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Polyamine Metabolism Responses to Biotic and Abiotic Stress

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Polyamines

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1694))

Abstract

Plants have developed different strategies to cope with the environmental stresses they face during their life cycle. The responses triggered under these conditions are usually characterized by significant modifications in the metabolism of polyamines such as putrescine, spermidine, and spermine. Several works have demonstrated that a fine-tuned regulation of the enzymes involved in the biosynthesis and catabolism of polyamines leads to the increment in the concentration of these compounds. Polyamines exert different effects that could help plants to deal with stressful conditions. For instance, they interact with negatively charged macromolecules and regulate their functions, they may act as compatible osmolytes, or present antimicrobial activity against plant pathogens. In addition, they have also been proven to act as regulators of gene expression during the elicitation of stress responses. In this chapter, we reviewed the information available till date in relation to the roles played by polyamines in the responses of plants during biotic and abiotic stress.

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References

  1. Michael AJ (2016) Polyamines in eukaryotes, bacteria and archaea. J Biol Chem 291:14896–14903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Igarashi K, Kashiwagi K (2000) Polyamines: mysterious modulators of cellular functions. Biochem Biophys Res Commun 271:559–564

    Article  CAS  PubMed  Google Scholar 

  3. Poulin R, Coward JK, Lakanen JR, Pegg AE (1993) Enhancement of the spermidine uptake system and lethal effects of spermidine overaccumulation in ornithine decarboxylase-overproducing L1210 cells under hyposmotic stress. J Biol Chem 268:4690–4698

    PubMed  CAS  Google Scholar 

  4. Jiménez-Bremont JF, Marina M, Guerrero-González ML, Rossi FR, Sánchez-Rangel D, Rodríguez-Kessler M, Ruiz OA, Gárriz A (2014) Physiological and molecular implications of plant polyamine metabolism during biotic interactions. Front Plant Sci 5:95

    PubMed  PubMed Central  Google Scholar 

  5. Alcazar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    Article  CAS  PubMed  Google Scholar 

  6. Pandey S, Ranade SA, Nagar PK, Kumar N (2000) Role of polyamines and ethylene as modulators of plant senescence. J Biosci 25:291–299

    Article  CAS  PubMed  Google Scholar 

  7. Urano K, Maruyama K, Ogata Y, Morishita Y, Takeda M, Sakurai N, Suzuki H, Saito K, Shibata D, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant J 57:1065–1078

    Article  CAS  PubMed  Google Scholar 

  8. Yamasaki H, Cohen MF (2006) NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants? Trends Plant Sci 11:522–524

    Article  CAS  PubMed  Google Scholar 

  9. Tiburcio AF, Altabella T, Bitrián M, Alcázar R (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 240:1–18

    Article  CAS  Google Scholar 

  10. Walters DR (2003) Polyamines and plant disease. Phytochemistry 64:97–107

    Article  CAS  PubMed  Google Scholar 

  11. Walters DR (2000) Polyamines in plant-microbe interactions. Physiol Mol Plant Pathol 57:137–146

    Article  CAS  Google Scholar 

  12. Broetto F, Marchese JA, Leonardo M, Regina M (2005) Fungal elicitor- mediated changes in polyamine content, phenylalanine-ammonia lyase and peroxidase activities in bean cell culture. Gen Appl Plant Physiol 31:235–246

    Google Scholar 

  13. Rodríguez-Kessler M, Ruiz OA, Maiale S, Ruiz-Herrera J, Jiménez-Bremont JF (2008) Polyamine metabolism in maize tumors induced by Ustilago maydis. Plant Physiol Biochem 46:805–814

    Article  PubMed  Google Scholar 

  14. Rossi FR, Marina M, Pieckenstain FL (2015) Role of arginine decarboxylase (ADC) in Arabidopsis thaliana defence against the pathogenic bacterium Pseudomonas viridiflava. Plant Biol 17:831–839

    Article  CAS  PubMed  Google Scholar 

  15. Fernández-Crespo E, Scalschi L, Llorens E, García-Agustín P, Camañes G (2015) NH4+ protects tomato plants against Pseudomonas syringae by activation of systemic acquired acclimation. J Exp Bot 66:6777–6790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Marini F, Betti L, Scaramagli S, Biondi S, Torrigiani P (2001) Polyamine metabolism is upregulated in response to tobacco mosaic virus in hypersensitive, but not in susceptible, tobacco. New Phytol 149:301–309

    Article  CAS  Google Scholar 

  17. Mo H, Wang X, Zhang Y, Yang J, Ma Z (2015) Cotton ACAULIS5 is involved in stem elongation and the plant defense response to Verticillium dahliae through thermospermine alteration. Plant Cell Rep 34:1975–1985

    Article  CAS  PubMed  Google Scholar 

  18. Mo H, Wang X, Zhang Y, Zhang G, Zhang J, Ma Z (2015) Cotton polyamine oxidase is required for spermine and camalexin signalling in the defence response to Verticillium dahliae. Plant J 83:962–975

    Article  CAS  PubMed  Google Scholar 

  19. Mo H-J, Sun Y-X, Zhu X-L, Wang X-F, Zhang Y, Yang J, Yan G-J, Ma Z-Y (2016) Cotton S-adenosylmethionine decarboxylase-mediated spermine biosynthesis is required for salicylic acid- and leucine-correlated signaling in the defense response to Verticillium dahliae. Planta 243:1023–1039

    Article  CAS  PubMed  Google Scholar 

  20. Gonzalez ME, Marco F, Minguet EG, Carrasco-Sorli P, Blazquez MA, Carbonell J, Ruiz OA, Pieckenstain FL (2011) 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 156:2266–2277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Marco F, Busó E, Carrasco P (2014) Overexpression of SAMDC1 gene in Arabidopsis thaliana increases expression of defense-related genes as well as resistance to Pseudomonas syringae and Hyaloperonospora arabidopsidis. Front Plant Sci 5:115

    Article  PubMed  PubMed Central  Google Scholar 

  22. Marina M, Sirera FV, Rambla JL, Gonzalez ME, Blázquez MA, Carbonell J, Pieckenstain FL, Ruiz OA (2013) Thermospermine catabolism increases Arabidopsis thaliana resistance to Pseudomonas viridiflava. J Exp Bot 64:1393–1402

    Article  CAS  PubMed  Google Scholar 

  23. Sagor GHM, Takahashi H, Niitsu M, Takahashi Y, Berberich T, Kusano T (2012) Exogenous thermospermine has an activity to induce a subset of the defense genes and restrict cucumber mosaic virus multiplication in Arabidopsis thaliana. Plant Cell Rep 31:1227–1232

    Article  CAS  PubMed  Google Scholar 

  24. Marina M, Maiale SJ, Rossi FR, Romero FM, Rivas EI, Garriz A, Ruiz OA, Pieckenstain FL (2008) Apoplastic polyamine oxidation plays different roles in local responses of tobacco to infection by the necrotrophic fungus Sclerotinia sclerotiorum and the biotrophic bacterium Pseudomonas viridiflava. Plant Physiol 147:2164–2178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10:751–757

    Article  CAS  PubMed  Google Scholar 

  26. Moschou PN, Sarris PF, Skandalis N, Andriopoulou AH, Paschalidis KA, Panopoulos NJ, Roubelakis-Angelakis KA (2009) Engineered polyamine catabolism preinduces tolerance of tobacco to bacteria and oomycetes. Plant Physiol 149:1970–1981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Yoda H, Fujimura K, Takahashi H, Munemura I, Uchimiya H, Sano H (2009) Polyamines as a common source of hydrogen peroxide in host- and nonhost hypersensitive response during pathogen infection. Plant Mol Biol 70:103–112

    Article  CAS  PubMed  Google Scholar 

  28. Lou Y-R, Bor M, Yan J, Preuss AS, Jander G (2016) Arabidopsis NATA1 acetylates putrescine and decreases defense-related hydrogen peroxide accumulation. Plant Physiol 171:1443–1455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Jasso-Robles FI, Jiménez-Bremont JF, Becerra-Flora A, Juárez-Montiel M, Gonzalez ME, Pieckenstain FL, García de la Cruz RF, Rodríguez-Kessler M (2016) Inhibition of polyamine oxidase activity affects tumor development during the maize-Ustilago maydis interaction. Plant Physiol Biochem 102:115–124

    Article  CAS  PubMed  Google Scholar 

  30. Stes E, Biondi S, Holsters M, Vereecke D (2011) Bacterial and plant signal integration via D3-type cyclins enhances symptom development in the Arabidopsis-Rhodococcus fascians interaction. Plant Physiol 156:712–725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Hewezi T, Howe PJ, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ (2010) Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiol 152:968–984

    Article  PubMed  PubMed Central  Google Scholar 

  32. Zhang Z, Chen H, Huang X, Xia R, Zhao Q, Lai J, Teng K, Li Y, Liang L, Du Q, Zhou X, Guo H, Xie Q (2011) BSCTV C2 attenuates the degradation of SAMDC1 to suppress DNA methylation-mediated gene silencing in Arabidopsis. Plant Cell 23:273–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Kim NH, Kim BS, Hwang BK (2013) Pepper arginine decarboxylase is required for polyamine and γ-aminobutyric acid signaling in cell death and defense response. Plant Physiol 162:2067–2083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Menéndez AB, Rodriguez AA, Maiale SJ, Rodriguez-Kessler M, Jimenez-Bremont JF, Ruiz OA (2013) Polyamines contribution to the improvement of crop plants tolerance to abiotic stress. In: Tuteja N, Gill SS (eds) Crop improvement under adverse conditions. Springer New York, New York, NY, pp 113–136

    Chapter  Google Scholar 

  35. Do PT, Degenkolbe T, Erban A, Heyer AG, Kopka J, Köhl KI, Hincha DK, Zuther E (2013) Dissecting rice polyamine metabolism under controlled long-term drought stress. PLoS One 8(4):e60325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Yang W, Yin Y, Li Y, Cai T, Ni Y, Peng D, Wang Z (2014) Interactions between polyamines and ethylene during grain filling in wheat grown under water deficit conditions. Plant Growth Regul 72:189–201

    Article  CAS  Google Scholar 

  37. Li Z, Zhou H, Peng Y, Zhang X, Ma X, Huang L, Yan Y (2015) Exogenously applied spermidine improves drought tolerance in creeping bentgrass associated with changes in antioxidant defense, endogenous polyamines and phytohormones. Plant Growth Regul 76:71–82

    Article  CAS  Google Scholar 

  38. Talaat NB, Shawky BT (2016) 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 Regul 35:518–533

    Article  CAS  Google Scholar 

  39. Hussain S, Farooq M, Wahid M, Wahid A (2013) Seed priming with putrescine improves the drought resistance of maize hybrids. Int J Agric Biol 15:1349–1353

    Google Scholar 

  40. 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

    Article  CAS  PubMed  Google Scholar 

  41. Li Z, Zhang Y, Xu Y, Zhang X, Peng Y, Ma X, Huang L, Yan Y (2016) Physiological and iTRAQ-based proteomic analyses reveal the function of spermidine on improving drought tolerance in white clover. J Proteome Res 15:1563–1579

    Article  CAS  PubMed  Google Scholar 

  42. Espasandin FD, Maiale SJ, Calzadilla P, Ruiz OA, Sansberro PA (2014) Transcriptional regulation of 9-cis-epoxycarotenoid dioxygenase (NCED) gene by putrescine accumulation positively modulates ABA synthesis and drought tolerance in Lotus tenuis plants. Plant Physiol Biochem 76:29–35

    Article  CAS  PubMed  Google Scholar 

  43. Do PT, Drechsel O, Heyer AG, Hincha DK, Zuther E (2014) 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 5:182

    Article  PubMed  PubMed Central  Google Scholar 

  44. Zhang N, Shi X, Guan Z, Zhao S, Zhang F, Chen S, Fang W, Chen F (2016) Treatment with spermidine protects chrysanthemum seedlings against salinity stress damage. Plant Physiol Biochem 105:260–270

    Article  CAS  PubMed  Google Scholar 

  45. Nahar K, Hasanuzzaman M, Rahman A, Alam MM, Mahmud J-A, Suzuki T, Fujita M (2016) 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 7:1104

    Article  PubMed  PubMed Central  Google Scholar 

  46. Zhang G-w, Xu S-c, Hu Q-z, Mao W-h, Gong Y-m (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

    Article  CAS  Google Scholar 

  47. Yuan Y, Zhong M, Shu S, Du N, Sun J, Guo S (2016) Proteomic and physiological analyses reveal putrescine responses in roots of cucumber stressed by NaCl. Front Plant Sci 7:1035

    PubMed  PubMed Central  Google Scholar 

  48. 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

    Article  CAS  PubMed  Google Scholar 

  49. Sudhakar C, Veeranagamallaiah G, Nareshkumar A, Sudhakarbabu O, Sivakumar M, Pandurangaiah M, Kiranmai K, Lokesh U (2015) Polyamine metabolism influences antioxidant defense mechanism in foxtail millet (Setaria italica L.) cultivars with different salinity tolerance. Plant Cell Rep 34:141–156

    Article  CAS  PubMed  Google Scholar 

  50. Pillai MA, Akiyama T (2004) Differential expression of an S-adenosyl-L-methionine decarboxylase gene involved in polyamine biosynthesis under low temperature stress in japonica and indica rice genotypes. Mol Genet Genomics 271:141–149

    Article  CAS  PubMed  Google Scholar 

  51. Song Y, Diao Q, Qi H (2015) Polyamine metabolism and biosynthetic genes expression in tomato (Lycopersicon esculentum Mill.) seedlings during cold acclimation. Plant Growth Regul 75:21–32

    Article  CAS  Google Scholar 

  52. Shen W, Nada K, Tachibana S (2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiol 124:431–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Cuevas JC, López-Cobollo R, Alcázar 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

    Article  PubMed  PubMed Central  Google Scholar 

  54. Alet AI, Sanchez DH, Cuevas JC, del Valle S, Altabella T, Tiburcio AF, Marco F, Ferrando A, Espasandín FD, González ME, Carrasco P, Ruiz OA (2011) Putrescine accumulation in Arabidopsis thaliana transgenic lines enhances tolerance to dehydration and freezing stress. Plant Signal Behav 6:278–286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Tian X, Liu Y, Huang Z, Duan H, Tong J, He X, Gu W, Ma H, Xiao L (2015) Comparative proteomic analysis of seedling leaves of cold-tolerant and -sensitive spring soybean cultivars. Mol Biol Rep 42:581–601

    Article  CAS  PubMed  Google Scholar 

  56. Yang Y-W, Chen H-C, Jen W-F, Liu L-Y, Chang M-C (2015) Comparative transcriptome analysis of shoots and roots of TNG67 and TCN1 rice seedlings under cold stress and following subsequent recovery: insights into metabolic pathways, phytohormones, and transcription factors. PLoS One 10:e0131391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Dametto A, Sperotto RA, Adamski JM, Blasi ÉAR, Cargnelutti D, de Oliveira LFV, Ricachenevsky FK, Fregonezi JN, Mariath JEA, da Cruz RP, Margis R, Fett JP (2015) Cold tolerance in rice germinating seeds revealed by deep RNAseq analysis of contrasting indica genotypes. Plant Sci 238:1–12

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants of Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) (PICT 2011-1612, 2014-3718, 2014-3648, and 2013-0477) and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) (PIP 0363 and 0980). A.G, M.M, F.R.R, S.J.M and O.A.R are members of the Research Career of Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). FMR is postdoctoral fellow of ANPCyT.

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Romero, F.M., Maiale, S.J., Rossi, F.R., Marina, M., Ruíz, O.A., Gárriz, A. (2018). Polyamine Metabolism Responses to Biotic and Abiotic Stress. In: Alcázar, R., Tiburcio, A. (eds) Polyamines. Methods in Molecular Biology, vol 1694. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7398-9_3

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  • DOI: https://doi.org/10.1007/978-1-4939-7398-9_3

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