Effects of Polyamines on Plant Growth and Development with a Current Perspective

Yıl 2022, Cilt: 9 Sayı: 2, 255 - 264, 15.08.2022

Günce Şahin , Mehmet Örgeç

https://doi.org/10.19159/tutad.1088744

Cited By: 2

Öz

Polyamines are aliphatic, amine-containing polycationic molecules with a low molecular weight that are present in almost all cells. They've been considered a new class of plant growth regulators because they play critical roles in a variety of growth, developmental and physiological processes such as cell division and differentiation, protein synthesis, DNA replication, gene expression, somatic embryogenesis, dormancy breaking in seed germination, flower and fruit development, senescence, and enhancing stress tolerance. Although polyamines are known to be involved in various plant processes, their precise role remains unclear. This review includes current research on polyamine metabolism and function, metabolic mechanisms involved in polyamine formation and degradation, genetic and molecular approaches in plants, as well as studies using metabolic inhibitors to better understand the roles of polyamines. Polyamines and their modifications in transgenics are explored from a molecular perspective, and significant variations in polyamine titers in response to other plant regulators and stress factors are also discussed.

Anahtar Kelimeler

Poliamins, putrescine, spermidine, spermine, stress adaptation

Güncel Bir Bakış Açısıyla Poliaminlerin Bitki Büyüme ve Gelişimi Üzerine Etkileri

Öz

Poliaminler, hemen hemen tüm hücrelerde bulunan, düşük moleküler ağırlığa sahip, alifatik, amin içeren polikatyonik moleküllerdir. Hücre bölünmesi ve farklılaşması, protein sentezi, DNA replikasyonu, gen ekspresyonu, somatik embriyogenez, tohum çimlenmesinde dormansinin kırılması, çiçek ve meyve gelişimi, yaşlanma ve stres toleransını arttırma gibi çeşitli büyüme, gelişimsel ve fizyolojik süreçlerde kritik rol oynadıkları için yeni bir bitki büyüme düzenleyici sınıfı olarak kabul edilmektedirler. Poliaminlerin, çeşitli bitki süreçlerinde yer aldıkları bilinse de kesin rolleri belirsizliğini korumaktadır. Bu derleme, poliaminlerin rollerini daha iyi anlamak için, poliamin metabolizması ve işlevi, poliamin oluşumu ve yıkımında rol oynayan metabolik mekanizmalar, bitkilerde genetik ve moleküler yaklaşımların yanı sıra metabolik inhibitörleri kullanan çalışmalar hakkında güncel araştırmalara yer vermektedir. Poliaminler ve bunların transgeniklerdeki modifikasyonları moleküler bir perspektiften araştırılmış ve ayrıca diğer bitki düzenleyicilerine ve stres faktörlerine yanıt olarak poliamin titrelerindeki önemli varyasyonlar da tartışılmıştır.

Anahtar Kelimeler

Poliaminler, putresin, spermidin, spermin, stres adaptasyonu

Kaynakça

• Adamipour, N., Khosh-Khui, M., Salehi, H., Razi, H., Karami, A., Moghadam, A., 2020. 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 Physiology and Biochemistry, 148: 53-61.
• Agurla, S., Gayatri, G., Raghavendra, A.S., 2018. Polyamines increase nitric oxide and reactive oxygen species in guard cells of Arabidopsis thaliana during stomatal closure. Protoplasma, 255: 153-162.
• Aloisi, I., Cai, G., Faleri, C., Navazio, L., Serafini-Fracassini, D., Del Duca, S., 2017. Spermine regulates pollen tube growth by modulating Ca2+ dependent actin organization and cell wall structure. Frontiers Plant Science, 8: 1701.
• Astarita, L.V., Handro, W., Floh, E.I.S., 2003. Changes in polyamines content associated with zygotic embryogenesis in the Brazilian pine, Araucaria angustifolia (Bert.) O. Ktze. Brazilian Journal of Botany, 26(2): 163-168.
• Bais, H.P., Bhagyalakshmi, N., Rajasekaran, T., Ravishankar, G.A., 2000a. Influence of polyamines on growth and production of secondary metabolites in hairy root cultures of Beta vulgaris and Tagetes patula. Acta Physiologiae Plantarum, 22: 151-158.
• Bais, H.P., George, J., Ravishankar, G.A., 1999. Influence of polyamines on growth of hairy root cultures of witloof chicory (Cichorium intybus L. cv. Lucknow Local) and formation of coumarins. Journal of Plant Growth Regulation, 18(1): 33-37.
• Bais, H.P., Sudha, G., Ravishankar, G.A., 2000b. Putrescine and silver nitrate influences shoot multiplication, in vitro flowering and endogenous titres of polyamines in Cichorium intybus L. cv. Lucknow local. Journal of Plant Growth Regulation,19(2): 238-248.
• Baraldi, R., Bertazza, G., Bregoli, A.M., Fasolo, F., Rotondi, A., Predieri, S., Serafini-Fracassini, D., Slovin, J.P., Cohen, J.D., 1995. Auxins and polyamines in relation to differential in vitro root induction on micro cuttings of two pear cultivars. Journal of Plant Growth Regulation, 14: 49-59.
• Baxter, C., Coscia, C.J., 1973. In vitro synthesis of spermidine in higher plant Vinca rosea. Biochemical and Biophysical Research Communications, 54(1): 147-154.
• Berlin, J., Forche, E., 1981. DL-α-difluoromethylornithine causes enlargement of cultured tobacco cells. Zeitschrift für Pflanzenphysiologie, 101(3): 272-282.
• Berta, G., Altamura, M.M., Fusconi, A., Cerruti, F., Capitani, F., Bagni, N., 1997. The plant cell wall is altered by inhibition of polyamine biosynthesis. New Phytologist, 137(4): 569-577.
• Bitrián, M., Zarza, X., Altabella, T., Tiburcio, A.F., Alcázar, R., 2012. Polyamines under abiotic stress: metabolic crossroads and hormonal crosstalks in plants. Metabolites, 2(3): 516-528.
• Çetinbaş-Genç, A., Cai, G., Del Duca, S., Vardar, F., Ünal, M., 2020. The effect of putrescine on pollen performance in hazelnut (Corylus avellana L.). Scientia Horticulturae, 261: 108971.
• Del Duca, S., Serafini-Fracassini, D., Bonner, P.L.R., Cresti, M., Cai, G., 2009. Effects of post-translational modifications catalyzed by pollen transglutaminase on the functional properties of microtubules and actin filaments. Biochemical Journal, 418(3): 651-664.
• Deng, H., Bloomfield, V.A., Benevides, J.M., Thomas, G.J., 2000. Structural Basis of Polyamine-DNA Recognition: Spermidine and Spermine Interactions with Genomic B-DNAs of Different GC Content Probed by Raman Spectroscopy. Nucleic Acids Research, 28(17): 3379-3385.
• Dixin, C., Shaoling, Z., 2002. Effects of polyamines and polyamine synthesis inhibitor on in vitro pollen germination and tube growth in pears. Journal of Fruit Science, 19(6): 377-380.
• Du, H.Y., Liu, G.T., Hua, C.M., Liu, D.X., He, Y.G., Liu, H.P., Kurtenbach, R., Ren, D.T., 2021. Exogenous melatonin alleviated chilling injury in harvested plum fruit via affecting the levels of polyamines conjugated to plasma membrane. Postharvest Biology and Technology, 179: 111585.
• Evans, P.T., Malmberg, R.L., 1989. Do polyamines have a role in plant development? Annual Review of Plant Physiology and Plant Molecular Biology, 40: 235-269.
• Faivre-Rampant, O., Kevers, C., Dommes, J., Gaspar, T., 2000. The recalcitrance to rooting of the micro propagated shoots of the rac tobacco mutant: Implications of polyamines and of the polyamine metabolism. Plant Physiology and Biochemistry, 38(6): 441-448.
• Falhof, J., Pedersen, J.T., Fuglsang, A.T., Palmgren, M., 2016. Plasma membrane H+-ATPase regulation in the center of plant physiology. Molecular Plant, 9: 323-337.
• Fortes, A.M., Teixeira, R.T., Agudelo-Romero, P., 2015. Complex interplay of hormonal signals during grape berry ripening. Molecules, 20(5): 9326-9343.
• Fuhrer, J., Kaur-Sawhney, R., Shih, L.M., Galston, A.W., .1982. Effects of exogenous 1,3-diaminopropane and spermidine on senescence of oat leaves. Plant Physiology, 70(6): 1597-1600.
• Galston, A.W., 1983. Polyamines as modulators of plant development. Bioscience, 33(6): 382-388.
• Galston, A.W., Kaur-Sawhney, R., 1987. Polyamines as endogenous growth regulators. In: P.J. Davies (Ed.), Plant Hormones and their Role in Plant Growth and Development, Martinus Nijhoff, Dordrecht, pp. 280-295.
• Guo, J., Wang, S., Yu, X., Dong, R., Li, Y., Mei, X., Yuanyue, S., 2018. Polyamines regulate strawberry fruit ripening by abscisic acid, auxin, and ethylene. Plant Physiology, 177(1): 339-351.
• Heimer, Y.H., Mizrahi, Y., Bachrach, U., 1979. Ornithine decarboxylase activity in rapidly proliferating plant cells. FEBS Letters, 104(1): 146-149.
• Huang, Y., Lin, C., He, F., Li, Z., Guan, Y., Hu, Q., Hu, J., 2017. Exogenous spermidine improves seed germination of sweet corn via involvement in phytohormone interactions, H2O2 and relevant gene expression. BMC Plant Biology, 17(1): 1-16.
• Hussain, S.S., Ali, M., Ahmad, M., Siddique, K.H.M., 2011. Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnology Advances, 29(3): 300-311.
• Hyun, T.K., Eom, S.H., Jeun, Y.C., Han, S.H., Kim, J-S., 2013. Identification of glutamate decarboxylases as a γ-aminobutyric acid (GABA) biosynthetic enzyme in soybean. Industrial Crops and Products, 49: 864-870.
• Janicka-Russak, M., Kabala, K., Mlodzinska, E., Klobus, G., 2010. The role of polyamines in the regulation of the plasma membrane and the tonoplast proton pumps under salt stress. Journal of Plant Physiology, 167(4): 261-269.
• Kakkar, R.K., Sawhney, V.K., 2002. Polyamine research in plants-a changing perspective. Physiologia Plantarum, 116(3): 281-292.
• Kallio, A., McCann, P., Bey, P., 1981. DL-α-(difluoromethyl)arginine: a potent enzyme-activated inhibitor of bacterial arginine decarboxylase. Biochemistry, 20(11): 3163-3166.
• Kaur-Sawhney, R., Tiburcio, A.F., Galston, A.W., 1988. Spermidine and floral bud differentiation in thin layer explants of tobacco. Planta, 173: 282-284.
• Kevers, C., Le Gal, N., Monteiro, M., Dommes, J., Gaspar, T., 2000. Somatic embryogenesis of Panax ginseng in liquid cultures: a role for polyamines and their metabolic pathways. Plant Growth Regulation, 31: 209-214.
• Kiełkowska, A., Dziurka, M., 2021. Changes in polyamine pattern mediates sex differentiation and unisexual flower development in monoecious cucumber (Cucumis sativus L.). Physiologia Plantarum, 171(1): 48-65.
• Kumar, A., Altabella, T., Taylor, M.A., Tiburcio, A.F., 1997. Recent advances in polyamine research. Trends Plant Science, 2(4): 124-130.
• Kushad, M.M., Richardson, D.G., Ferro, A.J., 1983. Intermediates in the recycling of 5’-methylthioribose to methionine in fruits. Plant Physiology, 73(2): 257-261.
• Li, Z., Hou, J., Zhang, Y., Zeng, W., Cheng, B., Hassan, M.J., Zhang, Y., Pu, Q., Peng, Y., 2020. Spermine regulates water balance associated with Ca2+-dependent aquaporins (TrTIP2-1, TrTIP2-2, and TrPIP2-7) expression in plants under water stress. Plant Cell Physiology, 61(9): 1576-1589.
• Li, Z., Peng, Y., Zhang, X.Q., Ma, X., Huang, L.K., Yan, Y.H., 2014. Exogenous spermidine improves seed germination of white clover under water stress via involvement in starch metabolism, antioxidant defenses and relevant gene expression. Molecules, 19: 18003-18024.
• Lieberman, M., 1979. Biosynthesis and action of ethylene. Annual Review of Plant Physiology, 30: 533-591.
• Mattoo, A.K., Minocha, S.C., Minocha, R., Handa, A.K., 2010. Polyamines and cellular metabolism in plants: transgenic approaches reveal different responses to diamine putrescine versus higher polyamines spermidine and spermine. Amino Acids, 38(2): 405-413.
• Miyamoto, M., Shimao, S., Tong, W., Motose, H., Takahashi, T., 2019. Effect of thermospermine on the growth and expression of polyamine-related genes in rice seedlings. Plants, 8(8): 269-270.
• Mo, A., Xu, T., Bai, Q., Shen, Y., Gao, F., Guo, J., 2020. FaPAO5 regulates Spm/Spd levels as a signaling during strawberry fruit ripening. Plant Direct, 4(5): 1-14.
• Moschou, P.N., Delis, I.D., Paschalidis, K.A., Roubelakis-Angelakis, K.A., 2008. Transgenic tobacco plants overexpressing polyamine oxidase are not able to cope with oxidative burst generated by abiotic factors. Physiologia Plantarum, 133(2): 140-156.
• Osorio, S., Carneiro, R.T., Lytovchenko, A., McQuinn, R., Sørensen, I., Vallarino, J.G., James, J.G., Alisdair, R.F., Jocelyn, K.C.R., 2020. Genetic and metabolic effects of ripening mutations and vine detachment on tomato fruit quality. Plant Biotechnology Journal, 18(1): 106-118.
• Pal, M., Szalai, G., Janda, T., 2015. Speculation: polyamines are important in abiotic stress signaling. Plant Science, 237: 16-23.
• Parra-Lobato, M.C., Gomez-Jimenez, M.C., 2011. Polyamine-induced modulation of genes involved in ethylene biosynthesis and signaling pathways and nitric oxide production during olive mature fruit abscission. Journal of Experimental Botany, 62(13): 4447-4465.
• Pegg, A.E., Jacobs, G., 1983. Comparison of inhibitors of S-adenosylmethionine decarboxylase from different species. Biochemical Journal, 213(2): 495-502.
• Pistocchi, R., Bagni, N., 1990. Effect of Calcium on Spermine Uptake in Carrot Cell Cultures and Protoplasts. Journal of Plant Physiology, 136(6): 728-733.
• Roberts, D.R., Dumbroff, E.F., Thompson, J.E., 1986. Exogenous polyamines alter membrane fluidity in bean leaves-a basis for potential misinterpretation of their true physiological role. Planta, 167(3): 395-401.
• Roberts, D.R., Walker, M.A., Thompson, J.E., Dumbroff, E.B., 1984. The effect of inhibitors of polyamine and ethylene biosynthesis on senescence, ethylene production and polyamine levels in cut carnations. Plant Cell Physiology, 25(2): 315-322.
• Santa-Catarina, C., Silveira, V., Scherer, G.F.E., Floh, E.I.S., 2007. Polyamine and nitric oxide levels relate with morphogenetic evolution in somatic embryogenesis of Ocotea catharinensis. Plant Cell Tissue Organ Culture, 90: 93-101.
• Sauve, D.M., Anderson, H.J., Ray, J.M., James, W.M., Roberge, M., 1991. Phosphorylation-induced rearrangement of the histone H3 NH2-terminal domain during mitotic chromosome condensation. Journal of Cell Biology, 145(2): 225-235.
• Savvides, A., Ali, S., Tester, M., Fotopoulos, V., 2016. Chemical priming of plants against multiple abiotic stresses: mission possible? Trends Plant Science, 21(4): 329-340.
• Schoofs, G., Teichmann, S., Hartmann, T., Wink, M., 1983. Lysine decarboxylase in plants and its integration in quinolizidine alkaloid biosynthesis. Phytochemistry, 22(1): 65-69.
• Simpson, C.G., Cullen, D.W., Hackett, C.A., Smith, K., Hallett, P.D., McNicol, J., Mary, W., Julie, G., 2017. Mapping and expression of genes associated with raspberry fruit ripening and softening. Theoretical and Applied Genetics, 130(3): 557-–572.
• Sindhu, R.K., Cohen, S.S., 1984. Subcellular localization of spermidine synthase in the protoplasts of Chinese cabbage leaves. Plant Physiology, 76(1): 219-223.
• Sindhu, R.K., Desai, H.V., 1979. Purification and properties of agmatine aminohydrolase from groundnut cotyledons. Phytochemistry, 18: 1937-1938.
• Slocum, R.D., Kaur-Sawhney, R., Galston, A.W., 1984. The physiology and biochemistry of polyamines in plants. Archives of Biochemistry and Biophysics, 235(2): 283-303.
• Smith, T.A., 1965. N-Carbamylputrescine amidohydrolase of higher plants and its relation to potassium nutrition. Phytochemistry, 4(4): 599-607.
• Smith, T.A., 1981. Amines. In: P.K. Stumpf and E.E. Conn (Eds.), The Biochemistry of Plants, Academic Press, New York, Vol. 7, pp. 249-268.
• Sorkheh, K., Shiran, B., Rouhi, V., Khodambashi, M., Wolukau, J.N., Ercisli, S., 2011. Response of in vitro pollen germination and pollen tube growth of almond (Prunus dulcis Mill.) to temperature, polyamines, and polyamine synthesis inhibitor. Biochemical Systematics and Ecology, 39(4-6): 749-757.
• Srivastava, S.K., Vashi, D.J., Naik, B.I., 1983. Control of senescence by polyamines and guanidines in young and mature barley leaves. Phytochemistry, 22(10): 2151-2154.
• Srivenugopal, K.S., Adiga, P.R., 1981. Enzymic conversion of agmatine to putrescine in Lathyrus seedlings. Purification and properties of a multifunctional enzyme (putrescine synthase). Journal of Biological Chemistry, 256(18): 9532-9541.
• Sundararajan, S., Sivakumar, H.P., Nayeem, S., Rajendran, V., Subiramani, S., Ramalingam, S., 2021. Influence of exogenous polyamines on somatic embryogenesis and regeneration of fresh and long-term cultures of three elite indica rice cultivars. Cereal Research Communications, 49: 245-253.
• Tabor, C.W., Tabor, H., 1984. Polyamines. Annual Review of Biochemistry, 53: 749-790.
• Takahashi, T., Kakehi, J., 2010. Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Annals of Botany, 105(1): 1-6.
• Tiburcio, A.F., 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.
• Tsaniklidis, G., Kotsiras, A., Tsafouros, A., Roussos, P.A., Aivalakis, G., Katinakis, P., Costas, D., 2016. Spatial and temporal distribution of genes involved in polyamine metabolism during tomato fruit development. Plant Physiology and Biochemistry, 100: 27-36.
• Van Doorn, W.G., Woltering, E.J., 2008. Physiology and molecular biology of petal senescence. Journal of Experimental Botany, 59(3): 453-480.
• Williams, J.H., Reese, J.B., 2019. Evolution of development of pollen performance. In: U. Grossniklaus (Ed.), Current Topics in Developmental Biology, Elsevier, Switzerland, pp. 299-336.
• Wolukau, J.N., Zhang, S., Xu, G., Chen, D., 2004. The effect of temperature, polyamines and polyamine synthesis inhibitor on in vitro pollen germination and pollen tube growth of Prunus mume. Scientia Horticulturae, 99(3-4): 289-299.
• Wu, J., Shang, Z., Wu, J., Jiang, X., Moschou, P.N., Sun, W., Roubelakis-Angelakis, K.A., Zhang, S., 2010. Spermidine oxidase‐ derived H2O2 regulates pollen plasma membrane hyperpolarization‐ activated Ca2+ permeable channels and pollen tube growth. The Plant Journal, 63(6): 1042-1053.
• Xin, S.Q., Gao, Y., Zhao, J.M., Liu, X.M., 2010. Effect of seed soaking in spermidine (Spd) under salt stress on rice seed germination. North Rice, 40: 23-25.
• Xu, Q., Li, H., Liu, S. Wenpei, H., Xiaolin, X., Qing, L., Yue, L., Rui, C., Zechen, S., Yuanzhi, P., 2022. Gibberellin and spermidine synergistically regulate polyamine metabolism during the development of Rhododendron flowers. Plant Growth Regulation, 96(6): 37-50.
• Yanasigawa, H., Suzuki, Y., 1982. Purification and properties of N-carbamoyl-putrescine aminohydrolase from maize shoots. Phytochemistry, 21: 2201-2203.
• Yang, L.I.U., Hong, X.U., Xiao-Xia, W.E.N., Yun-Cheng, L.I.A.O., 2016. Effect of polyamine on seed germination of wheat under drought stress is related to changes in hormones and carbohydrates. Journal of Integrative Agriculture, 15(12): 2759-2774.
• Zhang, H.S., Zhou, C.J., 2013. Signal transduction in leaf senescence. Plant Molecular Biology, 82(6): 539-545.
• Zhou, T., Wang, P., Gu, Z.X., Ma, M., Yang, R.Q., 2020. Spermidine improves antioxidant activity and energy metabolism in mung bean sprouts. Food Chemistry, 309: 125759.