1932

Abstract

This review focuses on the intricate relationship between plant polyamines and the genetic circuits and signaling pathways that regulate various developmental programs and the defense responses of plants when faced with biotic and abiotic aggressions. Particular emphasis is placed on genetic evidence supporting the involvement of polyamines in specific processes, such as the pivotal role of thermospermine in regulating xylem cell differentiation and the significant contribution of polyamine metabolism in enhancing plant resilience to drought. Based on the numerous studies describing effects of the manipulation of plant polyamine levels, two conceptually different mechanisms for polyamine activity are discussed: direct participation of polyamines in translational regulation and the indirect production of hydrogen peroxide as a defensive mechanism against pathogens. By describing the multifaceted functions of polyamines, this review underscores the profound significance of these compounds in enabling plants to adapt and thrive in challenging environments.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-070623-110056
2024-07-22
2025-02-08
Loading full text...

Full text loading...

/deliver/fulltext/arplant/75/1/annurev-arplant-070623-110056.html?itemId=/content/journals/10.1146/annurev-arplant-070623-110056&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abbasi NA, Ali I, Hafiz IA, Khan AS. 2017.. Application of polyamines in horticulture: a review. . Int. J. Biosci. 10:(5):31942
    [Crossref] [Google Scholar]
  2. 2.
    Ahmed S, Ariyaratne M, Patel J, Howard AE, Kalinoski A, et al. 2017.. Altered expression of polyamine transporters reveals a role for spermidine in the timing of flowering and other developmental response pathways. . Plant Sci. 258::14655
    [Crossref] [Google Scholar]
  3. 3.
    Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, et al. 2010.. Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. . Planta 231:(6):123749
    [Crossref] [Google Scholar]
  4. 4.
    Alcázar R, Bueno M, Tiburcio AF. 2020.. Polyamines: small amines with large effects on plant abiotic stress tolerance. . Cells 9:(11):2373
    [Crossref] [Google Scholar]
  5. 5.
    Alcázar R, Cuevas JC, Planas J, Zarza X, Bortolotti C, et al. 2011.. Integration of polyamines in the cold acclimation response. . Plant Sci. 180:(1):3138
    [Crossref] [Google Scholar]
  6. 6.
    Alcázar R, Planas J, Saxena T, Zarza X, Bortolotti C, et al. 2010.. Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants over-expressing the homologous Arginine decarboxylase 2 gene. . Plant Physiol. Biochem. 48:(7):54752
    [Crossref] [Google Scholar]
  7. 7.
    Alet AI, Sánchez DH, Cuevas JC, del Valle S, Altabella T, et al. 2011.. Putrescine accumulation in Arabidopsis thaliana transgenic lines enhances tolerance to dehydration and freezing stress. . Plant Signal. Behav. 6:(2):27886
    [Crossref] [Google Scholar]
  8. 8.
    Alet AI, Sánchez DH, Cuevas JC, Marina M, Carrasco P, et al. 2012.. New insights into the role of spermine in Arabidopsis thaliana under long-term salt stress. . Plant Sci. 182:(1):94100
    [Crossref] [Google Scholar]
  9. 9.
    Alexandrov T. 2020.. Spatial metabolomics and imaging mass spectrometry in the age of artificial intelligence. . Annu. Rev. Biomed. Data Sci. 3::6187
    [Crossref] [Google Scholar]
  10. 10.
    Applewhite PB, Kaur-Sawhney R, Galston AW. 2000.. A role for spermidine in the bolting and flowering of Arabidopsis. . Physiol. Plant. 108:(3):31420
    [Crossref] [Google Scholar]
  11. 11.
    Balasundaram D, Tabor CW, Tabor H. 1991.. Spermidine or spermine is essential for the aerobic growth of Saccharomyces cerevisiae. . PNAS 88:(13):587276
    [Crossref] [Google Scholar]
  12. 12.
    Belda-Palazón B, Almendáriz C, Martí E, Carbonell J, Ferrando A. 2016.. Relevance of the axis spermidine/eIF5A for plant growth and development. . Front. Plant Sci. 7::245
    [Crossref] [Google Scholar]
  13. 13.
    Belda-Palazón B, Nohales MA, Rambla JL, Aceña JL, Delgado O, et al. 2014.. Biochemical quantitation of the eIF5A hypusination in Arabidopsis thaliana uncovers ABA-dependent regulation. . Front. Plant Sci. 5::202 13. Provided the first functional analysis of eIF5A hypusination in plants.
    [Google Scholar]
  14. 14.
    Belda-Palazón B, Ruiz L, Martí E, Tárraga S, Tiburcio AF, et al. 2012.. Aminopropyltransferases involved in polyamine biosynthesis localize preferentially in the nucleus of plant cells. . PLOS ONE 7:(10):e46907
    [Crossref] [Google Scholar]
  15. 15.
    Beninati S, Bergamini CM, Piacentini M. 2009.. An overview of the first 50 years of transglutaminase research. . Amino Acids 36:(4):59198
    [Crossref] [Google Scholar]
  16. 16.
    Borrell A, Culianez-Macia FA, Altabella T, Besford RT, Flores D, Tiburcio AF. 1995.. Arginine decarboxylase is localized in chloroplasts. . Plant Physiol. 109:(3):77176
    [Crossref] [Google Scholar]
  17. 17.
    Bortolotti C, Cordeiro A, Alcazar R, Borrell A, Culianez-Macia FA, et al. 2004.. Localization of arginine decarboxylase in tobacco plants. . Physiol. Plant. 120:(1):8492
    [Crossref] [Google Scholar]
  18. 18.
    Burkart GM, Brandizzi F. 2021.. A tour of TOR complex signaling in plants. . Trends Biochem. Sci. 46:(5):41728
    [Crossref] [Google Scholar]
  19. 19.
    Buskirk AR, Green R. 2017.. Ribosome pausing, arrest and rescue in bacteria and eukaryotes. . Philos. Trans. R. Soc. B 372:(1716):20160183
    [Crossref] [Google Scholar]
  20. 20.
    Cacciapuoti G, Porcelli M, Moretti MA, Sorrentino F, Concilio L, et al. 2007.. The first agmatine/cadaverine aminopropyl transferase: biochemical and structural characterization of an enzyme involved in polyamine biosynthesis in the hyperthermophilic archaeon Pyrococcus furiosus. . J. Bacteriol. 189:(16):605767
    [Crossref] [Google Scholar]
  21. 21.
    Cai G, Sobieszczuk-Nowicka E, Aloisi I, Fattorini L, Serafini-Fracassini D, Del Duca S. 2015.. Polyamines are common players in different facets of plant programmed cell death. . Amino Acids 47:(1):2744
    [Crossref] [Google Scholar]
  22. 22.
    Cai Q, Fukushima H, Yamamoto M, Ishii N, Sakamoto T, et al. 2016.. The SAC51 family plays a central role in thermospermine responses in Arabidopsis. . Plant Cell Physiol. 57:(8):158392
    [Crossref] [Google Scholar]
  23. 23.
    Carbonell J, Blázquez MA. 2009.. Regulatory mechanisms of polyamine biosynthesis in plants. . Genes Genom. 31::10718
    [Crossref] [Google Scholar]
  24. 24.
    Chang KS, Lee SH, Hwang SB, Park KY. 2000.. Characterization and translational regulation of the arginine decarboxylase gene in carnation (Dianthus caryophyllus L.). . Plant J. 24:(1):4556
    [Crossref] [Google Scholar]
  25. 25.
    Chávez-Martínez AI, Ortega-Amaro MA, Torres M, Serrano M, Jiménez-Bremont JF. 2020.. Arabidopsis adc-silenced line exhibits differential defense responses to Botrytis cinerea and Pseudomonas syringae infection. . Plant Physiol. Biochem. 156::494503
    [Crossref] [Google Scholar]
  26. 26.
    Clay NK, Nelson T. 2005.. Arabidopsis thickvein mutation affects vein thickness and organ vascularization, and resides in a provascular cell-specific spermine synthase involved in vein definition and in polar auxin transport. . Plant Physiol. 138:(2):76777
    [Crossref] [Google Scholar]
  27. 27.
    Cuevas JC, López-Cobollo R, Alcázar R, Zarza X, Koncz C, 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:(2):1094105
    [Crossref] [Google Scholar]
  28. 28.
    Dalton HL, Blomstedt CK, Neale AD, Gleadow R, Deboer KD, Hamill JD. 2016.. Effects of down-regulating ornithine decarboxylase upon putrescine-associated metabolism and growth in Nicotiana tabacum L. . J. Exp. Bot. 67:(11):336781
    [Crossref] [Google Scholar]
  29. 29.
    De Oliveira LF, Elbl P, Navarro BV, Macedo AF, dos Santos ALW, Floh EIS. 2017.. Elucidation of the polyamine biosynthesis pathway during Brazilian pine (Araucaria angustifolia) seed development. . Tree Physiol. 37:(1):11630
    [Crossref] [Google Scholar]
  30. 30.
    De Rybel B, Möller B, Yoshida S, Grabowicz I, Barbier de Reuille P, et al. 2013.. A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. . Dev. Cell 24:(4):42637
    [Crossref] [Google Scholar]
  31. 31.
    Deeb F, van der Weele CM, Wolniak SM. 2010.. Spermidine is a morphogenetic determinant for cell fate specification in the male gametophyte of the water fern Marsilea vestita. . Plant Cell 22:(11):367891
    [Crossref] [Google Scholar]
  32. 32.
    Del Duca S, Serafini-Fracassini D, Cai G. 2014.. Senescence and programmed cell death in plants: polyamine action mediated by transglutaminase. . Front. Plant Sci. 5::120
    [Crossref] [Google Scholar]
  33. 33.
    Delbecq P, Werner M, Feller A, Filipkowski RK, Messenguy F, Piérard A. 1994.. A segment of mRNA encoding the leader peptide of the CPA1 gene confers repression by arginine on a heterologous yeast gene transcript. . Mol. Cell. Biol. 14:(4):237890
    [Google Scholar]
  34. 34.
    Dever TE, Dinman JD, Green R. 2018.. Translation elongation and recoding in eukaryotes. . Cold Spring Harb. Perspect. Biol. 10:(8):a032649
    [Crossref] [Google Scholar]
  35. 35.
    Dever TE, Ivanov IP. 2018.. Roles of polyamines in translation. . J. Biol. Chem. 293::1871929
    [Crossref] [Google Scholar]
  36. 36.
    Dmochowska-Boguta M, Kloc Y, Orczyk W. 2021.. Polyamine oxidation is indispensable for wheat (Triticum aestivum L.) oxidative response and necrotic reactions during leaf rust (Puccinia triticina Eriks.) infection. . Plants 10:(12):2787
    [Crossref] [Google Scholar]
  37. 37.
    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::87243
    [Crossref] [Google Scholar]
  38. 38.
    Ebeed HT. 2022.. Genome-wide analysis of polyamine biosynthesis genes in wheat reveals gene expression specificity and involvement of STRE and MYB-elements in regulating polyamines under drought. . BMC Genom. 23:(1):734
    [Crossref] [Google Scholar]
  39. 39.
    Fang P, Wang Z, Sachs MS. 2000.. Evolutionarily conserved features of the arginine attenuator peptide provide the necessary requirements for its function in translational regulation. . J. Biol. Chem. 275:(35):2671019
    [Crossref] [Google Scholar]
  40. 40.
    Flores T, Todd CD, Tovar-Mendez A, Dhanoa PK, Correa-Aragunde N, et al. 2008.. Arginase-negative mutants of Arabidopsis exhibit increased nitric oxide signaling in root development. . Plant Physiol. 147:(4):193646
    [Crossref] [Google Scholar]
  41. 41.
    Foresi N, Caló G, Del Castello F, Nejamkin A, Salerno G, et al. 2022.. Arginine as the sole nitrogen source for Ostreococcus tauri growth: insights on nitric oxide synthase enzyme. . Front. Mar. Sci. 9::1064077
    [Crossref] [Google Scholar]
  42. 42.
    Fuell C, Elliott KA, Hanfrey CC, Franceschetti M, Michael AJ. 2010.. Polyamine biosynthetic diversity in plants and algae. . Plant Physiol. Biochem. 48:(7):51320
    [Crossref] [Google Scholar]
  43. 43.
    Ge C, Cui X, Wang Y, Hu Y, Fu Z, et al. 2006.. BUD2, encoding an S-adenosylmethionine decarboxylase, is required for Arabidopsis growth and development. . Cell Res. 16:(5):44656
    [Crossref] [Google Scholar]
  44. 44.
    Gemperlová L, Fischerová L, Cvikrová M, Malá J, Vondráková Z, et al. 2009.. Polyamine profiles and biosynthesis in somatic embryo development and comparison of germinating somatic and zygotic embryos of Norway spruce. . Tree Physiol. 29:(10):128798
    [Crossref] [Google Scholar]
  45. 45.
    Gerlin L, Baroukh C, Genin S. 2021.. Polyamines: double agents in disease and plant immunity. . Trends Plant Sci. 26:(10):106171
    [Crossref] [Google Scholar]
  46. 46.
    Gonzalez ME, Marco F, Minguet EG, Carrasco-Sorli P, Blázquez MA, et al. 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:(4):226677
    [Crossref] [Google Scholar]
  47. 47.
    Groppa MD, Benavides MP. 2008.. Polyamines and abiotic stress: recent advances. . Amino Acids 34:(1):3545
    [Crossref] [Google Scholar]
  48. 48.
    Guerrero-González ML, Ortega-Amaro MA, Juárez-Montiel M, Jiménez-Bremont JF. 2016.. Arabidopsis Polyamine oxidase-2 uORF is required for downstream translational regulation. . Plant Physiol. Biochem. 108::38190
    [Crossref] [Google Scholar]
  49. 49.
    Gupta K, Sengupta A, Chakraborty M, Gupta B. 2016.. Hydrogen peroxide and polyamines act as double edged swords in plant abiotic stress responses. . Front. Plant Sci. 7::1343
    [Google Scholar]
  50. 50.
    Hanfrey C, Elliott KA, Franceschetti M, Mayer MJ, Illingworth C, Michael AJ. 2005.. A dual upstream open reading frame-based autoregulatory circuit controlling polyamine-responsive translation. . J. Biol. Chem. 280:(47):3922937
    [Crossref] [Google Scholar]
  51. 51.
    Hanfrey C, Franceschetti M, Mayer MJ, Illingworth C, Michael AJ. 2002.. Abrogation of upstream open reading frame-mediated translational control of a plant S-adenosylmethionine decarboxylase results in polyamine disruption and growth perturbations. . J. Biol. Chem. 277:(46):4413139
    [Crossref] [Google Scholar]
  52. 52.
    Hanfrey C, Sommer S, Mayer MJ, Burtin D, Michael AJ. 2001.. Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. . Plant J. 27:(6):55160
    [Crossref] [Google Scholar]
  53. 53.
    Hanzawa Y, Takahashi T, Komeda Y. 1997.. ACL5: an Arabidopsis gene required for internodal elongation after flowering. . Plant J. 12:(4):86374
    [Crossref] [Google Scholar]
  54. 54.
    Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, et al. 2000.. ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. . EMBO J. 19:(16):424856
    [Crossref] [Google Scholar]
  55. 55.
    Horyn O, Luhovyy B, Lazarow A, Daikhin Y, Nissim I, et al. 2005.. Biosynthesis of agmatine in isolated mitochondria and perfused rat liver: studies with 15N-labelled arginine. . Biochem. J. 388:(Part 2):41925
    [Crossref] [Google Scholar]
  56. 56.
    Hu W-W, Gong H, Pua EC. 2005.. The pivotal roles of the plant S-adenosylmethionine decarboxylase 5′ untranslated leader sequence in regulation of gene expression at the transcriptional and posttranscriptional levels. . Plant Physiol. 138:(1):27686
    [Crossref] [Google Scholar]
  57. 57.
    Illingworth C, Mayer MJ, Elliott K, Hanfrey C, Walton NJ, Michael AJ. 2003.. The diverse bacterial origins of the Arabidopsis polyamine biosynthetic pathway. . FEBS Lett. 549:(1–3):2630
    [Crossref] [Google Scholar]
  58. 58.
    Illingworth C, Michael AJ. 2012.. Plant ornithine decarboxylase is not post-transcriptionally feedback regulated by polyamines but can interact with a cytosolic ribosomal protein S15 polypeptide. . Amino Acids 42:(2–3):51927
    [Crossref] [Google Scholar]
  59. 59.
    Imai A, Akiyama T, Kato T, Sato S, Tabata S, et al. 2004.. Spermine is not essential for survival of Arabidopsis. . FEBS Lett. 556:(1–3):14852
    [Crossref] [Google Scholar]
  60. 60.
    Imai A, Hanzawa Y, Komura M, Yamamoto KT, Komeda Y, Takahashi T. 2006.. The dwarf phenotype of the Arabidopsis acl5 mutant is suppressed by a mutation in an upstream ORF of a bHLH gene. . Development 133:(18):357585 60. Demonstrated for the first time that thermospermine regulates uORF-mediated translation of SACL transcripts.
    [Crossref] [Google Scholar]
  61. 61.
    Imai A, Komura M, Kawano E, Kuwashiro Y, Takahashi T. 2008.. A semi-dominant mutation in the ribosomal protein L10 gene suppresses the dwarf phenotype of the acl5 mutant in Arabidopsis thaliana. . Plant J. 56:(6):88190
    [Crossref] [Google Scholar]
  62. 62.
    Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, et al. 2004.. Spermidine synthase genes are essential for survival of Arabidopsis. . Plant Physiol. 135:(3):156573
    [Crossref] [Google Scholar]
  63. 63.
    Iyo AH, Zhu MY, Ordway GA, Regunathan S. 2006.. Expression of arginine decarboxylase in brain regions and neuronal cells. . J. Neurochem. 96:(4):104250
    [Crossref] [Google Scholar]
  64. 64.
    Jasso-Robles FI, Gonzalez ME, Pieckenstain FL, Ramírez-García JM, Guerrero-González ML, et al. 2020.. Decrease of Arabidopsis PAO activity entails increased RBOH activity, ROS content and altered responses to Pseudomonas. . Plant Sci. 292::110372
    [Crossref] [Google Scholar]
  65. 65.
    Kakehi J, Kawano E, Yoshimoto K, Cai Q, Imai A, Takahashi T. 2015.. Mutations in ribosomal proteins, RPL4 and RACK1, suppress the phenotype of a thermospermine-deficient mutant of Arabidopsis thaliana. . PLOS ONE 10:(1):e0117309
    [Crossref] [Google Scholar]
  66. 66.
    Kakehi JI, Kuwashiro Y, Niitsu M, Takahashi T. 2008.. Thermospermine is required for stem elongation in Arabidopsis thaliana. . Plant Cell Physiol. 49::134249
    [Crossref] [Google Scholar]
  67. 67.
    Kamada-Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M. 2008.. A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. . Plant Cell Physiol. 49:(9):127282
    [Crossref] [Google Scholar]
  68. 68.
    Karousis ED, Mühlemann O. 2019.. Nonsense-mediated mRNA decay begins where translation ends. . Cold Spring Harb. Perspect. Biol. 11:(2):a032862
    [Crossref] [Google Scholar]
  69. 69.
    Katayama H, Iwamoto K, Kariya Y, Asakawa T, Kan T, et al. 2015.. A negative feedback loop controlling bHLH complexes is involved in vascular cell division and differentiation in the root apical meristem. . Curr. Biol. 25:(23):314450 69. Describes the mechanism by which thermospermine regulates vascular cell divisions (see also Reference 141).
    [Crossref] [Google Scholar]
  70. 70.
    Kaur H, Heinzel N, Schöttner M, Baldwin IT, Gális I. 2010.. R2R3-NaMYB8 regulates the accumulation of phenylpropanoid-polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. . Plant Physiol. 152:(3):173147
    [Crossref] [Google Scholar]
  71. 71.
    Kaur-Sawhney R, Flores HE, Galston AW. 1981.. Polyamine oxidase in oat leaves: a cell wall-localized enzyme. . Plant Physiol. 68::49498
    [Crossref] [Google Scholar]
  72. 72.
    Kim DW, Watanabe K, Murayama C, Izawa S, Niitsu M, et al. 2014.. Polyamine oxidase5 regulates Arabidopsis growth through thermospermine oxidase activity. . Plant Physiol. 165:(4):157590
    [Crossref] [Google Scholar]
  73. 73.
    Klink VP, Wolniak SM. 2001.. Centrin is necessary for the formation of the motile apparatus in spermatids of Marsilea. . Mol. Biol. Cell 12:(3):76176
    [Crossref] [Google Scholar]
  74. 74.
    Korolev S, Ikeguchi Y, Skarina T, Beasley S, Arrowsmith C, et al. 2002.. The crystal structure of spermidine synthase with a multisubstrate adduct inhibitor. . Nat. Struct. Biol. 9:(1):2731
    [Crossref] [Google Scholar]
  75. 75.
    Kozak M. 1999.. Initiation of translation in prokaryotes and eukaryotes. . Gene 234:(2):187208
    [Crossref] [Google Scholar]
  76. 76.
    Kuroha K, Akamatsu M, Dimitrova L, Ito T, Kato Y, et al. 2010.. Receptor for activated C kinase 1 stimulates nascent polypeptide-dependent translation arrest. . EMBO Rep. 11:(12):95661
    [Crossref] [Google Scholar]
  77. 77.
    Lightfoot HL, Hall J. 2014.. Endogenous polyamine function—the RNA perspective. . Nucleic Acids Res. 42:(18):1127590
    [Crossref] [Google Scholar]
  78. 78.
    Liu C, Atanasov KE, Arafaty N, Murillo E, Tiburcio AF, et al. 2020.. Putrescine elicits ROS-dependent activation of the salicylic acid pathway in Arabidopsis thaliana. . Plant Cell Environ. 43:(11):275568
    [Crossref] [Google Scholar]
  79. 79.
    Liu C, Atanasov KE, Tiburcio AF, Alcázar R. 2019.. The polyamine putrescine contributes to H2O2 and RbohD/F-dependent positive feedback loop in Arabidopsis PAMP-triggered immunity. . Front. Plant Sci. 10::894
    [Crossref] [Google Scholar]
  80. 80.
    Liu M, Chen J, Guo Z, Lu S. 2017.. Differential responses of polyamines and antioxidants to drought in a centipedegrass mutant in comparison to its wild type plants. . Front. Plant Sci. 8::792
    [Crossref] [Google Scholar]
  81. 81.
    Lv Y, Shao G, Jiao G, Sheng Z, Xie L, et al. 2021.. Targeted mutagenesis of POLYAMINE OXIDASE 5 that negatively regulates mesocotyl elongation enables the generation of direct-seeding rice with improved grain yield. . Mol. Plant 14:(2):34451
    [Crossref] [Google Scholar]
  82. 82.
    Majumdar R, Minocha R, Lebar MD, Rajasekaran K, Long S, et al. 2019.. Contribution of maize polyamine and amino acid metabolism toward resistance against Aspergillus flavus infection and aflatoxin production. . Front. Plant Sci. 10::692
    [Crossref] [Google Scholar]
  83. 83.
    Marco F, Alcázar R, Tiburcio AF, Carrasco P. 2011.. Interactions between polyamines and abiotic stress pathway responses unraveled by transcriptome analysis of polyamine overproducers. . OMICS 15:(11):77581
    [Crossref] [Google Scholar]
  84. 84.
    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
    [Crossref] [Google Scholar]
  85. 85.
    Marco F, Busó E, Lafuente T, Carrasco P. 2019.. Spermine confers stress resilience by modulating abscisic acid biosynthesis and stress responses in Arabidopsis plants. . Front. Plant Sci. 10::972
    [Crossref] [Google Scholar]
  86. 86.
    Marina M, Sirera FV, Rambla JL, Gonzalez ME, Blázquez MA, et al. 2013.. Thermospermine catabolism increases Arabidopsis thaliana resistance to Pseudomonas viridiflava. . J. Exp. Bot. 64:(5):1393402 86. Provides evidence that polyamine catabolism is necessary to increase pathogen resistance.
    [Crossref] [Google Scholar]
  87. 87.
    Meinke DW. 2020.. Genome-wide identification of EMBRYO-DEFECTIVE (EMB) genes required for growth and development in Arabidopsis. . New Phytol. 226:(2):30625
    [Crossref] [Google Scholar]
  88. 88.
    Michael AJ. 2017.. Evolution of biosynthetic diversity. . Biochem. J. 474:(14):227799
    [Crossref] [Google Scholar]
  89. 89.
    Michael AJ. 2016.. Polyamines in eukaryotes, bacteria, and archaea. . J. Biol. Chem. 291:(29):14896903
    [Crossref] [Google Scholar]
  90. 90.
    Milhinhos A, Bollhöner B, Blazquez MA, Novák O, Miguel CM, Tuominen H. 2020.. ACAULIS5 is required for cytokinin accumulation and function during secondary growth of Populus trees. . Front. Plant Sci. 11::601858
    [Crossref] [Google Scholar]
  91. 91.
    Miller-Fleming L, Olin-Sandoval V, Campbell K, Ralser M. 2015.. Remaining mysteries of molecular biology: the role of polyamines in the cell. . J. Mol. Biol. 427:(21):3389406
    [Crossref] [Google Scholar]
  92. 92.
    Minguet EG, Vera-Sirera F, Marina A, Carbonell J, Blázquez MA. 2008.. Evolutionary diversification in polyamine biosynthesis. . Mol. Biol. Evol. 25:(10):211928
    [Crossref] [Google Scholar]
  93. 93.
    Minocha SC, Minocha R. 1995.. Role of polyamines in somatic embryogenesis. . In Somatic Embryogenesis and Synthetic Seed, ed. YPS Bajaj , pp. 5370. Berlin:: Springer
    [Google Scholar]
  94. 94.
    Mitsuya Y, Takahashi Y, Berberich T, Miyazaki A, Matsumura H, et al. 2009.. Spermine signaling plays a significant role in the defense response of Arabidopsis thaliana to cucumber mosaic virus. . J. Plant Physiol. 166:(6):62643
    [Crossref] [Google Scholar]
  95. 95.
    Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, et al. 2008.. Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. . Plant Cell 20:(6):170824
    [Crossref] [Google Scholar]
  96. 96.
    Muñiz L, Minguet EG, Singh SK, Pesquet E, Vera-Sirera F, et al. 2008.. ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death. . Development 135:(15):257382
    [Crossref] [Google Scholar]
  97. 97.
    Nambeesan SU, Mattoo AK, Handa AK. 2019.. Nexus between spermidine and floral organ identity and fruit/seed set in tomato. . Front. Plant Sci. 10::1033
    [Crossref] [Google Scholar]
  98. 98.
    Nishimura K, Murozumi K, Shirahata A, Park MH, Kashiwagi K, Igarashi K. 2005.. Independent roles of eIF5A and polyamines in cell proliferation. . Biochem. J. 385:(Part 3):77985
    [Crossref] [Google Scholar]
  99. 99.
    Ohashi-Ito K, Bergmann DC. 2007.. Regulation of the Arabidopsis root vascular initial population by LONESOME HIGHWAY. . Development 134:(16):295968
    [Crossref] [Google Scholar]
  100. 100.
    Ohashi-Ito K, Oguchi M, Kojima M, Sakakibara H, Fukuda H. 2013.. Auxin-associated initiation of vascular cell differentiation by LONESOME HIGHWAY. . Development 140:(4):76569
    [Crossref] [Google Scholar]
  101. 101.
    Onkokesung N, Gaquerel E, Kotkar H, Kaur H, Baldwin IT, Galis I. 2012.. MYB8 controls inducible phenolamide levels by activating three novel hydroxycinnamoyl-coenzyme A:polyamine transferases in Nicotiana attenuata. . Plant Physiol. 158:(1):389407
    [Crossref] [Google Scholar]
  102. 102.
    Pagano A, Macovei A, Balestrazzi A. 2023.. Molecular dynamics of seed priming at the crossroads between basic and applied research. . Plant Cell Rep. 42:(4):65788
    [Crossref] [Google Scholar]
  103. 103.
    Panicot M, Minguet EG, Ferrando A, Alcázar R, Blázquez MA, et al. 2002.. A polyamine metabolon involving aminopropyl transferase complexes in Arabidopsis. . Plant Cell 14:(10):253951 103. Proposed for the first time that spermidine and spermidine production occur in a multienzyme complex.
    [Crossref] [Google Scholar]
  104. 104.
    Park MH. 2006.. The post-translational synthesis of a polyamine-derived amino acid, hypusine, in the eukaryotic translation initiation factor 5A (eIF5A). . J. Biochem. 139:(2):16169
    [Crossref] [Google Scholar]
  105. 105.
    Pegg AE. 2016.. Functions of polyamines in mammals. . J. Biol. Chem. 291:(29):1490412
    [Crossref] [Google Scholar]
  106. 106.
    Pelechano V, Alepuz P. 2017.. eIF5A facilitates translation termination globally and promotes the elongation of many non polyproline-specific tripeptide sequences. . Nucleic Acids Res. 45:(12):732638
    [Crossref] [Google Scholar]
  107. 107.
    Perez-Amador MA, Leon J, Green PJ, Carbonell J. 2002.. Induction of the arginine decarboxylase ADC2 gene provides evidence for the involvement of polyamines in the wound response in Arabidopsis. . Plant Physiol. 130:(3):145463
    [Crossref] [Google Scholar]
  108. 108.
    Poidevin L, Unal D, Belda-Palazón B, Ferrando A. 2019.. Polyamines as quality control metabolites operating at the post-transcriptional level. . Plants 8:(4):109
    [Crossref] [Google Scholar]
  109. 109.
    Pottosin I, Velarde-Buendía AM, Bose J, Zepeda-Jazo I, Shabala S, Dobrovinskaya O. 2014.. Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. . J. Exp. Bot. 65:(5):127183
    [Crossref] [Google Scholar]
  110. 110.
    Rastogi R, Sawhney VK. 1990.. Polyamines and flower development in the male sterile stamenless-2 mutant of tomato (Lycopersicon esculentum Mill.): II. Effects of polyamines and their biosynthetic inhibitors on the development of normal and mutant floral buds cultured in vitro. . Plant Physiol. 93:(2):44652
    [Crossref] [Google Scholar]
  111. 111.
    Rayson S, Arciga-Reyes L, Wootton L, de Torres Zabala M, Truman W, et al. 2012.. A role for nonsense-mediated mRNA decay in plants: Pathogen responses are induced in Arabidopsis thaliana NMD mutants. . PLOS ONE 7:(2):e31917
    [Crossref] [Google Scholar]
  112. 112.
    Roje S. 2006.. S-Adenosyl-l-methionine: beyond the universal methyl group donor. . Phytochemistry 67:(15):168698
    [Crossref] [Google Scholar]
  113. 113.
    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:(4):83139
    [Crossref] [Google Scholar]
  114. 114.
    Roy M, Wu R. 2001.. Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. . Plant Sci. 160:(5):86975
    [Crossref] [Google Scholar]
  115. 115.
    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:(3):595605
    [Crossref] [Google Scholar]
  116. 116.
    Sagor GHM, Zhang S, Kojima S, Simm S, Berberich T, Kusano T. 2016.. Reducing cytoplasmic polyamine oxidase activity in Arabidopsis increases salt and drought tolerance by reducing reactive oxygen species production and increasing defense gene expression. . Front. Plant Sci. 7::214
    [Crossref] [Google Scholar]
  117. 117.
    Salazar-Díaz K, Dong Y, Papdi C, Ferruzca-Rubio EM, Olea-Badillo G, et al. 2021.. TOR senses and regulates spermidine metabolism during seedling establishment and growth in maize and Arabidopsis. . iScience 24:(11):103260
    [Crossref] [Google Scholar]
  118. 118.
    Salvi D, Tavladoraki P. 2020.. The tree of life of polyamine oxidases. . Sci. Rep. 10:(1):17858
    [Crossref] [Google Scholar]
  119. 119.
    Sánchez-Rangel D, Chávez-Martínez AI, Rodríguez-Hernández AA, Maruri-López I, Urano K, et al. 2016.. Simultaneous silencing of two arginine decarboxylase genes alters development in Arabidopsis. . Front. Plant Sci. 7::300
    [Crossref] [Google Scholar]
  120. 120.
    Sekula B, Dauter Z. 2018.. Crystal structure of thermospermine synthase from Medicago truncatula and substrate discriminatory features of plant aminopropyltransferases. . Biochem. J. 475:(4):787802
    [Crossref] [Google Scholar]
  121. 121.
    Sengupta J, Nilsson J, Gursky R, Spahn CMT, Nissen P, Frank J. 2004.. Identification of the versatile scaffold protein RACK1 on the eukaryotic ribosome by cryo-EM. . Nat. Struct. Mol. Biol. 11:(10):95762
    [Crossref] [Google Scholar]
  122. 122.
    Sequera-Mutiozabal MI, Erban A, Kopka J, Atanasov KE, Bastida J, et al. 2016.. Global metabolic profiling of Arabidopsis Polyamine Oxidase 4 (AtPAO4) loss-of-function mutants exhibiting delayed dark-induced senescence. . Front. Plant Sci. 7::173
    [Crossref] [Google Scholar]
  123. 123.
    Serafini-Fracassini D, Di Sandro A, Del Duca S. 2010.. Spermine delays leaf senescence in Lactuca sativa and prevents the decay of chloroplast photosystems. . Plant Physiol. Biochem. 48:(7):60211
    [Crossref] [Google Scholar]
  124. 124.
    Shi J, Fu X-Z, Peng T, Huang X-S, Fan Q-J, Liu J-H. 2010.. Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. . Tree Physiol. 30:(7):91422
    [Crossref] [Google Scholar]
  125. 125.
    Shu S, Yuan L-Y, Guo S-R, Sun J, Yuan Y-H. 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::20916
    [Crossref] [Google Scholar]
  126. 126.
    Siddappa S, Marathe GK. 2020.. What we know about plant arginases?. Plant Physiol. Biochem. 156::60010
    [Crossref] [Google Scholar]
  127. 127.
    Sobieszczuk-Nowicka E. 2017.. Polyamine catabolism adds fuel to leaf senescence. . Amino Acids 49:(1):4956
    [Crossref] [Google Scholar]
  128. 128.
    Solé-Gil A, Hernández-García J, López-Gresa MP, Blázquez MA, Agustí J. 2019.. Conservation of thermospermine synthase activity in vascular and non-vascular plants. . Front. Plant Sci. 10::663
    [Crossref] [Google Scholar]
  129. 129.
    Soyka S, Heyer AG. 1999.. Arabidopsis knockout mutation of ADC2 gene reveals inducibility by osmotic stress. . FEBS Lett. 458:(2):21923
    [Crossref] [Google Scholar]
  130. 130.
    Tanou G, Ziogas V, Belghazi M, Christou A, Filippou P, et al. 2014.. Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress. . Plant Cell Environ. 37:(4):86485
    [Crossref] [Google Scholar]
  131. 131.
    Tao Y, Wang J, Miao J, Chen J, Wu S, et al. 2018.. The spermine synthase OsSPMS1 regulates seed germination, grain size, and yield. . Plant Physiol. 178:(4):152236
    [Crossref] [Google Scholar]
  132. 132.
    Tapia G, González M, Burgos J, Vega MV, Méndez J, Inostroza L. 2021.. Early transcriptional responses in Solanum peruvianum and Solanum lycopersicum account for different acclimation processes during water scarcity events. . Sci. Rep. 11:(1):15961
    [Crossref] [Google Scholar]
  133. 133.
    Tassoni A, van Buuren M, Franceschetti M, Fornalè S, Bagni N. 2000.. Polyamine content and metabolism in Arabidopsis thaliana and effect of spermidine on plant development. . Plant Physiol. Biochem. 38:(5):38393
    [Crossref] [Google Scholar]
  134. 134.
    Teuber M, Azemi ME, Namjoyan F, Meier AC, Wodak A, et al. 2007.. Putrescine N-methyltransferases—a structure-function analysis. . Plant Mol. Biol. 63:(6):787801
    [Crossref] [Google Scholar]
  135. 135.
    Thoma I, Loeffler C, Sinha AK, Gupta M, Krischke M, et al. 2003.. Cyclopentenone isoprostanes induced by reactive oxygen species trigger defense gene activation and phytoalexin accumulation in plants. . Plant J. 34:(3):36375
    [Crossref] [Google Scholar]
  136. 136.
    Tiburcio AF, Alcázar R. 2018.. Potential applications of polyamines in agriculture and plant biotechnology. . Methods Mol. Biol. 1694::489508
    [Crossref] [Google Scholar]
  137. 137.
    Tiburcio AF, Altabella T, Bitrian M, Alcázar R. 2014.. The roles of polyamines during the lifespan of plants: from development to stress. . Planta 240:(1):118
    [Crossref] [Google Scholar]
  138. 138.
    Uchiyama-Kadokura N, Murakami K, Takemoto M, Koyanagi N, Murota K, et al. 2014.. Polyamine-responsive ribosomal arrest at the stop codon of an upstream open reading frame of the AdoMetDC1 gene triggers nonsense-mediated mRNA decay in Arabidopsis thaliana. . Plant Cell Physiol. 55:(9):155667
    [Crossref] [Google Scholar]
  139. 139.
    Urano K, Hobo T, Shinozaki K. 2005.. Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. . FEBS Lett. 579:(6):155764
    [Crossref] [Google Scholar]
  140. 140.
    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:(2):36975
    [Crossref] [Google Scholar]
  141. 141.
    Vera-Sirera F, De Rybel B, Úrbez C, Kouklas E, Pesquera M, et al. 2015.. A bHLH-based feedback loop restricts vascular cell proliferation in plants. . Dev. Cell 35:(4):43243 141. Describes the mechanism by which thermospermine regulates vascular cell divisions (see also Reference 69).
    [Crossref] [Google Scholar]
  142. 142.
    Vera-Sirera F, Minguet EG, Singh SK, Ljung K, Tuominen H, et al. 2010.. Role of polyamines in plant vascular development. . Plant Physiol. Biochem. 48:(7):53439
    [Crossref] [Google Scholar]
  143. 143.
    Vondráková Z, Eliášová K, Vágner M, Martincová O, Cvikrová M. 2015.. Exogenous putrescine affects endogenous polyamine levels and the development of Picea abies somatic embryos. . Plant Growth Regul. 75:(2):40514
    [Crossref] [Google Scholar]
  144. 144.
    Vuosku J, Karppinen K, Muilu-Mäkelä R, Kusano T, Sagor GHM, et al. 2018.. Scots pine aminopropyltransferases shed new light on evolution of the polyamine biosynthesis pathway in seed plants. . Ann. Bot. 121:(6):124356
    [Crossref] [Google Scholar]
  145. 145.
    Walden R, Cordeiro A, Tiburcio AF. 1997.. Polyamines: small molecules triggering pathways in plant growth and development. . Plant Physiol. 113:(4):100913
    [Crossref] [Google Scholar]
  146. 146.
    Walters DR. 2003.. Polyamines and plant disease. . Phytochemistry 64:(1):97107
    [Crossref] [Google Scholar]
  147. 147.
    Wang W, Paschalidis K, Feng JC, Song J, Liu JH. 2019.. Polyamine catabolism in plants: a universal process with diverse functions. . Front. Plant Sci. 10::561
    [Crossref] [Google Scholar]
  148. 148.
    Watanabe SI, Kusama-Eguchi K, Kobayashi H, Igarashi K. 1991.. Estimation of polyamine binding to macromolecules and ATP in bovine lymphocytes and rat liver. . J. Biol. Chem. 266:(31):208039
    [Crossref] [Google Scholar]
  149. 149.
    Wimalasekera R, Schaarschmidt F, Angelini R, Cona A, Tavladoraki P, Scherer GFE. 2015.. POLYAMINE OXIDASE2 of Arabidopsis contributes to ABA mediated plant developmental processes. . Plant Physiol. Biochem. 96::23140
    [Crossref] [Google Scholar]
  150. 150.
    Wu D, von Roepenack-Lahaye E, Buntru M, de Lange O, Schandry N, et al. 2019.. A plant pathogen type III effector protein subverts translational regulation to boost host polyamine levels. . Cell Host Microbe 26:(5):638649.e5 150. Describes how a bacterium alters endogenous plant polyamine levels to inhibit other bacterial competitors.
    [Crossref] [Google Scholar]
  151. 151.
    Wu H, Fu B, Sun P, Xiao C, Liu J-H. 2016.. A NAC transcription factor represses putrescine biosynthesis and affects drought tolerance. . Plant Physiol. 172:(3):153247
    [Crossref] [Google Scholar]
  152. 152.
    Yadav JS, Rajam MV. 1997.. Spatial distribution of free and conjugated polyamines in leaves of Solanum melongena L. associated with differential morphogenetic capacity: efficient somatic embryogenesis with putrescine. . J. Exp. Bot. 48:(8):153745
    [Crossref] [Google Scholar]
  153. 153.
    Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, et al. 2006.. The polyamine spermine protects against high salt stress in Arabidopsis thaliana. . FEBS Lett. 580:(30):678388 153. Provided the first genetic evidence that spermine is required for complete protection against abiotic stress.
    [Crossref] [Google Scholar]
  154. 154.
    Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, et al. 2007.. A protective role for the polyamine spermine against drought stress in Arabidopsis. . Biochem. Biophys. Res. Commun. 352:(2):48690
    [Crossref] [Google Scholar]
  155. 155.
    Yamamoto M, Takahashi T. 2017.. Thermospermine enhances translation of SAC51 and SACL1 in Arabidopsis. . Plant Signal. Behav. 12:(1):e1276685
    [Crossref] [Google Scholar]
  156. 156.
    Zarza X, Atanasov KE, Marco F, Arbona V, Carrasco P, et al. 2017.. Polyamine oxidase 5 loss-of-function mutations in Arabidopsis thaliana trigger metabolic and transcriptional reprogramming and promote salt stress tolerance. . Plant Cell Environ. 40:(4):52742
    [Crossref] [Google Scholar]
  157. 157.
    Zeiss DR, Piater LA, Dubery IA. 2021.. Hydroxycinnamate amides: intriguing conjugates of plant protective metabolites. . Trends Plant Sci. 26:(2):18495
    [Crossref] [Google Scholar]
  158. 158.
    Zhang C, Atanasov KE, Alcázar R. 2023.. Spermine inhibits PAMP-induced ROS and Ca2+ burst and reshapes the transcriptional landscape of PAMP-triggered immunity in Arabidopsis. . J. Exp. Bot. 74:(1):42742
    [Crossref] [Google Scholar]
  159. 159.
    Zhang Q, Wang M, Hu J, Wang W, Fu X, Liu J-H. 2015.. PtrABF of Poncirus trifoliata functions in dehydration tolerance by reducing stomatal density and maintaining reactive oxygen species homeostasis. . J. Exp. Bot. 66:(19):591127
    [Crossref] [Google Scholar]
  160. 160.
    Zhu MD, Zhang M, Gao DJ, Zhou K, Tang SJ, et al. 2020.. Rice OsHSFA3 gene improves drought tolerance by modulating polyamine biosynthesis depending on abscisic acid and ROS levels. . Int. J. Mol. Sci. 21:(5):1857
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-arplant-070623-110056
Loading
/content/journals/10.1146/annurev-arplant-070623-110056
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error