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Polyamines and Their Metabolic Engineering for Plant Salinity Stress Tolerance

  • Tushar Khare
  • Amrita Srivastav
  • Samrin Shaikh
  • Vinay Kumar
Chapter

Abstract

Polyamines (PAs) are small polycationic aliphatic amines and are ubiquitous in the plant kingdom. They play important roles in plant growth, development, and stress responses. Several research reports have established a correlation between their accumulation and salt stress tolerance in different plant species. Creditable research in the recent past has proved their vital roles in stress responses and adaptation strategies employed by plants, including scavenging of free radicals, neutralization of acids, and stabilization of cell membranes. They are able to bind several charged molecules including DNA, proteins, membrane phospholipids, and pectic polysaccharides, and have been credited with roles in protein phosphorylation and post-transcriptional modifications. They also play important roles in plant growth regulation, as well as acting as signaling molecules. Owing to their diverse functions in plant growth, development, and stress responses, they have emerged as potent targets for metabolic engineering to confer salt stress tolerance on manipulated plants. This chapter highlights their biosynthesis and transport, their exogenous applications to alleviate salt stress, and their metabolic engineering for developing salt-tolerant plants.

Keywords

Salinity stress Polyamines Metabolic engineering Spermine Spermidine Putrescine Transgenics 

Abbreviations

ABA

Abscisic acid

ACC

Aminocyclopropane carboxylate

ADC

Arginine decarboxylase

APOX

Ascorbate peroxidase

cDNA

Complementary DNA

DAO

Diamine oxidase

dcSAM

Decarboxylated S-adenosylmethionine

EMS

Ethyl methanesulfonate

FAD

Flavin adenine dinucleotide

Fv/Fm

Variable fluorescence/maximum fluorescence

GABA

Gamma aminobutyric acid

GOT

Glutamate oxaloacetate transaminase

GPT

Glutamate pyruvate transaminase

GR

Glutathione reductase

GS

Glutamine synthetase

LAT

L-type amino acid transporter

NAD

Nicotinamide adenine dinucleotide

NADH

Reduced nicotinamide adenine dinucleotide

NADH-GDH

NADH-dependent glutamate dehydrogenase

NADH-GOGAT

NADH–glutamine oxoglutarate aminotransferase

NADPH

Reduced nicotinamide adenine dinucleotide phosphate

NDPK

Nucleoside diphosphate kinase

NO

Nitric oxide

ODC

Ornithine decarboxylic acid

ORF

Open reading frame

PA

Polyamine

PSII

Photosystem II

Put

Putrescine

PUT

Polyamine uptake transporter

ROS

Reactive oxygen species

SAM

S-adenosylmethionine

SAMDC

S-adenosylmethionine decarboxylase

SAMS

S-adenosylmethionine synthetase

SOD

Superoxide dismutase

Spd

Spermidine

SPDS

Spermidine synthase

Spm

Spermine

SPMS

Spermine synthase

tSpm

Thermospermine

Notes

Acknowledgements

The research work in the corresponding author’s laboratory is supported by Science and Engineering Research Board (SERB), Department of Science and Technology (DST), Government of India funds (grant number EMR/2016/003896). The authors acknowledge the use of facilities created under DST-FIST and DBT Star College Schemes implemented at Modern College, Ganeshkhind, Pune, India.

References

  1. Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio A (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249. https://doi.org/10.1007/s00425-010-1130-0 CrossRefPubMedGoogle Scholar
  2. Alcázar R, Bitrián M, Bartels D et al (2011) Polyamine metabolic canalization in response to drought stress in Arabidopsis and the resurrection plant Craterostigma plantagineum. Plant Signal Behav 6:243–250. https://doi.org/10.4161/psb.6.2.14317 CrossRefPubMedCentralPubMedGoogle Scholar
  3. Alet AI, Sánchez DH, Cuevas JC, Marina M, Carrasco P, Altabella T, Tiburcio AF, Ruiz OA (2012) New insights into the role of spermine in Arabidopsis thaliana under long-term salt stress. Plant Sci 182:94–100. https://doi.org/10.1016/j.plantsci.2011.03.013 CrossRefPubMedGoogle Scholar
  4. Ali RM (2000) Role of putrescine in salt tolerance of Atropa belladonna plant. Plant Sci 152:173–179CrossRefGoogle Scholar
  5. Amri E, Mirzaei M, Moradi M, Zare K (2011) The effects of spermidine and putrescine polyamines on growth of pomegranate (Punica granatum L. cv “Rabbab”) in salinity circumstance. Int J Plant Physiol Biochem 3:43–49Google Scholar
  6. Anjum MA (2011) Effect of exogenously applied spermidine on growth and physiology of citrus rootstock Troyer citrange under saline. Turk J Agric For 35:43–53. https://doi.org/10.3906/tar-0912-563 Google Scholar
  7. Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16. https://doi.org/10.1016/j.plantsci.2003.10.024 CrossRefGoogle Scholar
  8. Bachrach U (2005) Naturally occurring polyamines: interaction with macromolecules. Curr Protein Pept Sci 6:559–566. https://doi.org/10.2174/138920305774933240 CrossRefPubMedGoogle Scholar
  9. Basu HS, Schwietert HCA, Feuerstein BG, Marton LJ (1990) Effect of variation in the structure of spermine on the association with DNA and the induction of DNA conformational changes. Biochem J 269:329–334CrossRefPubMedCentralPubMedGoogle Scholar
  10. Beigbeder AR (1995) Influence of polyamine inhibitors on light independent and light dependent chlorophyll biosynthesis and on the photosyntetic rate. J Photochem Photobiol 28:235–242CrossRefGoogle Scholar
  11. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125. https://doi.org/10.1016/S0168-9452(98)00218-0 CrossRefGoogle Scholar
  12. Chai YY, Jiang CD, Shi L et al (2010) Effects of exogenous spermine on sweet sorghum during germination under salinity. Biol Plant 54:145–148. https://doi.org/10.1007/s10535-010-0023-1 CrossRefGoogle Scholar
  13. Cuevas JC, Lopez-Cobollo R, Alcazar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (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. https://doi.org/10.1104/pp.108.122945 CrossRefPubMedCentralPubMedGoogle Scholar
  14. D’Oraci D, Bagni N (1987) In vitro interactions between polyamines and pectic substances. Biochem Biophys Res Commun 148:1159–1163Google Scholar
  15. Demetriou G, Neonaki C, Navakoudis E, Kotzabasis K (2007) Salt stress impact on the molecular structure and function of the photosynthetic apparatus—the protective role of polyamines. 1767:272–280. https://doi.org/10.1016/j.bbabio.2007.02.020
  16. Drolet G, Dumbroff EB, Legge RL, Thompson JE (1986) Radical scavenging properties of polyamines. Phytochemistry 25:367–371. https://doi.org/10.1016/S0031-9422(00)85482-5 CrossRefGoogle Scholar
  17. Duan JJ, 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. https://doi.org/10.1016/j.jplph.2007.11.006 CrossRefPubMedGoogle Scholar
  18. Dupont-gillain CC, Quinet M, Ndayiragije A et al (2017) Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. 61:2719–2733. https://doi.org/10.1093/jxb/erq118
  19. El Ghachtoul N, Martin-Tangu J, Paynot M, Gianinazz S (1996) First report of the inhibition of arbuscular mycorrhizal infection of Pisum sativum by specific and irreversible inhibition of polyamine biosynthesis or by gibberellic treatment. FEBS Lett 385:189–192CrossRefGoogle Scholar
  20. Espasandin FD, Calzadilla PI, Maiale SJ, Ruiz OA, Sansberro PA (2017) Overexpression of the arginine decarboxylase gene improves tolerance to salt stress in Lotus tenuis plants. J Plant Growth Regul:1–10. https://doi.org/10.1007/s00344-017-9713-7
  21. Evans PT, Malmberg RL (1989) Do polyamines have roles in plant development? Annu Rev Plant Physiol Plant Mol Biol 40:235–269CrossRefGoogle Scholar
  22. Galston AW, Kaur-Sawhney RK (1990) Polyamines in plant physiology. Plant Physiol 94:406–410CrossRefPubMedCentralPubMedGoogle Scholar
  23. Galston AW, Kaur-Sawhney R (1995) Polyamines as endogenous growth regulators. In: Davies PJ (ed) lant hormones: physiology, biochemistry and molecular biology, 2nd edn. Kluwer Academic Publishers, Dordrecht, pp 158–178Google Scholar
  24. Galston AW, Kaur-Sawhney R, Altabella T, Tiburcio AF (1997) Plant polyamines in reproductive activity and response to abiotic stress. Bot Acta 110:197–207. https://doi.org/10.1111/j.1438-8677.1997.tb00629.x CrossRefGoogle Scholar
  25. Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5:26–33. https://doi.org/10.4161/psb.5.1.10291 CrossRefPubMedCentralPubMedGoogle Scholar
  26. Gong B, Li X, VandenLangenberg KM, Wen D, Sun S, Wei M, Li Y, Yang F, Shi Q, Wang X (2014) Overexpression of S-adenosyl-l-methionine synthetase increased tomato tolerance to alkali stress through polyamine metabolism. Plant Biotechnol J 12:694–708. https://doi.org/10.1111/pbi.12173 CrossRefPubMedGoogle Scholar
  27. Gong XQ, Zhang JY, Hu JB, Wang W, Wu H, Zhang QH, Liu JH (2015) FcWRKY70, a WRKY protein of Fortunella crassifolia, functions in drought tolerance and modulates putrescine synthesis by regulating arginine decarboxylase gene. Plant Cell Environ 38:2248–2262CrossRefPubMedGoogle Scholar
  28. Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45. https://doi.org/10.1007/s00726-007-0501-8 CrossRefPubMedGoogle Scholar
  29. Gupta B, Huang B, Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics 2014:1–18. https://doi.org/10.1155/2014/701596 CrossRefGoogle Scholar
  30. Gu-wen Z, Sheng-chun XU, Qi-zan HU et al (2014) Putrescine plays a positive role in salt-tolerance mechanisms by reducing oxidative damage in roots of vegetable soybean. J Integr Agric 13:349–357. https://doi.org/10.1016/S2095-3119(13)60405-0 CrossRefGoogle Scholar
  31. Heby O, Persson L (1990) Molecular genetics of polyamine synthesis in eukaryotic cells. Trends Biochem Sci 15:153–158CrossRefPubMedGoogle Scholar
  32. Hu X, Zhang Y, Shi Y et al (2012) Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity–alkalinity mixed stress. Plant Physiol Biochem 57:200–209. https://doi.org/10.1016/j.plaphy.2012.05.015 CrossRefPubMedGoogle Scholar
  33. Hussain SS, Ali M, Ahmad M, Siddique KHM (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29:300–311. https://doi.org/10.1016/j.biotechadv.2011.01.003 CrossRefPubMedGoogle Scholar
  34. Kasinathan V, Wingler A (2004) Effect of reduced arginine decarboxylase activity on salt tolerance and on polyamine formation during salt stress in Arabidopsis thaliana. Physiol Plant 121:101–107. https://doi.org/10.1111/j.0031-9317.2004.00309.x CrossRefPubMedGoogle Scholar
  35. Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (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. https://doi.org/10.1093/pcp/pch083 CrossRefPubMedGoogle Scholar
  36. Kaur-Sawhney R, Tiburcio AF, Altabella T, Galston AW (2003) Polyamines in plants: an overview. J Cell Mol Biol 2:1–12Google Scholar
  37. Koc E, Islek C, Kasko Arici Y (2017) Spermine and its interaction with proline induce resistance to the root rot pathogen Phytophthora capsici in pepper (Capsicum annuum). Hortic Environ Biotechnol 58:254–267CrossRefGoogle Scholar
  38. Kumria R, Rajam MV (2002) Ornithine decarboxylase transgene in tobacco affects polyamines, in vitro-morphogenesis and response to salt stress. J Plant Physiol159:983–90Google Scholar
  39. Kuznetsov VV, Shevyakova NI (2007) Polyamines and stress tolerance of plants. Plant Stress 1:50–71Google Scholar
  40. Legocka J, Kluk A (2005) Effect of salt and osmotic stress on changes in polyamine content and arginine decarboxylase activity in Lupinus luteus seedlings. J Plant Physiol 162:662–668. https://doi.org/10.1016/j.jplph.2004.08.009 CrossRefPubMedGoogle Scholar
  41. Li B, He L, Guo S et al (2013) Proteomics reveal cucumber Spd-responses under normal condition and salt stress. Plant Physiol Biochem 67:7–14. https://doi.org/10.1016/j.plaphy.2013.02.016 CrossRefPubMedGoogle Scholar
  42. Li S, Jin H, Zhang Q (2016) The effect of exogenous spermidine concentration on polyamine metabolism and salt tolerance in zoysia grass (Zoysia japonica Steud) subjected to short-term salinity stress. Front Plant Sci 7:1221. https://doi.org/10.3389/fpls.2016.01221 PubMedCentralPubMedGoogle Scholar
  43. Liu J, Jiang MY, Zhou YF, Liu Y-L (2005) Production of polyamines is enhanced by endogenous abscisic acid in maize seedlings subjected to salt stress. J Integr Plant Biol 47:1326–1334. https://doi.org/10.1111/j.1744-7909.2005.00183.x CrossRefGoogle Scholar
  44. Marco F, Bitrián M, Carrasco P, Alcázar R, Tiburcio AF (2015) Polyamine biosynthesis engineering as a tool to improve plant resistance to abiotic stress. In: Genetic manipulation in plants for mitigation of climate change. Springer India, pp 103–116. https://doi.org/10.1007/978-81-322-2662-8_5
  45. Martin-Tanguy J (1987) Hydroxycinnamic acid amides, hypersensitivity, flowering and sexual organogenesis in plants. In: Von Wettstein D, Chua DN (eds) Plant molecular biology. Plenum Publishing Corporation, New York, pp 253–263CrossRefGoogle Scholar
  46. Mehta HS, Saftner RA, Mehta RA, Davies PJ (1994) Identification of posttranscriptionally modified 18-kilodalton protein from rice as eukaryotic translocation initiation factor 5A. Plant Physiol 106:1413–1419CrossRefPubMedCentralPubMedGoogle Scholar
  47. Moschou PN, Wu J, Tavladoraki P, Angelini R, Roubelakis-Angelakis KA (2012) The polyamines and their catabolic products are significant players in the turnover of nitrogenous molecules in plants. J Exp Bot 63:5003–5015. https://doi.org/10.1093/jxb/ers202 CrossRefPubMedGoogle Scholar
  48. 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. https://doi.org/10.1007/s11183-005-0005-x CrossRefGoogle Scholar
  49. Parvin S, Ran O, Sathiyaraj G et al (2014) Spermidine alleviates the growth of saline-stressed ginseng seedlings through antioxidative defense system. Gene 537:70–78CrossRefPubMedGoogle Scholar
  50. Pohjanpelto P, Höltta E (1996) Phosphorylation of Okazaki-like DNA fragments in mammalian cells and role of polyamines in the processing of this DNA. EMBO J 15:1193–1200PubMedCentralPubMedGoogle Scholar
  51. Qi YC, Wang FF, Zhang H, Liu WQ (2010) Overexpression of Suadea salsa S-adenosylmethionine synthetase gene promotes salt tolerance in transgenic tobacco. Acta Physiol Plant 32:263–269. https://doi.org/10.1007/s11738-009-0403-3 CrossRefGoogle Scholar
  52. Quinet M, Ndayiragije A, Lefèvre I et al (2010) Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. J Exp Bot 61:2719–2733. https://doi.org/10.1093/jxb/erq118 CrossRefPubMedCentralPubMedGoogle Scholar
  53. Roy M, Wu R (2001) Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Sci 160:869–875. https://doi.org/10.1016/S0168-9452(01)00337-5 CrossRefPubMedGoogle Scholar
  54. Roy M, Wu R (2002) Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride stress tolerance. Plant Sci 163:987–992. https://doi.org/10.1016/S0168-9452(02)00272-8 CrossRefGoogle Scholar
  55. Roy P, Niyogi K, Sengupta DN, Ghosh B (2005) Spermidine treatment to rice seedlings recovers salinity stress-induced damage of plasma membrane and PM-bound H+-ATPase in salt-tolerant and salt-sensitive rice cultivars. Plant Sci 168:583–591. https://doi.org/10.1016/j.plantsci.2004.08.014 CrossRefGoogle Scholar
  56. 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. https://doi.org/10.1016/j.jplph.2010.07.009 CrossRefPubMedGoogle Scholar
  57. Ruiz OA, Rodrı M, Jime JF (2007) Modulation of spermidine and spermine levels in maize seedlings subjected to long-term salt stress. Plant Physiol Biochem 45:812–821. https://doi.org/10.1016/j.plaphy.2007.08.001 CrossRefPubMedGoogle Scholar
  58. Sagor GHM, Berberich T, Takahashi Y, Niitsu M, Kusano T (2013) The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes. Transgenic Res 22:595–605. https://doi.org/10.1007/s11248-012-9666-3 CrossRefPubMedGoogle Scholar
  59. Saha J, Giri K (2017) Molecular phylogenomic study and the role of exogenous spermidine in the metabolic adjustment of endogenous polyamine in two rice cultivars under salt stress. Gene 609:88–103CrossRefPubMedGoogle Scholar
  60. Sang QQ, Shan X, An YH, Shu S, Sun J, Guo SR (2017) Proteomic analysis reveals the positive effect of exogenous spermidine in tomato seedlings’ response to high-temperature stress. Front Plant Sci 8:120PubMedCentralPubMedGoogle Scholar
  61. Shabala S, Cuin TA, Pottosin I (2007) Polyamines prevent NaCl-induced K+ efflux from pea mesophyll by blocking non-selective cation channels. FEBS Lett 581:1993–1999. https://doi.org/10.1016/j.febslet.2007.04.032 CrossRefPubMedGoogle Scholar
  62. Shevyakova NI, Rakitin VY, Stetsenko LA et al (2006a) Oxidative stress and fluctuations of free and conjugated polyamines in the halophyte Mesembryanthemum crystallinum L. under NaCl salinity. Plant Growth Regul 50:69–78. https://doi.org/10.1007/s10725-006-9127-1 CrossRefGoogle Scholar
  63. Shevyakova NI, Shorina MV, Rakitin VY, Kuznetsov VV (2006b) Stress-dependent accumulation of spermidine and spermine in the halophyte Mesembryanthemum crystallinum under salinity conditions. Russ J Plant Physiol 53:739–745. https://doi.org/10.1134/S1021443706060021 CrossRefGoogle Scholar
  64. Shi H, Chan Z (2014) Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. J Integr Plant Biol 56:114–121CrossRefPubMedGoogle Scholar
  65. Shi H, Ye T, Chan Z (2013) 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 12:4951–4964. https://doi.org/10.1021/pr400479k CrossRefPubMedGoogle Scholar
  66. Shu S, Yuan L, Guo S et al (2013) Effects of exogenous spermine on chlorophyll fluorescence, antioxidant system and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress. Plant Physiol Biochem 63:209–216CrossRefPubMedGoogle Scholar
  67. Slocum RD (1991) Tissue and subcellular localisation of polyamines and enzymes of polyamine metabolism. In: Slocum RD, Flores HE (eds) Biochemistry and physiology of polyamines in plants. CRC Press, Boca Raton, pp 93–105Google Scholar
  68. Tabor CW, Tabor H (1984) Polyamines. Annu Rev Biochem 53:749–790CrossRefPubMedGoogle Scholar
  69. Tang W, Newton RJ (2005) Polyamines reduce salt-induced oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine. Plant Growth Regul 46:31–43. https://doi.org/10.1007/s10725-005-6395-0 CrossRefGoogle Scholar
  70. Tassoni A, Antognoni F, Bagni N (1996) Polyamine binding to plasma membrane vesicles from zucchini hypocotyls. Plant Physiol 110:817–824CrossRefPubMedCentralPubMedGoogle Scholar
  71. Tavladoraki P, Cona A, Federico R, Tempera G, Viceconte N, Saccoccio S, Battaglia V, Toninello A, Agostinelli E (2012) Polyamine catabolism: target for antiproliferative therapies in animals and stress tolerance strategies in plants. Amino Acids 42:411–426. https://doi.org/10.1007/s00726-011-1012-1 CrossRefPubMedGoogle Scholar
  72. Tiburcio AF, Kaur-Sawhney R, Galston AW (1990) Polyamine metabolism. In: Miflin BJ, Lea PJ (eds) The biochemistry of plants, intermediary nitrogen fixation. Academic Press, New York, pp 283–325Google Scholar
  73. Tonon G, Kevers C, Faivre-Rampant O, Graziani M, Gaspar T (2004) Effect of NaCl and mannitol iso-osmotic stresses on proline and free polyamine levels in embryogenic Fraxinus angustifolia callus. J Plant Physiol 161:701–708CrossRefPubMedGoogle Scholar
  74. Urano K, Yoshiba Y, Nanjo T, Ito T, Yamaguchi-Shinozaki K, Shinozaki K (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. https://doi.org/10.1016/j.bbrc.2003.11.119 CrossRefPubMedGoogle Scholar
  75. Verma S, Mishra SN (2005) Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. J Plant Physiol 162:669–677. https://doi.org/10.1016/j.jplph.2004.08.008 CrossRefPubMedGoogle Scholar
  76. Waie B, Rajam MV (2003) Effect of increased polyamine biosynthesis on stress response in transgenic tobacco by introduction of human S-adenosylmethionine gene. Plant Sci 164:727–734. https://doi.org/10.1016/S0168-9452(03)00030-X CrossRefGoogle Scholar
  77. Walden R, Cordeiro A, Tiburcio AF (1997) Polyamines: small molecules triggering pathways in plant growth and development. Plant Physiol 113:1009–1013CrossRefPubMedCentralPubMedGoogle Scholar
  78. Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Michael AJ, Kusano T (2006) The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett 580:6783–6788. https://doi.org/10.1016/j.febslet.2006.10.078 CrossRefPubMedGoogle Scholar
  79. Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael AJ, Kusano T (2007) A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun 352:486–490. https://doi.org/10.1016/j.bbrc.2006.11.041 CrossRefPubMedGoogle Scholar
  80. Ye XS, Avdiushko SA, Kuc J (1994) Effect of polyamines on in vitro phosphorylation of soluble and plasma membrane proteins in tobacco, cucumber and Arabidopsis thaliana. Plant Sci 97: 109–118Google Scholar
  81. Zhang Y, Hu X, Shi Y et al (2013) Beneficial role of exogenous spermidine on nitrogen metabolism in tomato seedlings exposed to saline–alkaline stress. J Am Soc Hortic Sci 138:38–49Google Scholar
  82. Zhao FG, Qin P (2004) Protective effect of exogenous polyamines on root tonoplast function against salt stress in barley seedlings. Plant Growth Regul 42:97–103. https://doi.org/10.1023/B:GROW.0000017478.40445.bc CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Tushar Khare
    • 1
  • Amrita Srivastav
    • 1
  • Samrin Shaikh
    • 1
  • Vinay Kumar
    • 1
    • 2
  1. 1.Department of BiotechnologyModern College of Arts, Science and Commerce (Savitribai Phule Pune University)PuneIndia
  2. 2.Department of Environmental ScienceSavitribai Phule Pune UniversityPuneIndia

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