In recent years, research on spermine (Spm) has turned up a lot of new information about this essential polyamine, especially as it is able to counteract damage from abiotic stresses. Spm has been shown to protect plants from a variety of environmental insults, but whether it can prevent the adverse effects of drought has not yet been reported. Drought stress increases endogenous Spm in plants and exogenous application of Spm improves the plants' ability to tolerate drought stress. Spm's role in enhancing antioxidant defense mechanisms, glyoxalase systems, methylglyoxal (MG) detoxification, and creating tolerance for drought-induced oxidative stress is well documented in plants. However, the influences of enzyme activity and osmoregulation on Spm biosynthesis and metabolism are variable. Spm interacts with other molecules like nitric oxide (NO) and phytohormones such as abscisic acid, salicylic acid, brassinosteroids, and ethylene, to coordinate the reactions necessary for developing drought tolerance. This review focuses on the role of Spm in plants under severe drought stress. We have proposed models to explain how Spm interacts with existing defense mechanisms in plants to improve drought tolerance.

Department of Biology College of Science Imam Abdulrahman Bin Faisal University 383 Dammam 34212 Saudi Arabia

Department of Botany and Plant Physiology Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague 16500 Prague Czech Republic

Department of Botany Faculty of Sciences University of Agriculture Faisalabad Faisalabad 38000 Pakistan

Department of Horticulture Sher e Bangla Agricultural University Dhaka 1207 Bangladesh

Department of Plant Physiology Faculty of Agrobiology and Food Resources Slovak University of Agriculture 94976 Nitra Slovakia

Key Laboratory of Crop Physiology and Ecology in Southern China Ministry of Agriculture Nanjing Agricultural University Nanjing 210095 China

Key Laboratory of Southern Vegetable Crop Genetic Improvement in Ministry of Agriculture College of Horticulture Nanjing Agricultural University Nanjing 210095 China

State Key Laboratory of Grassland Agro Ecosystems School of Life Sciences Lanzhou University Lanzhou 730000 China

See more in PubMed

Tsaniklidis G., Pappi P., Tsafouros A., Charova S.N., Nikoloudakis N., Roussos P.A., Paschalidis K.A., Delis C. Polyamine Homeostasis in Tomato Biotic/Abiotic Stress Cross-Tolerance. Gene. 2020;727:144230. doi: 10.1016/j.gene.2019.144230. PubMed DOI

Hussain S.S., Ali M., Ahmad M., Siddique K.H. Polyamines: Natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol. Adv. 2011;29:300–311. doi: 10.1016/j.biotechadv.2011.01.003. PubMed DOI

Sequera-Mutiozabal M., Antoniou C., Tiburcio A.F., Alcázar R., Fotopoulos V. Polyamines: Emerging Hubs Promoting Drought and Salt Stress Tolerance in Plants. Curr. Mol. Bio. Rep. 2017;3:28–36. doi: 10.1007/s40610-017-0052-z. DOI

Zhang X., Shen L., Li F., Meng D., Sheng J. Methyl salicylate-induced arginine catabolism is associated with up-regulation of polyamine and nitric oxide levels and improves chilling tolerance in cherry tomato fruit. J. Agric. Food Chem. 2011;59:9351–9357. PubMed

Tiburcio A.F., Altabella T., Bitrián M., Alcázar R. The roles of polyamines during the lifespan of plants: From development to stress. Planta. 2014;240:1–18. doi: 10.1007/s00425-014-2055-9. PubMed DOI

Feng H.Y., Wang Z.M., Kong F.N., Zhang M.J., Zhou S.L. Roles of carbohydrate supply and ethylene, polyamines in maize kernel set. J. Integ. Plant Biol. 2011;53:388–398. doi: 10.1111/j.1744-7909.2011.01039.x. PubMed DOI

Alet A.I., Sánchez D.H., Cuevas J.C., Marina M., Carrasco P., Altabella T., Tiburcio A.F., Ruiz O.A. New insights into the role of spermine in Arabidopsis thaliana under long-term salt stress. Plant Sci. 2012;182:94–100. doi: 10.1016/j.plantsci.2011.03.013. PubMed DOI

Tavladoraki P., Cona A., Federico R., Tempera G., Viceconte N., Saccoccio S., Battaglia V., Toninello A., Agostinelli E. Polyamine catabolism: Target for antiproliferative therapies in animals and stress tolerance strategies in plants. Amino Acids. 2012;42:411–426. doi: 10.1007/s00726-011-1012-1. PubMed DOI

Hassan N., Ebeed H., Aljaarany A. Exogenous application of spermine and putrescine mitigate adversities of drought stress in wheat by protecting membranes and chloroplast ultra-structure. Physiol. Mol. Biol. Plants. 2020;26:233–245. doi: 10.1007/s12298-019-00744-7. PubMed DOI PMC

Dawood M.F., Abeed A.H. Spermine-priming restrained water relations and biochemical deteriorations prompted by water deficit on two soybean cultivars. Heliyon. 2020;6:e04038. doi: 10.1016/j.heliyon.2020.e04038. PubMed DOI PMC

Liu C.J., Wang H.R., Wang L., Han Y.Y., Hao J.H., Fan S.X. Effects of different types of polyamine on growth, physiological and biochemical nature of lettuce under drought stress. IOP Conf. Ser. Earth Environ. Sci. 2018;185:012010. doi: 10.1088/1755-1315/185/1/012010. DOI

Ebeed H.T., Hassan N.M., 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;118:438–448. doi: 10.1016/j.plaphy.2017.07.014. PubMed DOI

Li Z., Jing W., Peng Y., Zhang X.Q., Ma X., Huang L.K. Spermine alleviates drought stress in white clover with different resistance by influencing carbohydrate metabolism and dehydrins synthesis. PLoS ONE. 2015;10:e0120708. doi: 10.1371/journal.pone.0120708. PubMed DOI PMC

Taie H.A., El-Yazal M.A.S., Ahmed S.M., Rady M.M. Polyamines modulate growth, antioxidant activity, and genomic DNA in heavy metal–stressed wheat plant. Environ. Sci. Pollut. Res. 2019;1:1–13. doi: 10.1007/s11356-019-05555-7. PubMed DOI

Benavides M.P., Groppa M.D., Recalde L., Verstraeten S.V. Effects of polyamines on cadmium-and copper-mediated alterations in wheat (Triticum aestivum L.) and sunflower (Helianthus annuus L.) seedling membrane fluidity. Arch. Biochem. Biophys. 2018;654:27–39. doi: 10.1016/j.abb.2018.07.008. PubMed DOI

Rady M.M., Hemida K.A. Modulation of cadmium toxicity and enhancing cadmium-tolerance in wheat seedlings by exogenous application of polyamines. Ecotoxicol. Environ. Saf. 2015;119:178–185. PubMed

Fu X.Z., Xing F., Wang N.Q., Peng L.Z., Chun C.P., Cao L., Ling L.L., Jiang C.L. Exogenous spermine pretreatment confers tolerance to combined high-temperature and drought stress in vitro in trifoliate orange seedlings via modulation of antioxidative capacity and expression of stress-related genes. Biotech. Biotechnol. Equip. 2014;28:192–198. doi: 10.1080/13102818.2014.909152. PubMed DOI PMC

Jankovska-Bortkevič E., Gavelienè V., Šveikauskas V., Mockevičiutè R., Jankauskienè J., Todorova D., Sergiev I., Jurkonienè S. Foliar application of polyamines modulates winter oilseed rape responses to increasing cold. Plants. 2020;9:179. doi: 10.3390/plants9020179. PubMed DOI PMC

Nahar K., Hasanuzzaman M., Alam M.M., Rahman A., Mahmud J.A., Suzuki T., Fujita M. Insights into spermine-induced combined high temperature and drought tolerance in mung bean: Osmoregulation and roles of antioxidant and glyoxalase system. Protoplasma. 2017;254:445–460. doi: 10.1007/s00709-016-0965-z. PubMed DOI

Hasan M.M., Alharby H.F., Hajar A.S., Hakeem K.R., Alzahrani Y. The effect of magnetized water on the growth and physiological conditions of Moringa species under drought stress. Pol. J. Environ. Stud. 2019;28:1145–1155.

Hasan M.M., Alharby H.F., Uddin M.N., Ali M.A., Anwar Y., Fang X.W., Hakeem K.R., Alzahrani Y., Hajar A.S. Magnetized water confers drought stress tolerance in Moringa biotype via modulation of growth, gas exchange, lipid peroxidation and antioxidant activity. Pol. J. Environ. Stud. 2020;1:29.

Hasan M.M., Ali M.A., Soliman M.H., Alqarawi A.A., Abd Allah E.F., Fang X.-W. Insights into 28-homobrassinolide (HBR)-mediated redox homeostasis, AsA–GSH cycle, and methylglyoxal detoxification in soybean under drought-induced oxidative stress. J. Plant Inter. 2020;15:371–385. doi: 10.1080/17429145.2020.1832267. DOI

Khan A., Anwar Y., Hasan M., Iqbal A., Ali M., Alharby H.F., Hakeem K.R., Hasanuzzaman M. Attenuation of drought stress in Brassica seedlings with exogenous application of Ca2+ and H2O2. Plants. 2017;6:20. doi: 10.3390/plants6020020. PubMed DOI PMC

Ahammed G.J., Li X., Wan H., Zhou G., Cheng Y. SlWRKY81 reduces drought tolerance by attenuating proline biosynthesis in tomato. Scientia Hortic. 2020:270. doi: 10.1016/j.scienta.2020.109444. DOI

Ahammed G.J., Li X., Mao Q., Wan H., Zhou G., Cheng Y. The SlWRKY81 transcription factor inhibits stomatal closure by attenuating nitric oxide accumulation in the guard cells of tomato under drought. Physiol. Plantarum. 2020 doi: 10.1111/ppl.13243. PubMed DOI

Vanani F.R., Shabani L., Sabzalian M.R., Dehghanian F., Winner L. Comparative physiological and proteomic analysis indicates lower shock response to drought stress conditions in a self-pollinating perennial ryegrass. PLoS ONE. 2020;15:e0234317. doi: 10.1371/journal.pone.0234317. PubMed DOI PMC

Li K., Xing C., Yao Z., Huang X. Pbr MYB 21, a novel MYB protein of Pyrus betulaefolia, functions in drought tolerance and modulates polyamine levels by regulating arginine decarboxylase gene. Plant Biotechnol. J. 2017;15:1186–1203. doi: 10.1111/pbi.12708. PubMed DOI PMC

Adamipour N., Khosh-Khui M., Salehi H., Razi H., Karami A., Moghadam A. Role of genes and metabolites involved in polyamines synthesis pathways and nitric oxide synthase in stomatal closure on Rosa damascena Mill. under drought stress. Plant Physiol. Biochem. 2020;148:53–61. PubMed

Nahar K., Rahman M., Hasanuzzaman M., Alam M.M., Rahman A., Suzuki T., Fujita M. Physiological and biochemical mechanisms of spermine-induced cadmium stress tolerance in mung bean (Vigna radiata L.) seedlings. Environ. Sci. Pollut. Res. 2016;23:21206–21218. doi: 10.1007/s11356-016-7295-8. PubMed DOI

Rai P.K. Heavy metals/metalloids remediation from wastewater using free floating macrophytes of a natural wetland. Environ. Technol. Innovation. 2019;15:100393. doi: 10.1016/j.eti.2019.100393. DOI

Shelp B.J., Bozzo G.G., Trobacher C.P., Zarei A., Deyman K.L., Brikis C.J. Hypothesis/review: Contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress. Plant Sci. 2012;193:130–135. doi: 10.1016/j.plantsci.2012.06.001. PubMed DOI

Alcázar R., Altabella T., Marco F., Bortolotti C., Reymond M., Koncz C., Carrasco P., Tiburcio A.F. Polyamines: Molecules with regulatory functions in plant abiotic stress tolerance. Planta. 2010;231:1237–1249. PubMed

Sequera-Mutiozabal M., Tiburcio A.F., Alcázar R. Drought Stress Tolerance in Relation to Polyamine Metabolism in Plants. In: Hossain M., Wani S., Bhattacharjee S., Burritt D., Tran L.S., editors. Drought Stress Tolerance in Plants. Volume 1. Springer; Cham, Switzerland: 2016. DOI

Li H., Guo Y., Cui Q., Zhang Z., Yan X., Ahammed G.J., Yang X., Yang J., Wei C., Zhang X. Alkanes (C29 and C31)-Mediated Intracuticular Wax Accumulation Contributes to Melatonin- and ABA-Induced Drought Tolerance in Watermelon. J. Plant Growth Reg. 2020 doi: 10.1007/s00344-020-10099-z. DOI

Mueller N.D., Gerber J.S., Johnston M., Ray D.K., Ramankutty N., Foley J.A. Closing yield gaps through nutrient and water management. Nature. 2012 doi: 10.1038/nature11420. PubMed DOI

Iwuala E., Odjegba V., Sharma V., Alam A. Drought stress modulates expression of aquaporin gene and photosynthetic efficiency in Pennisetum glaucum (L.) R. Br. genotypes. Curr. Plant Biol. 2020;21:100131. doi: 10.1016/j.cpb.2019.100131. DOI

Maurel C., Boursiac Y., Luu D.T., Santoni V.R., Shahzad Z., Verdoucq L. Aquaporins in plants. Physiol. Rev. 2015;95:1321–1358. doi: 10.1152/physrev.00008.2015. PubMed DOI

Li Z., Hou J., Zhang Y., Zeng W., Cheng B., Hassan M.J., Zhang Y., Pu Q., Peng Y. Spermine regulates water balance associated with Ca2+-dependent aquaporins (TrTIP2-1, TrTIP2-2, and TrPIP2-7) expression in plants under water stress. Plant Cell Physiol. 2020;61:1576–1589. doi: 10.1093/pcp/pcaa080. PubMed DOI

Yang J., Zhang J., Liu K., Wang Z., Liu L. Involvement of polyamines in the drought resistance of rice. J. Exp. Bot. 2007;58:1545–1555. doi: 10.1093/jxb/erm032. PubMed DOI

Tiburcio A.F., Alcázar R. Potential Applications of Polyamines in Agriculture and Plant Biotechnology. In: Alcázar R., Tiburcio A., editors. Polyamines. Methods in Molecular Biology. Volume 1694. Humana Press; New York, NY, USA: 2018. PubMed DOI

Misra B.B., Acharya B.R., Granot D., Assmann S.M., Chen S. The guard cell metabolome: Functions in stomatal movement and global food security. Front. Plant Sci. 2015;6:1–13. doi: 10.3389/fpls.2015.00334. PubMed DOI PMC

Agurla S., Gayatri G., Raghavendra A.S. Polyamines increase nitric oxide and reactive oxygen species in guard cells of Arabidopsis thaliana during stomatal closure. Protoplasma. 2018;255:153–162. doi: 10.1007/s00709-017-1139-3. PubMed DOI

Fujita Y., Fujita M., Shinozaki K., Yamaguchi-Shinozaki K. ABA-mediated transcriptional regulation in response to osmotic stress in plants. J. Plant Res. 2011;124:509–525. doi: 10.1007/s10265-011-0412-3. PubMed DOI

Liu Y., Liang H., Lv X., Liu D., Wen X., Liao Y. Effect of polyamines on the grain filling of wheat under drought stress. Plant Physiol. Biochem. 2016;100:113–129. doi: 10.1016/j.plaphy.2016.01.003. PubMed DOI

Sánchez-Rodríguez E., Romero L., Ruiz J. Accumulation of free polyamines enhances the antioxidant response in fruits of grafted tomato plants under water stress. J. Plant Physiol. 2016;190:72–78. PubMed

Juzoń K., Czyczyło-Mysza I., Marcińska I., Dziurka M., Waligórski P., Skrzypek E. Polyamines in yellow lupin (Lupinus luteus L.) tolerance to soil drought. Acta Physiol. Plantarum. 2017;39:202. doi: 10.1007/s11738-017-2500-z. DOI

Shi H., Ye T., Chan Z. Comparative proteomic and physiological analyses reveal the protective effect of exogenous polyamines in the bermudagrass (Cynodon dactylon) response to salt and drought stresses. J. Proteome Res. 2013;12:4951–4964. doi: 10.1021/pr400479k. PubMed DOI

Krishnan S., Merewitz E.B. Polyamine application effects on gibberellic acid content in creeping bentgrass during drought stress. J. Amer. Soc. Hortic. Sci. 2017;142:135–142. doi: 10.21273/JASHS03991-16. DOI

Yamaguchi K., Takahashi Y., Berberich T., Imai A., Takahashi T., Michael A.J., Kusano T. A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem. Biophy.Res. Commun. 2007;352:486–490. doi: 10.1016/j.bbrc.2006.11.041. PubMed DOI

Arasimowicz-Jelonek M., Floryszak-Wieczorek J., Kubiś J. Interaction between polyamine and nitric oxide signalling in adaptive responses to drought in cucumber. J. Plant Growth Reg. 2009;28:177–186. doi: 10.1007/s00344-009-9086-7. DOI

Yin Z.P., Li S., Ren J., Song X.S. Role of spermidine and spermine in alleviation of drought-induced oxidative stress and photosynthetic inhibition in Chinese dwarf cherry (Cerasus humilis) seedlings. Plant Growth Reg. 2014;74:209–218. doi: 10.1007/s10725-014-9912-1. DOI

Talaat N.B., Shawky B.T. Dual application of 24-epibrassinolide and spermine confers drought stress tolerance in maize (Zea mays L.) by modulating polyamine and protein metabolism. J. Plant Growth Reg. 2016;35:518–533. doi: 10.1007/s00344-015-9557-y. DOI

Talaat N.B., Shawky B.T., Ibrahim A.S. Alleviation of drought-induced oxidative stress in maize (Zea mays L.) plants by dual application of 24-epibrassinolide and spermine. Environ. Exp. Bot. 2015;113:47–58. doi: 10.1016/j.envexpbot.2015.01.006. DOI

Farooq M., Wahid A., Lee D.-J. Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties. Acta Physiol. Plant. 2009;31:937–945. doi: 10.1007/s11738-009-0307-2. DOI

Shi J., Fu X.-Z., Peng T., Huang X.-S., Fan Q.-J., Liu J.-H. Spermine pre-treatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiol. 2010;30:914–922. doi: 10.1093/treephys/tpq030. PubMed DOI

Hassan F.A., Ali E.F., Alamer K.H. Exogenous application of polyamines alleviates water stress-induced oxidative stress of Rosa damascena Miller var. trigintipetala Dieck. S. Afr. J. Bot. 2018;116:96–102. doi: 10.1016/j.sajb.2018.02.399. DOI

Radhakrishnan R., Lee I.J. Spermine promotes acclimation to osmotic stress by modifying antioxidant, abscisic acid, and jasmonic acid signals in soybean. J. Plant Growth Reg. 2013;32:22–30. doi: 10.1007/s00344-012-9274-8. DOI

Mustafavi S.H., Shekari F., Maleki H.H. Influence of exogenous polyamines on antioxidant defence and essential oil production in valerian (Valeriana offcinalis L.) plants under drought stress. Acta Agric. Slov. 2016;107:81–91. doi: 10.14720/aas.2016.107.1.09. DOI

Montesinos-Pereira D., Barrameda-Medina Y., Romero L., Ruiz J.M., Sánchez-Rodríguez E. Genotype differences in the metabolism of proline and polyamines under moderate drought in tomato plants. Plant Biol. 2014;16:1050–1057. doi: 10.1111/plb.12178. PubMed DOI

Do P.T., Drechsel O., Heyer A.G., Hincha D.K., Zuther E. Changes in free polyamine levels, expression of polyamine biosynthesis genes, and performance of rice cultivars under salt stress: A comparison with responses to drought. Front. Plant Sci. 2014;5:182. doi: 10.3389/fpls.2014.00182. PubMed DOI PMC

Seifi H.S., Shelp B.J. Spermine differentially refines plant defense responses against biotic and abiotic stresses. Front. Plant Sci. 2019;10:117. doi: 10.3389/fpls.2019.00117. PubMed DOI PMC

Ma Y., Zhang J., Li X., Zhang S., Lan H. Effects of environmental stress on seed germination and seedling growth of Salsola ferganica (Chenopodiaceae) Acta Ecol. Sin. 2016;36:456–463. doi: 10.1016/j.chnaes.2016.09.008. DOI

Gill S.S., Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 2010;48:909–930. doi: 10.1016/j.plaphy.2010.08.016. PubMed DOI

Caverzan A., Casassola A., Brammer S.P. Abiotic and Biotic Stress in Plants—Recent Advances and Future Perspectives. InTech; London, UK: 2016. Reactive oxygen species and antioxidant enzymes involved in plant tolerance to stress.

Guler N.S., Pehlivan N. Exogenous low-dose hydrogen peroxide enhances drought tolerance of soybean (Glycine max L.) through inducing antioxidant system. Acta Biol. Hung. 2016;67:169–183. doi: 10.1556/018.67.2016.2.5. PubMed DOI

Abedi T., Pakniyat H. Antioxidant enzyme changes in response to drought stress in ten cultivars of oilseed rape (Brassica napus) Czech J. Genet. Plant Breed. 2010;46:27–34. doi: 10.17221/67/2009-CJGPB. DOI

Slabbert M.M., Krüger G.H.J. Antioxidant enzyme activity, proline accumulation, leaf area and cell membrane stability in water stressed Amaranthus leaves. S. Afr. J. Bot. 2014;95:123–128. doi: 10.1016/j.sajb.2014.08.008. DOI

Capell T., Bassie L., Christou P. Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc. Nat. Acad. Sci. USA. 2004;101:9909–9914. doi: 10.1073/pnas.0306974101. PubMed DOI PMC

Wimalasekera R., Tebartz F., Scherer G.F. Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci. 2011;181:593–603. doi: 10.1016/j.plantsci.2011.04.002. PubMed DOI

An Z.F., Jing W., Liu Y.L., Zhang W.H. Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J. Exp. Bot. 2008;59:815–825. doi: 10.1093/jxb/erm370. PubMed DOI

Alcázar R., Cuevas J.C., Patrón M., Altabella T., Tiburcio A.F. Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Physiol. Plant. 2006;128:448–455. doi: 10.1111/j.1399-3054.2006.00780.x. DOI

Marco F., Busó E., Lafuente T., Carrasco P. Spermine confers stress resilience by modulating abscisic acid biosynthesis and stress responses in Arabidopsis plants. Front. Plant Sci. 2019;10:972. doi: 10.3389/fpls.2019.00972. PubMed DOI PMC

Bitrián M., Zarza X., Altabella T., Tiburcio A.F., Alcázar R. Polyamines under abiotic stress: Metabolic crossroads and hormonal crosstalks in plants. Metabolites. 2012;2:516–528. doi: 10.3390/metabo2030516. PubMed DOI PMC

Klingler J.P., Batelli G., Zhu J.-K. ABA receptors: The START of a new paradigm in phytohormone signalling. J. Exp.Bot. 2010;61:3199–3210. doi: 10.1093/jxb/erq151. PubMed DOI PMC

Toumi I., Moschou P.N., Paschalidis K.A., Bouamama B., Salem-Fnayou A.B., Ghorbel A.W., Mliki A., Roubelakis-Angelakis K.A. Abscisic acid signals reorientation of polyamine metabolism to orchestrate stress responses via the polyamine exodus pathway in grapevine. J. Plant Physiol. 2010;167:519–525. doi: 10.1016/j.jplph.2009.10.022. PubMed DOI

Marco F., Alcázar R., Tiburcio A.F., Carrasco P. Interactions between polyamines and abiotic stress pathway responses unraveled by transcriptome analysis of polyamine overproducers. OMICS. 2011;15:775–781. doi: 10.1089/omi.2011.0084. PubMed DOI PMC

Tun N.N., Santa-Catarina C., Begum T., Silveira V., Handro W., Floh E.I.S., Scherer G.F.E. Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol. 2006;47:346–354. doi: 10.1093/pcp/pci252. PubMed DOI

Parra-Lobato M.C., Gomez-Jimenez M.C. Polyamine-induced modulation of genes involved in ethylene biosynthesis and signalling pathways and nitric oxide production during olive mature fruit abscission. J. Exp. Bot. 2011;62:4447–4465. doi: 10.1093/jxb/err124. PubMed DOI PMC

Yamasaki H., Cohen M.F. NO signal at the crossroads: Polyamine-induce nitric oxide synthesis in plants? Trends Plant Sci. 2006;11:522–524. doi: 10.1016/j.tplants.2006.09.009. PubMed DOI

Houben M., Van De Poel B. 1-Aminocyclopropane-1-carboxylic acid oxidase (ACO): The enzyme that makes the plant hormone ethylene. Front. Plant Sci. 2019;10:695. doi: 10.3389/fpls.2019.00695. PubMed DOI PMC

Pan C.Z., Zhang H., Ma Q.M., Fan F.J., Ahammed G.J., Yu J., Shi K. Role of ethylene biosynthesis and signaling in elevated CO2-induced heat stress response in tomato. Planta. 2019;250:563–572. PubMed

Del Duca S., Serafini-Fracassini D., Cai G. Senescence and programmed cell death in plants: Polyamine action mediated by transglutaminase. Front. Plant Sci. 2014;5:120. doi: 10.3389/fpls.2014.00120. PubMed DOI PMC

Alcázar R., Fortes A.M., Tiburcio A.F. Editorial: Polyamines in plant biotechnology, food nutrition and human health. Front. Plant Sci. 2020;11:120. doi: 10.3389/fpls.2020.00120. PubMed DOI PMC

Takahashi Y., Cong R., Sagor G., Niitsu M., Berberich T., Kusano T. Characterization of five polyamine oxidase isoforms in Arabidopsis thaliana. Plant Cell Rep. 2010;29:955–965. doi: 10.1007/s00299-010-0881-1. PubMed DOI

Pal M., Szalai G., Janda T. Speculation: Polyamines are important in abiotic stress signaling. Plant Sci. 2015;237:16–23. doi: 10.1016/j.plantsci.2015.05.003. PubMed DOI

Serna M., Coll Y., Zapata P.J., Botella M.Á., Pretel M.T., Amorós A. A brassinosteroid analogue prevented the effect of salt stress on ethylene synthesis and polyamines in lettuce plants. Sci. Hortic. 2015;185:105–112. doi: 10.1016/j.scienta.2015.01.005. DOI

Wang X.-L., Zhang Y.-X. Regulation of salicylic acid on polyamine synthesize under NaCl stress in leaves of the yali pear. Res. J. Appl. Sci. Eng. Technol. 2012;4:3704–3708.

Iqbal M., Ashraf M., Jamil A., Ur-Rehman S. Does seed priming induce changes in the levels of some endogenous plant hormones in hexaploid wheat plants under salt stress? J. Integr. Plant Biol. 2006;48:181–189. doi: 10.1111/j.1744-7909.2006.00181.x. DOI

Echevarría-Machado I., Ku-González A., Loyola-Vargas V.M., Hernández-Sotomayor S.T. Interaction of spermine with a signal transduction pathway involving phospholipase C, during the growth of Catharanthus roseus transformed roots. Physiol. Plant. 2004;120:140–151. doi: 10.1111/j.0031-9317.2004.0212.x. PubMed DOI

Zarza X., Shabala L., Fujita M., Shabala S., Haring M.A., Tiburcio A.F. Extracellular spermine triggers a rapid intracellular phosphatidic acid response in Arabidopsis, involving PLDδ activation and stimulating ion flux. Front. Plant Sci. 2019;10:601. doi: 10.3389/fpls.2019.00601. PubMed DOI PMC

Raman V.P., Rajam M.V. Polyamine accumulation in transgenic eggplant enhances tolerance to multiple abiotic stresses and fungal resistance. Plant Biotechnol. 2007;24:273–282.

Bassie L., Zhu C., Romagosa I., Christou P., Capell T. Transgenic wheat plants expressing an oat arginine decarboxylase cDNA exhibit increases in polyamine content in vegetative tissue and seeds. Mol. Breed. 2008;22:39–50.

Peremarti A., Bassie L., Christou P., Capell T. Spermine facilitates recovery from drought but does not confer drought tolerance in transgenic rice plants expressing Datura stramonium S-adenosylmethionine decarboxylase. Plant Mol. Biol. 2009;70:253–264. doi: 10.1007/s11103-009-9470-5. PubMed DOI

Momtaz O.A., Hussein E.M., Fahmy E.M., Ahmed S.E. Expression of S-adenosyl methionine decarboxylase gene for polyamine accumulation in Egyptian cotton Giza 88 and Giza 90. GM Crops. 2010;1:257–266. doi: 10.4161/gmcr.1.4.13779. PubMed DOI

Hazarika P., Rajam M.V. Biotic and abiotic stress tolerance in transgenic tomatoes by constitutive expression of S-adenosylmethionine decarboxylase gene. Physiol. Mol. Biol. Plants. 2011;17:115–128. doi: 10.1007/s12298-011-0053-y. PubMed DOI PMC

Yu L., Geng S., Zhao-Hui Z., Xue-Lian Z., Ke-Jun D. Overexpression of SAMDC gene from Salvia miltiorrhiza enhances drought tolerance in transgenic tobacco (Nicotiana tabacum) J. Agric. Biotech. 2017;25:729–738.

Jiang X., Zhan J., Wang Q., Wu X., Chen X., Jia B., Liu P., Liu L., Ye Z., Zhu L., et al. Overexpression of the pear PbSPMS gene in Arabidopsis thaliana increases resistance to abiotic stress. Plant Cell Tissue Organ Cult. 2020;140:389–401. doi: 10.1007/s11240-019-01735-y. DOI

Gonzalez M.E., Marco F., Minguet E.G., Carrasco-Sorli P., Blázquez M.A., Carbonell J., Ruiz O.A., Pieckenstain F.L. Perturbation of spermine synthase gene expression and transcript profiling provide new insights on the role of the tetraamine spermine in Arabidopsis defense against Pseudomonas viridiflava. Plant Physiol. 2011;156:2266–2277. doi: 10.1104/pp.110.171413. PubMed DOI PMC

Liu J.H., Wang W., Wu H., Gong X., Moriguchi T. Polyamines function in stress tolerance: From synthesis to regulation. Front. Plant Sci. 2015;6:827. doi: 10.3389/fpls.2015.00827. PubMed DOI PMC

Alcázar R., Bueno M., Tiburcio A.F. Polyamines: Small Amines with Large Effects on Plant Abiotic Stress Tolerance. Cells. 2020;9:2373. doi: 10.3390/cells9112373. PubMed DOI PMC

Zhao Y., Du H., Wang Z., Huang B. Identification of proteins associated with water-deficit tolerance in C4 perennial grass species, Cynodon dactylon× Cynodon transvaalensis and Cynodon dactylon. Physiol. Plant. 2011;141:40–55. doi: 10.1111/j.1399-3054.2010.01419.x. PubMed DOI

Progressive Genomic Approaches to Explore Drought- and Salt-Induced Oxidative Stress Responses in Plants under Changing Climate