Skip to main content
Log in

Polyamines: Involvement in Cellular Signaling and Plant Adaptation to the Effect of Abiotic Stressors

  • Published:
Cytology and Genetics Aims and scope Submit manuscript

Abstract

Polyamines (PA) are aliphatic amines found in all cells, including plant cells. Putrescine, spermidine, and spermine are the most common PA in higher plants. PA are localized in cell walls, vacuoles, mitochondria, chloroplasts, and the nucleus. Under adverse conditions, the content of PA in plant tissues increases significantly. These compounds are considered to be typical stress metabolites. They are involved in the stabilization of biomacromolecules and membrane structures. At the same time, in recent years, the functions of PA under stress conditions are considered in the context of their involvement in the processes of cellular signaling. The review presents current information on the synthesis and catabolism of PA. The processes of formation of hydrogen peroxide, which acts as one of the key signaling molecules, from PA are considered. A possible synthesis of nitric oxide during the oxidative degradation of PA is discussed. The information about the effect of PA on calcium homeostasis of plant cells and involvement of PA in the regulation of ionic (including calcium) channels are provided. A gasotransmitter hydrogen sulfide is considered as one of the mediators in the implementation of the effects of PA. The work summarizes information about the role of PA in the maintenance of redox balance in plant cells, their involvement in the regulation of the expression of stress protein genes, the state of the stomatal apparatus, and other processes related to the adaptation to adverse environmental factors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. 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

    Article  CAS  Google Scholar 

  2. 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

    Article  CAS  PubMed  Google Scholar 

  3. 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

    Article  CAS  PubMed  Google Scholar 

  4. 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

    Article  CAS  PubMed Central  Google Scholar 

  5. 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

    Article  CAS  PubMed  Google Scholar 

  6. 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

    Article  CAS  Google Scholar 

  7. 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

    Article  PubMed  PubMed Central  Google Scholar 

  8. 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

    Article  CAS  PubMed  Google Scholar 

  9. 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.

    Article  CAS  PubMed  Google Scholar 

  10. 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

    Book  Google Scholar 

  11. 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

    Article  CAS  PubMed  Google Scholar 

  12. 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

    Article  CAS  PubMed  Google Scholar 

  13. 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

    Article  Google Scholar 

  14. 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

    Article  CAS  PubMed  Google Scholar 

  15. 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

    Article  PubMed  PubMed Central  Google Scholar 

  16. 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

    Article  CAS  PubMed  Google Scholar 

  17. 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

    Article  CAS  PubMed  Google Scholar 

  18. 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

    Article  CAS  PubMed  Google Scholar 

  19. 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

    Article  PubMed  PubMed Central  Google Scholar 

  20. 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

    Article  CAS  Google Scholar 

  21. 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

    Article  CAS  PubMed  Google Scholar 

  22. 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

    Article  Google Scholar 

  23. 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

    Article  PubMed  PubMed Central  Google Scholar 

  24. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. 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

    Book  Google Scholar 

  26. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. 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

    Article  CAS  PubMed  Google Scholar 

  28. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. 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

    Article  CAS  Google Scholar 

  30. 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

    Article  PubMed  Google Scholar 

  31. 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

    Article  CAS  Google Scholar 

  32. 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

    Article  PubMed  Google Scholar 

  33. 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

    Article  CAS  Google Scholar 

  34. 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

    Article  CAS  PubMed  Google Scholar 

  35. 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

    Article  CAS  PubMed  Google Scholar 

  36. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. 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.

    Google Scholar 

  38. 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

    Article  CAS  Google Scholar 

  39. 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

  40. 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

    Article  Google Scholar 

  41. 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

    Article  Google Scholar 

  42. 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

  43. 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

    Article  CAS  PubMed  Google Scholar 

  44. 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

    Article  Google Scholar 

  45. 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

    Article  CAS  Google Scholar 

  46. 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

  47. 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

    Article  Google Scholar 

  48. 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

    Article  CAS  Google Scholar 

  49. 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

  50. 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

    Article  CAS  Google Scholar 

  51. 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

    Book  Google Scholar 

  52. 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

    Article  CAS  Google Scholar 

  53. 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

    Book  Google Scholar 

  54. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. 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

    Article  CAS  PubMed  Google Scholar 

  56. 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

    Article  CAS  Google Scholar 

  57. 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

    Article  CAS  PubMed  Google Scholar 

  58. 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

    Article  CAS  PubMed  Google Scholar 

  59. 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

    Article  CAS  Google Scholar 

  60. 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

    Article  CAS  PubMed  Google Scholar 

  61. 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

    Article  CAS  PubMed  Google Scholar 

  62. 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

    Article  CAS  PubMed  Google Scholar 

  63. 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

    Article  CAS  Google Scholar 

  64. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. 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

    Article  CAS  Google Scholar 

  66. 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

    Article  CAS  Google Scholar 

  67. 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

    Article  CAS  PubMed  Google Scholar 

  68. 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

    Article  CAS  PubMed  Google Scholar 

  69. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. 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

    Article  CAS  Google Scholar 

  71. 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

    Article  CAS  PubMed  Google Scholar 

  72. 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

    Article  PubMed  PubMed Central  Google Scholar 

  73. 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

    Article  PubMed  PubMed Central  Google Scholar 

  74. 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

    Article  CAS  PubMed  Google Scholar 

  75. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. 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

    Article  CAS  Google Scholar 

  77. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. 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

    Article  PubMed  PubMed Central  Google Scholar 

  79. 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

    Article  CAS  Google Scholar 

  80. 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

    Article  CAS  Google Scholar 

  81. 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

    Article  CAS  Google Scholar 

  82. 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

    Article  CAS  PubMed  Google Scholar 

  83. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. 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.

    Google Scholar 

  85. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. 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

    Article  CAS  PubMed  Google Scholar 

  87. 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

    Article  Google Scholar 

  88. 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

    Article  CAS  Google Scholar 

  89. 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

    Article  PubMed  PubMed Central  Google Scholar 

  90. 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

  91. 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

    Article  CAS  Google Scholar 

  92. 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

    Article  CAS  PubMed  Google Scholar 

  93. 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

    Article  CAS  PubMed  Google Scholar 

  94. 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

    Article  CAS  PubMed  Google Scholar 

  95. 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

    Article  CAS  Google Scholar 

  96. 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

    Article  PubMed  PubMed Central  Google Scholar 

  97. 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

    Article  CAS  Google Scholar 

  98. 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

    Article  CAS  Google Scholar 

  99. 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

  100. 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

    Article  CAS  PubMed  Google Scholar 

  101. 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

    Article  CAS  PubMed  Google Scholar 

  102. 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

    Book  Google Scholar 

  103. 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

    Article  CAS  PubMed  Google Scholar 

  104. 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

    Article  CAS  PubMed  Google Scholar 

  105. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. 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

    Article  CAS  Google Scholar 

  107. 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

    Article  CAS  PubMed  Google Scholar 

  108. 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

  109. 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

    Article  CAS  Google Scholar 

  110. 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

    Article  CAS  PubMed Central  Google Scholar 

  111. 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

    Article  CAS  PubMed  Google Scholar 

  112. 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

    Article  CAS  Google Scholar 

  113. 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

    Book  Google Scholar 

  114. 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

    Article  CAS  PubMed  Google Scholar 

  115. 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

    Article  CAS  PubMed  Google Scholar 

  116. 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

    Article  CAS  PubMed  Google Scholar 

  117. 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

    Article  Google Scholar 

  118. 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.

    Google Scholar 

  119. 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

    Article  CAS  PubMed  Google Scholar 

  120. 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

    Article  CAS  PubMed  Google Scholar 

  121. 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

    Article  Google Scholar 

  122. 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

    Book  Google Scholar 

  123. 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

    Book  Google Scholar 

  124. 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

    Article  CAS  PubMed Central  Google Scholar 

  125. 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

  126. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. 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

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was not funded by any specific grant from financial institutions in the state, commercial, or noncommercial sectors.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Yu. E. Kolupaev or A. P. Dmitriev.

Ethics declarations

The authors declare that they have no conflict of interests.

This article contains no studies involving human participants or animals as objects of study.

Additional information

Translated by A. Barkhash

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kolupaev, Y.E., Kokorev, A.I. & Dmitriev, A.P. Polyamines: Involvement in Cellular Signaling and Plant Adaptation to the Effect of Abiotic Stressors. Cytol. Genet. 56, 148–163 (2022). https://doi.org/10.3103/S0095452722020062

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0095452722020062

Navigation