Polyamines pp 25-35 | Cite as

Molecules for Sensing Polyamines and Transducing Their Action in Plants

  • Tomonobu KusanoEmail author
  • G. H. M. Sagor
  • Thomas Berberich
Part of the Methods in Molecular Biology book series (MIMB, volume 1694)


Polyamines play important roles in growth, development, and adaptive responses to various stresses. In the past two decades, progress in plant polyamine research has accelerated, and the key molecules and components involved in many biological events have been identified. Recently, polyamine sensors used to detect polyamine-enriched foods and polyamines derived from degrading flesh were identified in fly and zebrafish, respectively. Work has begun to identify such molecules in plants as well. Here, we summarize the current knowledge about polyamines in plants. Furthermore, we discuss the roles of key molecules, such as calcium ions, reactive oxygen species, nitric oxide, γ-aminobutyric acid, polyamine transporters, and the mitogen-activated protein kinase cascade, from the viewpoint of polyamine action.

Key words

Calcium ion Hydrogen peroxide Mitogen-activated protein kinase cascade Nitric oxide Polyamine sensor Reactive oxygen species 



This work was financially supported by JSPS KAKENHI (no. 15K14705) to T.K.


  1. 1.
    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 427:3389–3406CrossRefPubMedGoogle Scholar
  2. 2.
    Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381CrossRefPubMedGoogle Scholar
  3. 3.
    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 231:1237–1249CrossRefPubMedGoogle Scholar
  4. 4.
    Handa AK, Mattoo AK (2010) Differential and functional interactions emphasize the multiple roles of polyamines in plants. Plant Physiol Biochem 48:540–546CrossRefGoogle Scholar
  5. 5.
    Tiburcio AF, Altabella T, Bitrian M, Alcazar R (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 240:1–18CrossRefGoogle Scholar
  6. 6.
    Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Front Plant Sci 5:175CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Pal M, Szalai G, Janda T (2015) Speculation: polyamines are important in abiotic stress signaling. Plant Sci 237:16–23CrossRefPubMedGoogle Scholar
  8. 8.
    Oshima T (1979) A new polyamine, thermospermine, 1,12-diamino-4,8-diazadodecane, from an extreme thermophile. J Biol Chem 254:8720–8722PubMedGoogle Scholar
  9. 9.
    Knott JM, Römer P, Sumper M (2007) Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett 581:3081–3086CrossRefPubMedGoogle Scholar
  10. 10.
    Takano A, Kakehi J-I, Takahashi T (2012) Thermospermine is not a minor polyamine in the plant kingdom. Plant Cell Physiol 53:606–616CrossRefPubMedGoogle Scholar
  11. 11.
    Bunsupa S, Katayama K, Ikeura E, Oikawa A, Toyooka K, Saito K, Yamazaki M (2012) Lysine decarboxylase catalyzes the first step of quinolizidine alkaloid biosynthesis and coevolved with alkaloid production in leguminosae. Plant Cell 24:1202–1216CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Strohm AK, Vaughn LM, Masson PH (2015) Natural variation in the expression of organic cation transporter 1 affects root length responses to cadaverine in Arabidopsis. J Exp Bot 66:853–862CrossRefPubMedGoogle Scholar
  13. 13.
    Jancewicz AL, Gibbs NM, Masson PH (2016) Cadaverine’s functional role in plant development and environmental response. Front Plant Sci 7:870CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Fuell C, Elliott KA, Hanfrey CC, Franceschetti M, Michael AJ (2010) Polyamine biosynthetic diversity in plants and algae. Plant Physiol Biochem 48:513–520CrossRefPubMedGoogle Scholar
  15. 15.
    Cona A, Rea G, Angelini R, Federice R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11:1360–1385CrossRefGoogle Scholar
  16. 16.
    Rea G, Metoui O, Infantino A, Federico R, Angelini R (2002) Copper amine oxidase expression in defense responses to wounding and Ascochyta rabiei invasion. Plant Physiol 128:865–875CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Planas-Portell J, Gallart M, Tiburcio AF, Altabella T (2013) Copper-containing amine oxidases contribute to terminal polyamine oxidation in peroxisomes and apoplast of Arabidopsis thaliana. BMC Plant Biol 13:109CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Angelini R, Cona A, Federico R, Fincato P, Tavladoraki P, Tisi A (2010) Plant amine oxidases ‘on the move’: an update. Plant Physiol Biochem 48:560–564CrossRefGoogle Scholar
  19. 19.
    Kusano T, Kim DW, Liu T, Berberich T (2015) Polyamine catabolism in plants. In: Kusano T, Suzuki H (eds) Polyamine: a universal molecular nexus for growth, survival and specialised metabolism. Springer, Tokyo, pp 77–88Google Scholar
  20. 20.
    Tavladoraki P, Cona A, Angelini R (2016) Copper-containing amine oxidases and FAD-dependent polyamine oxidases are key players in plant tissue differentiation and organ development. Front Plant Sci 7:824CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Igarashi K, Kashiwagi K (2010) Characteristics of cellular polyamine transport in prokaryotes and eukaryotes. Plant Physiol Biochem 48:506–512CrossRefPubMedGoogle Scholar
  22. 22.
    Fujita M, Fujita Y, Iuchi S, Yamada K, Kobayashi Y, Urano K, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2012) Natural variation in a polyamine transporter determines paraquat tolerance in Arabidopsis. Proc Natl Acad Sci U S A 109:6343–6347CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Mulangi V, Phuntumart V, Aouida M, Ramotar D, Morris P (2012) Functional analysis of OsPUT1, a rice polyamine uptake transporter. Planta 235:1–11CrossRefPubMedGoogle Scholar
  24. 24.
    Fujita M, Shinozaki K (2014) Identification of polyamine transporters in plants: paraquat transport provides crucial clues. Plant Cell Physiol 55:855–861CrossRefPubMedGoogle Scholar
  25. 25.
    Pottosin I, Shabala S (2014) Polyamines control of cation transport across plant membrane: implications for ion homeostasis and abiotic stress signaling. Front Plant Sci 5:154CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Pottosin I, Velarde-Buendia 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 65:1271–1283CrossRefPubMedGoogle Scholar
  27. 27.
    Kahara C (2009) Antizyme and antizyme inhibitor, a regulatory tango. Cell Mol Life Sci 66:2479–2488CrossRefGoogle Scholar
  28. 28.
    Murai N (2015) Antizyme. In: Kusano T, Suzuki H (eds) Polyamines: a universal molecular nexus for growth, survival, and specialized metabolism. Springer, Tokyo, pp 91–99Google Scholar
  29. 29.
    Ruan H, Shantz LM, Pegg AE, Morris DR (1996) The upstream open reading frame of the mRNA encoding S-adenosylmethionine decarboxylase is a polyamine-responsive translational control element. J Biol Chem 271:29576–29582CrossRefPubMedGoogle Scholar
  30. 30.
    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 27:551–560CrossRefPubMedGoogle Scholar
  31. 31.
    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 280:39229–39237CrossRefPubMedGoogle Scholar
  32. 32.
    Hussain A, Saraiva LR, Ferrero DM, Ahuja G, Krishna VS, Liberles SD, Korsching SI (2013) High-affinity olfactory receptor for the death-associated odor cadaverine. Proc Natl Acad Sci U S A 110:19579–19584CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Hussain A, Zhang M, Ucpunar HK, Svensson T, Quillery E, Gompel N, Ignell R, Kadow G (2016) Ionotropic chemosensory receptors mediate the taste and smell of polyamines. PLoS Biol 14:e1002454CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Tong W, Imai A, Tabata R, Shigenobu S, Yamaguchi K, Yamada M, Hasebe M, Sawa S, Motose H, Takahashi T (2016) Polyamine resistance is increased by mutants in a nitrate transporter gene NRT1.3 (AtNPF6.4) in Arabidopsis thaliana. Front Plant Sci 7:834PubMedPubMedCentralGoogle Scholar
  35. 35.
    Tuteja N, Mahajan S (2007) Calcium signaling network in plants. Plant Signal Behav 2:79–85CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Takahashi Y, Berberich T, Miyazaki A, Seo S, Ohashi Y, Kusano T (2003) Spermine signaling in tobacco: activation of mitogen-activated protein kinases by spermine is mediated through mitochondrial dysfunction. Plant J 36:820–829CrossRefPubMedGoogle Scholar
  37. 37.
    Takahashi Y, Uehara Y, Berberich T, Ito A, Saitou H, Miyazaki A, Terauchi R, Kusano T (2004) A subset of the hypersensitive response marker genes including HSR203J is downstream target of spermine-signal transduction pathway in tobacco. Plant J 40:586–595CrossRefPubMedGoogle Scholar
  38. 38.
    Yoda H, Hiroi Y, Sano H (2006) Polyamine oxidase is one of the key elements for oxidative burst to induce programmed cell death in tobacco cultured cells. Plant Physiol 142:193–206CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Michael A, Kusano T (2006) The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett 580:6783–6788CrossRefPubMedGoogle Scholar
  40. 40.
    Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael A, Kusano T (2007) A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun 352:486–490CrossRefPubMedGoogle Scholar
  41. 41.
    Moschou PN, Sanmartin M, Andriopoulou AH, Rojo E, Sanchez-Serrano JJ, Roubelakis-Angelakis KA (2008) Bridging the gap between plant and mammalian polyamine catabolism: a novel peroxisomal polyamine oxidase responsible for a full back-conversion pathway in Arabidopsis. Plant Physiol 47:1845–1857CrossRefGoogle Scholar
  42. 42.
    Wu J, Shang Z, Wu J, Jiang X, Moschou PN, Sun W, Roubelakis-Angelakis KA, Zhang S (2010) Spermidine oxidase-derived H2O2 regulates pollen plasma membrane hyperpolarization-activated Ca2+-permeable channels and pollen tube growth. Plant J 63:1042–1053CrossRefPubMedGoogle Scholar
  43. 43.
    An Z, Jing W, Liu Y, Zhang W (2008) Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J Exp Bot 59:815–825CrossRefPubMedGoogle Scholar
  44. 44.
    Jang SJ, Wi SJ, Choi YJ, An G, Park KY (2012) Increased polyamine biosynthesis enhances stress tolerance by preventing the accumulation of reactive oxygen species: T-DNA mutational analysis of Oryza sativa lysine decarboxylase-like protein 1. Mol Cells 34:251–262CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Gupta K, Sengupta A, Chakraborty M, Gupta B (2016) Hydrogen peroxide and polyamines at as double edged swords in plant abiotic stress responses. Front Plant Sci 7:1343PubMedPubMedCentralGoogle Scholar
  46. 46.
    Moschou PN, Wu J, Cona A, 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 63:5003–5015CrossRefGoogle Scholar
  47. 47.
    Moschou PN, Delis ID, Paschalidis KA, Roubelakis-Angelakis KA (2008) Transgenic tobacco plants overexpressing polyamine oxidase are not able to cope with oxidative burst generated by abiotic factors. Physiol Plant 133:140–156CrossRefGoogle Scholar
  48. 48.
    Wang W, Liu J-H (2016) CsPAO4 of Citrus sinensis functions in polyamine terminal catabolism and inhibits plant growth under salt stress. Sci Rep 6:31384CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (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 20:1708–1724CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Tavladoraki P, Rossi MN, Saccuti G, Perez-Amador MA, Polticelli F, Angelini R, Federico R (2006) Heterologous expression and biochemical characterization of a polyamine oxidase from Arabidopsis involved in polyamine back conversion. Plant Physiol 141:1519–1532CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Ahou A, Martignago D, Alabdallah O, Tavazza R, Stano P, Macone A, Pivato M, Masi A, Rambla JL, Vera-Sirera F, Angelini R, Federico R, Tavladoraki P (2014) A plant spermine oxidase/dehydrogenase regulated by the proteasome and polyamines. J Exp Bot 65:1585–1603CrossRefPubMedGoogle Scholar
  52. 52.
    Kim DW, Watanabe K, Murayama C, Izawa S, Niitsu M, Michael AJ, Berberich T, Kusano T (2014) Polyamine oxidase 5 regulates Arabidopsis thaliana growth through a thermospermine oxidase activity. Plant Physiol 165:1575–1590CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    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 7:214CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Zarza X, Atanasov KE, Marco F, Arbona V, Carrasco P, Kopka J, Fotopoulos V, Munnik T, Gomez-Cadenas A, Tiburcio AF, Alcazar R (2016) 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):527–542. doi:10.1111/pce.12714CrossRefPubMedGoogle Scholar
  55. 55.
    Gemes K, Kim YJ, Park KY, Moschou PN, Andronis E, Valassaki C, Roussis A, Roubelakis-Angelakis KA (2016) An NADPH-oxidase/polyamine oxidase feedback loop controls oxidative burst under salinity. Plant Physiol 172:1418–1431CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Baudoulin E, Hancock JT (2014) Nitric acid signaling in plants. Front Plant Sci 4:553Google Scholar
  57. 57.
    Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011) On the origin of nitric oxide. Trends Plant Sci 16:160–168CrossRefPubMedGoogle Scholar
  58. 58.
    Wang Y, Loake GJ, Chu C (2013) Cross-talk of nitric oxide and reactive oxygen species in plant programed cell death. Front Plant Sci 4:314PubMedPubMedCentralGoogle Scholar
  59. 59.
    Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EI, Scherer GF (2006) Polyamines induce rapid synthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354CrossRefPubMedGoogle Scholar
  60. 60.
    Wimalasekera R, Tebartz F, Scherer GF (2011) Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci 181:593–603CrossRefGoogle Scholar
  61. 61.
    Wimalasekera R, Villar C, Begum T, Scherer GF (2011) Copper amine oxidase 1 (CuAO1) of Arabidopsis thaliana contributes to abscisic acid- and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction. Mol Plant 4:663–678CrossRefPubMedGoogle Scholar
  62. 62.
    Krasuska U, Ciacka K, Gniazdowska A (2016) Nitric oxide-polyamines cross-talk during dormany release and germination of apple embryos. Nitric Oxide 68:38–50. doi:10.1016/j.niox.2016.11.003CrossRefPubMedGoogle Scholar
  63. 63.
    Peng D, Wang X, Li Z, Zhang Y, Peng Y, Li Y, He X, Zhang X, Ma X, Huang L, Yan Y (2016) NO is involved spermidine-induced drought tolerance in white clover via activation of antioxidant enzymes and genes. Protoplasma 253:1243–1254CrossRefPubMedGoogle Scholar
  64. 64.
    Lin A, Wang Y, Tang J, Xue P, Li C, Liu L, Hu B, Yang F, Loake GJ, Chu C (2011) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiol 158:451–464CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Paris R, Iglesias MJ, Terrile MC, Casalongue CA (2013) Function of S-nitrosylation in plant hormone networks. Front Plant Sci 4:294PubMedGoogle Scholar
  66. 66.
    Tanou G, Ziogas V, Belghazi M, Christou A, Filippou P, Job D, Fotopoulos V, Kojassiotis A (2014) Polyamine reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress. Plant Cell Environ 37:864–885CrossRefPubMedGoogle Scholar
  67. 67.
    Jang EK, Min KH, Kim SH, Nam S-H, Zhang S, Kim YC, Cho BH, Yang K-Y (2009) Mitogen-activated protein kinase cascade in the signaling for polyamine biosynthesis in tobacco. Plant Cell Physiol 50:658–664CrossRefPubMedGoogle Scholar
  68. 68.
    Yamakawa H, Kamada H, Satoh M, Ohashi Y (1998) Spermine is a salicylate-independent endogenous inducer for both tobacco acidic pathogenesis-related proteins and resistance against tobacco mosaic virus infection. Plant Physiol 118:1213–1222CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Tateda C, Ozaki R, Onodera Y, Takahashi Y, Yamaguchi K, Berberich T, Koizumi N, Kusano T (2008) NtbZIP60, an endoplasmic reticulum-localized transcription factor, plays a role in defence response against bacterial pathogen in Nicotiana tabacum. J Plant Res 121:603–611CrossRefPubMedGoogle Scholar
  70. 70.
    Iwata Y, Koizumi N (2012) Plant transducers of the endoplasmic reticulum unfolded protein response. Trends Plant Sci 17:720–727CrossRefPubMedGoogle Scholar
  71. 71.
    Mitsuya Y, Takahashi Y, Berberich T, Miyazaki A, Matsumura H, Takahashi H, Terauchi R, Kusano T (2009) Spermine signaling plays a significant role in the defense response of Arabidopsis thaliana to cucumber mosaic virus. J Plant Physiol 166:626–643CrossRefPubMedGoogle Scholar
  72. 72.
    Sagor GHM, Chawla P, Kim DW, Berberich T, Kojima S, Niitsu M, Kusano T (2015) The polyamine spermine induces the unfolded protein response via the MAPK cascade in Arabidopsis. Front Plant Sci 6:687CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Mo H, Wang X, Zhang Y, Zhang G, Zhang J, Ma Z (2015) Cotton polyamine oxidase is required for spermine and camalexin signaling in the defence response to Verticillium dahliae. Plant J 83:962–975CrossRefPubMedGoogle Scholar
  74. 74.
    Liu T, Dobashi H, Kim DW, Sagor GHM, Niitsu M, Berberich T, Kusano T (2014) Arabidopsis mutant plants with diverse defects in polyamine metabolism show unequal sensitivity to exogenous cadaverine probably based on their spermine content. Physiol Mol Biol Plant 20:151–159CrossRefGoogle Scholar
  75. 75.
    Sagor GHM, Berberich T, Kojima S, Niitsu M, Kusano T (2016) Spermine modulates the expression of two probable polyamine transporter genes and determines growth responses to cadaverine in Arabidopsis. Plant Cell Rep 35:1247–1257CrossRefPubMedGoogle Scholar
  76. 76.
    Bolton MD (2009) Primary metabolism and plant defense-fuel for the fire. Mol Plant Microbe Interact 22:487–497CrossRefPubMedGoogle Scholar
  77. 77.
    Shelp B, Bown AW, Faure D (2006) Extracellular γ-aminobutyrate mediates communication between plants and other organisms. Plant Physiol 142:1350–1352CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Xing SG, Jun YB, Hau ZW, Liang LY (2007) Higher accumulation of γ-aminobutyric acid induced by salt stress through stimulating the activity of diamine oxidases in Glycine max (L.) Merr. roots. Plant Physiol Biochem 45:560–566CrossRefPubMedGoogle Scholar
  79. 79.
    Petrivalsky M, Brauner F, Luhova L, Gaqneul D, Sebela M (2007) Aminoaldehyde dehydrogenase activity during wound healing of mechanically injured pea seedlings. J Plant Physiol 164:1410–1418CrossRefPubMedGoogle Scholar
  80. 80.
    Hatmi S, Gruau C, Trotel-Aziz P, Villaume S, Rabenoelina F, Baillieul F, Eullaffroy P, Clement C, Ferchichi A, Aziz A (2015) Drought stress tolerance in grapevine involves activation of polyamine oxidation contributing to improved immune response and low susceptibility to Botrytis cinerea. J Exp Bot 66:775–787CrossRefPubMedGoogle Scholar
  81. 81.
    Zarei A, Trobacher CP, Shelp BJ (2016) Arabidopsis aldehyde dehydrogenase 10 family members confer salt tolerance through putrescine-derived 4-aminobutyrate (GABA) production. Sci Reports 6:35115CrossRefGoogle Scholar
  82. 82.
    Gilroy S, Suzuki N, Miller G, Choi W-G, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci 19:623–630CrossRefPubMedGoogle Scholar
  83. 83.
    Yoshimoto K, Noutoshi Y, Hayashi K, Shirasu K, Takahashi T, Motose H (2012) A chemical biology approach reveals an opposite action between thermospermine and auxin in xylem development in Arabidopsis. Plant Cell Physiol 53:635–645CrossRefPubMedGoogle Scholar
  84. 84.
    Baima S, Forte V, Possenti M, Penalosa A, Leoni G, Salvi S, Felici B, Ruberti I, Morelli G (2014) Negative feedback regulation of auxin signaling by ATHB8/ACL5-BUD2 transcription module. Mol Plant 7:1006–1025CrossRefPubMedGoogle Scholar

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© Springer Science+Business Media LLC 2018

Authors and Affiliations

  • Tomonobu Kusano
    • 1
    Email author
  • G. H. M. Sagor
    • 2
  • Thomas Berberich
    • 3
  1. 1.Graduate School of Life SciencesTohoku UniversitySendaiJapan
  2. 2.Department of Genetics & Plant BreedingBangladesh Agricultural UniversityMymensinghBangladesh
  3. 3.Laboratory CenterSenckenberg Biodiversity and Climate Research Centre (BiK-F)Frankfurt am MainGermany

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