://doi.org/10.1007/s11356-016-7295-8

Nayyar, H. and Chander, S., Protective effects of polyamines against oxidative stress induced by water and cold stress in chickpea, J. Agron. Crop Sci., 2004, vol. 190, no. 5, pp. 355–365. https://doi.org/10.1111/j.1439-037X.2004.00106.x

Neill, S.J. and Burnett, E.C., Regulation of gene expression during water deficit stress, Plant Growth Regul., 1999, vol. 29, pp. 23–33. https://doi.org/10.1023/A:1006251631570

Pal, M., Szalai, G., and Janda, T., Speculation: Polyamines are important in abiotic stress signaling, Plant Sci., 2015, vol. 237, pp. 16–23. https://doi.org/10.1016/j.plantsci.2015.05.003

Pal, M., Tajti, J., Szalai, G., Peeva, V., Balazs, V., and Janda, T., Interaction of polyamines, abscisic acid and proline under osmotic stress in the leaves of wheat plants, Sci. Rep., 2018, vol. 8, art. ID 12839. https://doi.org/10.1038/s41598-018-31297-6

Pang, X.M., Zhang, Z.Y., Wen, X.P., Ban, Y., and Moriguchi, T., Polyamines, all-purpose players in response to environment stresses in plants, Plant Stress, 2007, vol. 1, no. 2, pp. 173–188.

Pegg, A.E., Functions of polyamines in mammals, J. Biol. Chem., 2016, vol. 291, pp. 14904–14912. https://doi.org/10.1074/jbc.R116.731661

Pinero, M.C., Otálora, G., Collado, J., López-Marín, J., and del Amor, F.M., Foliar application of putrescine before a short-term heat stress improves the quality of melon fruits (Cucumis melo L.), J. Sci. Food Agric., 2021, vol. 101, no. 4, pp. 1428–1435. https://doi.org/10.1002/jsfa.10756

Piterková, J., Luhová, L., Zajoncová, L., Šebela, M., and Petřivalský, M., Modulation of polyamine catabolism in pea seedlings by calcium during salinity stress, Plant Prot. Sci., 2012, vol. 48, no. 2, pp. 53–64. https://doi.org/10.17221/62/2011-PPS

Pottosin, I., Velarde-Buendía, A.-M., Zepeda-Jazo, I., Dobrovinskaya, O., and Shabala, S., Synergism between polyamines and ROS in the induction of Ca2+ and K+ fluxes in roots, Plant Signaling Behav., 2012, vol. 7, no. 9, pp. 1084–1087. https://doi.org/10.4161/psb.21185

Pottosin, I. and Shabala, S., Polyamines control of cation transport across plant membranes: Implications for ion homeostasis and abiotic stress signaling, Front. Plant Sci., 2014, vol. 5, art. ID 154. https://doi.org/10.3389/fpls.2014.00154

Pottosin, I., Velarde-Buendía, A.M., Bose, J., Fuglsang, A.T., and Shabala, S., Polyamines cause plasma membrane depolarization, activate Ca2+-, and modulate H+-ATPase pump activity in pea roots, J. Exp. Bot., 2014, vol. 65, no. 9, pp. 2463–2472.https://doi.org/10.1093/jxb/eru133

Pradedova, E.V., Nimaeva, O.D., and Salyaev, R.K., Redox processes in biological systems, Russ. J. Plant Physiol., 2017, vol. 64, no. 6, pp. 822–832. https://doi.org/10.1134/S1021443717050107

Qu, Y., An, Z., Zhuang, B., Jing, W., Zhang, Q., and Zhang, W., Copper amine oxidase and phospholipase D act independently in abscisic acid (ABA)-induced stomatal closure in Vicia faba and Arabidopsis, J. Plant Res., 2014, vol. 127, no. 4, pp. 533–544. https://doi.org/10.1007/s10265-014-0633-3

Riemenschneider, A., Wegele, R., Schmidt, A., and Papenbrock, J., Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana, FEBS J., 2005, vol. 272, no. 5, pp. 1291–1304. https://doi.org/10.1111/j.1742-4658.2005.04567.x

Rosales, E.P., Iannone, M., Groppa, M.D., and Benavides, M.P., Polyamines modulate nitrate reductase activity in wheat leaves: involvement of nitric oxide, Amino Acids, 2012, vol. 42, pp. 857–865. https://doi.org/10.1007/s00726-011-1001-4

Sarwat, M. and Tuteja, N., Hormonal signaling to control stomatal movement during drought stress, Plant Gene, Part B, 2017, vol. 11, pp. 143–153. https://doi.org/10.1016/j.plgene.2017.07.007

Seo, S.Y., Kim, Y.J., and Park, K.Y., Increasing polyamine contents enhanced the stress tolerance via reinforcement of antioxidative properties, Front. Plant Sci., 2019, vol. 10, art. ID 1331. https://doi.org/10.3389/fpls.2019.01331

Shan, C., Zhang, S., and Zhou, Y., Hydrogen sulfide is involved in the regulation of ascorbate-glutathione cycle by exogenous ABA in wheat seedling leaves under osmotic stress, Cereal Res. Commun., 2017, vol. 45, no. 3, pp. 411–420. https://doi.org/10.1556/0806.45.2017.021

Sharova, E.I. and Medvedev, S.S., Redox reactions in apoplast of growing cells, Russ. J. Plant Physiol., 2017, vol. 64, no. 1, pp. 1–14. https://doi.org/10.1134/S1021443717010149

Shen, W., Nada, K., and Tachibana, S., Involvement of polyamines in the chilling tolerance of cucumber cultivars, Plant Physiol., 2000, vol. 124, no. 1, pp. 431–440.https://doi.org/10.1104/pp.124.1.431

Shen, W. and Huber, S.C., Polycations globally enhance binding of 14-3-3ω to target proteins in spinach leaves, Plant Cell Physiol., 2006, vol. 47, pp. 764–771. https://doi.org/10.1093/pcp/pcj050

Shi, H. and Chan, Z., Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway, J. Integr. Plant Biol., 2014, vol. 56, no. 2, pp. 114–121. https://doi.org/10.1111/jipb.12128

Singh, P., Basu, S., and Kumar, G., Polyamines metabolism: A way ahead for abiotic stress tolerance in crop plants, in Biochemical, Physiological and Molecular Avenues for Combating Abiotic Stress in Plants, Wani, S.H., Ed., Amsterdam: Elsevier, 2018, pp. 39–55. https://doi.org/10.1016/B978-0-12-813066-7.00003-6


Singh, S., Kumar, V., Kapoor. D., Kumar. S., Singh, S., Dhanjal, D.S., Datta, S., Samuel, Jastin., Dey, P., Wang, S., Prasad, R., and Singh, J., Revealing on hydrogen sulfide and nitric oxide signals co-ordination for plant growth under stress conditions, Physiol. Plant, 2020, vol. 168, no. 2, pp. 301–317. https://doi.org/10.1111/ppl.13002

Sobieszczuk-Nowicka, E., Polyamine catabolism adds fuel to leaf senescence, Amino Acids, 2017, vol. 49, no. 1, pp. 49–56. https://doi.org/10.1007/s00726-016-2377-y

Suhita, D., Raghavendra, A.S., Kwak, J.M., and Vavasseur, A., Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure, Plant Physiol., 2004, vol. 134, no. 4, pp. 1536–1545. https://doi.org/10.1104/pp.103.032250

Takahashi, Y., Tahara, M., Yamada, Y., et al., Characterization of the polyamine biosynthetic pathways and salt stress response in Brachypodium distachyon, J. Plant Growth Regul., 2017, vol. 37, pp. 625–634. https://doi.org/10.1007/s00344-017-9761-z

Tang, S., Zhang, H., Li, L., Liu, X., Chen, L., Chen, W., Ding, Y., Exogenous spermidine enhances the photosynthetic and antioxidant capacity of rice under heat stress during early grain-filling period, Funct. Plant Biol., 2018, vol. 45, pp. 911–921. https://doi.org/10.1071/FP17149

Todorova, D., Katerova, Z., Sergiev, I., and Alexieva, V., Role of polyamines in alleviating salt stress, in Ecophysiology and Responses of Plants under Salt Stress, Ahmad, P., Azooz, M.M., and Prasad, M.N.V., Eds., New York: Springer-Verlag, 2013, vol. 13, pp. 355–379.https://doi.org/10.1007/978-1-4614-4747-4_13

Tomar, P.C., Lakra, N., and Mishra, S.N., Cadaverine: A lysine catabolite involved in plant growth and development, Plant Signaling Behav., 2013, vol. 8, art. ID e25850. https://doi.org/10.4161/psb.25850

Toumi, I., Pagoulatou, M.G., Margaritopoulou, T., Milioni, D., and Roubelakis-Angelakis, K.A., Genetically modified heat shock protein90s and polyamine oxidases in Arabidopsis reveal their interaction under heat stress affecting polyamine acetylation, oxidation and homeostasis of reactive oxygen species, Plants (Basel), 2019, vol. 8, no. 9, art. ID 323. https://doi.org/10.3390/plants8090323

Wang, W., Vinocur, B., Shoseyov, O., and Altman, A., Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response, Trends Plant Sci., 2004, vol. 9, no. 5, pp. 244–252. https://doi.org/10.1016/j.tplants.2004.03.006

Wang, L., Hou, Z., Hou, L., Zhao, F., and Liu, X., H2S induced by H2O2 mediates drought-induced stomatal closure in Arabidopsis thaliana, Chinese Bull. Bot., 2012, vol. 47, pp. 217–225. https://doi.org/10.3724/SP.J.1259.2012.00217

Wen, X. and Moriguchi, T., Role of polyamines in stress response in horticultural crops, in Abiotic Stress Biology in Horticultural Plants, Kanayama, Y. and Kochetov, A., Eds., New York: Springer-Verlag, 2015, pp. 35–45. https://doi.org/10.1007/978-4-431-55251-2_3


Wi, S., Kim, W.T., and Park, K.Y., Overexpression of carnation S-adenosylmethionine decarboxylase gene generates a broad-spectrum tolerance to abiotic stresses in transgenic tobacco plants, Plant Cell Rep., 2006, vol. 25, pp. 1111–1121. https://doi.org/10.1007/s00299-006-0160-3

Wimalasekera, R., Villar, C., and Begum, T., and Sche-rer, G.F.E., COPPER AMINE OXIDASE 1 (CuAO1) of Arabidopsis thaliana contributes to abscisic acid-and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction, Mol. Plant, 2011, vol. 4, no. 4, pp. 663–678. https://doi.org/10.1093/mp/ssr023

Wimalasekera, R., Tebartz, F., and Scherer, G.F., Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses, Plant Sci., 2011, vol. 181, no. 5, pp. 593–603. https://doi.org/10.1016/j.plantsci.2011.04.002

Xu, C., Wu, X., and Zhang, H., Impact of D–Arg on drought resistance and endogenous polyamines in mycorrhizal Pinus massoniana, J. Nanjing For. Univ., 2009, vol. 33, pp. 19–23. https://doi.org/10.3969/j.issn.1000-2006.2009.04.004

Yadav, S.K., Pavan, K.D., Tiwari, Y.K., Jainender, J.L.N., Vanaja, M., and Maheswari, M., Exogenous application of bio-regulators for alleviation of heat stress in seedlings of maize, J. Agric. Res., 2017, vol. 2, no. 3, art. ID 000137.

Yamasaki, H. and Cohen, M.F., Biological consilience of hydrogen sulfide and nitric oxide in plants: Gases of primordial earth linking plant, microbial and animal physiologies, Nitric Oxide, 2016, vols. 55–56, pp. 91–100. https://doi.org/10.1016/j.niox.2016.04.002

Yang, B., Wu, J., Gao, F., Wang, J., and Su, G., Polyamine-induced nitric oxide generation and its potential requirement for peroxide in suspension cells of soybean cotyledon node callus, Plant Physiol. Biochem., 2014, vol. 79, pp. 41–47. https://doi.org/10.1016/j.plaphy.2014.02.025

Yastreb, T.O., Kolupaev, Yu.E., Kokorev, A.I., Horielova, E.I., and Dmitriev, A.P., Methyl jasmonate and nitric oxide in regulation of the stomatal apparatus of Arabidopsis thaliana, Cytol. Genet., 2018, vol. 52, no. 6, pp. 400–405. https://doi.org/10.3103/S0095452718060129

Yemets, A.I., Krasylenko, Y.A., and Blume, Y.B., Nitric oxide and UV-B radiation, in Nitric Oxide Action in Abiotic Stress Responses in Plants, Khan, M.N., Mobin, M., Mohammad, F., and Corpas, F.J., Eds., Cham: Springer-Verlag, 2015, pp. 141–154. https://doi.org/10.1007/978-3-319-17804-2_9


Yemets, A.I., Karpets, Yu.V., Kolupaev, Yu.E., and Blume, Ya.B., Emerging technologies for enhancing ROS/RNS homeostasis, in Reactive Oxygen, Nitrogen and Sulfur Species in Plants: Production, Metabolism, Signaling and Defense Mechanisms, Hasanuzzaman, M., Fotopoulos, V., Nahar, K., and Fujita, M., Eds., Chichester: Wiley, 2019, vol. 2, pp. 873–922. https://doi.org/10.1002/9781119468677.ch39


Yu, Z., Jia, D., and Liu, T., Polyamine oxidases play various roles in plant development and abiotic stress tolerance, Plants, 2019, vol. 8, art. ID 184. https://doi.org/10.3390/plants8060184

Yun, B.W., Feechan, A., Yin, M., Yin, M., Saidi, N.B.B., Bihan, T.L., Yu, M., Moore, J.W., Kang, J.-G., Kwon, E., Spoel, S.H., Pallas, J.A., and Loake, G.J., S-nitrosylation of NADPH oxidase regulates cell death in plant immunity, Nature, 2011, vol. 478, pp. 264–268. https://doi.org/10.1038/nature

Zhou, R., Hu, Q., Pu, Q., Chen, M., Zhu, X., Gao, C., Zhou, G., Liu, L., Wang, Z., Yang, J., Zhang, J., and Cao, Y., Spermidine enhanced free polyamine levels and expression of polyamine biosynthesis enzyme gene in rice spike lets under heat tolerance before heading, Sci. Rep., 2020, vol. 10, art. ID 8976. https://doi.org/10.1038/s41598-020-64978-2

Ziogas, V., Molassiotis, A., Fotopoulos, V., and Tanou, G., Hydrogen sulfide: A potent tool in postharvest fruit biology and possible mechanism of action, Front. Plant Sci., 2018, vol. 9, art. ID 1375. https://doi.org/10.3389/fpls.2018.01375