The role of polyamines in response to abiotic stresses

Document Type : Research Paper

Authors

1 Assistant professor, Department of Seed and Plant Certification and Registration Research Institute (SPCRI), Agricultural Research, Education and Extension Organization (AREEO), P. O. Box: 31535-1516, Karaj, Iran

2 Professor, Department of Agronomy and Plant Breeding Department, Agriculture and Natural Resources, University of Tehran, Karaj,

Abstract

Under the influence of various abiotic stresses, the growth, development and geographic distribution of plants change. In order to survive adverse environmental conditions and to sustain life, plants have evolved various combat and adaptive strategies to enviromntal stresses, which in the context of these defense mechanisms, is referred to metabolites accumulation such as common aliphatic polyamines (PAs) including putrescine, spermidine, and spermine.
Results
Over the last two decades, genetic, transcriptomic, proteomic, metabolomic, and phenomic modern approaches have unraveled many significant functions of different PAs in the regulation of plant abiotic stress tolerance. Studies have demonstrated that because of their polycationic nature at physiological pH, and strong binding ability to negatively charged molecules in cellular components such as nucleic acids, proteins, and phospholipids, PAs enable to largely modulate the homeostasis of reactive oxygen species (ROS) and also due to regulating and stabilizating antioxidant defense systems or suppressing ROS production improve stress tolerance in plants. Environmental stresses-induced oxidative stresses can be managed by both PAs biosynthesis and their degradation, leading protection of cell metabolism. This is ascribed to generating other metabolited and also signal molecules which participate in defense systems and energy production in Krebs cycle.
Conclusions
Important role of polyamines in stress tolerance by several lines of evidences has shown that transcript levels of polyamines-biosynthetic genes as well as the activity of related enzymes are induced by stresses. Increasing the polyamines level or expression of their biosynthetic genes through spraying with polyamines leads to an increase in stress tolerance. The reduction of polyamines has been associated with the reduction of tolerance to stress. Considering the variety of bioactivities of polyamines and their biosynthesis and degradating pathways in crop plants, this metabolic pathway in plants, identification of molecular networks and selection of effective genes can be used as candidates in breeding programs and production of stress-tolerant commercial cultivars.

Keywords


Ahou A, Martignago D, Alabdallah O, et al. (2014) A plant spermine oxidase/dehydrogenase regulated by the proteasome and polyamines. J Exp Bot 65(6), 1585-1603.
Alcázar R, Altabella T, Marco F et al.  (2010a) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231 (6), 1237-1249.
Alcázar R, Cuevas JC, Planas, J et al. (2011a) Integration of polyamines in the cold acclimation response. Plant Sci 180(1), 31-38.
Alcázar R, Cuevas JC, Planas J et al. (2011b) Integration of polyamines in the cold acclimation response. Plant Sci 180(1), 31-38.
Alcázar R, Planas J, Saxena T et al. (2010b) Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants over-expressing the homologous Arginine decarboxylase 2 gene. Plant Physiol Biochem 48(7), 547-552.
Alcázar R., Tiburcio AF (Eds.). (2018) Polyamines: Methods and Protocols. Humana Press.
Ali RM (2000) Role of putrescine in salt tolerance of Atropa belladonna plant. Plant Sci 152, 173–179
Ali S, Tyagi A, Bae H (2021) Ionomic approaches for discovery of novel stress-resilient genes in plants. Int J Mol Sci 22, 7182
Ali S, Tyagi A, Mushtaq M, et al. (2022b) Harnessingplant microbiome for mitigating arsenic toxicity in sustainable agriculture. Environ Pollut 300, 118940
Ali S, Tyagi A, Park S, et al. (2022a) Deciphering the plant microbiome to improve drought tolerance: mechanisms and perspectives. Environ Exp Bot 27, 104933
Angelini R, Cona A, Federico R, et al. (2010) Plant amine oxidases “on the move”: an update. Plant Physiol Biochem 48(7), 560-564.
Bano C, Amist N, Singh NB (2020) Role of polyamines in plants abiotic stress tolerance: advances and future prospects. In: Tripathi DK, Singh VP (eds) Plant life under changing environment: responses and management. Elsevier, Amsterdam, pp 481–496
Bitrián M, Zarza X, Altabella T et al. (2012) Polyamines under abiotic stress: metabolic crossroads and hormonal cross talks in plants. Metabolites 2(3), 516-528.
Bregier-Jarzębowska R, Łomozik L, Gąsowska A (2018) Influence of copper (II) ions on the noncovalent interactions between cytidine-5′-diphosphate or cytidine-5′-triphosphate and biogenic amines putrescine or spermidine. J Inorg Biochem 184, 27-33.
Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101, 9909–9914.
Chen D, Shao Q, Yin L et al. (2019) Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Front Plant Sci 9, 1945.
Choudhary SP, Bhardwaj R, Gupta BD et al. (2010) Changes induced by Cu2+ and Cr6+ metal stress in polyamines, auxins, abscisic acid titers and antioxidative enzymes activities of radish seedlings. Brazilian J Plant Physiol 22, 263–270.
Choudhary SP, Oral HV, Bhardwaj R et al. (2012) Interaction of brassinosteroids and polyamines enhances copper stress tolerance in raphanus sativus. J Exp Bot 63, 5659–5675.
Cona A, Rea G, Angelini R et al. (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11, 80-88.
Cuevas JC, López-Cobollo R, Alcázar R et al. (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148, 1094–1105.
Cuevas JC, Lopez-Cobollo R, Alcazar R et al. (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148, 1094–1105.
Du HY, Liu DX, Liu GT et al. (2018) Relationship between polyamines and anaerobicrespiration of wheat seedling root under waterlogging stress. Russ J Plant Physiol 65, 874–881.
Duan J, Li J, Guo S, Kang Y )2008( Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 165, 1620–1635.
Ebeed HT, Hassan NM, Aljarani AM (2017) 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 118, 438–448.
Erdal S, Genisel M, Turk H et al (2015) Modulation of alternative oxidase to enhance tolerance against cold stress of chickpea by chemical treatments. J Plant Physiol 175, 95–101.
Fargašová A (2004) Toxicity comparison of some possible toxic metals (Cd, Cu, Pb, Se, Zn) on young seedlings of Sinapis alba L. Plant Soil Environ 50, 33–38.
Fincato P, Moschou PN, Spedaletti V et al. (2011) Functional diversity inside the Arabidopsis polyamine oxidase gene family. J Exp Bot 62, 1155–1168.
Foyer CH, Fletcher JM (2001) Plant antioxidants: colour me healthy. Biologist 48, 115–120.
Gong X, Dou F, Cheng X et al. (2018) Genome-wide identification of genes involved in polyamine biosynthesis and the role of exogenous polyamines in Malus hupehensis Rehd. under alkaline stress. Gene 669, 52-62.
González-Aguilar GA, Fortiz J, Cruz R et al. (2000) Methyl jasmonate reduces chilling injury and maintains postharvest quality of mango fruit. J Agric Food Chem 48, 515–519.
González-Hernández AI, Scalschi L, Vicedo Bet al. (2022) Putrescine: a key metabolite involved in plant development, tolerance and resistance responses to stress. Int J Mol Sci 23(6), 2971
Groppa MD, Benavides MP, Tomaro ML (2003) Polyamine metabolism in sunflower and wheat leaf discs under cadmium or copper stress. Plant Sci 164, 293–299.
Groppa MD, Tomaro ML, Benavides MP (2007) Polyamines and heavy metal stress: the antioxidant behavior of spermine in cadmiumand copper-treated wheat leaves. Biometals 20, 185–195.
Groppa MD, Zawoznik MS, Tomaro ML, Benavides MP (2008) Inhibition of root growth and polyamine metabolism in sunflower (helianthus annuus) seedlings under cadmium and copper stress. Biol Trace Elem Res 126, 246–256.
Gupta A, Rico-Medina A, Caño-Delgado AI (2020) The physiology of plant responses to drought. Science 368(6488), 266–269
Gupta A (2012) Analysis of fruit characteristics in transgenic tomatoes with RNAi mediated silencing of ACC synthase genes and over expression of polyamine biosynthesis genes.
Handa AK, Fatima T, Mattoo AK (2018) Polyamines: bio-molecules with diverse functions in plant and human health and disease. Front Chem 6, 10.
Hanzawa Y, Imai A, Michael A J et al. (2002) Characterization of the spermidine synthase‐related gene family in Arabidopsis thaliana. FEBS letters, 527(1-3), 176-180.
Hanzawa Y, Takahashi T, Michael AJ et al. (2000) ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J 19(16), 4248-4256.
Ikbal FE, Hernández JA, Barba-Espín G et al. (2014). Enhanced salt-induced antioxidative responses involve a contribution of polyamine biosynthesis in grapevine plants. J Pant Physiol 171(10), 779-788.
Kamiab F, Talaie A, Khezri M, Javanshah A (2014) Exogenous applications of free polyamines enhance salt tolerance of pistachio (Pistacia vera L.) seedlings. Plant Growth Regul 72, 257–268.
Kasukabe Y, He L, Nada K et al. (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45, 712–722.
Kumar M, Kumari P, Gupta V et al. (2010) Differential responses to cadmium induced oxidative stress in marine macroalga Ulva lactuca (Ulvales, Chlorophyta). Biometals 23, 315–325.
Li Y, He J (2012) Advance in metabolism and response to stress of polyamines in plant. Acta Agric Boreali Sin 27, 240–245
Liu K, Fu H, Bei Q, Luan S (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol 124(3), e1315.
Liu Y, Liang H, Lv X et al. (2016b) Effect of polyamines on the grain filling of wheat under drought stress. Plant Physiol Biochem 100, 113–129.
Liu Y, Zuo Z, Hu J (2010) Effects of exogenous polyamines on growth and drought resistance of Apple seedlings. J Northwest for Univ 25, 39-42.
Lutts S, Kinet JM, Bouharmont J (1996) Ethylene production by leaves of rice (Oryza sativa L.) in relation to salinity tolerance and exogenous putrescine application. Plant Sci 116, 15–25.
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: An overview. Arch BiochemBiophys 24(8), 139-158.
Mantri NL, Ford R, Coram TE, Pang EC (2007) Transcriptional profiling of chickpea genes differentially regulated in response to high-salinity, cold and drought. BMC genomics 8(1), 303.
Mathews MB, Hershey JW (2015) The translation factor eIF5A and human cancer. Biochim Biophys Acta Gene Regul Mech 1849(7), 836-844.
Mitsuya Y, Takahashi Y, Berberich T et al. (2009) Spermine signaling plays a significant role in the defense response of Arabidopsis thaliana to cucumber mosaic virus. J Plant Physiol 166, 626-643.
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7,  405-410.
Mo H, Pua EC (2002). Up‐regulation of arginine decarboxylase gene expression and accumulation of polyamines in mustard (Brassica juncea) in response to stress. PhysiolPlant 114(3), 439-449.
Mohammadi H, Ghorbanpour M, Brestic M (2018) Exogenous putrescine changes redox regulations and essential oil constituents in field-grown Thymus vulgaris L. under well-watered and drought stress conditions. Ind Crops Prod 2018(05), e064.
Mohanta TK, Bashir T, Hashem A et al. (2018) Early events in plant abiotic stress signaling: interplay between calcium, reactive oxygen species and phytohormones. J Plant Growth Regul 37, 1033–1049.
Montesinos-Pereira D, Barrameda-Medina Y, Romero L et al. (2014) Genotype differences in the metabolism of proline and polyamines under moderate drought in tomato plants. Plant Biol 16, 1050–1057.
Moradi Peynevandi K, Razavi SM, Zahri S (2018) The ameliorating effects of polyamine supplement on physiological and biochemical parameters of Stevia rebaudiana Bertoni under cold stress. Plant Prod Sci 21, 123–131.
Moschou PN, Paschalidis KA, Roubelakis-Angelakis KA (2008b) Plant polyamine catabolism: the state of the art. Plant Signal Behave 3(12), 1061-1066.
Moschou PN, Sanmartin M, Andriopoulou AH, et al. (2008a). Bridging the gap between plant and mammalian polyamine catabolism: a novel peroxisomal polyamine oxidase responsible for a full back-conversion pathway in Arabidopsis. Plant Physiol 147(4), 1845-1857.
Moschou PN, Wu J, Cona A et al. (2012) The polyamines and their catabolic products are significant players in the turnover of nitrogenous molecules in plants. J Exp Bot 63, 5003–5015.
Mutlu F, Bozcuk S (2005) Effects of salinity on the contents of polyamines and some other compounds in sunflower plants differing in salt tolerance. Russ J Plant Physiol 52, 29–34.
Nayyar H, Satwinder K, Kumar S et al. (2005) Involvement of polyamines in the contrasting sensitivity of chickpea (Cicer arietinum L.) and soybean (Glycine max (L.) Merrill.) to water deficit stress. Bot Bull Acad Sin 46.
Nazari M, Amiri RM, Mehraban FH, Khaneghah HZ (2012) Change in antioxidant responses against oxidative damage in black chickpea following cold acclimation. Russ J plant Physiol 59(2), 183-189.
Pál M, Szalai G, Janda T (2015) Speculation: polyamines are important in abiotic stress signaling. Plant Sci 237, 16–23
Pegg, AE (2009) Mammalian polyamine metabolism and function. IUBMB life 61(9), 880-894.
Pottosin I, Velarde-Buendía AM, Zepeda-Jazo I et al. (2012) Synergism between polyamines and ROS in the induction of Ca2+ and K+ fluxes in roots. Plant Signal Behav 7, 1084–1087.
Ramani D, De Bandt JP, Cynober L (2014). Aliphatic polyamines in physiology and diseases. Clin Nutr 33(1), 14-22.
Rathinapriya P, Pandian S, Rakkammal K et al. (2020) The protective effects of polyamines on salinity stress tolerance in foxtail millet (Setaria italica L.), an important C4 model crop. Physiol Mol Biol Plants 26(9), 1815–1829
Rathinapriya P, Pandian S, Rakkammal K et al. (2020) The protective effects of polyamines on salinity stress tolerance in foxtail millet (Setaria italica L.), an important C4 model crop. Physiol Mol Biol Plants 26(9), 1815–1829
Raza A, Tabassum J, Fakhar AZet al. (2022) Smart reprograming of plants against salinity stress using modern biotechnological tools. Crit Rev Biotechol 12, 1–28
Raza A, Tabassum J, Fakhar AZ et al. (2022) Smart reprograming of plants against salinity stress using modern biotechnological tools. Crit Rev Biotechol 12, 1–28
Raza A, Tabassum J, Kudapa H, Varshney RK (2021) Can omics deliver temperature resilient ready-to-grow crops? Crit Rev Biotechol 41(8), 1209–1232
Roychoudhury A, Basu S, Sengupta DN (2012) Antioxidants and stress-related metabolites in the seedlings of two indica rice varieties exposed to cadmium chloride toxicity. Acta Physiol Plant 34, 835–847.
Roychoudhury A, Basu S, Sengupta DN (2011) Amelioration of salinity stress by exogenously applied spermidine or spermine in three varieties of indica rice differing in their level of salt tolerance. J Plant Physiol 168, 317–328.
Saeidnejad AH, Pouramir F, Naghizadeh M (2012) Improving chilling tolerance of maize seedlings under cold conditions by spermine application. Not Sci Biol 4(3), 110-117.
Sánchez-Rodríguez E, Romero L, Ruiz JM (2016) Accumulation on free polyamines enhanced antioxidant response in fruit of grafting tomato plants under water stress. J Plant Physiol 190, 72–78.
Sánchez-Rodríguez E, Romero L, Ruiz JM (2016) Accumulation of free polyamines enhances the antioxidant response in fruits of grafted tomato plants under water stress. J Plant Physiol 190, 72–78.
Scoccianti V, Bucchini AE, Iacobucci M et al. (2016) Oxidative stress and antioxidant responses to increasing concentrations of trivalent chromium in the Andean crop species Chenopodium quinoa Willd. Ecotoxicol Environ Saf 133, 25–35.
Serrano M, Martínez-Madrid MC, Pretel MT et al. (1997) Modified atmosphere packaging minimizes increases in putrescine and abscisic acid levels caused by chilling injury in pepper fruit. J Agric Food Chem 45, 1668–1672.
Serrano M, Pretel MT, Martínez-Madrid MC et al. (1998) CO2 treatment of zucchini squash reduces chilling-induced physiological changes. J Agric Food Chem 46, 2465–2468.
Serrano-Martínez F, Casas JL (2011) Effects of extended exposure to cadmium and subsequent recovery period on growth, antioxidant status and polyamine pattern in in vitro cultured carnation. Physiol Mol Biol Plants 17, 327–338.
Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31, 739–753.
Shao CG, Wang H, Yu-Fen BI (2015) Relationship between endogenous polyamines and tolerance in Medicago sativa L. under heat stress. Acta Agrestia Sin 23, 1214–1219
Sharma P, Gujral HS (2010) Antioxidant and polyphenol oxidase activity of germinated barley and its milling fractions. Food Chem 120(3), 673-678.
Takahashi T (2020) Plant polyamines. Plants 9(4), 511
Takahashi T, Kakehi JI (2009) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105(1), 1-6.
Tiburcio AF, Altabella T, Bitrián M, Alcázar R (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 240(1), 1-18.
Tyagi A, Sharma S, Ali S, Gaikwad K (2022) Crosstalk between H2S and NO: an emerging signalling pathway during waterlogging stress in legume crops. Plant Biol 24(4), 576–586
Urano K, Yoshiba Y, Nanjo T et al. (2004) Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochem Biophys Res Commun 313, 369–375.
Wang Q, Yin X (2014) Alleviative effects of different kinds of exogenous polyamines on salt injury of soybean seedlings. J Henan Agric Sci 43, 48–55
Wang Y, Lu W, Zhang Z, Xie H (2003) ABA and putrescine treatents alleviate chilling injury in banana fruits during storage at 8℃.  Zhi Wu Sheng Li Yu Fen Zi Sheng Wu Xue Xue Bao J 29, 549–554
Wimalasekera R, Villar C, Begum T, Scherer GFE (2011b) Copper amine oxidase1 (CuAO1) of Arabidopsis thaliana contributes to abscisic acid- and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction. Mol Plant 4, 663–678.
Wimalasekera R, Tebartz F, Scherer GF (2011a) Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci 181, 593–603.
Xu X, Shi G, Ding C, et al. (2011) Regulation of exogenous spermidine on the reactive oxygen species level and polyamine metabolism in Alternanthera philoxeroides (Mart.) Griseb under copper stress. Plant Growth Regul 63, 251–258.
Yamaguchi K, Takahashi Y, Berberich T et al. (2007) A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun.
Yang HY, Shi GX, Li WL, Wu WL (2013) Exogenous spermidine enhances Hydrocharis dubia cadmium tolerance. Russ J Plant Physiol 60, 770–775.
Yang Y, Yang X (2002) Effect of temperature on endogenous polyamines content of leaves in chinese kale (Brassica alboglabra bailey) seedlings. Hua Nan Nong Ye Da Xue Xue Bao = J South China Agric Univ 23, 9–12
Yiu JC, Juang LD, Fang DYT et al. (2009) Exogenous putrescine reduces flooding-induced oxidative damage by increasing the antioxidant properties of Welsh onion. Sci Hortic (Amsterdam) 120, 306–314.
Yruela I (2009) Copper in plants: Acquisition, transport and interactions. Funct Plant Biol 36, 409–430.
Zhang Q, Liu X, Zhang Z et al. (2019) Melatonin improved waterlogging tolerance in alfalfa (Medicago sativa) by reprogramming polyamine and ethylene metabolism. Front Plant Sci 10, e4.
Zheng YH, Li SY, Xi YF et al. (2000) Polyamine changes and chilling injury in cold-stored loquat fruits. J Integr Plant Biol 42, 824
Zhu T, Provart NJ (2003) Transcriptional responses to low temperature and their regulation in Arabidopsis. Can J Bot 56(6), 1168-1174.